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Evolution of breeding behavior in the magnificent frigatebird : copulatory pattern and parental investment

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Title:
Evolution of breeding behavior in the magnificent frigatebird : copulatory pattern and parental investment
Creator:
Osorno Cepeda, Jose Luis J., 1957-
Publication Date:
Language:
English
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xiv, 173 leaves : ill. ; 29 cm.

Subjects

Subjects / Keywords:
Animal nesting ( jstor )
Bird nesting ( jstor )
Birds ( jstor )
Breeding seasons ( jstor )
Chicks ( jstor )
Eggs ( jstor )
Family desertion ( jstor )
Female animals ( jstor )
Mating behavior ( jstor )
Sex ratio ( jstor )
Dissertations, Academic -- Zoology -- UF
Frigate-birds -- Behavior ( lcsh )
Frigate-birds -- Breeding ( lcsh )
Zoology thesis, Ph. D
Genre:
bibliography ( marcgt )
government publication (state, provincial, terriorial, dependent) ( marcgt )
non-fiction ( marcgt )

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1996.
Bibliography:
Includes bibliographical references (leaves 164-172).
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Jose Luis J. Osorno Cepeda .

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EVOLUTION OF BREEDING BEHAVIOR IN THE MAGNIFICENT
FRIGATEBIRD: COPULATORY PATTERN AND PARENTAL INVESTMENT












By


JOSE LUIS J. OSORNO CEPEDA


A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY


UNIVERSITY OF FLORIDA

1996


UNIVERSITY OF FLORIDA LIBRARIES
























To Rodrigo and Alejandro, My Children


To Guadalupe, My Wife To Doha Jose, My Mother To Chelin, Josue and Madai


To the people I love...


















ACKNOWLEDGMENTS


I thank Dr. Jane Brockmann for all her support and advice. Dr.

Brockmann encouraged me explicitly and implicitly, following her rigorous method and approach to the study of the behavior and evolution. She also encouraged me to get involved in all possible academic activities doing research and teaching. Her questions always took me to a new and novel analysis of my data. I especially appreciate the time she invested improving the English in my manuscript.

I thank Dr. Dewsbury, Dr. Guillette, Dr. Kiltie and Dr. Levey, my committee members, for their advice in the most difficult moments of my research and they encouraged me to keep working hard.

I am especially grateful to Dr. Hugh Drummond and all the people from his lab at the Centro de Ecologia, U.N.A.M. Dr. Drummond, my advisor in Mexico, has been the keystone in my formation. I am still learning from his suggestions made a long time ago, especially in these days of loose contact.

This work was possible because of the contributions to the fieldwork of many students of the Facultad de Ciencias and the Centro de Ecologia at the University of M6xico (UNAM). Thanks to Adrian Lecona, Suneeta Sing, Tarin Toledo, Lourdes Fernendez, Ines Arroyo, Elsa Saborio, Tonanzin and Cristina Rodriguez for their effort and enthusiasm in the field. They really did an


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excellent job and took the right decisions when I was not at the island with them. Constantino Macias and Juliet Vickery kindly helped me when they were at the island doing their own research. Many administrative tasks crucial for this project were accomplished by Cristina Rodriguez and Virgilio Lara from the Centro de Ecologia.

The Consejo Nacional de Ciencia y Tecnologia (CONACyT) in M6xico, The University of Florida, The Florida Foundation, The Centro de Ecologia and Sigma Xi provided financial support for this work. The Secretaria de Desarrollo Social (SEDESOL) in M6xico provided the permits to work at the island and the Secretaria de Marina provided logistical support and transportation to the island. Thanks to all these institutions.

Fishermen from San Blas and Boca de Camichin contributed in several ways to the accomplishing of this work, especially with their friendship.

Dr. Louis Guillette and Drew Crane advised and helped me and provided all materials for the hormone analysis (Chapter 2). Dr. Wayne Potts kindly helped me and provided the materials and time supervising my work at his molecular lab (Laboratory of Genetics and Mammalogy). Karen and Anthony Baker taught me DNA microsatellite techniques for the analysis of paternity. Unfortunately, this technique did not work properly with frigatebirds.

I am especially grateful to Guadalupe Hernendez, my wife, for the long talks about my hypotheses. After those long discussions about the different topics she really now understands the breeding biology of frigatebird better than

1.


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All my friends at the Centro de Ecologia and Facultad de Ciencias at the UNAM supported me when I needed help in several ways. They always have been there, with me. They know that.

Finally, thanks to Rodri and Ale, my children. They were always a source of support and excellent humor. They always encouraged me in the most crazy enterprises of my life. Their coming to live in Gainesville was only one test of their love.

The Universidad Nacional Aut6noma de M6xico generously provided the financial support (scholarship) to do my Ph.D. studies at the University of Florida. Thank you to the UNAM.


V











TABLE OF CONTENTS


A C K N O W LE D G M E N T S ................................................................................. . . ii

L IS T O F T A B L E S ............................................................................................ . . x

L IS T O F F IG U R E S ....................................................................................... . . x i

A B S T R A C T .........................................................................................................x iii

CHAPTERS

1 . IN T R O D U C T IO N ............................................................................1

Reproductive Biology of Frigatebirds with Emphasis in the Magnificent Frigatebird: Is Feeding Ecology Associated to
D ifferences in Life H istories? ........................................................1
Comparative Biology of Frigatebirds .........................................3
External m orphology............................................................ 3
C la ssifica tio n .................................................................... . 4
G eographic d istribution ..........................................................4
Breeding ecology-colony level patterns .................................5
Breeding ecology-individual patterns .....................................6
F e e d in g e co lo g y .....................................................................9
M e th o d s .......................................................... ...................... . 1 1
Individual Marking and Nest Visits.......................................12
C e n s u s e s ......................................................................... 1 3
Incubation and Brooding Periods ...........................................14
O bservations of M arked Birds ..............................................14
Behavioral O bservations .............................. ...................... 14
Behavioral C ategories .............................. .................... 15
Courtship period..............................15
Chick Feeding................................16
Data Analysis...................................16
C hick age estim ations .............. ....................... 16
Chick growth ....... ..................16
Sexing the chicks...................................17
Behavioral analysis............................... 17
Chick feedings................................18
R e s u lts ...........................1....8...................... 1 8
The Population View............. ...................18


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Breeding season...............................18
Mating success......................................... 19
Egg survival.............................................. 19
C hick survival................ ................................ 20
A d u lt d ispe rsio n .......... ......... ...............................2 0
T he Individ ua l V iew .................. .............................2 1
P a ir fo rm a tio n ............. ...................................... 2 1
Nest building and copulation behavior.............................22
Intra- and extra-pair copulation frequency .........................23
The role of adults during incubation and brooding ...............23
C h ic k re a rin g ........................................................................ 2 4
Chick growth, fledging and independence.......................25
A d u lt re -m a tin g .....................................................................2 5
Discussion............................... .......26
The Magnificent Frigatebird at the Isla Isabel ......................... 26
The Effects of Feeding Ecology on the Breeding Biology of
F rig a te b ird s ...........................................................................2 7
Causes of C hick M ortality..................................................... 33

2. A TEST OF THREE HYPOTHESES TO EXPLAIN THE
FUNCTION OF THE COPULATION PATTERN IN THE
MAGNIFICENT FRIGATEBIRD.................................................. 41

In tro d u ctio n ........................................................................... . . 4 1
Hypotheses to Explain Multiple Intra-pair Copulations ............42
The Fertilization Hypothesis............................................ .42
C onflict of interest............................................................. . 42
The Stimulation-Assessment Hypothesis........................43
The Sperm Competition Hypothesis.................................44
Hypotheses to explain the peak of copulations .................... 45
Determining the female's fertile period .................................45
Predictions From the Hypotheses applied to the Magnificent
F rig a te b ird ............................................................................4 7
M e th o d s ............................................................................... . . 4 9
The Description of the Copulatory Pattern......................... 49
B ehaviora l categories ...........................................................50
Experim ental D esign........................................................... 50
Fem ale's Fertile Period....................................................... 51
D ata A na lysis .................................................................... . . 5 3
Behavioral analysis........................................................... 53
S tatistical ana lysis......................................................... . . 54
R e s u lts ....................................................................................... 5 4
The Copulatory Pattern in the Magnificent Frigatebird: The
D escriptive A pproach ...........................................................54
Nest building and copulation behavior.............................55


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Intra-pair copulation frequency...................................... 55
Extra-pair copulation frequency. ................56
E xpe rim e nta l R e su lts ...............................................................56
Control and experimental nests........................................ 56
Fertilization H ypothesis ........................................................57
Stimulation-Assessment Hypothesis................................. 57
Sperm Competition Hypothesis........................................ 59
Peak of Copulation Hypothesis ............................................59
D is c u s s io n ..................................................................................6 0
Fertilization and Stimulation Hypotheses............................ 61
Sperm Competition Hypothesis ...............................................62
Peak of Copulation Hypothesis ............................................... 64

3. THE TIMING OF MALE DESERTION IN THE MAGNIFICENT
FRIGATEBIRD: A TRADE-OFF BETWEEN CURRENT AND
FUTURE REPRODUCTION ....................................................... 76

In tro d u ctio n ........................................................................... . . 7 6
Predictions Derived From the Parental Investment Theory .....81
M e th o d s ............................................................................... . . 8 2
M easurem ents.................................................................. . . 83
M a le d e s e rtio n ......................................................................8 3
Laying date estimation and settlement time .........................83
C hick age estim ations ...........................................................83
Chick feeding rate............................................................ 84
B ody cond ition ................................................................. . 84
Statistical Analysis.............................................................. 85
R e s u lts .................................................................................. . . 8 5
Time of Male Desertion....................................................... 85
Male Desertion and Body Condition ........................................86
Survival Probability of Chicks............................................. 86
Reproductive Benefit of Male Desertion ..................................87
Male and Female Contribution to Chick Feeding .................... 88
D iscu ss io n ............................................................................ . . 8 8
Chick Survival and Male Desertion..................................... 89
F e m a le C o ntrib utio n ................................................................9 3
The Trade-off Between Current and Future Reproduction ......93

4. FEMALE TACTICS TO COPE WITH MALE DESERTION IN
THE MAGNIFICENT FRIGATEBIRD ...................103

Introduction.................................... 103
Response to Desertion...............................105
Methods...................................... 109
Laying Date Estimation........................ ......................110


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Chick Age Estimations...........................................................110
C h ick F e e d ing R ate ...............................................................1 10
C h ic k G ro w th .........................................................................1 1 1
S e x in g F le d g lin g s ..................................................................1 1 1
S ta tistica l A n a lys is .................................................................1 1 1
R e s u lts ............................. .................................. ....................1 1 2
Female Compensation for the Male's Absence.....................112
Female Tactics Dealing W ith the Male's Desertion...............113
D is c u s s io n ................................................................................1 1 5

5. FLEDGING SEX RATIO AND THE COST OF REAR MALES
AND FEMALES BY A DESERTED FEMALE IN
FRIGATEBIRDS................................ 127

In tro d u c tio n ...............................................................................1 2 7
Facultative Sex Ratio.............................................................129
Sex Conflict About the Offspring Sex Ratio ...........................130
M e th o d s ....................................................................................1 3 3
Individual Marking and Nest Visits .........................................133
Behavioral Observations.......................................................134
C h ic k fe e d in g ......................................................................13 5
Observation of marked birds ...............................................135
D a ta A n a ly s is .........................................................................13 6
Chick age estimations .........................................................136
S exin g th e ch icks ................................................................136
C h ick g ro w th .......................................................................136
Behavioral analysis............................................................137
R e s u lts ......................................................................................1 3 8
C h ic k F e e d in g ................................................. ......................13 8
Chick growth and chick fledging.........................................139
F le d g in g se x ratio ...............................................................13 9
Chick Independence..............................................................140
D iscussio n .......................................................................... . 14 1
The Cost of Rearing Males and Females..............................141
The Condition Dependent Sex-bias Hypothesis....................144
Adult Male and Female Conflict About the Offspring SexR atio ................... .. . ........ 14 6

6. CONCLUSIONS. MAIN REMARKS AND FUTURE
RESEARCH.......................................156

LITERATURE CITED............................................164

BIOGRAPHICAL SKETCH..........................................173


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LIST OF TABLES


Table Page

1.1 Comparative breeding biology of the five species of frigatebirds
including this study......................................35

2.1 Reproductive success and nest failure in experimental and control
nests................................................68

2.2 Copulation rate in experimental nests and the frequency of egg
laying................................................ 69

3.1 Frequency of early and late-settled marked males seen and not
seen in the next breeding season ....................... ............. 96

4.1 Feeding rates of females to chicks of early and late-settled nests
as a function of chick age.............................................120

5.1 Comparisons of the average number of feedings delivered by the
mother to sons and daughters.........................................148

5.2 Mean of the asymptotic size at fledging of 23 male and 17 female
chicks....................... ............................... 149

5.3 The growth rate of male and female chicks............. .......150


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LIST OF FIGURES


Figure page

1.1 Schematic representation of the typical frigatebird breeding
from the point of view of populations and individuals............................... 36

1.2 Number of male magnificent frigatebirds displaying at the breeding
c o lo n y ... ............................................. ............................................. . . 3 7

1.3 Adult operational sex ratio per day at the reproductive site as a
function of the tim e of the year............................................................. 38

1.4 Adult sex ratio per day at a roosting site as a function of the time of
th e y e a r............... .............................................3 9

1.5 Feeding frequency of male and female adults as a function of the
chick age . . ........................... ...................... . 40

2.1 Proportion of time that males and females stayed at nest during
the nest-building and copulation period.............................................. 70

2.2 Proportion of time that males and females stayed at nest during the
nest-building and copulation period..................................................... 71

2.3 Rate of stick delivery by the male as a function of the nest-building
and copulation period....................................72

2.4 Copulation rate as a function of the days before egg laying.................... 73

2.5 Average copulation frequency at experimental and control nests ............74

2.6 Circulating concentrations of testosterone and estradiol in females
as a function of the days before egg laying.....................75

3.1 Frequency of male desertion as a function of the age of the chick ..........97











3.2 Frequency of male desertion as a function of the date of the year ..........98

3.3 Chick condition index at the time of male desertion as a function
of the age of the chick at mate desertion............................................ 99

3.4 C hick m ortality after m ale desertion....................................................... 100

3.5 Feeding frequency of males and females as a function of chick age .....101

3.6 Schematic representation of the trade-off between current and
future reproduction in frigatebirds ..........................................................102

4.1 Feeding rate delivered by early- and late-settled females.....................121

4.2 Total feeding rate delivered by males and females in early- and latesettled nests as a function of the time of the year ..................................122

4.3 Growth (weight) of the chicks from early- and late-settled nests ............123

4.4 Growth (culmen length) of the chicks from early- and late-settled
n e s ts ....................................................................................................... 1 2 4

4.5 Growth (ulna length) of the chicks from early- and late- settled
n e s ts .......................................................................................................1 2 5

4.6 Schematic representation of the female extra-compensation in
te rm s o f c h ic k su rv iva l............................................................................12 6

5.1 Feedings by the female to sons and daughters .....................................151

5.2 Feedings by the male to sons and daughters ........................................152

5.3 Growth (mass) of male and female chicks ..............................................153

5.4 Growth (culmen length) of male and female chicks ................................154

5.5 Growth rate (ulna length) of male and female chicks............................ 155

6.1 Schematic representation of the trade-off between current and
future reproduction in frigatebirds and female extra-compensation
in term s of chick survival ......... ............................... 163


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Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy


EVOLUTION OF BREEDING BEHAVIOR IN THE MAGNIFICENT
FRIGATEBIRD: COPULATORY PATTERN AND PARENTAL INVESTMENT By

Jose Luis J. Osorno Cepeda

August 1996

Chairman: Dr. H. Jane Brockmann
Major Department: Zoology


Frigatebirds are unusual in showing reversed sexual size dimorphism, in laying one egg, and in their pattern of parental care. These unusual features provide a good testing ground for theory on the evolution of mate desertion, copulation frequency, and sex ratios.
In most species of frigatebirds, males and females share equally the long (14-18 month) period of parental care, but in magnificent frigatebirds (Fregata magnificens) males desert the nest when the chick is 18 to 160 days old. After spending 5 months away, deserting males return to mate in the next breeding season while females are still feeding the fledged chicks. Courtship and nest building occur over a 4-month period and males that nest early desert at an older chick age than late-settled males. Since chick survivorship is correlated with chick size, when late-settled males desert they apparently sacrifice current chick survivorship for increased future reproductive success.


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Females are not passive to male desertion. Early- settled females compensate for the absence of the male by increasing chick feeding. Latesettled females compensate for the male's absence by increasing their feeding rate and consequently the chick's growth and development beyond that of earlysettled females. This extra-compensation could be a tactic of late-settled females to reduce the mortality of chicks when males desert.
Female chicks are 10% larger than males at fledging and somewhat more expensive, i.e. require more feedings and fledge at a later age. Fledging sex ratios do not differ from 1:1, but late-settled nests (where females are abandoned by males when chicks are younger) show a trend toward a malebiased sex ratio. Furthermore, males desert nests with female offspring somewhat later than those with male chicks. These results suggest conditiondependent sex ratios.
Frigatebirds lay only one egg, but pairs copulate many times over two weeks. By interrupting copulations I showed that low copulation frequency in experimental nests does not affect egg fertility when compared with controls, so multiple copulations do not function to insure fertilization. Extra-pair copulations occur in 9% of nests suggesting that by copulating frequently males may be protecting their paternity.













CHAPTER 1
INTRODUCTION



Reproductive Biology of Frigatebirds With Emphasis in the Magnificent
Frigatebird: Is Feeding Ecology Associated to Differences in Life Histories?



Food availability and feeding ecology may be considered two of the key factors promoting differences among populations and, ultimately, among species. In particular, theory has suggested that food abundance, distribution and defendibility affects the evolution of mating systems (Orians 1969) and social organization (Emlen and Oring 1977). An example of this is that some bird species are more polygynous in rich habitats (high food availability) and less so in poorer habitats (Dunn and Hannon 1992). Female preferences for males may be a function of food levels. Females may prefer mating polygynously in a good territory and monogamously in a poor habitat (Orians 1969, Dunn and Hannon 1992).

It has been suggested that monogamy is maintained because females

require the contribution of males to rear offspring. However, under conditions of high food availability, the importance of the male can be reduced and even made marginal. Increased food availability may increase the rearing abilities of adults. If females are able to raise the chicks alone because of improved food availability, males can desert and look for another partner (Maynard Smith 1977). Some male removal experiments have shown this (Bart and Tornes 1989), but others have shown no effect on female reproductive success (see ref.








in Bart and Tornes 1989). Food availability has rarely been mentioned explicitly in models of desertion (Maynard Smith 1977, Grafen and Sibly 1978, Beissinger 1987), but clearly this variable can alter the rearing abilities of the parents and the condition of the offspring (Dunn and Robertson 1992). Mate desertion occurs more frequently in populations with greater availability of food (Beissinger 1987, Whittingham and Robertson 1994, but see Dunn and Roberson 1992) and it is more likely in species with small clutches than those with large ones (Fujioka 1989, Beissinger 1987, 1990). A cascade of effects can be expected as a consequence of increased rearing abilities in parents: If individuals are deserting to increase their long-term reproductive success, intra- and intersexual competition for mates might increase (the intensity of sexual selection). In this case mixed reproductive strategies can evolve in populations (Trivers 1972) e.g., extra-pair copulations and egg dumping. Counter-strategies can also be predicted in this scenario to cope with cuckoldry: mate guarding and increased intra-pair copulations. In addition, if the cost of rearing males and females changes because of desertion, facultative sex-ratio adjustment may evolve. Other consequences of changes in food availability can be expected: changes in the length of laying periods, reproductive synchrony, attentive periods to the offspring and growth rate of the chicks. All aspects of reproductive biology then may be influenced by differences in food availability. I address some of these issues in the frigatebirds group (Fregata), specifically in the magnificent frigatebird (Fregata magnificens)

Similarities in frigatebirds can be expected because of the common

ancestry of the sister species. Differences are likely due to adaptive divergence to different conditions. Differences in food availability can play a pivotal role in the evolution of the different life histories of the frigatebirds. In this chapter I (1) summarize the information available about the biology of the five species of








frigatebirds, (2) add new information about the reproductive biology of the magnificent frigatebird (Fregata magnificens) and (3) I discuss the possible role of feeding ecology and distribution of frigatebirds on breeding differences among species. Most of this summary is based on the excellent review by Brian Nelson (1975) and on work concerning the magnificent frigatebird by Diamond (1972, 1973) and Durand (1992).


Comparative Biology of Frigatebirds


External morphology

The five recognized species of Frigatebirds are a morphologically unified group. Frigatebirds are relatively large seabirds with a large wing span ranging from 190 to 240 cm (Howell 1994). These birds are well adapted to economic flight as suggested by their great wing span to weight ratio (larger than any other seabird of comparable size) light skeleton (75-80 g dry-weight) and long and deeply forked tail (Nelson 1967). Frigatebirds have a long bill, strongly hooked at the tip (Eismann 1962, Nelson 1975, Sibley and Alquist 1992), short tarsi, small feet, webs restricted to the basal part of the toes (zygodactylous condition), vestigial uropygial gland. All five species are sexually dimorphic: males are 6 to 12% smaller in culmen length than females (Nelson 1975, Schreiber and Schreiber 1988); males are wholly or mainly glossy black and have a highly distensible gular pouch (scarlet red when in courtship). Females are black with more or less white underparts, except F. aquila. Juveniles are usually black with white underparts and in some species they have a rufoustinged head (Eisenmann 1962, Nelson 1975, Howell 1994).





4


Classification

The five species of frigatebirds are included in the Genus Fregata and the family Fregatidae. The five species are: F. aquila, F. andrewsi, F. ariel, F. minor and F. magnificens. This family has been considered part of the order Pelecaniformes since Linneaus' classification (Cracraft 1985, Sibley and Ahlquist 1992), and this placement has been corroborated using numerical cladistic analysis on morphological and behavioral characters by Cracraft (1987). However, a recent re-classification of avian taxa using molecular techniques (DNA hybridization) and maximum parsimony cladograms, suggested that the Frigatebird family should be included in the order Ciconiformes and that they are more related to Sphenicidae (penguins), Gavidae (loons) and Procelaridae (petrels and albatrosses; Sibley and Ahlquist 1992, Sibley et al. 1988) than to the Pelecanidae, Phaethodontidae, Phalacrocoracidae and Suloidea families, with which they are currently grouped. Even though the change in classification looks dramatic, Frigatebirds have always been considered a distant group from the other Pelecaniformes (Pelicans, Boobies, Tropic Birds, Cormorants and Anhingas). The new classification is still controversial because of criticisms about the way in which the DNA information is used to build phylogenies.

The Fregatidae family is a well defined group, but relationships inside the Family are still not well established. The only reference in Sibley and Ahlquist (1992) suggests that F. minor might have evolved before F. ariel and F. magnificens. DNA hybridization techniques were used to reach this conclusion.


Geographic distribution

All five species of frigatebirds are tropical and sub-tropical. Two of the five species have a highly restricted distribution. F. andrewsi is found nesting





5


only on Christmas Island in the Indian Ocean, and F. aquila is restricted to Ascension Island in the South Atlantic. Fregata minor and F. ariel, occur in the Indian and Pacific Oceans. Fregata magnificens occurs along the coast and islands of the Americas, from Ecuador to Baja California, Mexico in the Pacific and from Brazil to Florida in the Atlantic. Some overlap in distribution occurs. Fregata minor and F. ariel overlap in approximately half of their breeding localities (Nelson 1975) and F. minor overlaps with F. andrewsi at Christmas Island (Indian Ocean). Fregata minor is sympatric with F. magnificens on the Galapagos Islands (Nelson 1975), Isla Cocos, Central America and in San Benedicto Island at the Revillagigedo Archipelago in the Mexican Pacific (Howell 1994).


Breeding ecology-colony level patterns

Reproductive activity starts with male display and courtship. This period varies among species and populations. Some species are seasonal and synchronous (F. aquila, F. andewsi), whereas others are more asynchronous (F. minor, F. magnificens, F. aquila). In most species, the displaying and laying period occurs over a five -month period with clear peaks at different times during the year (Table 1.1; Nelson 1975). In one colony of F. magnificens at Barbuda Island in Lesser Antilles, laying occurs throughout the year (Diamond 1973). Except for this population, the main reproductive period is seasonal and occurs outside of the rainy season.

Reproductive colonies of frigatebirds are highly variable in size ranging from hundreds (Trivelpiece and Ferraris 1987, Howell 1994) to over 40,000 individuals (Moreno and Carmona 1988). The distribution of frigatebird nests is clumped (Reville 1988). Within groups, the density of nests varies from two nests per square meter in some groups of F. minor in the Galbpagos Islands to





6


0.06 nests per square meter in some groups of the same species at Tower Island. At Isla Isabel, F. magnificens nests are no more than 40 cm apart (per. obs.). Preferred breeding sites for F. ariel, F. andrewsi, F. aquila and F. minor are oceanic islands and coastal islands for F. magnificens and some populations of F. minor. The most common displaying and nesting places are low brushes and mangroves. One species (F. aquila) nests on rockey ground at Aldabra Atoll (Diamond 1973).

Low breeding success seems characteristic of frigatebirds. In all species, only 15 to 25% of the eggs laid produce a fledged young (Nelson 1975, Table

1.1). However some differences exist among groups in the same colony and in the same year (Reville 1988). Intra-specific disturbance (by conspecifics), chick starvation, and predation are the most frequently reported causes of nest failures. Since only 20% of the breeding population is successful in any one year and since offspring rearing takes more than one year, no more than 80% of the breeding age population attempts to breed each year.

Related to the extremely low energy consuming flying style (soaring most of the time), frigatebirds have a huge dispersion range. At least some of species are nomadic; at Aldabran Atoll, most of marked individuals of F. ariel were recovered 2000 to 3000 miles from the marking site (Sibley and Clapp 1967, Diamond 1973). Apparently prevailing winds are at least partially responsible for this dispersal.


Breeding ecology-individual patterns

The whole breeding cycle for a particular successful pair takes more than a year: 2 to 4 weeks for display and pair formation, eight weeks for incubation, about 20 to 24 weeks for growth of the nestling and from 4 to 14 months of postfledging feeding of juveniles (Figure 1.1).





7


The courtship period, including male display, nest building and

copulation, lasts about two weeks in all five species. All frigatebirds produce only one egg per clutch. The egg is 5 to 6% the female's weight (from 59 to 85 g in the different species, Table 1.1) and incubation takes 55 days in F. minor and 44 days in F. aquila. In the other three species, the incubation period is unknown. Chicks are borne naked and are extremely altricial. Hatchlings are in close contact with one adult at all times until they are from 30 to 45 days old, when parents begin to leave them unattended. Chicks grow slowly in the whole group. The lowest growth rate is reported in F ariel and in F. minor; followed by F. andrewsi, F. aquila and F. magnificens. The fastest rate occurs in populations of F. minor at Aldabra Atoll. Fledging takes from 20 to 24 weeks in all species. The first flight is not recorded in any species but it is estimated to occur at 5 to 6 months of chick age in all species (166 days in F. magnificens; 130-160 days in F. minor and F. aquila; 140 days in F. ariel; 155 days in F. andrewsi). No clear data exist about chick independence but some reports indicate that chicks are at least partially dependent on the parents for four to 14 months after fledging (four to 14 months in F. minor 9 to 10 months in F. andrewsi and about four months or more in F. magnificens and F. ariel). The post fledging period is not recorded in F. aquila.
Interesting differences in the parental care occur in frigatebirds. In three of the species (F. aquila, F. ariel and F. andrewsi), male and female share all the duties of caring and feeding the chick to independence. Interestingly, in one population of F. minor in the Galepagos Islands, both parents share the feeding of the chick to independence (Nelson 1975, Coello et al. 1977) but in the same species at Aldabra atoll, females apparently give more feedings to the chick than do males (Diamond 1973). In F. magnificens, both parents attend the egg and the small chick equally until the chick is from 20 to 125 days of chick age









(Diamond 1973, Coello et al. 1977, Trivelpiece and Ferraris 1987, Durand 1992). Then, males desert and females complete the rearing process of the chick alone.

Chicks are very resistant to starvation in all species. Feeding frequency of the chick varies with the locality and species. In F. andrewsi, chicks received food once every two days; in F. minor once every three days (Coello et al. 1977); in F. ariel once every 2.4 days (Nelson 1975); in F. magnificens once every two days (calculated from Coello et al. 1977).

Sex ratio of fledglings has been estimated in a small sample of juveniles in only three populations of F. magnificens and one population of F. minor. Two estimates of F. magnificens from the Galepagos Islands suggests a strong bias toward female production (1 male to 1.8 females, Diamond 1973; 1 male to 1.5 females, Coello et al. 1977). In contrast, at Isla Isabel the sex ratio of fledglings was estimated to be not statistically different from a 1:1 ratio (Durand 1992). Only Durand's study, however, offered statistical support for the sex ratio comparison and sexing method. In the only fledgling sex-ratio estimation in F. minor, males were as abundant as females (1 male to 1 female, Coello et al. 1977).

The age of first breeding is unknown in frigatebirds. However, estimates based on several different plumage categories suggest that it takes from 5 to 7 years to reach maturity (Nelson 1975).

Apparently, frigatebirds molt only outside the breeding period. Of all species of frigatebirds, only F. minor has been found with an interrupted molt while breeding (Coello et al 1977). Other species have been recorded as molting out of the breeding period (Nelson 1975). Frigatebirds thus may require several months to complete their molt and Nelson (1975) has speculated that the molt prevents continuous breeding in a relatively seasonless environment.








Since in all species of frigatebirds, breeding takes more than a year and since frigatebirds molt between consecutive reproductive periods, there has been speculation that reproductive periodicity in all species of frigatebirds is biennial except in F. magnificens in which because of the disparate sex roles in feeding the chick, successful males may be able to reproduce every year whereas females are biennial. However, before this work there were no data available with marked birds.


Feeding ecoloqy

Frigatebirds depend on food resources of irregular availability associated with complicated feeding techniques and a strictly limited foraging area in the water column. Their unusual feeding ecology seems to influence all aspects of their natural history. They feed mainly on tropical pelagic (blue-water) seas but one species (F. magnificens) is coastal and presumably feeds there. Frigatebirds catch food strictly from the sea surface by dipping the bill into the water (limited to 20 to 30 cm from the sea surface) Since the uropygial oil gland is vestigial in frigatebirds (Nelson 1975), they are unable to plunge dive like all other members of the order and most marine birds. During surface-dipping, frigatebirds are only able to submerge the bill or the head into the water and consequently, the availability of food is limited, fluctuating and highly unpredictable. Fishing success at sea is unknown but based on an estimate made on Albatrosses, probably the bird with the most similar feeding and breeding ecology, a bird fishing from the surface is only able to pick up one item every 100 km on average (Weimerskirch and Salamolard 1993).

The feeding ecology of frigatebirds has been studied in some detail, particularly the behavior of food stealing or kleptoparasitism (Nelson 1975, Osorno et al. 1992, Vickery and Brooke 1994, Gilardi 1995, Cummins 1995).








Although probably direct fishing is the most important feeding technique of frigatebirds (Nelson 1975), it is well known that frigatebirds steal food from other species of seabirds. Kleptoparasitism and other opportunistic feeding techniques seem to be strategies to cope with food scarcity, and which take advantage of their very well developed flying skills. Kleptoparasitism is common, but the incidence and success of this feeding technique varies among localities, ranging from 6% to 63% success depending on the host species and locality and the frigatebird species (Nelson 1975, Osorno et al. 1992, Vickery and Brooke 1994, Gilardi 1994, Cummins 1995).

Foraging distances have not been recorded in any species of frigatebirds. However, looking at the length of the attentive periods (periods of continuous nest attendance) during courtship, incubation and chick rearing ranging from one to 15 days and assuming the length of the attentive period is correlated to the foraging distance, the foraging area for these birds may be very large. At Isla Isabel in the Mexican Pacific, frigatebirds associate with shrimp boats in order to gather food items and probably most of the diet of this population is derived from this source (Calixto 1993).

The diet of all frigatebirds includes flying fishes and squids at many localities (Diamond 1973, Nelson 1975), but anchovies have been reported (Moreno and Carmona 1988) . At Isla Isabel, the magnificent frigatebird included a large variety of fishes from 26 families, squid were only a minor proportion of the diet (Calixto 1993). The large variety of fishes in the diet resembled the composition of fish species captured during the shrimp fishing by the shrimp boats around the island. It seems that this population is taking advantage of a predictable food source around the island (Calixto 1993).

In the second section of this Chapter I describe the breeding biology of the magnificent frigatebird (F. magnificens). Several studies have reported








information about the breeding biology of this frigatebird, but the information available is inadequate to analyze and explain the costs, benefits, mechanisms and constraints and conditions shaping the biology of this bird. In this chapter I describe, at the individual level, the reproductive biology of the magnificent frigatebird nesting on the Isla Isabel, off the Pacific Coast of M6xico. In addition, I compare this information with the available information for the other four species of frigatebirds. I particularly describe here the role of the sexes during courtship and nest building, incubation, brooding and chick feeding. In subsequent chapters I analyze hypotheses about the function of the intra-pair copulation pattern, male desertion, and the growth and production of male and female chicks.




Methods




I studied the magnificent frigatebird population at the Isla Isabel, State of Nayarit, M6xico (210 52' N, 1050 54' W). This colony was estimated as 3,600 nests distributed in patches on the 2-Km2 island (Osorno unpbl. data). It consisted of three dense nesting aggregations: Cerro Pel6n at the NW end of the island, Costa Fragatas along the SE shore and Bahia de los Pescadores along the SW of the island. This work was conducted on a sample of nests at the Bahia de los Pescadores zone. Frigatebirds nest here on branches at the top of small (from 1-5 m in high) deciduous trees, Crataeva tapia. Nests are often no more than 50 cm apart, creating a clumped aggregation.








The field work was conducted from 15 November 1993 to 27 July 1994 from 10 November to 28 December 1994 and from 27 March to 10 April 1995. I was assisted by 3-5 students from the Centro de Ecologia, University of M6xico.


Individual Marking and Nest Visits


We marked every accessible nest or display site and the adults mating there with plastic numbered tags as soon as I recorded a pair in courtship. A display site was a branch at the top of a tree where a male perched while usually showing his inflated red gular pouch. The nest was a 20 cm round platform made of sticks and cemented with guano. It contained an egg or chick and was guarded by an adult or chick. We captured a displaying male (i.e. a male with the red gular pouch inflated or deflated) or a pair of adults (male with the red gular pouch and female) standing at the site. Birds were captured by hand at night when they were at the nest and marked with 3-digit numbered wing tags. I marked nests and birds at night because frigatebirds are very sensitive to daytime disturbance. During the day when a frigatebird is disturbed at her/his nest, immediately other individuals, especially males, arrive at the site and try to steal the nest or nesting material. At night, frigatebirds are perched at the nest site or on other tree branches at the island.

Extensive marking was performed at the beginning of the breeding season from 17 to 21 November 1993 and from 10 to 27 November 1994. During these periods we marked 275 and 100 birds, respectively. Other birds were marked subsequently as they were captured at their nest. For each adult bird captured we recorded his/her mass and the culmen and ulna lengths.

We visited every nest in the sample once a week to check for the

presence of the egg or chick. We monitored the survivorship of every chick up to








fledging. We weighed chicks at the nest using a Pesola spring balance ( 12.5 g) and measured their culmen and ulna lengths using a measuring tape ( 0.5 mm). Since nest disturbance causes chick loss when they are small (less than 20 days old), we started our weekly visits to nests after this age. We also checked for the presence of the chick or egg at the nest from the observation site during the behavioral observation sessions (see below).


Censuses


We estimated the ratio of adult males to females from censuses at the

breeding and roosting sites in one daily census immediately before dusk (17:30 h) when a great number of the birds remain perched. We determined adults by their plumage. We counted the number of males and females perched on a branch in a designated area (quadrat) marked by natural references (trees, rocks or paths) at a breeding and roosting site. We alternated the census between the defined breeding and roosting sites. Censuses were performed daily from 25 November 1993 to 13 March 1994, and then, once every two days from 21 March to 14 June 1994.

To estimate the duration of the courtship period of the population, we

recorded the number of males with the red gular pouch partially to totally inflated at the breeding site. These censuses were performed using the scan sampling method. These censuses of gular pouches were conducted every hour during our behavioral observations from 28 November 1993 to 13 February 1994, except for the period between 31 December 1993 to 17 January 1994 when we recorded it twice a day. We also performed censuses every hour for three consecutive days per week from 16 February to 27 June 1994.





14


Incubation and Broodinq Periods


We recorded the presence of incubating adults on nests in a sub-sample of 57 nests. This sample size changed as new nests were added and nests with chicks were dropped to include them in other records. We recorded the presence and identity of the adult at the nest three times per day (0800, 1300 and 1700 h) during our behavioral observations (scan sampling). These records began on 25 December 1993 and ended on 27 June 1994.


Observations of marked birds


We also conducted observations of the presence of marked birds (juveniles and adults) at the breeding site. These observations were opportunistic during our regular behavioral observations. In addition, once per week we walked at dusk around the island looking for marked frigatebirds.


Behavioral Observations


We observed and recorded the behavior of adults and chicks at the nest. Behavioral observations were conducted from 20 November 1993 to 21 July 1994. Every observation site was covered by two observers alternating observation sessions every two hours from 0800 to 1800. We recorded the behavior at the displaying site or nest daily during courtship, incubation and the first 30 days after chick hatching. Then, during the chick-rearing period (from 40 days to 6 months chick age), we observed nests, three consecutive days per week, from 0800 to 1900 h (from 16 February to 20 July 1994). The observation post was located at the top of a building, located 30 to 150 m from the focal








nests. We observed up to 36 nests simultaneously. This large number of nests was possible because we recorded a few specific behavioral categories and because behavioral categories were conspicuous (see below). In addition, every behavioral category was easy to record since frigatebirds are large birds (females are almost 2 m wingspan) and behavioral patterns occurred infrequently.


Behavioral Categories


Nest-building period

Nest-building period includes the nest-construction activities (males

bringing nest material and females building the nest) and the copulation period. For every displaying site or nest we recorded (1) the presence of the male, and the female at the beginning of every recording session; (2) the time of arrival or departure of each adult or flying chick to and from the nest; (3) every copulation or copulation attempt. "Copulation" is defined as occurring when the male mounts the female's back, wings extended and he orients in the same direction as the female's head. The female extends her neck straight forward and the male touches her neck with his bill and grasps the neck feathers of the female. In this position the male moves backward over the female's back, moves his tail feathers and pelvic zone laterally and pushes the tail feathers of the female to one side. The female lifts her tail feathers and the male moves his pelvis down until his cloaca reaches the cloaca of the female. Cloacal contact lasts only 2 to

4 sec with two or three spasmodic movements of the male. We did not record cloacal contact because the birds' relative position on the nest and vegetation precluded observing this event reliably. (4) We recorded any stick of branch





16


carried by the male to the nest, which was usually incorporated into the nest by the female.

Chick feeding. We recorded every chick feeding that occurred during the day. Feedings were recorded when the chick put its bill into the open mouth of the parent. In every interaction, we recorded the identity (number) and sex of the parent and the identity of the chick involved. Since some unknown amount of feedings occurred at night, I assumed that our chick feeding rates were only estimates of the real feeding rate. Feedings to chicks smaller than 20 days old were very difficult to see, so I excluded them from the analysis.


Data Analysis


Chick age estimations

Since we recorded chick growth after 40 days, the precise age of chicks in our sample was unknown. We estimated the age of the chicks in the sample by interpolation from the culmen length growth curve fitted to chicks of this population in 1991 (Durand 1992). The average estimated age of the chicks in the sample was 40.6 days (SE=2.28, n=43).


Chick growth

Growth rate was estimated for each chick in the sample from a polynomial function of the form:

y=A+Bx+Cx2+Dx3+Ex4

Where, A, B, C, D. and E represent constants defining the form of the curve, y represents the age of the chick and x represents the variable (mass in grams, culmen length or ulna length in millimeters). Detailed information about









chick growth is analyzed in Chapters 4 and 5. Here I just present descriptive information.


Sexinq the chicks

Reversed sexual size dimorphism is expressed by the time that chicks fledge: female chicks are larger than males. Sexing a chick was possible from culmen and ulna lengths of fledglings fitted to a discriminant function. Chicks were sexed using a discriminant function calculated for fledglings in this population in 1991 (Durand 1992). The discriminant function was validated using the culmen and ulna length of 18 chicks of known sex (11 females and 7 males as determined by laparotomy and disection, Durand 1992). The function was:

y=-40.51 99+0.12260(culmen length)+0.08955(ulna length); (p<00001) where if y>0 then female and if y

Behavioral analysis

A clear temporal pattern of the presence of male and female at the display site in every courting pair and the different duration of nest-building periods per nest precluded my averaging the data on a daily basis taking the laying of the egg as a reference point. Instead, the data were analyzed by dividing the nestbuilding period for each pair in the sample into three equal parts (close to Mating (when the female remained at the displaying site of a particular male), Middle part of the nest-building and the part close to Laying). For simplicity I called these thirds as: "early", "middle" and "late" nest-building period. For every nest in each third of the period, the time spent by the adults at the nest, the number of sticks carried by the male to the female, the time the adult spent together at the








nest and the number of copulations and copulation attempts, were averaged. Copulations and copulation attempts were sometimes pooled (see bellow).


Chick feedings

Chick feeding frequencies were calculated in periods of three days per week as recorded in the field (number of feedings per three consecutive days per week). Time at the nest by the adults was estimated for those individuals during incubation only. I used non-parametric tests (Mann-Whitney U, Wilcoxon test and Chi square and Fisher exact probability test) because of the small sample sizes, non-normal distributions, or non-homocedasticity precluded me from using parametric statistics (t-test, one- and two-way ANOVA and Parsons Correlation test).




Results




The Population View


Breeding season

The frigatebird breeding season at the Isla Isabel colony began before we arrived at the island in early November 1993. The total reproductive season including courtship, mating, incubation, brooding, chick growth and fledging (up to the flight of the chicks) lasted more than 9 months. Courtship started in early October 1993, the egg-laying period peaked on 10 November (estimated retrospectively from the age of the chicks) and most of the chicks fledged in late July 1994 (30 out of 36 chicks fledged in July). The following breeding season





19


started in early November 1994 and ended in late July 1995. This second season started earlier than November but was destroyed by a hurricane that passed through the island in late October 1994.

Breeding at the colony was not synchronous as indicated by the extended period of courtship. The courtship period, judged by the number of red inflated gular pouches counted at the breeding site, started in early October 1993 and finished in 7 April 1994, when the last inflated gular pouch was seen. The peak of the courtship period occurred in December (Figure 1.2). Probably another peak occurred early in the breeding season before our arrival at the study site. The abundance of adult males and females varied as the breeding season progressed. The number of males perched at a reproductive site outnumbered the number of adult females in November. This ratio decreased to close to one in December and continued to decrease up to June (Figure 1.3). In June almost all males had left the colony. At the perching site the sex ratio indicated a preponderance of females during the whole season but the number of males peaked in March and then declined again in June (Figure 1.4).


Matinq success

We observed 154 pairs in courtship. Only 51 pairs (33%) laid an egg for certain and 21 (14%) probably laid an egg based on the behavior of the adults at the nest and their extended courtship period, but the nest failed before we saw the egg. All other pairs (82 cases, 53%) left before laying an egg.


Eq survival

We observed 68 pairs with an egg (51 observed from mating and 17 added subsequently). Fifty four (79%) of the eggs were lost during the incubation period and in only 14 of these cases (21%) we saw the hatchling





20


before nest failure occurred. The causes of egg loss were unknown, but intraspecific interference is common (other males stealing nesting material).


Chick survival

Since most of the pairs we observed during nest building failed to lay an egg during courtship or lost their egg during the incubation period, we added nests with chicks to our sample as we found them. In our total sample of 78 chicks, 38 (49%) died or disappeared from the nest. In nine cases the corpses were found and in 29 cases the chick just disappeared. We do not know the causes of these deaths or disappearances but in 13 cases (43%), the chicks died or disappeared after a continuous period of weight loss. These 13 chicks were 27% below the average mass of the surviving chicks of the same age (SE=3.91). In the other 17 cases (57%), chicks were in good condition and some were even 21 % over the average mass of the surviving chicks of the same age (SE=3.52).


Adult dispersion

I do not have data concerning adult dispersion but my marked birds were commonly seen by fishermen at Islas Marias (60 km East of the island), on the mainland (72 Km) near San Blss in the state of Nayarit, and at Topolobampo, in the State of Sinaloa, M6xico (about 500 km to the North of the Island) where 12 marked birds were seen.





21


The Individual View


Pair formation

Courtship occurred during an extended period in the magnificent

frigatebird. The courtship period involved two components: the process of obtaining a mate (male displaying) and the process of copulation and nest construction (nest-building period). I concentrated my efforts on quantifying the behavior of the adults during the copulation and nest-construction period and made only qualitative observations during the mate-selection period. As described elsewhere (Diamond 1973), during the male-displaying period, males inflate their scarlet gular pouch while perched on a branch at the top of a tree (displaying site). Females fly over the colony and sometimes hover (remain static in the air for seconds beating their wings) over a displaying male and sometimes land on the branch of a particular male. The arrival of the female to the displaying site starts the nest-building period. Typically, during the first day of the arrival of the female at the perching site, the male continued displaying his inflated gular pouch to other females while the female remained at the displaying site in close physical contact with the male. During the second day, typically males deflate their gular pouch and both adults remained inactive at the displaying site. The displaying site invariably became the nest. From the third day and until egg laying, the male brought nesting material to the female while the female built the nest. It is during this nest-building period at the displaying site that the pair copulated. Once the pair is at the displaying site, the site is always guarded by at least one adult during the whole courtship, nest-building, incubation and brooding period. If the nest is left unattended even for seconds, other males immediately take over the site or the nesting material. Both males and females remained at the nest almost 70% of the time during the first part of





22


the nest-building and copulation period (early period). Then, during the middle and late third of the nest-building period, the male decreased his time at the nest and started to bring nesting material to the female. During the late third of the nest-building period (close to laying) males and females were observed to spend 45 and 60% of the total day-time at the nesting site. Consistent with this figure, males and females remained at the nest together about 40 percent of the time during the "early" period and then during the "middle" and "late" thirds of the nest-building period, the time at the nest together decreased dramatically.


Nest building and copulation behavior

A detailed analysis of the copulation frequency and nest building activities is presented in Chapter 2.

Nest construction activities peaked during the second third ("middle") of the courtship period (between 5 and 8 days before the egg laying). Males brought an average of 1.3 sticks per day during the nest building period (SE=0.22, n=22) and a total of 17.3 sticks during the whole period (SE=3.55, n=22; Chapter 2).

The average individual nest-building period in this colony lasted 13.2

days (SE=0.89, range=7 to 23, n=22) for the sample of nests where we recorded the beginning of the nest building and the egg-laying date. Copulations occurred only at the nest site during the nest-building period. Copulations occurred more frequently during the first and the second third of the nestbuilding period and decreased during the late third (Figure 1.8). Even though the clutch size is only one egg, these birds copulated on average16.2 times per clutch (SE=2.2, range=2 to 44 copulations, n=22). Copulations occurred only during the day, from very early in the morning to dusk. We did not noticed a








copulation occurring at night even when we spent much time marking animals and weighing chicks.

Intra- and extra-pair copulation frequency. Frigatebirds copulated with their mate 1.3 times per day on average (SE=0.2, range=0 to 10, n=22) and the copulation frequency peaked 14 days before egg laying and decreased dramatically two days before laying. Extra-pair copulations occurred in at least 8% (12/151) of the pairs observed. Extra-pair copulations occurred at the nest site and almost all occurred during the second part of the courtship period (Chapter 2). Extra-pair copulations occurred when females were visited by other males at the nest.


The role of adults during incubation and brooding

In frigatebirds the egg is always guarded by one adult. In a small sample of nests in which I recorded accurately both the laying and hatching dates of the egg (n=7), the incubation period lasted 56 days (mean=56.4 days, SE=1.1, range=53 to 61). In a more extensive sample of nests in which I knew the laying date but where the hatching date was not accurately recorded, the incubation time was shared almost equally by both male and female. Males were at the nest on average 51 % of the total incubation time (mean proportion= 0.51, SE=0.0008, n=38). Every adult remained at the nest incubating for periods of 3 days on average before being replaced by the partner (range=<1 to 9 days). Females remained at the nest slightly more time than males before being replaced by the partner but this difference was not significant (males: mean=2.99 days, SE=0.20, range=1 to 6, n=36; females: mean=3.4 days, SE=0.25, range=1 to 7, n=36; Wilcoxon test, T=24.5, p=0.85).

Chicks hatched naked and were unable to control their body temperature during the first days of life (Dunn 1975). During the first 10 days of brooding,





24


adults stayed at the nest and the chick was covered by the adult continuously as the egg had been, and parents shared the care of the chick. I considered this period as an extension of the incubation period because I could not always tell whether the chick was hatched.


Chick rearing

At 49 days old on average (SE=2.36, n=30, range from 28 to 88 days)

chicks remained alone at the nest, but one adult frequently perched near by. At 53 days of age (SE=2.49, n=39, range from 25 to 93 days), adults often left the chick unattended and only visited the nest to feed it. Males deserted chick feeding at variable times of chick age, ranging from 18 to 161 days (mean=77.1 days, SE=4.98, n=33). This figure includes the last time a male was seen at the nest, not necessarily feeding the chick. Seventy-four percent (31 out of 42) of males deserted during a short period of time during the year (March-April). After male desertion, females fed the chick alone up to fledging (the age of the first flight, 175.6 days for males and 185.0 days for females). In 12 cases chicks continued to be fed nine more months after chick fledging up to independence.

Chick feeding was extremely infrequent. They received food only 0.87 times per three-day period during a week on average (SE=0.095, n=28). Males and females contributed to chick feeding of hatchlings but males contributed less frequently than females when they were brooding (Mann-Whitney U=1412, p<0.0001, n=31). Males contributed a maximum of 40% of chick feedings on average at the beginning of our observations (40 days after hatching) but a constant decline occurred up to 161 days of chick age when the last male deserted the nest (Figure 1.5; see Chapter 3 and 4).





25


Chick growth, fledging and independence

Chicks grew slowly. The average trajectory of male and female growth

shows sexual differences at 40 days and until chick fledging (mass, culmen and ulna length; Figures 5.3 to 5.5 in Chapter 5). Near fledging, female chicks were 11.7% heavier, 9.8% larger in culmen length and 5.7% larger in ulna length on average. Sexual differences are analyzed in detail in Chapter 5.

Attaining chick independence was a long process in frigatebirds. After fledging, chicks returned to the nesting area to be fed by the female. We recorded 22 (56%) of the fledglings marked in July 1994 (n=39) still present near their nest-area in November 1994; 23 (59%) were recorded present in December 1994. Still, 13 (31%) were present in March and April 1995, respectively. We also recorded 13 (59 %) and 8 (34%) of the chicks being fed exclusively by their mothers in November and December, respectively, when our observations were more extensive.


Adult re-mating

Unsuccessful adults (adults that lost their chick or egg) rarely attracted another mate or constructed a new nest at the island in the same breeding season. In the next breeding season, 34 (55%) of the successful (adults that rear their chicks to fledging and were alive when we left the island on July 1994) marked adults (n=62) from the previous season were seen again at the breeding site (47% males and 53% females). In all cases marked males were seen the following breeding season at least with the red gular pouch, indicating reproductive condition. Successful females (n= 18) were seen feeding their fledglings during the next breeding season and none of these marked females was recorded to visit a displaying male. In six cases both adults of a successful pair in the previous breeding season were seen at the island near their previous








reproductive site. In each case, the female was feeding the chick and the male was in reproductive condition (red gular pouch).




Discussion




The Maqnificent Frigatebird at the Isla Isabel


Information on the breeding biology of the magnificent frigatebird obtained in this study is summarized in Table 1.1 at the level of the population and at the level of individual pairs. At the level of the population, the colony starts reproduction annually in September-October, immediately after the rainy season and chicks fledge in July-August. The colony is asynchronous and courtship lasts about six months (from early October to March). Male and female adults were abundant early in the season but the proportion of males decreased constantly until they were rare in late April. Nest failure and chick mortality were high; only 17% of the observed nests produced a fledged chick. At the level of individual pairs, copulation and nest building lasted 13 days; pairs copulated 16 times on average. Incubation lasted 56 days. Incubation and brooding was shared equally by male and female parents; chicks were left alone at the nest at 53 days of age on average. After this, parents returned to the nest only to feed the chick once in three days. The time that every adult remained at the nest before being replaced by the mate (attentive period) during incubation and brooding lasted 3 days. Once chicks were able to remain alone at the nest, males deserted. Males deserted when the chick was from 18 to 161 days old, in late March and early April. Chicks fledged and were able to fly at 180 days and





27


the sex ratio of fledglings was not different from 1:1. Females were seen feeding fledglings from the previous season and males were seen in reproductive condition the next breeding season. Successful males may be able to reproduce annually but successful females only can reproduce biennially.


The Effects of Feeding Ecology on the Breeding Biology of Frigatebirds


In spite of all the similarities, interesting differences exist among the five frigatebird species. All the species are tropical and subtropical but F. ariel and F. andrewsi are distributed locally whereas F. magnificens, F. minor, and F. aquila are broadly distributed (Nelson 1975). Most of the frigatebirds are pelagic foragers but F. magnificens and probably some populations of F. minor are shoreline foragers (Diamond 1973, Nelson 1975, Calixto 1993). There may be an association between these two types of foraging and frigatebird breeding ecology. Pelagic foragers (1) have narrow and specialized diets and, consequently (2) are more synchronous in their breeding; (3) they have longer attentive periods at the nest during incubation and chick rearing; (4) their chicks grow up more slowly; (5) males and females contribute more equally to incubation, chick rearing and chick feeding; (6) the first flight of the chick occurs earlier, but (7) probably the period of post-fledging dependence is longer than for shoreline foragers.

The main hypothesis here is that food availability (feeding conditions) could be responsible for the differences in natural history. As demonstrated in Everglades kites (Beissinger 1987), food availability improves the rearing conditions of the adults and in consequence sets the conditions for the desertion of one individual in the pair. Only one study with frigatebirds refers to the abundance of food and the breeding biology of the magnificent frigatebird. The





'-8


data are qualitative but show that chick rearing coincides with an increase in food availability (estimated in the number of tons of fish captured commercially; Carmona et al. 1995).

Males deserted their nests when the chick was between 18 and 161 days old. This range is between the age ranges reported in the literature for frigatebirds (Diamond 1973, Coello et al. 1977, Trivelpiece and Ferraris 1987, Durand 1992,). However, since males desert during a restricted two-month window of time, this variation is only a consequence of the dates of pairing at the beginning of the breeding season. An analysis of mate desertion and its consequences is presented in Chapter 4. Male desertion has important consequences. Female magnificent frigatebirds are able to rear the chick alone at a rate equal to or faster than growth rates attained by the other species of frigatebirds (Nelson 1975). Successful females are limited to biennial reproduction but successful males and all unsuccessful individuals are probably able to try reproduction the following year. Dependence by the magnificent frigatebird on a rich food supply as compared with that of other frigatebirds may be associated with the ability of females to feed the chick alone for long periods (up to 14 months). Other effects can occur after male desertion evolved. Rearing costs of male and female chicks can vary for the pair and for the deserted females. The consequent increased male-male competition may favor promiscuous activities and increased sexual selection.

A cascade of other changes can be expected. Since clutch size is

constant in these birds, male emancipation can be a quick response to changes in food abundance. Fregata magnificens is the only species of frigatebird breeding and possibly feeding in less erratic food sources (i.e., at Isla Isabel this bird feeds at shrimp boats) whereas the other four species of the genus breed and probably feed at more pelagic places. A broad diet reported in magnificent








frigatebirds (Calixto 1993), feeding areas that are closer to the coast, shorter attendance periods at the nest, higher chick growth rate, suggest the dependency of this species of frigatebirds on a more abundant and, perhaps more predictable food supply.

The long reproductive period of the frigatebirds is the consequence of a long period of courtship, nest-building, incubation, chick feeding and post fledging dependence. This bird is dependent usually on highly dispersed and fluctuating food resources. However, at this locality (Isla Isabel), it seems that the ability of birds to obtain food from shrimp boats could be responsible for the large size of this colony. The Isla Isabel colony is one of the largest colonies reported to date with the exception of the Santa Margarita island population (Moreno and Carmona 1988). Santa Margarita Island is located in a highly productive zone near the California current, in Baja California Mexico.

Chick growth also appears consistent with the dependence of these

frigatebirds on sparse, fluctuating and scarce food resources. Chicks grew very slowly compared with other seabirds of similar mass. However, compared with other frigatebirds, the magnificent frigatebird chicks grew faster (Nelson 1975, Diamond 1973). Probably again, this could be attributed to the dependence of these birds on more abundant and predictable food souces close to the island (shrimp boats; Calixto 1993).

When chicks become independent is not known and is still not known after this study. However, my observations on marked juveniles suggest that independence rarely occurs before nine months after fledging; i.e. at 15 months of chick age. This prolonged period of partial or total dependence could be related to the acquisition of difficult feeding techniques of these birds and the dependence of frigatebirds on unpredictable food sources, as speculated by several authors (Diamond 1973, Nelson 1975).





30


Even though the colony is not synchronous in their breeding (the

courtship period extended for almost 6 months), the colony is clearly annual. Every year after the high rainfall season (late May to August), the population starts a new reproductive cycle. In fact there is a strong effect of the season on the survival and growth of the chicks from parents that settled early and late (see Chapter 4). Not all individuals, however, are able to re-mate annually. Floating and unsuccessful individuals from the previous breeding season and successful males could attempt annual reproduction. However, successful females feed chicks for more than nine months after fledging and are constrained at least to biennial reproduction.

As seen at other colonies of the magnificent frigatebird, at Isla Isabel

males abandoned nests and left the island as the breeding season progressed (Figures 1.3 and 1.4). Males were as abundant as females during the beginning of the courtship period, but as the breeding season progressed their abundance decreased to a point such that in July it was difficult to see a male at the island. It is interesting that the most intense drop in the abundance of males occurred during April-May, suggesting that most of the males left the island during that period. This finding also coincides with the time that males of the successful nests deserted from the nest (see Chapter 4).

I do not have good data about adult dispersion. However, I received

reports from fisherman of several marked birds flying almost 500 Km to the N of the island, 60 Km to the SW, 72 Km to the NE and 120 Km to the SE. Some of these ranges overlap with known reproductive colonies of this bird. At Isla Isabel, birds tended to remain close to the site where they were marked and did not move elsewhere on the island if they failed in the current reproductive effort. In our weekly walks around the island looking for marked birds, we only rarely saw marked birds perched outside the breeding site.





31


As noted by Diamond (1975), copulation takes place without obvious

preliminaries and brief head waving frequently follows. The copulation pattern is unexpected based on available information about egg fertilization. According to the literature in chickens and other birds, the fertilization window is about 24 hours prior to egg laying (Birkhead and Moller 1992). Therefore, one would expect that only few copulations one day before egg laying should be sufficient to fertilize the one egg produced by the female. However, frigatebirds copulate about 13 times to fertilize that one egg and the peak of copulations occurs during the first two thirds of the courtship period, eight days prior to the egg laying, rather than close to egg laying. The possible significance of the copulation pattern is discussed in Chapter 2.

As in other species of frigatebirds, incubation in F. magnificens is long, 56 days. Both male and female shared the incubation and brooding duties almost equally. Although long attendance periods during incubation were even smaller in F. magnificens than the ranges reported for F. minor and F. ariel.

As described in other populations of the magnificent frigatebird, these birds are socially monogamous in one reproductive cycle. We never saw a mated individual incubating and brooding more than one nest in the same breeding season, and only seven males (out of 230 pairs) mated sequentially in the same breeding season after a failure. However, since males begin a new breeding cycle while their mate is still feeding the chick, the pair-bond is not maintained for more than one season. Over the long term, the system could be considered sequential monogamy (Gowaty 1985). In spite of this one-season monogamy, extra-pair copulations occur (See Chapter 2). Since the social bond appears to be monogamous while individuals are sometimes copulating with other mates, the system is only "apparently monogamous" (Gowaty 1985). The









consequences of these extra-pair copulations has not been explored. In this dissertation some hypotheses are discussed (Chapter 2).

Clear reversal of sexual size dimorphism is seen in male and female

fledglings. Females were between 6 and 11 % larger than males at the age of the first flying, However, in spite of this dimorphism, males and females developed at the same growth rate and reached the asymptotic size at the same age (Chapter 5). This suggests that males and females fed with similar frequencies must have processed the food differently and used the same energy in different ways to attain different sizes at the same time (see Chapter 5). Alternatively, my methods or sample size may have been insufficient to detect differences between males and females.

A female-biased sex ratio at fledging was found in one population of

frigatebirds in the Caribbean sea (Diamond 1972) and a similar bias was found in a population from the Galepagos islands (Coello et al. 1977). I did not find a female-biased sex ratio in my sample (Chapter 5) nor was a bias found in this populations three years ago (Durand 1992). Diamond speculated that excess numbers of fledged females was a strategy connected with different breeding rates of males and females in this species of frigatebirds (Diamond 1972). If males are reproducing more frequently than females, it could be advantageous for individuals to produce more females he argued. However, since the benefits of the extra-production of male and female offspring is clearly frequency dependent, this explanation is not likely to be an explanation for the propagation of wide sex-ratio bias. A broader discussion about sex ratios is presented in Chapter 5.









Causes of Chick Mortalitv


As described in other colonies, mortality rates are very high in these birds. Considering that only 40 nests were constructed out of 230 pairs that started courtship (including here those nests added to the sample with an egg or chick), only 17% of the breeding attempts produced a fledged chick. This is nearly the figure established in other populations and even other species of frigatebirds (Nelson 1975). I do not know the sources of chick death or nest failure in most cases, but cats introduced to the island at least 40 years ago, strong winds, intraspecific interference, and our own presence, were observed as causes of nest abandonment, death of chicks, nest disappearance and egg loss. The main cause of egg loss, however, was intra-specific interference. Other males stealing nesting material frequently resulted in eggs dropping to the ground. Our activities also provoked some egg loss and some unknown and unestimated nest desertion. Cats preyed upon frigatebird chicks immediately after hatching to almost fledging. We saw three instances in which a cat was in the tree branches immediately behind a nest containing a chick. In one other case, a mother cat was seen bringing a dead chick to her kittens. In other cases, one healthy marked fledgling (hand-reared) was clearly preyed upon by a cat. We only found the wings of this bird with fresh flesh remains. Small unattended chicks were more likely to fall from the nest. Fishermen at the island reported a high rate of chicks falling down from nests (up to five chicks falling down from nests in just one day). We have one clear observation of an adult male removing a small unattended chick from the nest and throwing it out of the nest. This behavior has been observed also in F. ariel (Dill 1916). We do not have a clear idea of how frequent this intra-specific interference occurs and its





'1


possible function. In the observed case, after chick removal the nest was abandoned and not used by another bird.

In summary, the breeding biology of the magnificent frigatebird is

markedly different from the other species of frigatebirds. Fregata minor appears to be an intermediate between the extremes. A clear association between the geographic distribution and feeding places, diet and probably food abundance seems to be associated with the adjustments in natural history. Food abundance and predictability may increase the feeding abilities of males and females in the magnificent frigatebird and produce a cascade of changes in breeding frequencies, rearing costs, breeding synchrony, chick growth and mating competition. Still more detailed studies should be conducted to test predictions from this speculation.






35


Table 1.1 Comparative breeding biology of the five species of frigatebirds including this study. Variable F minor F aquila F anel F magnificens F andrewsi

Dimorphism 1 18-1.28 depending 1.14 about 1.14 1.23 1.11


on the locality


February-April September-November


August-November


October- January, October-March


April-June


Egg weight (%of female's weight)

Incubation period (days)

Role of sexes feeding the chick


Attentive period at nest during incubation

Age when chick is left unattended

Growth rate Weight at week 7 (growth rate, g/day)


Feeding rate


85 g (5.2%)


55


shared role up to chick independence but females give more
feedings in some
colonies


9.5 to 11.5 days


31 days


980 g (Aldabra) (19.28);
390 g (Galapagos)
(7.14)

once every 3 days


75.8 g (6%)


44


shared role up to chick independence


unknown


about 35-40 days


680 g (12.8)


unknown


59 g (6.9%)


unknown


shared role up to chick independence


2 to 6 days about 35 days


390 g
(7.14)


once every 2.4 days


unknown


56
(SE=1.1)


shared role until 1-3 months, then female feeds the chick alone. But males desert in March-April


1 to 9 days
(mean=3.2 days)


49 days (SE=2.36)


750 g
(16.4); 721 g
(15.07 at Isla Isabel)

once every 3 days


82 g (5.3%)


54 (estimated)


shared role up to chick independence


2 to 3 days about 45 days


540 g (12.8)


once every 2 days


Fledging period Post-fledging dependence Fledgling sex ratio



Breeding success (# initial nests/# nests with fledged chicks)

Breeding habitat


Breeding periodicity of successful individuals


24 weeks


about 9 or more
months

1 male to 1 female


19%


pelagic and some coastal colonies

presumed biennial;
under special circumstances 18
months


about 20-24 weeks


not-recorded


unknown


about 15-20%


pelagic


annual; not well established


20 weeks


at least 4 months; probably longer


unknown


about 15-20%


pelagic


unknown; suspected
biennial


26 weeks


more than 9 months


1 male to 1.8, 1 5 and 1 females in different
colonies


about 17%


coastal


female probably biennial; male annual


24 weeks


up to 9 to 10 months


unknown about 30%


pelagic biennial


Female/male weight ratio Laying period


Information based on Nelson's review (1975) but complemented with information from Coello et al. (1977), Moreno and Carmona (1988), Reville (1988), Trivelpiece and Ferraris (1988), Schreiber and Schreiber (1989), Durand (1992) and Howell (1995) and this study.





36


POPULATION SCALE


COURTSHIP EGG LAYING INCUBATION CHICK REARING FLEDGING





SEPT OCT NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEPT
0 30 60 90 120 150 180 210 240 270 300 330 350
TIME
COURTSHIP (days)
NEST-BUILDING
AND COPULATION INCUBATION
BROODING AND CHICK REARING POST-FLEDGING FEEDING
INDIVIDUAL SCALE







Figure 1.1 Schematic representation of the typical frigatebird breeding from the point of view of the population and the individual. Curves represent the frequency of nests in that activity. Lines represent the duration of the activity for a hypothetical pair.






37


120 100 80 60


40 20


0


1 10


31


31


} 21


f 12


12 17 15


I I I I I - I =-


E
0
0


I.
0 .0
E
0
C-,
0
0


Cu
C
Cu


1...
0.


Cu
.0
0 U-


Cu


0
C


Figure 1.2 Number of male magnificent frigatebirds displaying (mean t SE) at the breeding colony. Numbers close to the squares are sample sizes (number of
observations per month). July-October no males are present.


-1
_0


0) Co

(L
C
_0




E
-




2

E
4
0






38


1 . 1.


ot jo . , -IbarLL(SHARE'S) PO BoxA 1 7001 245 LibrarY \est..
Gainesvij~e FL 3,26V1700
6


1.4

1.2

1 0.8 0.6 0.4 0.2

0

-0.2 -


15


6


f5


4


f 7


6


i i I i i a I


E
0
Z


0 .0
E
0
U
0
0


Cu Cu


Cu
I.
.0
0 LL


U Cu


0.


Figure 1.3 Adult operational sex ratio per day (male/female) at the reproductive site (mean SE) as a function of the time of the year. Numbers close to the squares are sample sizes (number of observations per month).


A


0


x

_0
-,)


a,

E CU
2!






39


0.3 -


0.25


0.2 0.15 0.1 0.05


0


12


78


6


f7


f6


3


I I I I I I I


E
0
0


E
w
U


Cu Cu


Cu
I
.0
0 LL


U
Cu


CL


0
0


Cu


Figure 1.4 Adult sex ratio per day (male/female) at a roosting site (mean SE) as a function of the time of the year. Numbers close to the squares are sample
sizes (number of observations per month).


0



a) U,

E


'





40


Tv


T








(4


--- Females
-a-- Males


I I


I





- U- 4


a) U,
0


50


100


150


200


250


Chick age (days)






Figure 1.5 Feeding frequency (mean SE) of male and female adults as a function of the chick age. Sample size was 38 nests. For males sample size
dropped as they deserted. Observations started at 40 days on average.


I - - - - - - - - - ~- LL~ L~


0


4-


I













CHAPTER 2
A TEST OF THREE HYPOTHESES TO EXPLAIN THE FUNCTION OF THE INTRA-PAIR COPULATORY PATTERN IN THE MAGNIFICENT FRIGATEBIRD




Introduction


Multiple copulations are common in many species of birds. In some species, females copulate with several males (extra-pair copulations), but in others, females copulate repeatedly with the same partner (intra-pair copulations). Extra-pair copulations have clear advantages for some males and some advantages have been suggested for females (Westneat et al. 1990, Birkhead and Moller 1992). However, evidence of advantages to females are more theoretical than empirical (Lifjeld et al. 1994). Multiple intra-pair copulations, on the other hand, are puzzling. Since only one ejaculate contains a huge number of sperm cells, enough to fertilize all the mature follicles produced by the female, it is not clear why individuals copulate frequently with the same partner. Furthermore, considering that multiple intra-pair copulations could involve costs (increased predation risk, time invested that could be used for extra-pair copulations, risk of sexually transmitted diseases, etc.) affecting Darwinian fitness without the benefits of mating with several partners, it is difficult to explain frequent intra-pair copulations.

Two aspects of the multiple intra-pair copulations are interesting:

frequency and peak in relation to the laying date. I refer to both of them here as the "copulatory pattern". Several hypotheses have been suggested to explain


41








diversity in copulatory patterns (Birkhead 1989, 1991, Petri 1992. Hunter et al. 1993, Birkhead and Moller 1993). Some of them have been tested using the comparative approach (Birkhead et al. 1987), but this problem has been rarely scrutinized experimentally (Petri 1992, Hunter et al. 1993). In this study I first present alternative hypotheses and then evaluate them based on a study of the magnificent frigatebird (Fregata magnificens).


Hypotheses to Explain Multiple, Intra-Pair Copulations


The Fertilization Hypothesis

The Fertilization Hypothesis states that multiple, intra-pair copulations are the way for a female to insure that all follicles are inseminated (Hunter et al. 1993). Since birds do not normally have an intromittant organ (with some interesting exceptions in 2% of species; Birkhead and Moller 1992), copulation would seem to be a very difficult task; copulation occurs in a short period of time and in a very unstable posture. It could be important to copulate several times in order to reduce the incidence or risk of egg infertility. In addition, because of sperm depletion in males (Birkhead 1989, 1991), not all successful copulations result in sperm transfer. Under this hypothesis, the risk of insemination failure is reduced by frequent copulation (Birkhead 1991).


Conflict of interest

Copulations are necessary for reproduction in sexual species but, given its consequences on fitness, copulations may be manipulated by one sex. The Fertilization Hypothesis suggests no conflict between males and females, i.e. both agree on the frequency of intra-pair copulations. However, since different selective pressures clearly act on males and females, a large group of








hypotheses can be derived based on different benefits to males and females. I include here two variants: the Stimulation-Assessment Hypothesis (Hunter et al. 1993) and the Sperm Competition Hypothesis (Birkhead et al. 1987). Conflicts of interest can result in an evolutionary arms race (Dawkins and Krebs 1979, Lifjeld 1993). Mate guarding, female sperm expulsion and aggression during copulation, forced copulations, female solicitation, may all be the evolutionary outcome of sexual conflict. Ecological conditions, asymmetries in payoffs, power or information, alternative strategies or differences in costs to individuals could determine who is "winning" the conflict.


The Stimulation-Assessment Hypothesis

The Stimulation-Assessment Hypothesis (a mechanistic hypothesis),

suggests that multiple intra-pair copulation stimulates females to ovulate (Hunter et al. 1993). This mechanism is well known in mammals (e.g. mice: Estep 1973, 1975, Gray 1974). In birds the Stimulation-Assessment Hypothesis has been suggested as a mechanism for maintaining the pair-bond. This is an explanation for copulations occurring without sperm transfer or outside of the fertile period of the female. Female stimulation and pair bond manteniment are mecanistic explanatins. A functional interpretation of this hypothesis has not been proposed for birds, but some adaptive advantages for females could be attributed to this mechanism (e.g. female ovulation threshold correlated with male quality; Moore and Moore 1988). Although stimulation during the courtship period is only known in doves and few other species of birds (Birkhead et al.1987, Birkhead and Moller 1992), it is common in mammals, so this hypothesis is actually a possible alternative explanation for multiple, intra-pair copulation.


4 -





44


From the point of view of the female, multiple copulations can allow her to evaluate the quality of the male or his condition if a female is stimulated to produce an egg only after a high rate of intra-pair copulation (suggested in Westneat et al. 1990). This hypothesis assumes that the copulation rate is correlated with male quality and/or male condition. The prediction here is simply that copulation rate is correlated with egg production and male quality: if the rate of copulation is poor, there should be a high incidence of nest failure before egg laying.


The Sperm Competition Hypothesis

This hypothesis is derived from an argument similar to those used to

explain mate guarding: under some ecological conditions (food sources far from the nesting place and where the nest site must be guarded by the mate) that constrain males to stay with the mate, males will act to protect their paternity. Predictions from this hypothesis have been confirmed in tree swallows (Venier and Robertson 1991), northern fulmar (Hunter et al. 1992) and northern harriers (Simmons 1990), but the ecological conditions are particularly appropriate for marine birds (Birkhead et al. 1987). The Sperm Competition Hypothesis states that repeated copulation with the same partner could have sources of benefit for the male and female. For males the possible benefits could be to increase their paternity (Paternity Assurance Hypothesis, Birkhead et al. 1987) (1) by devaluing the sperm of other males (dilution effect), or (2) by being the last individual to copulate with a female under the last male precedence mechanism (see below) or (3) by reducing the time available for females to look for extrapair copulations, i.e. a type of mate guarding by the male through copulations. Benefits for males are obvious but females can benefit from frequent intra-pair copulations (1) by increasing male paternity confidence and consequently (a) by









securing immediate material benefits (food, nest material) or (b) future benefits (parental care, territory, protection); (2) by guarding the male (by depleting the sperm of males, and the time and motivation for extra-pair copulations) or to avoid mate loss (Petri 1992, Hunter et al. 1993).


Hypotheses to explain the peak of copulations

Several hypotheses have been formulated to explain why birds stop

copulating when the female is still fertile (Birkhead and Moller 1993). However, only three of these apply to a single egg species like the magnificent frigatebird:

(1) males are unavailable to copulate because they are engaged in extra-pair copulations (this is an alternative of the female mate-guarding hypothesis of the previous section); (2) eggs are no longer available to fertilize as laying approaches; (3) copulation may cause damage to the unlaid egg. In these hypotheses it is assumed that the fertilization period concludes about 24 hours before egg laying. This assumption is problematic in a species laying only one egg like frigatebirds since the fertile period is not easy to estimate in the absence of a second egg . Here I use hormon analysis in an attempt to estimate the fertile period of female frigatebirds.


Determining the female's fertile period

For some hypotheses copulation is expected to correspond with the fertile period of the female (the period when the mature follicle is ovulated and is susceptible to being fertilized). However, in a number of species, pairs copulate a long time before the beginning of the egg-laying period, indicating that most of these copulations occurred outside the fertile period of the female (Birkhead and Moller 1992). In addition, clear information about fertilization time and fertile period is largely unknown in wild birds (Birkhead and Moller 1992). In most





46


studies, the fertile period of the female has been assumed or it has been estimated only from the laying date (Birkhead et al. 1987, Birkhead and Moller 1992). Establishing the real fertile period of the female is important for evaluating predictions (Hunter et al. 1993).

The physiology of fertilization in birds indicates that the release of the mature follicle by the female occurs approximately 24 hours before laying and fertilization occurs during the first hour after the egg is released (Birkhead and Moller 1992). Depending on the clutch size and the laying interval, the fertile period could extend from 24 hours to three days before the last egg is laid (Birkhead and Moller 1992). Particularly for seabirds that lay only one egg, intervals between ovulation and fertilization are unknown.

The fertile period of females could be extended by sperm storage

structures in the female's reproductive tract (Birkhead and Moller 1992). These structures are small tubules located between the uterus and the vagina (Birkhead and Moller 1992). Sperm storage structures have been found in every species that has been analyzed to date, and it is possible that sperm storage structures occur in all birds (Birkhead 1994, Birkhead and Moller 1992). Sperm viability is extended up to eight days in ring doves and 42 days in turkeys before egg laying due to these sperm-storage structures (Birkhead and Moller 1992). The sperm-storage structures are thought to have evolved as a consequence of the interaction between male-male competition and sperm selection by females inside their reproductive tracts (Westneat et al. 1993). In any case several studies indicate that the existence of these storage structures results in more complex effects of copulations and fertilizations (Birkhead 1989, 1991, Westneat 1996). An experimental study in mallards (Anas platyrhynchos), for example, demonstrated that there was a preponderance of the last insemination siring the progeny (Cheng et al. 1983). This evidence suggests that the most probable









mechanism of sperm release from the storage structures is inversely related to the deposition order (last sperm precedence). Sperm-storage structures extend the fertile period of the female and introduce variable conditions that will affect the evolution of different copulatory patterns depending on how these structures work (Westneat 1996).


Predictions From the Hypotheses Applied to the Maqnificent Fripatebird.


I describe in this Chapter the copulatory behavior of the magnificent

frigatebird (Fregata magnificens). By disrupting copulations, I experimentally tested the predictions of the Fertilization, Stimulation and some forms of the Sperm Competition Hypotheses for this species.

The Fertilization Hypothesis states that high intra-pair frequency of

copulation insures egg fertilization. The main prediction from this hypothesis is that (1) experimentally disrupted pairs with a low copulatory rate will have a higher incidence of egg infertility than controls with high copulatory rates and (2) copulations will take place only during the fertile period of the female. The Stimulation-Assessment Hypothesis in the form used here states that only high rates of intra-pair copulations will stimulate the female to produce a mature follicle. Predictions from this hypothesis are that: (3) copulations occur before and during the fertile period of the female, and (4) experimentally disrupted individuals with the lowest intra-pair copulatory frequency will have a low incidence of egg laying (high incidence of laying failure). This hypothesis assumes that cloacal contact is the stimulus that induces ovulation although this is not known for certain. The Sperm Competition Hypotheses indicate that in a population with strong mate competition, where individuals perform long feeding travels and where extra-pair copulations occur, males will increase their





48


probability of fathering offspring by copulating repeatedly with the same mate, thus reducing the possibility of being parasitized by other males. Two forms of this paternity protection are (a) to dilute the sperm of other males or (b) to copulate frequently to reduce the time available for the mate to engage in extrapair activities (mate guarding). Since I do not have information on paternity, I tested here only the second possibility. I predict that (5) if extra-pair copulations occur, their incidence will be higher in experimentally disrupted pairs (copulation disrupted) than in control nests (disrruption out of copulation).

Females may benefit from repeated intra-pair copulation. If females are to benefit from short-term (immediate) material benefits in the form of nesting material, for example, I expect that (6) in experimental nests with low copulatory rates, males will deliver lower rates of nesting material to females if females are guarding the males by copulating frequently then (7) the incidence of nest failures will be greater in experimental nests than in control nests.

In frigatebirds copulations peak 6 days before egg laying (see

description). I suggest here that the decline in the frequency of copulations prior to egg laying in frigatebirds is due to the egg already being fertilized some period of time before laying, i.e. that the female is no longer fertile. This hypothesis assumes some cost of continuing to copulate for males and females (i.e. damage to the fertilized egg) and no additional benefit. The prediction from this hypothesis is that (8) when copulation drops, the egg is inside the uterus of the female.









Methods


The Description of the Copulatory Pattern

The descriptive part of the study was conducted from 15 November, 1993 to 10 March 1994. We (my assistants and I) marked every accessible nest or display site and the adults mating there with plastic numbered tags as soon as I recorded a pair in courtship. A display site was a branch at the top of a tree where a male perched while showing his inflated red gular pouch. We captured a displaying male (i.e. a male with the red gular pouch inflated or deflated) or a pair of adults (male with the red gular pouch and female) standing at the displaying site. Birds were captured by hand at night when they were at the nest and marked with 3-digit numbered wing tags. I marked nests and birds at night because frigatebirds are very sensitive to day-time disturbance. During the day when a frigatebird is disturbed at her/his nest, immediately other individuals, especially males, arrive at the site and try to steal the nest or nesting material.

We observed and recorded the behavior of adults and chicks at the nest. Behavioral observations were conducted from 20 November 1993 to 10 March 1994. Every observation site was covered by two observers alternating observation sessions every two hours from 0800 to 1800. The observation site was located at the top of a building 30 to 150 m apart from focal pairs. We observed up to 36 nests simultaneously. This large number of nests was possible because we recorded a few specific behavioral categories and because behavioral categories were conspicuous (see below). In addition, every behavioral category was easy to record since frigatebirds are large birds (adult females are almost 2 m wingspan) and behavioral patterns occurred infrequently.





10


Behavioral categories

For every displaying site we recorded (1) the presence of the male and female at the beginning of every recording session (2) the time of arrival or departure of each adult to and from the nest; (3) every copulation or copulation attempt. "Copulation" is defined as occurring when the male mounts the female's back, wings extended and he orients in the same direction as the female's head. The female extends her neck straight forward and the male touches her neck with his bill and grasps the female's neck feathers. In this position the male moves backward over the female's back, moves his tail feathers and pelvic zone laterally and pushes the tail feathers of the female to one side. The female lifts her tail feathers and the male moves his pelvis down until his cloaca reaches the cloaca of the female. Cloacal contact lasts only 2 to

4 sec with two or three spasmodic movements of the male. We did not record cloacal contact because the bird's relative position on the nest and the vegetation around precluded observing this event clearly. "Copulation attempts" were scored when the male's tail feathers were not seen to drop down or when the female did not lift her tail feathers precluding cloacal apposition. (4) In addition we recorded the frequency of visits by the male to the nest carrying nesting material.


Experimental Design


Manipulations were performed from 28 November to 27 December 1994. Chick hatching and chick presence were recorded from 28 March to 10 April 1995. We observed the behavior of the adults at every nest in the sample daily from 0800 to 1800 h from a distance of 5 to 20 m. Adults were not individually marked to avoid disturbance during courtship which often caused nest-site









abandonment. We marked some individuals by spraying paint from a distance of at least 1 m from the nest. The egg laying date was checked by the presence of the egg at the nest during the observation sessions and during visits to the nest by lifting up the incubating adult. We used the same behavioral categories as described above.

We interrupted most of copulations experimentally in 22 nests.

Copulations were interrupted by shooting water at pairs initiating copulation. Using a water gun, I directed water shots to the male when he was on the back of the female, immediately before copulation took place. When the water was shot, males flew away from the nest while females remained at the nest. This reaction was very important because when both adults flew away from the nest some other adult, usually another male, took over the nest. Controls consisted of 8 nests where males were shot when they were at the nest with the female but not in any copulatory interaction. As in the experimental treatment, control males flew as a response to the water shot and females stayed at the nest. For the analysis, I considered interrupted copulations of experimental nests the same as a copulations in conrtrols.


Female's fertile period

I tried to estimate the fertile period of the female based on the

concentrations of steroid hormones in the blood of 15 females. A longitudinal blood sample (sequential samples from the same individuals) was very difficult to obtain without unacceptably high levels of disturbance to females. As an alternative, I sampled blood from different females during the copulation period and I recorded their laying dates. The fertile period was estimated from concentrations of estradiol and testosterone hormones in 30 blood samples obtained from a group of females at known moments before egg laying (females









were outside the experimental sub-colony). Estradiol is a hormone commonly associated with ovulation. It usually peaks immediately before the release of the mature follicle (Bluhm 1988). Circulating concentrations of hormones were evaluated using the radioimmunoassay protocol (RIA, Guillette et al. 1996, Guillette et al. submitted). This technique uses radiolabeling to quantify the amount of unknown antigen and is based on competition between known and unknown amounts of antigen for antibodies specific for the hormone assayed.

For testosterone determination, frigatebird plasma (50 [l; all samples

were performed in duplicate) was extracted twice with ethyl ether to remove the lipophilic steroids. After drying the sample, ether extracts where filtered with low humidity air and the samples were resuspended with 100 pl borate buffer (0.5 M, pH 8.0). Androgen antibody (100 pl; final dilution 1:36,000), BSA/borate buffer (100 pl; 0.5 M borate buffer, 7.5% BSA), and radiolabeled testosterone (100 P1 of 9000 cpm; TRK 402; 102 Ci/mmol; Amersham Life Science Inc., Arlington Heights, IL) were added and the tubes were vortexed and incubated overnight at 40 C. Bound-free separation was accomplished by adding 500 pl of 5% charcoal/0.5% dextran and centrifuging the tubes for 30 min at 2,000 g. The supernatant was decanted, diluted with a scintillation cocktail and counted on a Beckman LS 5801 scintillation counter. Concentrations were estimated by commercially available software (Beckman Instruments).

For estradiol determination, 50 pl of plasma was extracted twice with ethyl ether. Estradiol antisera (E26-47; Endocrine Sciences, Calabasas Hills, CA) was used at a final concentration of 1:95,000. Cross-reactivities of this antisera to other ligands are as follows: estrone, 1.3%; estriol, 0.6%; 16-keto-estriol,

0.2%' all other ligands < 0.2%. Estradiol label (TRK.587; Amersham International, Arlington Heights, IL) was used at 10,000 cpm per tube. To reduce non-specific binding, bovine serum albumen was added at a final









concentration of 1.5%. Antisera, label, and BSA were diluted in assay buffer (0.5 M borate buffer, pH 8.0 with 10 N NaOH).

To determine the presence of the egg inside the female's reproductive tract (uterus) prior to egg laying, I felt for the egg by introducing a gloved finger into the female's cloaca.




Data Analysis


Behavioral analysis.

A clear temporal pattern of the presence of the male and female at the display site in every copulating pair and the different duration of nest-building periods per nest precluded my averaging the data on a daily basis or taking the laying of the egg as a reference point. Instead, the data were analyzed by dividing the nest-building period (during nest construction when copulations occurred; see Chapter 1) into three equal parts for each pair in the sample (close to Mating, Middle part of the nest-building period and close to Laying). For simplicity I called these: "initial", "middle" and "late". For every nest in each third of the nest-building period, the time spent by the adults at the nest, the number of sticks carried by the male to the female, the time the adults spent together at the nest and the number of copulations and copulation attempts were averaged. I averaged the occurrence of the behavioral categories per nest and then I averaged the means. When copulations and copulation attempts were pooled it is mentioned in the text.





54


Statistical analysis.

I used non-parametric tests (Mann-Whitney U, Spearmann Rank

Correlation and Fisher's Exact Probability Test) since samples were small and not normally distributed. I tested specific predictions derived from the hypotheses by using one-tailed statistical tests at a 95% confidence limit.




Results




The Copulatory Pattern in the Magnificent Frigatebird: The Descriptive Approach

Typically, during the first day of the arrival of the female at the displaying site, the male continued displaying his inflated gular pouch to other females while the female remained at the displaying site in close physical contact with the male. During the second day together, typically males deflate their gular pouch and both adults remained inactive at the displaying site. The displaying site invariably became the nest site. From the third day and until egg laying, the male brought nesting material to the female while the female built the nest. It is during this nest building period at the displaying site that the pair copulated. Once the pair is at the displaying site, the site is always guarded by at least one adult during the whole courtship, nest-building, incubation and brooding period. If the nest is left unattended even for seconds, other males immediately take over the site or the nesting material. I observed this dozens of times. Both males and females remained at the nest almost 70% of the time during the first part of the nest-building and copulation period (initial). Then, during the middle and late third (laying) of the nest-building period, the male decreased his time at the nest and started to bring nesting material to the female (Figure 2.1). During









the last third of the nest-building period (close to laying) males and females were observed to spend 45 and 60% of the total day-time at the nesting site. Consistent with this figure, males and females remained at the nest together about 40 percent of the time during the "initial" period and then during the middle" and "late" periods, the time at the nest together decreased dramatically (Figure 2.2).


Nest building and copulation behavior.

We observed 22 nests from the beginning of the nest building and copulation period to egg laying in 1993-1994 breeding season. Nest construction activities peaked during the second third (middle third) of the whole nest-building period (between 5 and 8 days before the egg laying; Figure 2.3). Males brought an average of 1.3 sticks per day during the copulation and courtship period (SE=0.22, n=22) and a total of 17.3 sticks during the whole period (SE=3.55, n=22). There was a weak but significant association between the number of sticks brought by the male and the number of copulations (Spearmann Rank correlation r=0.32, p=0.009, n=66). I used here an extensive sample of nests where the number of copulations and the rate of bringing nest material by the male was recorded, but where no egg was necesarily laid.

Intra-pair copulation frequency. During the nest-building period

copulations occurred only during the day, from very early in the morning to dusk. We rarely noticed a copulation at night even when we spent much time marking animals and weighing chicks at night. The average individual nest-building period in this colony lasted 13.2 days (SE=0.89, range=7 to 23, n=22) for the sample of nests where we recorded the beginning of the nest building and the egg-laying date. Copulations occurred only at the nest site during the nestbuilding period. Copulations occurred more frequently during the first and the





56


second third of the nest-building period and decreased during the last third (Figure 2.4). Even though the clutch size is only one egg, these birds copulated on average16.2 times per clutch (SE=2.2, range=2 to 44 copulations, n=22). Frigatebirds copulated with their mate 1.3 times per day on average (SE=0.2, range=0 to 10, n=22) and the copulation frequency peaked 6 days before egg laying and decreased dramatically two days before laying (Figure 2.4). Intra-pair copulation attempts occurred on average 3.4 times per clutch (SE=0.79, range=O to 13 attempts per nest, n=22).

Extra-pair copulation frequency. Extra-pair copulations occurred in at

least 8% (12/151) of the pairs observed. In a restricted sample where we knew the laying date (n=26 nests), the proportion of nests where at least one extrapair copulation occurred was 11% (3 extra-pair copulations in 26 pairs). Extrapair copulations occurred at the nest site and almost all occurred during the second part of the courtship period. Extra-pair copulations occurred 6, 14 and 18 days before egg laying and in no case was the extra-pair copulation the last copulation before laying. Extra-pair copulation attempts occurred at similar frequency to the extra-pair copulation rate (4 in 26 pairs).


Experimental Results


Control and experimental nests

Shots from water guns were a good technique to discourage copulation in experimental nests. Not all copulations were interrupted in experimental nests. We interrupted 88% (388) of all (441) copulations recorded in 22 experimental nests. Copulations in control nests were 9 times more frequent than in experimental nests (Figure 2.5). During the nest-building period males stayed at nests with females only for short periods of time if they were not copulating. As








a result, control nests were necessarily shot with water at a lower frequency than experimental nests (Figure 2.5).

Water shots did not influence the nest-building behavior and copulatory

period of experimental nests, compared with controls. The frequency and rate of sticks brought by the male to the female for nest construction in those nests where the egg was laid (13 experimental and 6 control), did not vary between experimental and control nests (experimental frequency=71.85 sticks, SE=16.16, n=13: controls: frequency=46.33 sticks, SE=8.46, n=6, Mann-Whitney U=33.5, p=0.64 two tailed test experimental rate=5.63 sticks per day, SE=1.17, n=13; control rate=5.30 sticks per day, SE=1.7, n=6, Mann -Whitney U=36.00, p=0.83, two-tailed test).


Fertilization Hypothesis

Although we interrupted 88% of copulations in experimental nests, there was a higher proportion of nests with a live chick in March in experimental (8/13) than in control (1/6) nests (Fisher Exact Test, p=0.14, two-tailed test; Table 2.1). This result contradicts the prediction of the Fertilization Hypothesis.


Stimulation-Assessment Hypothesis

The proportion of females that laid an egg at experimental nests (59%) was not different from the proportion in control nests (75%; Fisher Exact Test, p=0.34). In addition, the copulation rate (copulations in controls or interrupted copulation in experimental nests per day per nest) was not higher in experimental than control nests (Experimental: mean=1.74, SE=0.17, n=13; Control: mean=2.25, SE=0.35, n=6; Mann-Whitney U=29.5, p=0.21, n=13, 6). Also, egg laying was not more delayed in experimental (mean=12.5 days, SE=0.7, n=13) than in control nests (mean=10.7 days, SE=1.9, n=6; Mann-


5'









Whitney U= 27, p=0. 17). These results are inconsistent with the predictions from the Stimulation-Assessment Hypothesis,

The Stimulation-Assessment Hypothesis implies that high copulation rates (copulations per day) stimulate egg production in females. There was a significant association between the proportion of nests that produced an egg and high copulation rate in experimental nests (Fisher Exact Test, p=0.04, Table

2.2), but no such association was found in controls (Fisher Exact Test, p=1.0).

I could not test if copulations occurred outside the fertile period of the female as predicted from this hypothesis since no peak of estradiol (indicating the releasing of the mature follicle) occurred during the copulatory period in which samples were taken. A more dramatic effect occurred in testosterone where concentrations declined from 1000 to 250 pg/ml on the day of egg laying (Figure 2.6). However, most of the copulations occurred during the first part of the nest-building period. Copulation frequency decreased with the testosterone concentration, but the correlation was not significant (Spearman Rank Correlation r=0.71, p=0.14, n=6, two-tailed test). Estradiol concentrations did not correlate with copulation frequency (Spearman Rank Correlation r=-0.09, p=0.92, n=6, two-tailed test). However, testosterone and estradiol correlated with each other (Spearmann Rank Correlation r=0.69, p=0.016, n=1 1).

The number and rate at which sticks were brought by the male to the

female for nest construction did not vary between experimental and control nests (experimentals: frequency=71.8 sticks, SE=16.2, n=13: controls: frequency=46.3 sticks, SE=8.5, n=6, Mann-Whitney U=33.5, p=0.32, experimentals rate=5.6 sticks per day, SE=1.17, n=1 3; controls: rate=5.3 sticks per day, SE=1.7, n=6, Mann -Whitney U=36.00, p=0.41). There was no association between the rate of sticks brought to the nest and the copulation rate in experimental (Spearmann rank correlation r=0.16, p=0.60, n=13; two tailed-test) or control nests









(Spearmann rank correlation r=0.60, p=0.42, n=6; two-tailed test). Also, the incidence of nest failures before egg laying, though larger in experimentals (9/22) did not differ statistically from controls (2/8) (Fisher Exact test=0.29). Taken together, the results contradict the predictions of the Female-StimulationAssessment Hypothesis.


Sperm Competition Hypothesis

At least one extra-pair copulation occurred in 21% nests. This sample included all the observed nests (22 experimental and 8 controls;n=30). Inconsistent with the predictions of this hypothesis, however, the incidence of extra-pair copulations in experimental nests (3/22) did not differ from control nests (4/8) (Fisher Exact test=0.06).


Peak of Copulations Hypothesis

In order to explain the peak of copulations 14 days before egg laying, I

examined the female for the presence of the egg inside the uterus in a sample of individuals obtained outside the experimental sub-colony. In 13 instances I had both the egg-laying date and whether the egg was present inside the female's reproductive tract. On average the egg was present in the uterus 1.85 days before laying (SE=0.32). In four instances in which I checked the same female twice I did not find an egg both times. The average time before egg laying where I did not detect an egg (but an egg was eventually produced) was 5.5 days (SE=1.26).





60


Discussion




The copulatory pattern observed in the magnificent frigatebird can be

summarized as follows: females invariably laid a single egg per clutch but pairs copulated 16.2 times during an average period of 13 days before the female laid the egg. Pairs initiated copulations up to 22 days before laying and copulation peaks 6 days before laying and then declined to become rare two days (1.85) before laying. Sticks brought to the female by the male for nest construction showed a weak but significant positive correlation with the copulation frequency.

The copulation pattern of frigatebirds (frequency and peak) was similar to other seabirds and to other species of birds laying only a single egg. Species laying only one-egg clutches have high copulation frequencies; most of the reported species copulated 5 to 100 times per clutch (Birkhead et al 1987). Only a few descriptions of the copulation pattern in seabirds are available but in general, copulations occurred longer before egg laying than in land birds, suggesting that seabirds store sperm for longer periods of time (Birkhead et al. 1987, Simmons 1990, Venier and Robertson 1991, Hunter at al. 1992). Time periods from the last recorded copulation and the egg-laying date range from 8 days in guillemots to 60 days in petrels (see ref. in Birkhead et al. 1987).

The copulation pattern in seabirds is unexpected based on available

information about egg fertilization. According to the literature, in chickens and other birds, the fertilization window is about 24 hours prior to egg laying (Birkhead and Moller 1992). Therefore, one would expect that only a few copulations one day before egg laying should be sufficient to fertilize the one egg produced by the female. However, frigatebirds copulate about 16 times to fertilize the egg and the peak of copulations occurred during the first two thirds





61


of the courtship period, 6 days prior to the egg laying, rather than close to egg laying (Figure 2.7).


Fertilization and Stimulation Hypotheses

Evidence from the experiment does not support neither the Fertilization nor the Stimulation-Assessment Hypotheses. Contrary to the Fertilization Hypothesis, even though I did not record the fertility of eggs and I did not check for the presence of the egg up to hatching, chicks were present one month later in 43% (8 out of 13) of experimental nests where an egg was laid as compared with 5% of the control nests (1 out of 6). The higher proportion of experimental nests with a chick suggests that hatching failure may have been even higher in controls than experimental nests. This result implies that only a few copulations are necessary to fertilize the egg.

The Stimulation-Assessment Hypothesis was not supported because

experimental females were able to produce an egg as frequently as controls and during a similar period of time (copulation and nest construction period). There was, however, an association between high copulation rate (rate of copulation attempts) and the proportion of nests that produced an egg. This result alone does not support the Stimulation-Assessment Hypothesis since it might be that some female assessment occurs but the mechanism is not necessarily stimulation of the female to release the egg from the follicle. In fact, in support of the Assessment Hypothesis (but not the Stimulation Hypothesis) in natural nests observed in the descriptive part of this work, there were a weak but significant association between the number of sticks brought by the male and the number of copulations (see below).

I was unable to determine the duration of the female's fertile period in frigatebirds using circulating hormone levels. Estradiol is known to rise some








hours after ovulation in hens (Lance and Callard 1978). However, the only peak found during the copulatory period of frigatebirds occurred one day before egg laying, when the egg was detected in the uterus. This peak could be only a late manifestation of ovulation in frigatebirds. I was unable to assay other hormones because of technical limitations. Copulations occurring as early as 22 days before egg laying might support the Stimulation-Assessment Hypothesis since this hypothesis predicts that copulations begin before the fertile period of the females. However, since the fertile period may be extended by the presence of sperm storage structures inside the reproductive tract of most female birds and especially in seabirds the length of the fertilization period is uncertain (Birkhead et al. 1987).


Sperm Competition Hypothesis

I did not obtain unequivocal evidence in favor of the Sperm Competition

Hypothesis since a strong ongoing El Nio effect in the Pacific coast affected the survivorship of the chicks included in this experiment and consequently I could not obtain enough blood samples from families for paternity analysis. However, the descriptive study in this colony indicated that conservative amounts of extrapair copulations occur in this population. Extra-pair copulations were detected in 9% of the pairs observed in 1992-1993. Since no evidence was found in favor of the Fertilization and only weak support was found for the Stimulation Hypotheses, the Sperm Competition hypothesis is a good candidate to explain the evolution of the copulatory pattern (frequency and peak) in frigatebirds.

Several forms of the Sperm Competition Hypothesis could be plausible here but in particular I tested one prediction of the Mate Guarding Hypothesis from the point of view of males. Although extra-pair copulation occurred in 7 out of 30 manipulated nests (experimentals and controls), against this hypothesis









the incidence of extra-pair copulations was not more frequent in experimental than control nests, suggesting that the probability of having an extra-pair copulation does not depend on the number of successful copulations. In other words, copulation frequency does not apparently function as a mate guarding tactic for males.

If males are not guarding the female by copulating frequently, the

alternative is that males are protecting their paternity by diluting the sperm of other males that previously copulated with the female (Paternity Assurance Hypothesis). This is in fact a viable alternative. On the other hand, if sperm precedence is a possible mechanism promoted by sperm-storage structures in females, by copulating frequently males can increase their likelihood of being the last male copulating with the female, increasing their probabilities of fathering the chick. Both hypotheses predict that, in an experimental situation like that used here, the incidence of false paternity will be higher in experimental than in control nests. Since many of the chicks in the sample disappeared before I took the blood samples from the experimental and control families, these hypotheses remain to be tested. However, since extra-pair copulations occur and if alternative explanations do not explain multiple intra-pair copulations, multiple copulations by the same male is a likely explanation.

From the point of view of the female, I tested two alternatives: The MaleGuarding and the Immediate Material Benefits Hypotheses. The results are equivocal. Contrary to the Mate Guarding Hypothesis, there were no more nest failures before laying in experimental than in control nests, suggesting that by copulating less frequently in experimental nests, females were no more likely to lose their mates than in control nests. However, the significant association between high copulation rates (copulation per day) and reduced probability of









nest failure in experimentals suggests that female mate guarding could be one of the functions of the high copulation rates in frigatebirds.

Inconsistent with the prediction of the Immediate Material Benefit

Hypothesis, males did not bring more nesting material to control nests than to experimental nests. However, in support to the Immediate Material Benefit Hypothesis, manipulated nests (experimental and control nests) had higher copulatory rates and higher delivery rates of nesting material than natural nest from the descriptive part of the study. This result suggests that males, obligated to leave the nest more frequently looked for more nesting material and increased the copulation frequency of the pairs. Additional support for this hypothesis comes from the observation of natural pairs: there was a weak but significant association between copulation frequency and nesting material brought by the male to the female.

The Future Material Benefits Hypothesis (Hunter et al. 1993) hardly

applies to the frigatebird system. Since obligate male desertion occurs in this species, and desertion seems dependent on the time of the year (Chapter 4), this explanation is unlikely. Females do not gain any extra help from males since the only variable that counts to explain variability in desertion date of males is how early in the season a pair becomes established (Chapter 3).


Peak of Copulation Hypothesis

Copulations peaked in frigatebirds about 6 days before egg laying. Hypotheses about a decline in copulation frequency before egg laying (and presumably when the female is still fertile) have been advanced under the assumption that the fertile period extends to the laying date (Birkhead and Moller 1993). The evidence presented here suggests that the decline in copulation frequency occurs about two days before egg laying when the females









are no longer fertile, based on the presence of the egg inside the female's uterus. This is not unusual since other birds have similar periods of egg retention (birds laying eggs two days apart; Birkhead and Moller 1992). If the fertilized egg is in the uterus two days before laying, there is no additional benefit for females to continue copulating. In addition, if males are able to detect that the egg is fertilized, there is no additional benefit for the male in continuing to copulate. If frequent copulations involve a cost to both parents of the possible damage to the developing unlaid egg, males and females should stop copulating before the laying of the egg.

Water shots were a good method for discouraging copulations in

frigatebirds. However, the manipulation had some influence on control and experimental nests (manipulated nests) compared with non-manipulated nests observed from November 1993 to March 1994. Males brought 4 and 2.7 times more nesting material to experimental and control nests respectively than to non-manipulated nests. Nonetheless, copulation frequency (copulation attempts plus copulations) and the copulation period of manipulated nests (control and experimental) were not different from those in unmanipulated nests during 19931994. The comparison suggests that by disrupting copulations I increased the activity of males only, but females still copulated at similar rates and this activity of males did not affect the laying date. Even with this effect on the behavior of males, the results are still valid.

High levels of estradiol and moderate levels of testosterone have been

associated with female reproductive and copulatory behavior in birds (Lance and Callard 1978, van Tienhoven 1983, Wingfield et al. 1989, Hannon and Wingfielg 1990, Wingfield 1994). Estradiol levels in frigatebirds were comparable to concentrations reported for other birds (e.g. ptarmigans; Hannon and Wingfield 1990) fluctuating from 20 to 200 pg/ml. However, In frigatebirds the circulating








level estradiol declines as the copulation period progresses and estradiol concentrations did not correlate with the copulation rate. There was a better but still non significant correlation between testosterone levels and copulation frequency in frigatebirds suggesting some functional connection. Frigatebird testosterone levels were higher compared with concentrations of this hormone in females but smaller than in males of other species (Wingfield et al 1989, Hannon and Wingfield 1989). There is no information about the hormone levels in frigatebird males but different ratios of male and female testosterone concentrations are different in different mating systems (Wingfield 1983). Male/female testosterone ratio seems to be low in species with slight sexual dimorphism. Since frigatebird females are constantly competing for males, raised testosterone levels may be a sub-product of strong female-female competition (the Challenge Hypothesis, Wingfield et al. 1987). Since changes in plasma testosterone appear to mirror those of the estradiol during the ovulatory cycle of hens (Lance and Callard 1978), it is not surprising that estradiol and testosterone are correlated in frigatebirds.

In summary, frigatebirds copulated about 16 times during a period of 13 days. Copulations peaked at 6 days before egg laying and then declined. The experimental manipulation of copulation frequency in the magnificent frigatebird did not support the Fertilization and the Stimulation-Assessment Hypotheses as explanations for the frequent copulation in this bird. Data indicated that only a few copulations are sufficient to fertilize the egg. In addition, like many other birds, copulation frequency was independent of egg laying in these birds. In the context of the Sperm Competition Hypothesis, frequent intra-pair copulations could serve the interest of males and females. By copulating frequently males may be increasing their paternity (Paternity Assurance Hypothesis) and females could be assessing the quality of the mate. The paternity analysis is needed to









demonstrate that the incidence of extra-pair paternity was lower in control than in experimental nests. The presence of the fertilized egg inside the reproductive tract of the female could be associated with the decline in intra-pair copulations. The copulation pattern of males and females in frigatebirds may be the outcome of conflicting reproductive interests of both sexes.





68


Table 2.1 Reproductive success and nest failure in experimental and control nests.

frequency of each treatment

variable experimental control


Initial sample size 22 8
Egg observed 13/22 (59%) 6/8 (75%)
Failure before laying 9/22 (41%) 2/8(25%)
Chick observed 8/13 (61%) 1/6(12%)
Failure after laying 5/13 (38%) 5/6 (63%)





69


Table 2.2 Copulation rate (interrupted copulations) in experimental nests and the frequency of egg laying. High and low copulation rate are above and below the mean (1.7 copulations per nest per day).

frequency of

copulation rate egg laying nest failure
(no egg laid)


high 9(41%) 2(9%)
low 4(18%) 7(32%)

One-tailed Fisher Exact test for the entire table, p=0.04





70


Initial


N Male [ Female


Middle


Late


Nest-building and copulation period (thirds)




Figure 2.1 Proportion of time that males and females stayed at the nest (n=22)
during the nest-building and copulation period.


E

0
C
0
0 0.


0.8 0.7 0.6 0.5

0.4 0.3


-.
C,,
a)
C


0.2

0.1


r_


I





71


0.45

0.4
0.35 0.3 0.25

0.2 0.15 0.1 0.05
0


+


r * I I


Initial


Middle


Late


Nest-building and copulation period (thirds)




Figure 2.2 Proportion of time that males and females stayed together at nest
during the nest-building and copulation period (n=22 nests).


+,)
C


E,
a> 0)


0
.6c

a)
E


ZZ
0
C:


a_





72


2.5





1.5


1~ 0.5


0


f


iI


I I I


Initial


Middle


Late


Nest-building and copulation period (thirds)




Figure 2.3 Rate of stick delivery by the male (mean SE) as a function of the
nest-building and copulation period (n=22 nests).


U)

a
a),
0




0





73


3 -


L

a,
4-

0
-I.



CL
0
0


2













0-


24




26 2


8 T


26


0


5


10


15


20


25


Days before egg laying





Figure 2.4 Copulation rate (mean SE) as a function of the days before egg laying. Day 0 corresponds with egg laying. Numbers near the dots represent sample sizes.























Experimental (n=13) Control (n=6)


Copulations


Interrupted copulations


Water shots
(outside copualtion)


Figure 2.5 Average copulation frequency at experimental and control nests. In experimental nests copulations were interrupted using water shots. In control
nests water shots were used outside of the copulation interaction.


74


25

20 15 10 5'


0

E
z


0'-





75


* Testosterone M Estradiol


1200 a 1000 800 600



400


10
I


T 2
T5


3


0


0 I I I


0 2 4 6 8 10


12


14


Days before egg laying


Figure 2.6 Circulating concentrations of testosterone and estradiol in females as a function of the days before egg laying. Day 0 was the day when the egg was
laid. Sample sizes (numbers close to the dots) are the same for dots and
squares. For comparison, sticks brought by the male occurred from day 14 to 2
and then declined. Copulations started at day 14, peaked at day 6 and then declined to day 2 before egg laying.


4


E


0


0
C




0
0
0


1


1
el


0


1


3


~ ~J ~.J


.


M


U
U


M













CHAPTER 3
THE TIMING OF MALE DESERTION IN THE MAGNIFICENT FRIGATEBIRD: A
TRADE-OFF BETWEEN CURRENT AND FUTURE REPRODUCTION




Introduction




Differences in parental care between males and females within a pair

have been reported in several species (Ridley 1978). The extreme case of this inequality is mate desertion. Desertion is defined as the termination of offspring attendance by one parent before offspring independence (Fujioka 1989). Desertion by the male is commonly reported in birds (Ezaki 1988) but females desert in some species (Eens and Pinxten 1995). In some other species of birds like kites and little egrets, either sex may desert (ambisexual desertion, Beissinger 1986, 1987a, 1987b, Fujioka 1989, Persson and Ohrstr6n 1989). Desertion could be flexible, as in polygynous species or inflexible as in frigatebirds in terms of its occurrence, the sex of the deserter (Beissinger 1990), and the time of desertion. In the former case the interesting question could be why individuals desert or stay, but in the second case the desertion time is more interesting.

Parental investment is defined as everything that the parent does for the survivorship and future reproduction of the offspring at a cost to the parent in her/his ability to invest in other (current or future) offspring (Trivers 1972). With this definition Trivers put the main prediction of parental investment theory in the


76









context of the trade-off between current and future reproductive success. The main idea here is that individuals are expected to optimize their parental investment to produce the maximum number of offspring with the minimum cost over their lifetime. From this perspective, mate desertion is expected to evolve only when the reproductive advantages to deserters is larger or at least equal to that of non deserters. This theory gives us the framework to generate many hypotheses to explain reproductive patterns observed in the field and, even better, to derive precise predictions and test them in the field. According to Parental Investment Theory (Trivers 1972), we can expect mixed reproductive strategies by males and females of sexual species in order to increase their individual life-time reproductive success (Darwinian fitness). Since males and females are under different selective pressures to maximize reproductive success, conflicts arise over the amount and time of parental investment (Trivers 1972). The recent literature suggests that the diversity of reproductive strategies results from sexual conflict (Trivers 1972, Rodwe et al. 1994; Kempenaers 1995; Gowaty 1996) constrained by the distribution and availability of resources (Orians 1969).

Although the concept of Parental Investment has been very useful for the development of models, Parental investment has been rarely used because it is difficult to measure (Evans 1990, Clutton-Brock 1991, Clutton-Brock and Godfray 1991). The alternative in the field is to use the concept of Parental Care and Reproductive Success as a substitute for Parental Investment. Parental care is the amount of energy, time and risks incurred by a parent in caring for the offspring and Reproductive Success is the number of chicks produced to independence (Clutton-Brock 1991). In the context of the trade-off between current and future reproduction, the loss of potential mating opportunities represents an additional cost.





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Two types of models to explain and predict desertion have been

developed, depending on the cost-benefit equation for deserters and non deserters (optimizing and dynamic modeling: Grafen and Sibly 1978, Winkler 1987, Kelly and Kennedy 1993) or the outcome of the conflict between the male and female strategies in the mating pair (frequency-dependent models: Maynard Smith 1977, Lazarus 1990). However, only a few field studies have tested the predictions from the models. Both types of theoretical modeling approaches to mate desertion have indicated that any strategy of stay or leave the offspring by either or both parents could reach an evolutionarily stable state. The outcome depends on three initial conditions: (a) the ability of one parent to complete the rearing of the offspring alone (this factor also depends on the feeding and caring demands of the offspring and the abilities of parents to complete the care of the chicks alone); (b) the opportunity for additional matings after desertion (operational sex ratio, sensu Orians 1969); and (c) paternity certainty (Maynard Smith 1977, Grafen and Sibly 1978, Lazarus 1990, Whittingham et al. 1992, Xia 1992, Houston 1995).

Although the factors influencing desertion have been analyzed in some detail (Fujioka 1989, Westneat 1988, 1993, Whittingham and Robertson 1994), little attention has been paid to the main prediction of parental investment theory: the trade-off between current and future reproductive benefits (Kelly and Kennedy 1993). According to the theory, we expect mate desertion to be favored by natural selection when the reproductive benefit of the deserters is higher than the reproductive outcome for non deserters. High reproductive success for nondeserters in the current reproductive season does not rule out the possibility that in the long run, deserters may have a better or at least equal expectation of long-term reproductive success.





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The trade-off resulting from the decision to leave or stay and care for the offspring or the decision about the timing of desertion depends on (1) the probability of finding another partner and rearing another brood (this includes the time for breeding recovery), and (2) whether the current offspring are going to survive after desertion with the attention will the mate only. Under this circumstance it is expected that deserters to take into account variables influencing the survival probabilities of the offspring (e.g. female, offspring and own physical condition). If one parent is able to rear the chick alone from the beginning, we can expect that male desertion will occur shortly after copulation or immediately after the female lays the egg. However, if the offspring demands more post-zygotic care than one parent can supply or deliver even temporarily, then it can be predicted that the male will delay desertion until such a time when offspring demands decrease to a point where one parent is able to feed (and protect) the chick alone (feeding threshold).

Although all models have assumed this trade-off, unfortunately, the

systems in which models have been validated have not yet offered information about the current and future reproductive benefits of deserters simultaneously (Beissinger 1987a, b, Fijioka 1989, Kelly and Kennedy 1993). In the specific case in which a model was developed and validated using information coming from several populations of the Cooper's hawk, the key factor influencing desertion was the interaction between the threat to the future reproduction of the deserters (the female in this case) and the nestlings' risk of death. However, the trade-off was not tested since none of the deserter females re-nested after desertion (Kelly and Kennedy 1993).

Experimental manipulation of the deserters is essential to demonstrate the costs and benefits between the current and future reproduction (trade-off), but the manipulation itself could be very difficult and probably uninformative,








since the feeding rates of males and females and the growth rates of the offspring might have coevolved (Clutton-Brock 1991). This means that when the mate is removed, the offspring always dies, thus confounding the effects of desertion and disturbance. To circumvent this problem, we can analyze the timing of desertion in natural populations and look for the reproductive trade-off for early and late deserters. I used this approach to test the main qssumption of parental investment theory and the role of the mate during and after mate desertion, using the male desertion system of the magnificent frigatebird. I derive here a set of predictions taking into account the reproductive biology of this seabird.

Frigatebirds are socially monogamous seabirds that rear one altricial chick for 12 to more than 18 months (Chapter 1). Although biparental care seems to be the rule in frigatebirds, in one species, F. magnificens, there is a dramatic division of labor between the sexes in caring for the chick. In this species males and females share the incubation and the first three weeks of brooding equally (see Chapter 1). However, when the chick is still small and unable to survive without parental attention (the male stays 17 to 50% of the total time that the chick is at the nest and from 7 to 20% if we add the dependence period up to independence), the male deserts the nest leaving the female to feed the chick for a long period of time ranging from 12 to 15 months. Obligate male desertion has been consistently reported in the magnificent frigatebird (Diamond 1972, 1973, Nelson 1975, Coello et al 1977, Trivelpiece and Ferraris 1987, Durand 1992). In addition, successful frigatebirds are unable to reproduce again in the same breeding season (this study) and it has been suggested that frigatebirds undergo a 5-month molt between consecutive reproductive periods (Diamond 1972). Furthermore, all breeding colonies of frigatebirds restart reproduction annually. However, it has been speculated that





81


if males are deserting their chick after 6 months of parental effort (from courtship to chick rearing), even if they molt, they can re-mate again in the next breeding season, whereas females are limited to biennial breeding constrained by feeding of the chick (Diamond 1972).


Predictions Derived From the Parental Investment Theory


All males leave so this decision is obligate but individuals still have to

decide the proper time to leave in terms of the trade-off between the current and future reproduction. Two aspects of this trade-off are (1) the survivorship of the current offspring and (2) the probability of recovering and finding another mate. In frigatebirds the best time to leave is affected by the age and condition of the chick: (a) when the chicks are able to survive with the care of the female alone (when the probability of chick survival highest), and (b) the condition of the female caring for the chick, and the condition of the male. A more specific prediction is a negative correlation between the desertion date in terms of chick age and the body condition of the female, chick or the deserting male. Since successful frigatebirds are unable to reproduce again in the same breeding season and because a 5-month recovery period is required in these birds, males only increase their future reproduction in the next breeding season. Thus, the prediction here is that the deserting males will be looking for mates in the next breeding season. Since the proper time for desertion should be a compromise between these two conflicting times, the proper comparison is the reproductive success and the remating time between early and late deserters. The individuals deserting very early in the life of their chick are going to sacrifice chick survival. In contrast, those individuals deserting late are going to sacrifice future reproduction.









All this is predicted assuming that females are able to rear the chick alone as soon as the chick is able to remain safely at the nest. The ability of females to care for the chick alone could be because the chick has already passed the peak period of vulnerability to predation or the peak feeding requirement or because the chick is more resistant to periods of starvation or because the female increases her effort to cover the chick's feeding demands. If females are compensating for the absence of males, I expect a significant increase in the feeding rate of females after male desertion.




Methods




We followed 95 nests that contained chicks for 40 days each after

hatching until fledging. In 40 nests at least one parent was marked and in 47 both parents were marked and in seven only chicks were marked. All chicks in the sample were individually marked with numbered wing tags. Chick survivorship was checked once a week and monitored three consecutive days per week during behavioral observations. Chicks were weighed and their culmen and ulna lengths were measured once a week from 40 days of age to fledging. Chicks were handled at night to minimize disturbance. To monitor parental care and chick feeding, we made behavioral observations from 20 February to 21 July 1994 and on an opportunistic basis from 17 November to 27 December 1994 when chicks fledged and from 28 March to 12 April 1995. We recorded chick feeding frequency and the arrivals and departures of adults to and from the nest for three consecutive days per week from 0800 to 1800 h. We made focal observations on up to 36 nests simultaneously from an observation





83


site located 30 to 150 m from the focal nests. It was possible to observe such a large group of nests because we recorded only a few conspicuous behavioral categories occurring infrequently. In addition to our focal recording methods, we scanned for the presence of parents and chick at every nest every hour.


Measurements


Male desertion.

Since we followed every nest up to chick fledging, male desertion was
determined in all successful nests as the last time we recorded the presence of the male at the nest, not necessarily feeding the chick. In unsuccessful nests we scored desertion if the chick survived attended by one parent only and the mate was not seen visiting the nest for more than three consecutive days. We could not distinguish male desertion from nest failure when the death or disappearance of the chick coincided with the time of mate desertion.


Layinq date estimation and settlement time.

Laying dates in every nest were calculated retrospectively from chick age by adding 56 days (incubation period, Chapter 1). For analysis, nests in the sample were divided into those established early and those established late in the season. I called them: early- and late-settled nests. The division between early- and late-settled nests was the mean laying date in the sample.


Chick age estimations.

Chick age was estimated from the culmen (upper mandible) length the
first day we measured it or included the chick in the sample. We measured it by placing a measuring tape ( 0.5 mm) at the base of the bill and following its








curvature. We interpolated the age of the chick from the growth curve fitted in 1991 for this population (Durand 1992). Durand's data were based on a weekly measurements of 13 chicks of known age.




Chick feeding rate.
Feeding was infrequent in frigatebirds (once each 3 days). I report here the frequency of feedings that occurred during three consecutive days per week as a feeding rate. Since some unknown frequency of feedings occurred at night, I assume here that our chick feeding rates were only estimates of the real feeding rate.


Body condition.

Body condition of males, females and chicks were estimated from the mass and culmen length measurements. Chick body condition was calculated from measurements taken on the closest date to male desertion. While adult body-condition indexes may not be biased, the chick body condition is correlated with age because of the allometry between mass and culmen length. In the case of the chicks, I estimated body condition from the residuals of the regression between the natural logarithm of the mass3 (to work in the same dimension) and the natural logarithm of the culmen length. Since residuals give the distance between the average and each chick measurement, this method estimates the individual condition controlling for biases by sex, age and settling time. In the case of adults I estimated condition as the mass/culmen length ratio since there was no correlation between the log mass3 and log culmen length. For the analyses of chicks, I correlated the residuals of the log mass3 and log culmen length with chick age at the time of male desertion following the predictions








derived from theory (see introduction) and between the mass/culmen length and chick age at the time of male desertion in the case of adults.


Statistical Analysis.


Comparisons were made using non-parametric tests (Mann-Whitney U, Wilcoxon and Spearmann Rank Correlation tests) because small samples and heterogeneous variances precluded me from using parametric tests (unpaired and paired t-tests and Pearsosn's Correlation). In addition, I used Chi Square tests to analyze frequencies and the Fisher Exact Probability test when some observed values were zero or when sample sizes were small. Statistical tests were one-tailed when I tested directional alternative hypothesis and null hypotheses were rejected at the 95% confidence level.




Results




Time of Male Desertion


The age of the chick when males deserted (age of desertion) was variable, ranging from 18 to 161 days (Figure 3.1). Surprisingly, all males deserted the nest and eventually the colony during a short period of time during the year. Most of the desertions (74%) occurred before May (between March and April 1994; Figure 3.2). Differences in male desertion dates was a consequence of variation in the laying date, with early-settled males deserting older chicks and late settlers deserting younger ones (laying date vs. deserting









date; r=-0.78, p=0.0001, n=42). In fact, early-settled males deserted their nest when chicks were 40 days older on average (105.3 days, SE=5.4, n=18) than late-settled males (65.4 days, SE=4.1, n=14; Mann-Whitney U=15.5, p<0.0001). In spite of the large difference in chick age at the time of desertion between early- and late-settled males, early- settled males deserted only 10 days before the late-settled males on average considering the desertion dates during the year (early-settled males deserted on 27 March, SE=6.4 days, n=18; late-settlers deserted on 7 April, SE=3.2 days, n=14). The average difference in desertion date during the year was not significant (Mann-Whitney U=79, p=0.08).


Male Desertion and Body Condition


Contrary to my prediction, the age of the chick at the time of male desertion did not correlate with the female ( r=0.1, p=0.30, n=32) or male (r=0.003, p=0.49, n=26) body condition. However, in support of my prediction, a negative correlation was found between chick body condition and chick age at desertion (r=-0.47, p=0.003, n=32, Figure 3.3): males deserted chicks in good condition earlier than those in poor condition. No correlation occurred in earlysettled nests (r=0.17, p=0.25, n=18; Figure 3.3), but the same correlation was strong, negative and highly significant for late-settled males (r=-0.78, p=0.0005, n=14; Figure 3.3).


Survival Probability of Chicks


The importance of the male's contribution to the feeding and care of the chick decreased continuously up to desertion at 100 days of chick age (Figure 3.4). No eggs nor chicks survived when one adult deserted during incubation,




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EVOLUTION OF BREEDING BEHAVIOR IN THE MAGNIFICENT FRIGATEBIRD: COPULATORY PATTERN AND PARENTAL INVESTMENT By JOSE LUIS J. OSORNO CEPEDA A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 1996 UNIVERSITY OF FLORIDA LIBRARES

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To Rodrigo and Alejandro, My Children To Guadalupe, My Wife To Dona Jose, My Mother To Chelin, Josue and Madai To the people I love...

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ACKNOWLEDGMENTS I thank Dr. Jane Brockmann for all her support and advice. Dr. Brockmann encouraged me explicitly and implicitly, following her rigorous method and approach to the study of the behavior and evolution. She also encouraged me to get involved in all possible academic activities doing research and teaching. Her questions always took me to a new and novel analysis of my data. I especially appreciate the time she invested improving the English in my manuscript. I thank Dr. Dewsbury, Dr. Guillette, Dr. Kiltie and Dr. Levey, my committee members, for their advice in the most difficult moments of my research and they encouraged me to keep working hard. I am especially grateful to Dr. Hugh Drummond and all the people from his lab at the Centre de Ecologia, U.N.A.M. Dr. Drummond, my advisor in Mexico, has been the keystone in my formation. I am still learning from his suggestions made a long time ago, especially in these days of loose contact. This work was possible because of the contributions to the fieldwork of many students of the Facultad de Ciencias and the Centre de Ecologia at the University of Mexico (UNAM). Thanks to Adrian Lecona, Suneeta Sing, Tan'n Toledo, Lourdes Fernandez, Ines Arroyo, Elsa Saborlo, Tonanzin and Cristina Rodriguez for their effort and enthusiasm in the field. They really did an

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excellent job and took the right decisions when I was not at the island with them. Constantino Macfas and Juliet Vickery kindly helped me when they were at the island doing their own research. Many administrative tasks crucial for this project were accomplished by Cristina Rodriguez and Virgilio Lara from the Centre de Ecologia. The Consejo Nacional de Ciencia y Tecnologia (CONACyT) in Mexico, The University of Florida, The Florida Foundation, The Centre de Ecologia and Sigma Xi provided financial support for this work. The Secretaria de Desarrollo Social (SEDESOL) in Mexico provided the permits to work at the island and the Secretaria de Marina provided logistical support and transportation to the island. Thanks to all these institutions. Fishermen from San Bias and Boca de Camichin contributed in several ways to the accomplishing of this work, especially with their friendship. Dr. Louis Guillette and Drew Crane advised and helped me and provided all materials for the hormone analysis (Chapter 2). Dr. Wayne Potts kindly helped me and provided the materials and time supervising my work at his molecular lab (Laboratory of Genetics and Mammalogy). Karen and Anthony Baker taught me DNA microsatellite techniques for the analysis of paternity. Unfortunately, this technique did not work properly with frigatebirds. I am especially grateful to Guadalupe Hernandez, my wife, for the long talks about my hypotheses. After those long discussions about the different topics she really now understands the breeding biology of frigatebird better than I. iv

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All my friends at the Centro de Ecologia and Facultad de Ciencias at the UNAM supported me when I needed help in several ways. They always have been there, with me. They know that. Finally, thanks to Rodri and Ale, my children. They were always a source of support and excellent humor. They always encouraged me in the most crazy enterprises of my life. Their coming to live in Gainesville was only one test of their love. The Universidad Nacional Autonoma de Mexico generously provided the financial support (scholarship) to do my Ph.D. studies at the University of Florida. Thank you to the UNAM. V

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TABLE OF CONTENTS ACKNOWLEDGMENTS LIST OF TABLES x LIST OF FIGURES xi ABSTRACT xiii CHAPTERS 1. INTRODUCTION 1 Reproductive Biology of Frigatebirds with Emphasis in the Magnificent Frigatebird: Is Feeding Ecology Associated to Differences in Life Histories? 1 Comparative Biology of Frigatebirds 3 External morphology 3 Classification 4 Geographic distribution 4 Breeding ecology-colony level patterns 5 Breeding ecology-individual patterns 6 Feeding ecology 9 Methods 11 Individual Marking and Nest Visits 12 Censuses 13 Incubation and Brooding Periods 14 Observations of Marked Birds 14 Behavioral Observations 14 Behavioral Categories 15 Courtship period 15 Chick Feeding 16 Data Analysis 16 Chick age estimations 16 Chick growth 16 Sexing the chicks 17 Behavioral analysis 17 Chick feedings 18 Results 18 The Population View 18 vi

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Breeding season 18 Mating success 19 Egg survival 19 Chick survival 20 Adult dispersion 20 The Individual View 21 Pair formation 21 Nest building and copulation behavior 22 Intraand extra-pair copulation frequency 23 The role of adults during incubation and brooding 23 Chick rearing 24 Chick growth, fledging and independence 25 Adult re-mating 25 Discussion 26 The Magnificent Frigatebird at the Isia Isabel 26 The Effects of Feeding Ecology on the Breeding Biology of Frigatebirds 27 Causes of Chick Mortality 33 A TEST OF THREE HYPOTHESES TO EXPLAIN THE FUNCTION OF THE COPULATION PATTERN IN THE MAGNIFICENT FRIGATEBIRD 41 Introduction 41 Hypotheses to Explain Multiple Intra-pair Copulations 42 The Fertilization Hypothesis 42 Conflict of interest 42 The Stimulation-Assessment Hypothesis 43 The Sperm Competition Hypothesis 44 Hypotheses to explain the peak of copulations 45 Determining the female's fertile period 45 Predictions From the Hypotheses applied to the Magnificent Frigatebird 47 Methods 49 The Description of the Copulatory Pattern 49 Behavioral categories 50 Experimental Design 50 Female's Fertile Period 51 Data Analysis 53 Behavioral analysis 53 Statistical analysis 54 Results 54 The Copulatory Pattern in the Magnificent Frigatebird: The Descriptive Approach 54 Nest building and copulation behavior 55 vii

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Intra-pair copulation frequency 55 Extra-pair copulation frequency 56 Experimental Results 56 Control and experimental nests 56 Fertilization Hypothesis 57 Stimulation-Assessment Hypothesis 57 Sperm Competition Hypothesis 59 Peak of Copulation Hypothesis 59 Discussion 60 Fertilization and Stimulation Hypotheses 61 Sperm Competition Hypothesis 62 Peak of Copulation Hypothesis 64 3. THE TIMING OF MALE DESERTION IN THE MAGNIFICENT FRIGATEBIRD: A TRADE-OFF BETWEEN CURRENT AND FUTURE REPRODUCTION 76 Introduction 76 Predictions Derived From the Parental Investment Theory 81 Methods 82 Measurements 83 Male desertion 83 Laying date estimation and settlement time 83 Chick age estimations 83 Chick feeding rate 84 Body condition 84 Statistical Analysis 85 Results 85 Time of Male Desertion 85 Male Desertion and Body Condition 86 Survival Probability of Chicks 86 Reproductive Benefit of Male Desertion 87 Male and Female Contnbution to Chick Feeding 88 Discussion 88 Chick Survival and Male Desertion 89 Female Contribution 93 The Trade-off Between Current and Future Reproduction 93 4. FEMALE TACTICS TO COPE WITH MALE DESERTION IN THE MAGNIFICENT FRIGATEBIRD 103 Introduction 103 Response to Desertion 105 Methods 109 Laying Date Estimation 110 viii

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Chick Age Estimations 110 Chick Feeding Rate 110 Chick Growth Ill Sexing Fledglings 11 1 Statistical Analysis 111 Results : 112 Female Compensation for the Male's Absence 112 Female Tactics Dealing With the Male's Desertion 113 Discussion 115 5. FLEDGING SEX RATIO AND THE COST OF REAR MALES AND FEMALES BY A DESERTED FEMALE IN FRIGATEBIRDS 127 Introduction 127 Facultative Sex Ratio 129 Sex Conflict About the Offspring Sex Ratio 130 Methods 133 Individual Marking and Nest Visits 133 Behavioral Observations 134 Chick feeding 135 Observation of marked birds 135 Data Analysis 136 Chick age estimations 136 Sexing the chicks 136 Chick growth 136 Behavioral analysis 137 Results 138 Chick Feeding 138 Chick growth and chick fledging 139 Fledging sex ratio 139 Chick Independence 140 Discussion 141 The Cost of Rearing Males and Females 141 The Condition Dependent Sex-bias Hypothesis 144 Adult Male and Female Conflict About the Offsphng SexRatio 146 6. CONCLUSIONS: MAIN REMARKS AND FUTURE RESEARCH 156 LITERATURE CITED 164 BIOGRAPHICAL SKETCH 173 ix

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LIST OF TABLES Table Page 1 . 1 Comparative breeding biology of the five species of frigatebirds including this study 35 2.1 Reproductive success and nest failure in experimental and control nests 68 2.2 Copulation rate in experimental nests and the frequency of egg laying 69 3.1 Frequency of early and late-settled marked males seen and not seen in the next breeding season 96 4. 1 Feeding rates of females to chicks of early and late-settled nests as a function of chick age 120 5. 1 Comparisons of the average number of feedings delivered by the mother to sons and daughters 148 5.2 Mean of the asymptotic size at fledging of 23 male and 1 7 female chicks 149 5.3 The growth rate of male and female chicks 150

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LIST OF FIGURES Figure page 1.1 Schematic representation of the typical frigatebird breeding from the point of view of populations and individuals 36 1 .2 Number of male magnificent frigatebirds displaying at the breeding colony 37 1 .3 Adult operational sex ratio per day at the reproductive site as a function of the time of the year 38 1 .4 Adult sex ratio per day at a roosting site as a function of the time of the year 39 1 .5 Feeding frequency of male and female adults as a function of the chick age 40 2.1 Proportion of time that males and females stayed at nest during the nest-building and copulation period 70 2.2 Proportion of time that males and females stayed at nest during the nest-building and copulation period 71 2.3 Rate of stick delivery by the male as a function of the nest-building and copulation period 72 2.4 Copulation rate as a function of the days before egg laying 73 2.5 Average copulation frequency at experimental and control nests 74 2.6 Circulating concentrations of testosterone and estradiol in females as a function of the days before egg laying 75 3. 1 Frequency of male desertion as a function of the age of the chick 97 xi

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3.2 Frequency of male desertion as a function of the date of the year 98 3.3 Chick condition index at the time of male desertion as a function of the age of the chick at mate desertion 99 3.4 Chick mortality after male desertion 100 3.5 Feeding frequency of males and females as a function of chick age 101 3.6 Schematic representation of the trade-off between current and future reproduction in frigatebirds 102 4.1 Feeding rate delivered by earlyand late-settled females 121 4.2 Total feeding rate delivered by males and females in earlyand latesettled nests as a function of the time of the year 122 4.3 Growth (weight) of the chicks from earlyand late-settled nests 123 4.4 Growth (culmen length) of the chicks from earlyand late-settled nests 124 4.5 Growth (ulna length) of the chicks from earlyand latesettled nests 125 4.6 Schematic representation of the female extra-compensation in terms of chick survival 126 5. 1 Feedings by the female to sons and daughters 151 5.2 Feedings by the male to sons and daughters 152 5.3 Growth (mass) of male and female chicks 1 53 5.4 Grov^h (culmen length) of male and female chicks 154 5.5 Growth rate (ulna length) of male and female chicks 155 6.1 Schematic representation of the trade-off between current and future reproduction in frigatebirds and female extra-compensation in terms of chick survival 163 xii

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Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy EVOLUTION OF BREEDING BEHAVIOR IN THE MAGNIFICENT FRIGATEBIRD: COPULATORY PATTERN AND PARENTAL INVESTMENT By Jose Luis J. Osorno Cepeda August 1996 Chairman: Dr. H. Jane Brockmann Major Department: Zoology Frigatebirds are unusual in showing reversed sexual size dimorphism, in laying one egg, and in their pattern of parental care. These unusual features provide a good testing ground for theory on the evolution of mate desertion, copulation frequency, and sex ratios. In most species of frigatebirds, males and females share equally the long (14-18 month) penod of parental care, but in magnificent frigatebirds {Fregata magnificens) males desert the nest when the chick is 18 to 160 days old. After spending 5 months away, deserting males return to mate in the next breeding season while females are still feeding the fledged chicks. Courtship and nest building occur over a 4-month period and males that nest early desert at an older chick age than late-settled males. Since chick survivorship is correlated with chick size, when late-settled males desert they apparently sacrifice current chick survivorship for increased future reproductive success. xiii

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Females are not passive to male desertion. Earlysettled females compensate for the absence of the male by increasing chick feeding. Latesettled females compensate for the male's absence by increasing their feeding rate and consequently the chick's growth and development beyond that of earlysettled females. This extra-compensation could be a tactic of late-settled females to reduce the mortality of chicks when males desert. Female chicks are 10% larger than males at fledging and somewhat more expensive, i.e. require more feedings and fledge at a later age. Fledging sex ratios do not differ from 1:1, but late-settled nests (where females are abandoned by males when chicks are younger) show a trend toward a malebiased sex ratio. Furthermore, males desert nests with female offspring somewhat later than those with male chicks. These results suggest conditiondependent sex ratios. Frigatebirds lay only one egg, but pairs copulate many times over two weeks. By interrupting copulations I showed that low copulation frequency in experimental nests does not affect egg fertility when compared with controls, so multiple copulations do not function to insure fertilization. Extra-pair copulations occur in 9% of nests suggesting that by copulating frequently males may be protecting their paternity. xiv

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CHAPTER 1 INTRODUCTION Reproductive Biology of Friqatebirds With Emphasis in the Magnificent Friqatebird; Is Feeding Ecology Associated to Differences in Life Histories? Food ayailability and feeding ecology may be considered two of the key factors promoting differences among populations and, ultimately, among species. In particular, theory has suggested that food abundance, distribution and defendibility affects the eyolution of mating systems (Orians 1969) and social organization (Emien and Oring 1977). An example of this is that some bird species are more polygynous in rich habitats (high food availability) and less so in poorer habitats (Dunn and Hannon 1992). Female preferences for males may be a function of food levels. Females may prefer mating polygynously in a good territory and monogamously in a poor habitat (Orians 1969, Dunn and Hannon 1992). It has been suggested that monogamy is maintained because females require the contribution of males to rear offspring. However, under conditions of high food availability, the importance of the male can be reduced and even made marginal. Increased food availability may increase the rearing abilities of adults. If females are able to raise the chicks alone because of improved food ayailability, males can desert and look for another partner (Maynard Smith 1977). Some male removal experiments have shown this (Bart and Tornes 1989), but others have shown no effect on female reproductive success (see ref.

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2 in Bart and Tomes 1989). Food availability has rarely been mentioned explicitly in models of desertion (Maynard Smith 1977, Grafen and Sibly 1978, Beissinger 1987), but clearly this variable can alter the rearing abilities of the parents and the condition of the offspring (Dunn and Robertson 1 992). Mate desertion occurs more frequently in populations with greater availability of food (Beissinger 1987, Whittingham and Robertson 1994, but see Dunn and Roberson 1992) and it is more likely in species with small clutches than those with large ones (Fujioka 1 989, Beissinger 1 987, 1 990). A cascade of effects can be expected as a consequence of increased reahng abilities in parents: If individuals are deserting to increase their long-term reproductive success, intraand intersexual competition for mates might increase (the intensity of sexual selection). In this case mixed reproductive strategies can evolve in populations (Trivers 1972) e.g., extra-pair copulations and egg dumping. Counter-strategies can also be predicted in this scenario to cope with cuckoldry: mate guarding and increased intra-pair copulations. In addition, if the cost of rearing males and females changes because of desertion, facultative sex-ratio adjustment may evolve. Other consequences of changes in food availability can be expected: changes in the length of laying periods, reproductive synchrony, attentive periods to the offspring and growth rate of the chicks. All aspects of reproductive biology then may be influenced by differences in food availability. I address some of these issues in the frigatebirds group (Fregata), specifically in the magnificent frigatebird (Fregata magnificens) Similarities in frigatebirds can be expected because of the common ancestry of the sister species. Differences are likely due to adaptive divergence to different conditions. Differences in food availability can play a pivotal role in the evolution of the different life histories of the frigatebirds. In this chapter I (1 ) summarize the information available about the biology of the five species of

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3 frigatebirds, (2) add new information about the reproductive biology of the magnificent frigatebird {Fregata magnificens) and (3) I discuss the possible role of feeding ecology and distribution of frigatebirds on breeding differences among species. Most of this summary is based on the excellent review by Brian Nelson (1975) and on work concerning the magnificent frigatebird by Diamond (1972, 1973) and Durand (1992). Comparative Biology of Frigatebirds External morphology The five recognized species of Frigatebirds are a morphologically unified group. Frigatebirds are relatively large seabirds with a large wing span ranging from 190 to 240 cm (Howell 1994). These birds are well adapted to economic flight as suggested by their great wing span to weight ratio (larger than any other seabird of comparable size) light skeleton (75-80 g dry-weight) and long and deeply forked tail (Nelson 1967). Frigatebirds have a long bill, strongly hooked at the tip (Eismann 1962, Nelson 1975, Sibley and Alquist 1992), short tarsi, small feet, webs restricted to the basal part of the toes (zygodactylous condition), vestigial uropygial gland. All five species are sexually dimorphic: males are 6 to 12% smaller in culmen length than females (Nelson 1975, Schreiber and Schreiber 1988); males are wholly or mainly glossy black and have a highly distensible gular pouch (scarlet red when in courtship). Females are black with more or less white underparts, except F. aquila. Juveniles are usually black with white underparts and in some species they have a rufoustinged head (Eisenmann 1962, Nelson 1975, Howell 1994).

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4 Classification The five species of frigatebirds are included in the Genus Fregata and the family Fregatidae. The five species are: F. aquila, F. andrewsi, F. ariel, F. minor and F. magnificens. This family has been considered part of the order Pelecaniformes since Linneaus' classification (Cracraft 1985, Sibley and Ahlquist 1992), and this placement has been corroborated using numerical cladistic analysis on morphological and behavioral characters by Cracraft (1987). However, a recent re-classification of avian taxa using molecular techniques (DNA hybridization) and maximum parsimony cladograms, suggested that the Frigatebird family should be included in the order Ciconiformes and that they are more related to Sphenicidae (penguins), Gavidae (loons) and Procelaridae (petrels and albatrosses; Sibley and Ahlquist 1992, Sibley et al. 1988) than to the Pelecanidae, Phaethodontidae, Phalacrocoracidae and Suloidea families, with which they are currently grouped. Even though the change in classification looks dramatic, Frigatebirds have always been considered a distant group from the other Pelecaniformes (Pelicans, Boobies, Tropic Birds, Cormorants and Anhingas). The new classification is still controversial because of criticisms about the way in which the DNA information is used to build phylogenies. The Fregatidae family is a well defined group, but relationships inside the Family are still not well established. The only reference in Sibley and Ahlquist (1992) suggests that F. minor might have evolved before F. ariel and F. magnificens. DNA hybridization techniques were used to reach this conclusion. Geographic distribution All five species of frigatebirds are tropical and sub-tropical. Two of the five species have a highly restricted distribution. F. andrewsi is found nesting

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5 only on Christmas Island in the Indian Ocean, and F. aquila is restricted to Ascension Island in the South Atlantic. Fregata minor and F. ariel, occur in the Indian and Pacific Oceans. Fregata magnificens occurs along the coast and islands of the Americas, from Ecuador to Baja California, Mexico in the Pacific and from Brazil to Florida in the Atlantic. Some overlap in distribution occurs. Fregata minor and F. ariel overlap in approximately half of their breeding localities (Nelson 1975) and F. m/nor overlaps with F. andrevi/s/ at Christmas Island (Indian Ocean). Fregata minor is sympatric with F. magnificens on the Galapagos Islands (Nelson 1975), Isia Cocos, Central Amenca and in San Benedicto Island at the Revillagigedo Archipelago in the Mexican Pacific (Howell 1994). Breeding ecology-colony level patterns Reproductive activity starts with male display and courtship. This period varies among species and populations. Some species are seasonal and synchronous (F. aquila, F. andewsi), whereas others are more asynchronous (F. minor, F. magnificens, F. aquila). in most species, the displaying and laying period occurs over a five -month period with clear peaks at different times during the year (Table 1.1; Nelson 1975). In one colony of F. magnificens at Barbuda Island in Lesser Antilles, laying occurs throughout the year (Diamond 1973). Except for this population, the main reproductive period is seasonal and occurs outside of the rainy season. Reproductive colonies of frigatebirds are highly variable in size ranging from hundreds (Trivelpiece and Ferrahs 1987, Howell 1994) to over 40,000 individuals (Moreno and Carmona 1988). The distribution of frigatebird nests is clumped (Reville 1988). Within groups, the density of nests vanes from two nests per square meter in some groups of F. minor in the Galapagos Islands to

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6 0.06 nests per square meter in some groups of the same species at Tower Island. At Isia Isabel, F. magnificens nests are no more than 40 cm apart (per. obs.). Preferred breeding sites for F. ariel, F. andrewsi, F. aquila and F. minor are oceanic islands and coastal islands for F. magnificens and some populations of F. minor. The most common displaying and nesting places are low brushes and mangroves. One species {F. aquila) nests on rockey ground at Aldabra Atoll (Diamond 1973). Low breeding success seems characteristic of frigatebirds. In all species, only 15 to 25% of the eggs laid produce a fledged young (Nelson 1975, Table 1.1). However some differences exist among groups in the same colony and in the same year (Reville 1988). Intra-specific disturbance (by conspecifics), chick starvation, and predation are the most frequently reported causes of nest failures. Since only 20% of the breeding population is successful in any one year and since offspring rearing takes more than one year, no more than 80% of the breeding age population attempts to breed each year. Related to the extremely low energy consuming flying style (soaring most of the time), frigatebirds have a huge dispersion range. At least some of species are nomadic; at Aldabran Atoll, most of marked individuals of F. ariel ^eie recovered 2000 to 3000 miles from the marking site (Sibley and Clapp 1967, Diamond 1973). Apparently prevailing winds are at least partially responsible for this dispersal. Breeding ecology-individual patterns The whole breeding cycle for a particular successful pair takes more than a year: 2 to 4 weeks for display and pair formation, eight weeks for incubation, about 20 to 24 weeks for growth of the nestling and from 4 to 14 months of postfledging feeding of juveniles (Figure 1.1).

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7 The courtship period, including male display, nest building and copulation, lasts about two weeks in all five species. All frigatebirds produce only one egg per clutch. The egg is 5 to 6% the female's weight (from 59 to 85 g in the different species, Table 1.1 ) and incubation takes 55 days in F. minor and 44 days in F. aquila. In the other three species, the incubation period is unknown. Chicks are borne naked and are extremely altricial. Hatchlings are in close contact with one adult at all times until they are from 30 to 45 days old, when parents begin to leave them unattended. Chicks grow slowly in the whole group. The lowest growth rate is reported in F ariel and in F. minor, followed by F. andrewsi, F. aquila and F. magnificens. The fastest rate occurs in populations of F. minor at Aldabra Atoll. Fledging takes from 20 to 24 weeks in all species. The first flight is not recorded in any species but it is estimated to occur at 5 to 6 months of chick age in all species (166 days in F. magnificens; 130-160 days in F. minor an6 F. aquila; 140 days in F. ariel; 155 days in F. andrewsi). No clear data exist about chick independence but some reports indicate that chicks are at least partially dependent on the parents for four to 14 months after fledging (four to 14 months in F. minor, 9 to 10 months in F. andrewsi and about four months or more in F. magnificens and F. ariel). The post fledging period is not recorded in F. aquila. Interesting differences in the parental care occur in frigatebirds. In three of the species (F. aquila, F. ariel and F. andrewsi), male and female share all the duties of caring and feeding the chick to independence. Interestingly, in one population of F. minor in the Galapagos Islands, both parents share the feeding of the chick to independence (Nelson 1975, Coello et al. 1977) but in the same species at Aldabra atoll, females apparently give more feedings to the chick than do males (Diamond 1973). In F. magnificens, both parents attend the egg and the small chick equally until the chick is from 20 to 125 days of chick age

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8 (Diamond 1973, Coello et al. 1977, Trivelpiece and Ferraris 1987, Durand 1 992). Then, males desert and females complete the rearing process of the chick alone. Chicks are very resistant to starvation in all species. Feeding frequency of the chick varies with the locality and species. In F. andrewsi, chicks received food once every two days; in F. minor once every three days (Coello et al. 1977); in F. ariel once every 2.4 days (Nelson 1 975); in F. magnificens once every two days (calculated from Coello et al. 1977). Sex ratio of fledglings has been estimated in a small sample of juveniles in only three populations of F. magnificens and one population of F. minor. Two estimates of F. magnificens from the Galapagos Islands suggests a strong bias toward female production (1 male to 1.8 females. Diamond 1973; 1 male to 1.5 females, Coello et al. 1977). In contrast, at Isia Isabel the sex ratio of fledglings was estimated to be not statistically different from a 1:1 ratio (Durand 1992). Only Durand's study, however, offered statistical support for the sex ratio comparison and sexing method. In the only fledgling sex-ratio estimation in F. minor, males were as abundant as females (1 male to 1 female, Coello et al. 1977). The age of first breeding is unknown in frigatebirds. However, estimates based on several different plumage categories suggest that it takes from 5 to 7 years to reach matuhty (Nelson 1975). Apparently, frigatebirds molt only outside the breeding period. Of all species of frigatebirds, only F. minor has been found with an interrupted molt while breeding (Coello et al 1977). Other species have been recorded as molting out of the breeding pehod (Nelson 1975). Frigatebirds thus may require several months to complete their molt and Nelson (1975) has speculated that the molt prevents continuous breeding in a relatively seasonless environment.

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9 Since in all species of frigatebirds, breeding takes more than a year and since frigatebirds molt between consecutive reproductive periods, there has been speculation that reproductive periodicity in all species of fngatebirds is biennial except in F. magnificens in which because of the disparate sex roles in feeding the chick, successful males may be able to reproduce every year whereas females are biennial. However, before this work there were no data available with marked birds. Feeding ecology Frigatebirds depend on food resources of irregular availability associated with complicated feeding techniques and a strictly limited foraging area in the water column. Their unusual feeding ecology seems to influence all aspects of their natural history. They feed mainly on tropical pelagic (blue-water) seas but one species {F. magnificens) is coastal and presumably feeds there. Frigatebirds catch food strictly from the sea surface by dipping the bill into the water (limited to 20 to 30 cm from the sea surface) Since the uropygial oil gland is vestigial in frigatebirds (Nelson 1975), they are unable to plunge dive like all other members of the order and most marine birds. During surface-dipping, frigatebirds are only able to submerge the bill or the head into the water and consequently, the availability of food is limited, fluctuating and highly unpredictable. Fishing success at sea is unknown but based on an estimate made on Albatrosses, probably the bird with the most similar feeding and breeding ecology, a bird fishing from the surface is only able to pick up one item every 100 km on average (Weimerskirch and Salamolard 1993). The feeding ecology of frigatebirds has been studied in some detail, particularly the behavior of food stealing or kleptoparasitism (Nelson 1975, Osorno et al. 1992, Vickery and Brooke 1994, Gilardi 1995, Cummins 1995).

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10 Although probably direct fishing is the most important feeding technique of frigatebirds (Nelson 1975), it is well known that frigatebirds steal food from other species of seabirds. Kleptoparasitism and other opportunistic feeding techniques seem to be strategies to cope with food scarcity, and which take advantage of their very well developed flying skills. Kleptoparasitism is common, but the incidence and success of this feeding technique varies among localities, ranging from 6% to 63% success depending on the host species and locality and the frigatebird species (Nelson 1975, Osorno et al. 1992, Vickery and Brooke 1994, Gilardi 1994, Cummins 1995). Foraging distances have not been recorded in any species of frigatebirds. However, looking at the length of the attentive periods (periods of continuous nest attendance) during courtship, incubation and chick rearing ranging from one to 15 days and assuming the length of the attentive period is correlated to the foraging distance, the foraging area for these birds may be very large. At Isia Isabel in the Mexican Pacific, frigatebirds associate with shrimp boats in order to gather food items and probably most of the diet of this population is dehved from this source (Calixto 1993). The diet of all frigatebirds includes flying fishes and squids at many localities (Diamond 1973, Nelson 1975), but anchovies have been reported (Moreno and Carmona 1988) . At Isia Isabel, the magnificent frigatebird included a large variety of fishes from 26 families, squid were only a minor proportion of the diet (Calixto 1993). The large variety of fishes in the diet resembled the composition offish species captured during the shrimp fishing by the shrimp boats around the island. It seems that this population is taking advantage of a predictable food source around the island (Calixto 1993). In the second section of this Chapter I describe the breeding biology of the magnificent frigatebird (F. magnificens). Several studies have reported

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11 information about the breeding biology of this frigatebird, but the information available is inadequate to analyze and explain the costs, benefits, mechanisms and constraints and conditions shaping the biology of this bird. In this chapter I describe, at the individual level, the reproductive biology of the magnificent frigatebird nesting on the Isia Isabel, off the Pacific Coast of Mexico. In addition, I compare this information with the available information for the other four species of frigatebirds. I particularly describe here the role of the sexes during courtship and nest building, incubation, brooding and chick feeding. In subsequent chapters I analyze hypotheses about the function of the intra-pair copulation pattern, male desertion, and the growth and production of male and female chicks. Methods I studied the magnificent frigatebird population at the Isia Isabel, State of Nayarit, Mexico (21° 52' N, 105° 54' W). This colony was estimated as 3,600 nests distributed in patches on the 2-Km^ island (Osorno unpbl. data). It consisted of three dense nesting aggregations: Cerro Pelon at the NW end of the island, Costa Fragatas along the SE shore and Bahia de los Pescadores along the SW of the island. This work was conducted on a sample of nests at the Bahia de los Pescadores zone. Frigatebirds nest here on branches at the top of small (from 1-5 m in high) deciduous trees, Crataeva tapia. Nests are often no more than 50 cm apart, creating a clumped aggregation.

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12 The field work was conducted from 15 November 1993 to 27 July 1994; from 10 November to 28 December 1994 and from 27 March to 10 April 1995, I was assisted by 3-5 students from the Centre de Ecologi'a, University of Mexico. Individual Marking and Nest Visits We marked every accessible nest or display site and the adults mating there with plastic numbered tags as soon as I recorded a pair in courtship. A display site was a branch at the top of a tree where a male perched while usually showing his inflated red gular pouch. The nest was a 20 cm round platform made of sticks and cemented with guano. It contained an egg or chick and was guarded by an adult or chick. We captured a displaying male (i.e. a male with the red gular pouch inflated or deflated) or a pair of adults (male with the red gular pouch and female) standing at the site. Birds were captured by hand at night when they were at the nest and marked with 3-digit numbered wing tags. I marked nests and birds at night because frigatebirds are very sensitive to daytime disturbance. During the day when a frigatebird is disturbed at her/his nest, immediately other individuals, especially males, arrive at the site and try to steal the nest or nesting material. At night, frigatebirds are perched at the nest site or on other tree branches at the island. Extensive marking was performed at the beginning of the breeding season from 17 to 21 November 1993 and from 10 to 27 November 1994. During these penods we marked 275 and 100 birds, respectively. Other birds were marked subsequently as they were captured at their nest. For each adult bird captured we recorded his/her mass and the culmen and ulna lengths. We visited every nest in the sample once a week to check for the presence of the egg or chick. We monitored the survivorship of every chick up to

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13 fledging. We weighed chicks at the nest using a Pesola spring balance (+12.5 g) and measured their culmen and ulna lengths using a measuring tape (+0.5 mm). Since nest disturbance causes chick loss when they are small (less than 20 days old), we started our weekly visits to nests after this age. We also checked for the presence of the chick or egg at the nest from the observation site dunng the behavioral observation sessions (see below). Censuses We estimated the ratio of adult males to females from censuses at the breeding and roosting sites in one daily census immediately before dusk (17:30 h) when a great number of the birds remain perched. We determined adults by their plumage. We counted the number of males and females perched on a branch in a designated area (quadrat) marked by natural references (trees, rocks or paths) at a breeding and roosting site. We alternated the census between the defined breeding and roosting sites. Censuses were performed daily from 25 November 1993 to 13 March 1994, and then, once every two days from 21 March to 14 June 1994. To estimate the duration of the courtship period of the population, we recorded the number of males with the red gular pouch partially to totally inflated at the breeding site. These censuses were performed using the scan sampling method. These censuses of gular pouches were conducted every hour during our behavioral observations from 28 November 1993 to 13 February 1994, except for the period between 31 December 1993 to 17 January 1994 when we recorded it twice a day. We also performed censuses every hour for three consecutive days per week from 16 February to 27 June 1994.

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14 Incubation and Brooding Periods We recorded the presence of incubating adults on nests in a sub-sample of 57 nests. This sample size changed as new nests were added and nests with chicks were dropped to include them in other records. We recorded the presence and identity of the adult at the nest three times per day (0800, 1300 and 1700 h) duhng our behavioral observations (scan sampling). These records began on 25 December 1993 and ended on 27 June 1994. Observations of marked birds We also conducted observations of the presence of marked birds (juveniles and adults) at the breeding site. These observations were opportunistic during our regular behavioral observations. In addition, once per week we walked at dusk around the island looking for marked frigatebirds. Behavioral Observations We observed and recorded the behavior of adults and chicks at the nest. Behavioral observations were conducted from 20 November 1993 to 21 July 1 994. Every observation site was covered by two observers alternating observation sessions every two hours from 0800 to 1 800. We recorded the behavior at the displaying site or nest daily during courtship, incubation and the first 30 days after chick hatching. Then, during the chick-rearing period (from 40 days to 6 months chick age), we observed nests, three consecutive days per week, from 0800 to 1900 h (from 16 February to 20 July 1994). The observation post was located at the top of a building, located 30 to 150 m from the focal

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15 nests. We observed up to 36 nests simultaneously. This large number of nests was possible because we recorded a few specific behavioral categories and because behavioral categories were conspicuous (see below). In addition, every behavioral category was easy to record since frigatebirds are large birds (females are almost 2 m wingspan) and behavioral patterns occurred infrequently. Behavioral Categories Nest-building period Nest-building period includes the nest-construction activities (males bringing nest material and females building the nest) and the copulation period. For every displaying site or nest we recorded (1 ) the presence of the male, and the female at the beginning of every recording session; (2) the time of arrival or departure of each adult or flying chick to and from the nest; (3) every copulation or copulation attempt. "Copulation" is defined as occurring when the male mounts the female's back, wings extended and he orients in the same direction as the female's head. The female extends her neck straight forward and the male touches her neck with his bill and grasps the neck feathers of the female. In this position the male moves backward over the female's back, moves his tail feathers and pelvic zone laterally and pushes the tail feathers of the female to one side. The female lifts her tail feathers and the male moves his pelvis down until his cloaca reaches the cloaca of the female. Cloacal contact lasts only 2 to 4 sec with two or three spasmodic movements of the male. We did not record cloacal contact because the birds' relative position on the nest and vegetation precluded observing this event reliably. (4) We recorded any stick of branch

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16 carried by the male to the nest, which was usually incorporated into the nest by the female. Chick feeding . We recorded every chick feeding that occurred during the day. Feedings were recorded when the chick put its bill into the open mouth of the parent. In every interaction, we recorded the identity (number) and sex of the parent and the identity of the chick involved. Since some unknown amount of feedings occurred at night, I assumed that our chick feeding rates were only estimates of the real feeding rate. Feedings to chicks smaller than 20 days old were very difficult to see, so I excluded them from the analysis. Data Analysis Chick age estimations Since we recorded chick growth after 40 days, the precise age of chicks in our sample was unknown. We estimated the age of the chicks in the sample by interpolation from the culmen length growth curve fitted to chicks of this population in 1991 (Durand 1992). The average estimated age of the chicks in the sample was 40.6 days (SE=2.28, n=43). Chick growth Growth rate was estimated for each chick in the sample from a polynomial function of the form: y=A+Bx+Cx^+Dx^+Ex'^ Where, A, B, C, D. and E represent constants defining the form of the curve, y represents the age of the chick and x represents the variable (mass in grams, culmen length or ulna length in millimeters). Detailed information about

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17 chick growth is analyzed in Chapters 4 and 5. Here I just present descriptive information. Sexinq the chicks Reversed sexual size dimorphism is expressed by the time that chicks fledge: female chicks are larger than males. Sexing a chick was possible from culmen and ulna lengths of fledglings fitted to a discriminant function. Chicks were sexed using a discriminant function calculated for fledglings in this population in 1991 (Durand 1992). The discriminant function was validated using the culmen and ulna length of 18 chicks of known sex (1 1 females and 7 males as determined by laparotomy and disection, Durand 1992). The function was: y=-40.5199+0.12260(culmen length)+0.08955(ulna length); (p<00001) where if y>0 then female and if y<0 then male (Durand 1992). Behavioral analysis A clear temporal pattern of the presence of male and female at the display site in every courting pair and the different duration of nest-building periods per nest precluded my averaging the data on a daily basis taking the laying of the egg as a reference point. Instead, the data were analyzed by dividing the nestbuilding period for each pair in the sample into three equal parts (close to Mating (when the female remained at the displaying site of a particular male), Middle part of the nest-building and the part close to Laying). For simplicity I called these thirds as: "early", "middle" and "late" nest-building period. For every nest in each third of the penod, the time spent by the adults at the nest, the number of sticks carried by the male to the female, the time the adult spent together at the

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18 nest and the number of copulations and copulation attempts, were averaged. Copulations and copulation attempts were sometimes pooled (see bellow). Chick feedings Chick feeding frequencies were calculated in periods of three days per week as recorded in the field (number of feedings per three consecutive days per week). Time at the nest by the adults was estimated for those individuals during incubation only. I used non-parametric tests (Mann-Whitney U, Wilcoxon test and Chi square and Fisher exact probability test) because of the small sample sizes, non-normal distributions, or non-homocedasticity precluded me from using parametric statistics (t-test, oneand two-way ANOVA and Parsons Correlation test). Results The Population View Breeding season The frigatebird breeding season at the Isia Isabel colony began before we arrived at the island in early November 1993. The total reproductive season including courtship, mating, incubation, brooding, chick growth and fledging (up to the flight of the chicks) lasted more than 9 months. Courtship started in early October 1993, the egg-laying period peaked on 10 November (estimated retrospectively from the age of the chicks) and most of the chicks fledged in late July 1994 (30 out of 36 chicks fledged in July). The following breeding season

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19 Started in early November 1994 and ended in late July 1995. This second season started earlier than November but was destroyed by a hurricane that passed through the island in late October 1994. Breeding at the colony was not synchronous as indicated by the extended period of courtship. The courtship period, judged by the number of red inflated gular pouches counted at the breeding site, started in early October 1993 and finished in 7 April 1994, when the last inflated gular pouch was seen. The peak of the courtship penod occurred in December (Figure 1 .2). Probably another peak occurred early in the breeding season before our arrival at the study site. The abundance of adult males and females varied as the breeding season progressed. The number of males perched at a reproductive site outnumbered the number of adult females in November. This ratio decreased to close to one in December and continued to decrease up to June (Figure 1 .3). In June almost all males had left the colony. At the perching site the sex ratio indicated a preponderance of females during the whole season but the number of males peaked in March and then declined again in June (Figure 1 .4). Mating success We observed 154 pairs in courtship. Only 51 pairs (33%) laid an egg for certain and 21 (14%) probably laid an egg based on the behavior of the adults at the nest and their extended courtship period, but the nest failed before we saw the egg. All other pairs (82 cases, 53%) left before laying an egg. Egg survival We observed 68 pairs with an egg (51 observed from mating and 17 added subsequently). Fifty four (79%) of the eggs were lost during the incubation pehod and in only 14 of these cases (21%) we saw the hatchling

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20 before nest failure occurred. The causes of egg loss were unknown, but intraspeclfic interference is common (other males stealing nesting matenal). Chick survival Since most of the pairs we observed during nest building failed to lay an egg during courtship or lost their egg during the incubation period, we added nests with chicks to our sample as we found them. In our total sample of 78 chicks, 38 (49%) died or disappeared from the nest. In nine cases the corpses were found and in 29 cases the chick just disappeared. We do not know the causes of these deaths or disappearances but in 13 cases (43%), the chicks died or disappeared after a continuous period of weight loss. These 13 chicks were 27% below the average mass of the surviving chicks of the same age (SE=3.91 ). In the other 17 cases (57%), chicks were in good condition and some were even 21 % over the average mass of the surviving chicks of the same age (SE=3.52). Adult dispersion I do not have data concerning adult dispersion but my marked birds were commonly seen by fishermen at Islas Marias (60 km East of the island), on the mainland (72 Km) near San Bias in the state of Nayarit, and at Topolobampo, in the State of Sinaloa, Mexico (about 500 km to the North of the Island) where 12 marked birds were seen.

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21 The Individual View Pair formation Courtship occurred during an extended period in the magnificent frigatebird. The courtship period involved two components: the process of obtaining a mate (male displaying) and the process of copulation and nest construction (nest-building period). I concentrated my efforts on quantifying the behavior of the adults during the copulation and nest-construction period and made only qualitative observations during the mate-selection period. As deschbed elsewhere (Diamond 1973), during the male-displaying period, males inflate their scarlet gular pouch while perched on a branch at the top of a tree (displaying site). Females fly over the colony and sometimes hover (remain static in the air for seconds beating their wings) over a displaying male and sometimes land on the branch of a particular male. The arrival of the female to the displaying site starts the nest-buiiding period. Typically, during the first day of the arhval of the female at the perching site, the male continued displaying his inflated gular pouch to other females while the female remained at the displaying site in close physical contact with the male. During the second day, typically males deflate their gular pouch and both adults remained inactive at the displaying site. The displaying site invariably became the nest. From the third day and until egg laying, the male brought nesting material to the female while the female built the nest. It is duhng this nest-building period at the displaying site that the pair copulated. Once the pair is at the displaying site, the site is always guarded by at least one adult during the whole courtship, nest-building, incubation and brooding period. If the nest is left unattended even for seconds, other males immediately take over the site or the nesting material. Both males and females remained at the nest almost 70% of the time during the first part of

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22 the nest-building and copulation period (early period). Then, during the middle and late third of the nest-building period, the male decreased his time at the nest and started to bnng nesting material to the female. During the late third of the nest-building period (close to laying) males and females were observed to spend 45 and 60% of the total day-time at the nesting site. Consistent with this figure, males and females remained at the nest together about 40 percent of the time during the "early" period and then during the "middle" and "late" thirds of the nest-building period, the time at the nest together decreased dramatically. Nest building and copulation behavior A detailed analysis of the copulation frequency and nest building activities is presented in Chapter 2. Nest construction activities peaked during the second third ("middle") of the courtship pehod (between 5 and 8 days before the egg laying). Males brought an average of 1 .3 sticks per day during the nest building period (SE=0.22, n=22) and a total of 17.3 sticks during the whole period (SE=3.55, n=22; Chapter 2). The average individual nest-building period in this colony lasted 13.2 days (SE=0.89, range=7 to 23, n=22) for the sample of nests where we recorded the beginning of the nest building and the egg-laying date. Copulations occurred only at the nest site during the nest-building period. Copulations occurred more frequently during the first and the second third of the nestbuilding period and decreased during the late third (Figure 1 .8). Even though the clutch size is only one egg, these birds copulated on average16.2 times per clutch (SE=2.2, range=2 to 44 copulations, n=22). Copulations occurred only during the day, from very early in the morning to dusk. We did not noticed a

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23 copulation occurring at night even when we spent much time marking animals and weighing chicks. Intraand extra-pair copulation frequency . Frigatebirds copulated with their mate 1.3 times per day on average (SE=0.2, range=0 to 10, n=22) and the copulation frequency peaked 14 days before egg laying and decreased dramatically two days before laying. Extra-pair copulations occurred in at least 8% (12/151) of the pairs observed. Extra-pair copulations occurred at the nest site and almost all occurred during the second part of the courtship period (Chapter 2). Extra-pair copulations occurred when females were visited by other males at the nest. The role of adults during incubation and brooding In frigatebirds the egg is always guarded by one adult. In a small sample of nests in which I recorded accurately both the laying and hatching dates of the egg (n=7), the incubation period lasted 56 days (mean=56.4 days, SE=1.1, range=53 to 61 ). In a more extensive sample of nests in which I knew the laying date but where the hatching date was not accurately recorded, the incubation time was shared almost equally by both male and female. Males were at the nest on average 51 % of the total incubation time (mean proportion= 0.51 , SE=0.0008, n=38). Every adult remained at the nest incubating for periods of 3 days on average before being replaced by the partner (range=<1 to 9 days). Females remained at the nest slightly more time than males before being replaced by the partner but this difference was not significant (males: mean=2.99 days, SE=0.20, range=1 to 6, n=36; females: mean=3.4 days, SE=0.25, range=1 to 7, n=36; Wilcoxon test, T=24.5, p=0.85). Chicks hatched naked and were unable to control their body temperature during the first days of life (Dunn 1975). During the first 10 days of brooding,

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24 adults stayed at the nest and the chick was covered by the adult continuously as the egg had been, and parents shared the care of the chick. I considered this period as an extension of the incubation period because I could not always tell whether the chick was hatched. Chick rearing At 49 days old on average (SE=2.36, n=30, range from 28 to 88 days) chicks remained alone at the nest, but one adult frequently perched near by. At 53 days of age (SE=2.49, n=39, range from 25 to 93 days), adults often left the chick unattended and only visited the nest to feed it. Males deserted chick feeding at vanable times of chick age, ranging from 18 to 161 days (mean=77.1 days, SE=4.98, n=33). This figure includes the last time a male was seen at the nest, not necessarily feeding the chick. Seventy-four percent (31 out of 42) of males deserted during a short period of time during the year (March-April). After male desertion, females fed the chick alone up to fledging (the age of the first flight, 175.6 days for males and 185.0 days for females). In 12 cases chicks continued to be fed nine more months after chick fledging up to independence. Chick feeding was extremely infrequent. They received food only 0.87 times per three-day period during a week on average (SE=0.095, n=28). Males and females contributed to chick feeding of hatchlings but males contributed less frequently than females when they were brooding (Mann-Whitney U=1412, p<0.0001 , n=31 ). Males contributed a maximum of 40% of chick feedings on average at the beginning of our observations (40 days after hatching) but a constant decline occurred up to 161 days of chick age when the last male deserted the nest (Figure 1 .5; see Chapter 3 and 4).

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25 Chick growth, fledging and independence Chicks grew slowly. The average trajectory of male and female growth shows sexual differences at 40 days and until chick fledging (mass, culmen and ulna length; Figures 5.3 to 5.5 in Chapter 5). Near fledging, female chicks were 11.7% heavier, 9.8% larger in culmen length and 5.7% larger in ulna length on average. Sexual differences are analyzed in detail in Chapter 5. Attaining chick independence was a long process in frigatebirds. After fledging, chicks returned to the nesting area to be fed by the female. We recorded 22 (56%) of the fledglings marked in July 1994 (n=39) still present near their nest-area in November 1994; 23 (59%) were recorded present in December 1994. Still, 13 (31%) were present in March and April 1995, respectively. We also recorded 13 (59 %) and 8 (34%) of the chicks being fed exclusively by their mothers in November and December, respectively, when our observations were more extensive. Adult re-mating Unsuccessful adults (adults that lost their chick or egg) rarely attracted another mate or constructed a new nest at the island in the same breeding season. In the next breeding season, 34 (55%) of the successful (adults that rear their chicks to fledging and were alive when we left the island on July 1994) marked adults (n=62) from the previous season were seen again at the breeding site (47% males and 53% females). In all cases marked males were seen the following breeding season at least with the red gular pouch, indicating reproductive condition. Successful females (n= 18) were seen feeding their fledglings during the next breeding season and none of these marked females was recorded to visit a displaying male. In six cases both adults of a successful pair in the previous breeding season were seen at the island near their previous

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26 reproductive site. In each case, the female was feeding the chick and the male was in reproductive condition (red gular pouch). Discussion The Magnificent Frigatebird at the Isia Isabel Information on the breeding biology of the magnificent frigatebird obtained in this study is summarized in Table 1 .1 at the level of the population and at the level of individual pairs. At the level of the population, the colony starts reproduction annually in September-October, immediately after the rainy season and chicks fledge in July-August. The colony is asynchronous and courtship lasts about six months (from early October to March). Male and female adults were abundant early in the season but the proportion of males decreased constantly until they were rare in late April. Nest failure and chick mortality were high; only 17% of the observed nests produced a fledged chick. At the level of individual pairs, copulation and nest building lasted 13 days; pairs copulated 16 times on average. Incubation lasted 56 days. Incubation and brooding was shared equally by male and female parents; chicks were left alone at the nest at 53 days of age on average. After this, parents returned to the nest only to feed the chick once in three days. The time that every adult remained at the nest before being replaced by the mate (attentive period) during incubation and brooding lasted 3 days. Once chicks were able to remain alone at the nest, males deserted. Males deserted when the chick was from 18 to 161 days old, in late March and early April. Chicks fledged and were able to fly at 180 days and

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27 the sex ratio of fledglings was not different from 1:1. Females were seen feeding fledglings from the previous season and males were seen in reproductive condition the next breeding season. Successful males may be able to reproduce annually but successful females only can reproduce biennially. The Effects of Feeding Ecology on the Breeding Biology of Friqatebirds In spite of all the similahties, interesting differences exist among the five frigatebird species. All the species are tropical and subtropical but F. ariel and F. andrewsi are distributed locally whereas F. magnificens, F. minor, and F. aquila are broadly distributed (Nelson 1975). Most of the frigatebirds are pelagic foragers but F. magnificens and probably some populations of F. minor are shoreline foragers (Diamond 1973, Nelson 1975, Calixto 1993). There may be an association between these two types of foraging and frigatebird breeding ecology. Pelagic foragers (1 ) have narrow and specialized diets and, consequently (2) are more synchronous in their breeding; (3) they have longer attentive periods at the nest during incubation and chick rearing; (4) their chicks grow up more slowly; (5) males and females contribute more equally to incubation, chick rearing and chick feeding; (6) the first flight of the chick occurs earlier, but (7) probably the period of post-fledging dependence is longer than for shoreline foragers. The main hypothesis here is that food availability (feeding conditions) could be responsible for the differences in natural history. As demonstrated in Everglades kites (Beissinger 1987), food availability improves the rearing conditions of the adults and in consequence sets the conditions for the desertion of one individual in the pair. Only one study with frigatebirds refers to the abundance of food and the breeding biology of the magnificent frigatebird. The

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28 data are qualitative but show that chick rearing coincides with an increase in food availability (estimated in the number of tons offish captured commercially; Carmona et al. 1995). Males deserted their nests when the chick was between 18 and 161 days old. This range is between the age ranges reported in the literature for frigatebirds (Diamond 1973, Coello et al. 1977, Trivelpiece and Ferrahs 1987, Durand 1992,). However, since males desert during a restricted two-month window of time, this variation is only a consequence of the dates of pairing at the beginning of the breeding season. An analysis of mate desertion and its consequences is presented in Chapter 4. Male desertion has important consequences. Female magnificent frigatebirds are able to rear the chick alone at a rate equal to or faster than growth rates attained by the other species of frigatebirds (Nelson 1975). Successful females are limited to biennial reproduction but successful males and all unsuccessful individuals are probably able to try reproduction the following year. Dependence by the magnificent frigatebird on a rich food supply as compared with that of other frigatebirds may be associated with the ability of females to feed the chick alone for long periods (up to 14 months). Other effects can occur after male desertion evolved. Rearing costs of male and female chicks can vary for the pair and for the deserted females. The consequent increased male-male competition may favor promiscuous activities and increased sexual selection. A cascade of other changes can be expected. Since clutch size is constant in these birds, male emancipation can be a quick response to changes in food abundance. Fregata magnificens is the only species of frigatebird breeding and possibly feeding in less erratic food sources (i.e., at Isia Isabel this bird feeds at shrimp boats) whereas the other four species of the genus breed and probably feed at more pelagic places. A broad diet reported in magnificent

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29 frigatebirds (Calixto 1993), feeding areas that are closer to the coast, shorter attendance periods at the nest, higher chick growth rate, suggest the dependency of this species of frigatebirds on a more abundant and, perhaps more predictable food supply. The long reproductive period of the frigatebirds is the consequence of a long period of courtship, nest-building, incubation, chick feeding and post fledging dependence. This bird is dependent usually on highly dispersed and fluctuating food resources. However, at this locality (Isia Isabel), it seems that the ability of birds to obtain food from shrimp boats could be responsible for the large size of this colony. The Isia Isabel colony is one of the largest colonies reported to date with the exception of the Santa Margarita island population (Moreno and Carmona 1988). Santa Margarita Island is located in a highly productive zone near the California current, in Baja California Mexico. Chick grovi^h also appears consistent with the dependence of these frigatebirds on sparse, fluctuating and scarce food resources. Chicks grew very slowly compared with other seabirds of similar mass. However, compared with other frigatebirds, the magnificent frigatebird chicks grew faster (Nelson 1975, Diamond 1973). Probably again, this could be atthbuted to the dependence of these birds on more abundant and predictable food souces close to the island (shrimp boats; Calixto 1993). When chicks become independent is not known and is still not known after this study. However, my observations on marked juveniles suggest that independence rarely occurs before nine months after fledging; i.e. at 15 months of chick age. This prolonged period of partial or total dependence could be related to the acquisition of difficult feeding techniques of these birds and the dependence of frigatebirds on unpredictable food sources, as speculated by several authors (Diamond 1973, Nelson 1975).

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30 Even though the colony is not synchronous in their breeding (the courtship pehod extended for almost 6 months), the colony is clearly annual. Every year after the high rainfall season (late May to August), the population starts a new reproductive cycle. In fact there is a strong effect of the season on the survival and grov^^h of the chicks from parents that settled early and late (see Chapter 4). Not all individuals, however, are able to re-mate annually. Floating and unsuccessful individuals from the previous breeding season and successful males could attempt annual reproduction. However, successful females feed chicks for more than nine months after fledging and are constrained at least to biennial reproduction. As seen at other colonies of the magnificent frigatebird, at Isia Isabel males abandoned nests and left the island as the breeding season progressed (Figures 1 .3 and 1 .4). Males were as abundant as females during the beginning of the courtship period, but as the breeding season progressed their abundance decreased to a point such that in July it was difficult to see a male at the island. It is interesting that the most intense drop in the abundance of males occurred during April-May, suggesting that most of the males left the island during that period. This finding also coincides with the time that males of the successful nests deserted from the nest (see Chapter 4). I do not have good data about adult dispersion. However, I received reports from fisherman of several marked birds flying almost 500 Km to the N of the island, 60 Km to the SW , 72 Km to the NE and 120 Km to the SE. Some of these ranges overlap with known reproductive colonies of this bird. At Isia Isabel, birds tended to remain close to the site where they were marked and did not move elsewhere on the island if they failed in the current reproductive effort. In our weekly walks around the island looking for marked birds, we only rarely saw marked birds perched outside the breeding site.

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31 As noted by Diamond (1975), copulation takes place without obvious preliminaries and brief head waving frequently follows. The copulation pattern is unexpected based on available information about egg fertilization. According to the literature in chickens and other birds, the fertilization window is about 24 hours prior to egg laying (Birkhead and M0ller 1992). Therefore, one would expect that only few copulations one day before egg laying should be sufficient to fertilize the one egg produced by the female. However, frigatebirds copulate about 13 times to fertilize that one egg and the peak of copulations occurs during the first two thirds of the courtship period, eight days prior to the egg laying, rather than close to egg laying. The possible significance of the copulation pattern is discussed in Chapter 2. As in other species of frigatebirds, incubation in F. magnificens is long, 56 days. Both male and female shared the incubation and brooding duties almost equally. Although long attendance periods during incubation were even smaller in F. magnificens than the ranges reported for F. minor and F. ariel. As described in other populations of the magnificent frigatebird, these birds are socially monogamous in one reproductive cycle. We never saw a mated individual incubating and brooding more than one nest in the same breeding season, and only seven males (out of 230 pairs) mated sequentially in the same breeding season after a failure. However, since males begin a new breeding cycle while their mate is still feeding the chick, the pair-bond is not maintained for more than one season. Over the long term, the system could be considered sequential monogamy (Gowaty 1985). In spite of this one-season monogamy, extra-pair copulations occur (See Chapter 2). Since the social bond appears to be monogamous while individuals are sometimes copulating with other mates, the system is only "apparently monogamous" (Gowaty 1985). The

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32 consequences of these extra-pair copulations has not been explored. In this dissertation some hypotheses are discussed (Chapter 2). Clear reversal of sexual size dimorphism is seen in male and female fledglings. Females were between 6 and 11% larger than males at the age of the first flying, However, in spite of this dimorphism, males and females developed at the same growth rate and reached the asymptotic size at the same age (Chapter 5). This suggests that males and females fed with similar frequencies must have processed the food differently and used the same energy in different ways to attain different sizes at the same time (see Chapter 5). Alternatively, my methods or sample size may have been insufficient to detect differences between males and females. A female-biased sex ratio at fledging was found in one population of frigatebirds in the Caribbean sea (Diamond 1972) and a similar bias was found in a population from the Galapagos islands (Coello et al. 1 977). I did not find a female-biased sex ratio in my sample (Chapter 5) nor was a bias found in this populations three years ago (Durand 1992). Diamond speculated that excess numbers of fledged females was a strategy connected with different breeding rates of males and females in this species of frigatebirds (Diamond 1972). If males are reproducing more frequently than females, it could be advantageous for individuals to produce more females he argued. However, since the benefits of the extra-production of male and female offspnng is clearly frequency dependent, this explanation is not likely to be an explanation for the propagation of wide sex-ratio bias. A broader discussion about sex ratios is presented in Chapter 5.

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33 Causes of Chick Mortality As described in other colonies, mortality rates are very high in these birds. Considering that only 40 nests were constructed out of 230 pairs that started courtship (including here those nests added to the sample with an egg or chick), only 17% of the breeding attempts produced a fledged chick. This is nearly the figure established in other populations and even other species of frigatebirds (Nelson 1975). I do not know the sources of chick death or nest failure in most cases, but cats introduced to the island at least 40 years ago, strong winds, intraspecific interference, and our own presence, were observed as causes of nest abandonment, death of chicks, nest disappearance and egg loss. The main cause of egg loss, however, was intra-specific interference. Other males stealing nesting material frequently resulted in eggs dropping to the ground. Our activities also provoked some egg loss and some unknown and unestimated nest desertion. Cats preyed upon frigatebird chicks immediately after hatching to almost fledging. We saw three instances in which a cat was in the tree branches immediately behind a nest containing a chick. In one other case, a mother cat was seen bringing a dead chick to her kittens. In other cases, one healthy marked fledgling (hand-reared) was clearly preyed upon by a cat. We only found the wings of this bird with fresh flesh remains. Small unattended chicks were more likely to fall from the nest. Fishermen at the island reported a high rate of chicks falling down from nests (up to five chicks falling down from nests in just one day). We have one clear observation of an adult male removing a small unattended chick from the nest and throwing it out of the nest. This behavior has been observed also in F. arlel (Dill 1916). We do not have a clear idea of how frequent this intra-specific interference occurs and its

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34 possible function. In the observed case, after chick removal the nest was abandoned and not used by another bird. In summary, the breeding biology of the magnificent frigatebird is markedly different from the other species of frigatebirds. Fregata minor appears to be an intermediate between the extremes. A clear association between the geographic distribution and feeding places, diet and probably food abundance seems to be associated with the adjustments in natural history. Food abundance and predictability may increase the feeding abilities of males and females in the magnificent frigatebird and produce a cascade of changes in breeding frequencies, rearing costs, breeding synchrony, chick growth and mating competition. Still more detailed studies should be conducted to test predictions from this speculation.

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35 Table 1.1 Comparative breeding biology of the five species of frigatebirds including this study. Variable F. minor F. aquila F. ariel F. magnificens F. andrewsi Dimorphism: Female/male weight ratio Laying period Egg weight (% of female's weight) Incubation period (days) Role of sexes feeding the chick 1.18-1.28 depending on the locality February-April 85 g (5.2%) 55 shared role up to chick independence but females give more feedings in some colonies 1.14 about 1.14 September-November August-November 75.8 g (6%) 44 shared role up to chick independence 59 g (6.9%) unknown shared role up to chick independence 1.23 OctoberJanuary, October-March unknown 56 (SE=1.1) shared role until 1 -3 months, then female feeds the chick alone. But males desert in March-April 1.11 April-June 82 g (5.3%) 54 (estimated) shared role up to chick independence Attentive period at nest during incubation Age when chick is left unattended Growth rate Weight at week 7 (grovirth rate, g/day) Feeding rate Fledging period Post-fledging dependence 9.5 to 11 .5 days 31 days 980 g (Aldabra) (19.28); 390 g (Galapagos) (7.14) once every 3 days 24 weeks at)out 9 or more months Fledgling sex ratio 1 male to 1 female Breeding success (# initial nests/# nests with fledged chicks) Breeding habitat Breeding periodicity of successful individuals 19% pelagic and some coastal colonies presumed biennial; under special circumstances 18 months unknown atKJUt 35-40 days 680 g (12.8) unknown about 20-24 weeks not-recorded unknown about 15-20% pelagic annual; not well established 2 to 6 days about 35 days 390 g (7.14) once every 2.4 days 20 weeks at least 4 months; probably longer unknown about 15-20% pelagic unknown; suspected biennial 1 to 9 days (mean=3.2 days) 49 days (SE=2.36) 750 g (16.4); 721 g (15.07 at Isia Isabel) once every 3 days 26 weeks more than 9 months 1 male to 1 .8, 1 5 and 1 females in different colonies about 17% coastal female probably biennial; male annual 2 to 3 days about 45 days 540 g (12.8) once every 2 days 24 weeks up to 9 to 10 months unknown about 30% pelagic biennial Information based on Nelson's review (1975) but complemented wXh information from Coello et al. (1977), Moreno and Carmona (1988), Reville (1988), Trivelpiece and Ferraris (1988), Schreiber and Schreiber (1989) Durand (1992) and Howell (1995) and this study.

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36 POPULATION SCALE COURTSHIP EGG LAYING INCUBATION CHICK REARING FLEDGING SEPT OCT NOV DEC JAN FEB MAR APR MAY JUN JUL AUG SEPT ~0 30 60 90 120 150 180 iTo 240 270 300 330 350 TIME COURTSHIP ^_ (days) NESTBUILDING AND GOPUUMION INCUBATION BROODING AND CHICK REARING POST-FLEDGING FEEDING INDIVIDUAL SCALE Figure 1.1 Schematic representation of the typical frigatebird breeding from the point of view of the population and the individual. Curves represent the frequency of nests in that activity. Lines represent the duration of the activity for a hypothetical pair.

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37 a I o 0) E o Q (0 c re u. a < 17 I ra 15 t c 3 Figure 1 .2 Number of male magnificent frigatebirds displaying (mean ± SE) at the breeding colony. Numbers close to the squares are sample sizes (number of observations per month). July-October no males are present.

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Figure 1.3 Adult operational sex ratio per day (male/female) at the reproductive site (mean ± SE) as a function of the time of the year. Numbers close to the squares are sample sizes (number of observations per month).

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39 I 12 (U E > o z 0) E a> u 0) Q n 3 C 3 n u (0 a < 0) c 3 Figure 1 .4 Adult sex ratio per day (male/female) at a roosting site (mean ± SE) as a function of the time of the year. Numbers close to the squares are sample sizes (number of observations per month).

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40 Figure 1 .5 Feeding frequency (mean ± SE) of male and female adults as a function of the chick age. Sample size was 38 nests. For males sample size dropped as they deserted. Observations started at 40 days on average.

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CHAPTER 2 A TEST OF THREE HYPOTHESES TO EXPLAIN THE FUNCTION OF THE INTRA-PAIR COPULATORY PATTERN IN THE MAGNIFICENT FRIGATEBIRD Introduction Multiple copulations are common in many species of birds. In some species, females copulate with several males (extra-pair copulations), but in others, females copulate repeatedly with the same partner (intra-pair copulations). Extra-pair copulations have clear advantages for some males and some advantages have been suggested for females (Westneat et al. 1990, Birkhead and Moller 1992). However, evidence of advantages to females are more theoretical than empirical (Lifjeld et al. 1994). Multiple intra-pair copulations, on the other hand, are puzzling. Since only one ejaculate contains a huge number of sperm cells, enough to fertilize all the mature follicles produced by the female, it is not clear why individuals copulate frequently with the same partner. Furthermore, considenng that multiple intra-pair copulations could involve costs (increased predation risk, time invested that could be used for extra-pair copulations, risk of sexually transmitted diseases, etc.) affecting Darwinian fitness without the benefits of mating with several partners, it is difficult to explain frequent intra-pair copulations. Two aspects of the multiple intra-pair copulations are interesting: frequency and peak in relation to the laying date. I refer to both of them here as the "copulatory pattern". Several hypotheses have been suggested to explain 41

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42 diversity in copulatory patterns (Birkhead 1989, 1991, Petri 1992, Hunter et al. 1993, Birkhead and Moller 1993). Some of them have been tested using the comparative approach (Birkhead et al. 1987), but this problem has been rarely scrutinized experimentally (Petn 1992, Hunter et al, 1993). In this study I first present alternative hypotheses and then evaluate them based on a study of the magnificent frigatebird (Fregata magnificens). Hypotheses to Explain Multiple. Intra-Pair Copulations The Fertilization Hypothesis The Fertilization Hypothesis states that multiple, intra-pair copulations are the way for a female to insure that all follicles are inseminated (Hunter et al. 1993). Since birds do not normally have an intromittant organ (with some interesting exceptions in 2% of species; Birkhead and Moller 1992), copulation would seem to be a very difficult task; copulation occurs in a short period of time and in a very unstable posture. It could be important to copulate several times in order to reduce the incidence or risk of egg infertility. In addition, because of sperm depletion in males (Birkhead 1989, 1991), not all successful copulations result in sperm transfer. Under this hypothesis, the risk of insemination failure is reduced by frequent copulation (Birkhead 1991). Conflict of interest Copulations are necessary for reproduction in sexual species but, given its consequences on fitness, copulations may be manipulated by one sex. The Fertilization Hypothesis suggests no conflict between males and females, i.e. both agree on the frequency of intra-pair copulations. However, since different selective pressures clearly act on males and females, a large group of

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43 hypotheses can be denved based on different benefits to males and females. I include here two vanants: the Stimulation-Assessment Hypothesis (Hunter et al. 1993) and the Sperm Competition Hypothesis (Birkhead et al. 1987). Conflicts of interest can result in an evolutionary arms race (Dawkins and Krebs 1979, Lifjeld 1993). Mate guarding, female sperm expulsion and aggression during copulation, forced copulations, female solicitation, may all be the evolutionary outcome of sexual conflict. Ecological conditions, asymmetries in payoffs, power or information, alternative strategies or differences in costs to individuals could determine who is "winning" the conflict. The Stimulation-Assessment Hypothesis The Stimulation-Assessment Hypothesis (a mechanistic hypothesis), suggests that multiple intra-pair copulation stimulates females to ovulate (Hunter et al. 1993). This mechanism is well known in mammals (e.g. mice: Estep 1973, 1975, Gray 1974). In birds the Stimulation-Assessment Hypothesis has been suggested as a mechanism for maintaining the pair-bond. This is an explanation for copulations occurring without sperm transfer or outside of the fertile period of the female. Female stimulation and pair bond manteniment are mecanistic explanatins. A functional interpretation of this hypothesis has not been proposed for birds, but some adaptive advantages for females could be attributed to this mechanism (e.g. female ovulation threshold correlated with male quality; Moore and Moore 1988). Although stimulation duhng the courtship period is only known in doves and few other species of birds (Birkhead et al.1987, Birkhead and Moller 1992), it is common in mammals, so this hypothesis is actually a possible alternative explanation for multiple, intra-pair copulation.

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44 From the point of view of the female, multiple copulations can allow her to evaluate the quality of the male or his condition if a female is stimulated to produce an egg only after a high rate of intra-pair copulation (suggested in Westneat et al. 1990). This hypothesis assumes that the copulation rate is correlated with male quality and/or male condition. The prediction here is simply that copulation rate is correlated with egg production and male quality: if the rate of copulation is poor, there should be a high incidence of nest failure before egg laying. The Sperm Competition Hypothesis This hypothesis is derived from an argument similar to those used to explain mate guarding: under some ecological conditions (food sources far from the nesting place and where the nest site must be guarded by the mate) that constrain males to stay with the mate, males will act to protect their paternity. Predictions from this hypothesis have been confirmed in tree swallows (Venier and Robertson 1991), northern fulmar (Hunter et al. 1992) and northern harriers (Simmons 1990), but the ecological conditions are particularly approphate for mahne birds (Birkhead et al. 1987). The Sperm Competition Hypothesis states that repeated copulation with the same partner could have sources of benefit for the male and female. For males the possible benefits could be to increase their paternity (Paternity Assurance Hypothesis, Birkhead et al. 1987) (1) by devaluing the sperm of other males (dilution effect), or (2) by being the last individual to copulate with a female under the last male precedence mechanism (see below) or (3) by reducing the time available for females to look for extrapair copulations, i.e. a type of mate guarding by the male through copulations. Benefits for males are obvious but females can benefit from frequent intra-pair copulations (1) by increasing male paternity confidence and consequently (a) by

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45 securing immediate material benefits (food, nest material) or (b) future benefits (parental care, territory, protection); (2) by guarding the male (by depleting the sperm of males, and the time and motivation for extra-pair copulations) or to avoid mate loss (Petri 1992, Hunter et al. 1993). Hypotheses to explain the peak of copulations Several hypotheses have been formulated to explain why birds stop copulating when the female is still fertile (Birkhead and M0ller 1993). However, only three of these apply to a single egg species like the magnificent frigatebird: (1) males are unavailable to copulate because they are engaged in extra-pair copulations (this is an alternative of the female mate-guarding hypothesis of the previous section); (2) eggs are no longer available to fertilize as laying approaches; (3) copulation may cause damage to the unlaid egg. In these hypotheses it is assumed that the fertilization period concludes about 24 hours before egg laying. This assumption is problematic in a species laying only one egg like frigatebirds since the fertile period is not easy to estimate in the absence of a second egg . Here I use hormon analysis in an attempt to estimate the fertile period of female frigatebirds. Determining the female's fertile period For some hypotheses copulation is expected to correspond with the fertile period of the female (the period when the mature follicle is ovulated and is susceptible to being fertilized). However, in a number of species, pairs copulate a long time before the beginning of the egg-laying period, indicating that most of these copulations occurred outside the fertile period of the female (Birkhead and M0ller 1992). In addition, clear information about fertilization time and fertile period is largely unknown in wild birds (Birkhead and M0ller 1992). In most

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46 Studies, the fertile period of the female has been assumed or it has been estimated only from the laying date (Birkhead et al. 1987, Birkhead and Moller 1992). Establishing the real fertile pehod of the female is important for evaluating predictions (Hunter et al. 1993). The physiology of fertilization in birds indicates that the release of the mature follicle by the female occurs approximately 24 hours before laying and fertilization occurs during the first hour after the egg is released (Birkhead and M0ller 1992). Depending on the clutch size and the laying interval, the fertile period could extend from 24 hours to three days before the last egg is laid (Birkhead and Moller 1992). Particularly for seabirds that lay only one egg, intervals between ovulation and fertilization are unknown. The fertile period of females could be extended by sperm storage structures in the female's reproductive tract (Birkhead and Moller 1992). These structures are small tubules located between the uterus and the vagina (Birkhead and Moller 1992). Sperm storage structures have been found in every species that has been analyzed to date, and it is possible that sperm storage structures occur in all birds (Birkhead 1994, Birkhead and Moller 1992). Sperm viability is extended up to eight days in ring doves and 42 days in turkeys before egg laying due to these sperm-storage structures (Birkhead and M0ller 1992). The sperm-storage structures are thought to have evolved as a consequence of the interaction between male-male competition and sperm selection by females inside their reproductive tracts (Westneat et al. 1993). In any case several studies indicate that the existence of these storage structures results in more complex effects of copulations and fertilizations (Birkhead 1989, 1991, Westneat 1996). An experimental study in mallards {Anas platyrhynchos), for example, demonstrated that there was a preponderance of the last insemination siring the progeny (Cheng et al. 1 983). This evidence suggests that the most probable

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47 mechanism of sperm release from the storage structures is inversely related to the deposition order (last sperm precedence). Sperm-storage structures extend the fertile penod of the female and introduce vahable conditions that will affect the evolution of different copulatory patterns depending on how these structures work (Westneat 1996). Predictions From the Hypotheses Applied to the Magnificent Frigatebird. I describe in this Chapter the copulatory behavior of the magnificent frigatebird {Fregata magnificens). By disrupting copulations, I experimentally tested the predictions of the Fertilization, Stimulation and some forms of the Sperm Competition Hypotheses for this species. The Fertilization Hypothesis states that high intra-pair frequency of copulation insures egg fertilization. The main prediction from this hypothesis is that (1 ) experimentally disrupted pairs with a low copulatory rate will have a higher incidence of egg infertility than controls with high copulatory rates and (2) copulations will take place only during the fertile period of the female. The Stimulation-Assessment Hypothesis in the form used here states that only high rates of intra-pair copulations will stimulate the female to produce a mature follicle. Predictions from this hypothesis are that: (3) copulations occur before and during the fertile period of the female, and (4) experimentally disrupted individuals with the lowest intra-pair copulatory frequency will have a low incidence of egg laying (high incidence of laying failure). This hypothesis assumes that cloacal contact is the stimulus that induces ovulation although this is not known for certain. The Sperm Competition Hypotheses indicate that in a population with strong mate competition, where individuals perform long feeding travels and where extra-pair copulations occur, males will increase their

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48 probability of fathering offspring by copulating repeatedly with the same mate, thus reducing the possibility of being parasitized by other males. Two forms of this paternity protection are (a) to dilute the sperm of other males or (b) to copulate frequently to reduce the time available for the mate to engage in extrapair activities (mate guarding). Since I do not have information on paternity, I tested here only the second possibility. I predict that (5) if extra-pair copulations occur, their incidence will be higher in experimentally disrupted pairs (copulation disrupted) than in control nests (disrruption out of copulation). Females may benefit from repeated intra-pair copulation. If females are to benefit from short-term (immediate) material benefits in the form of nesting material, for example, I expect that (6) in experimental nests with low copuiatory rates, males will deliver lower rates of nesting material to females; if females are guarding the males by copulating frequently then (7) the incidence of nest failures will be greater in experimental nests than in control nests. In frigatebirds copulations peak 6 days before egg laying (see description). I suggest here that the decline in the frequency of copulations prior to egg laying in frigatebirds is due to the egg already being fertilized some pehod of time before laying, i.e. that the female is no longer fertile. This hypothesis assumes some cost of continuing to copulate for males and females (i.e. damage to the fertilized egg) and no additional benefit. The prediction from this hypothesis is that (8) when copulation drops, the egg is inside the uterus of the female.

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49 Methods The Description of the Copulatory Pattern The descriptive part of the study was conducted from 1 5 November, 1 993 to 10 March 1994. We (my assistants and I) marked every accessible nest or display site and the adults mating there with plastic numbered tags as soon as I recorded a pair in courtship. A display site was a branch at the top of a tree where a male perched while showing his inflated red gular pouch. We captured a displaying male (i.e. a male with the red gular pouch inflated or deflated) or a pair of adults (male with the red gular pouch and female) standing at the displaying site. Birds were captured by hand at night when they were at the nest and marked with 3-digit numbered wing tags. I marked nests and birds at night because frigatebirds are very sensitive to day-time disturbance. During the day when a frigatebird is disturbed at her/his nest, immediately other individuals, especially males, arrive at the site and try to steal the nest or nesting material. We observed and recorded the behavior of adults and chicks at the nest. Behavioral observations were conducted from 20 November 1993 to 10 March 1994. Every observation site was covered by two observers alternating observation sessions every two hours from 0800 to 1800. The observation site was located at the top of a building 30 to 1 50 m apart from focal pairs. We observed up to 36 nests simultaneously. This large number of nests was possible because we recorded a few specific behavioral categories and because behavioral categories were conspicuous (see below). In addition, every behavioral category was easy to record since frigatebirds are large birds (adult females are almost 2 m wingspan) and behavioral patterns occurred infrequently.

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50 Behavioral categories For every displaying site we recorded (1 ) the presence of the male and female at the beginning of every recording session: (2) the time of arrival or departure of each adult to and from the nest; (3) every copulation or copulation attempt. "Copulation" is defined as occurring when the male mounts the female's back, wings extended and he orients in the same direction as the female's head. The female extends her neck straight forward and the male touches her neck with his bill and grasps the female's neck feathers. In this position the male moves backward over the female's back, moves his tail feathers and pelvic zone laterally and pushes the tail feathers of the female to one side. The female lifts her tail feathers and the male moves his pelvis down until his cloaca reaches the cloaca of the female. Cloacal contact lasts only 2 to 4 sec with two or three spasmodic movements of the male. We did not record cloacal contact because the bird's relative position on the nest and the vegetation around precluded observing this event clearly. "Copulation attempts" were scored when the male's tail feathers were not seen to drop down or when the female did not lift her tail feathers precluding cloacal apposition. (4) In addition we recorded the frequency of visits by the male to the nest carrying nesting material. Experimental Design Manipulations were performed from 28 November to 27 December 1994. Chick hatching and chick presence were recorded from 28 March to 10 April 1 995. We observed the behavior of the adults at every nest in the sample daily from 0800 to 1800 h from a distance of 5 to 20 m. Adults were not individually marked to avoid disturbance during courtship which often caused nest-site

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51 abandonment. We marked some individuals by spraying paint from a distance of at least 1 m from the nest. The egg laying date was checked by the presence of the egg at the nest during the observation sessions and during visits to the nest by lifting up the incubating adult. We used the same behavioral categories as described above. We interrupted most of copulations experimentally in 22 nests. Copulations were interrupted by shooting water at pairs initiating copulation. Using a water gun, I directed water shots to the male when he was on the back of the female, immediately before copulation took place. When the water was shot, males flew away from the nest while females remained at the nest. This reaction was very important because when both adults flew away from the nest some other adult, usually another male, took over the nest. Controls consisted of 8 nests where males were shot when they were at the nest with the female but not in any copulatory interaction. As in the experimental treatment, control males flew as a response to the water shot and females stayed at the nest. For the analysis, I considered interrupted copulations of experimental nests the same as a copulations in conrtrols. Female's fertile period I tried to estimate the fertile period of the female based on the concentrations of steroid hormones in the blood of 15 females. A longitudinal blood sample (sequential samples from the same individuals) was very difficult to obtain without unacceptably high levels of disturbance to females. As an alternative, I sampled blood from different females during the copulation period and I recorded their laying dates. The fertile period was estimated from concentrations of estradiol and testosterone hormones in 30 blood samples obtained from a group of females at known moments before egg laying (females

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52 were outside the experimental sub-colony). Estradiol is a hormone commonly associated with ovulation. It usually peaks immediately before the release of the mature follicle (Bluhm 1988). Circulating concentrations of hormones were evaluated using the radioimmunoassay protocol (RIA, Guillette et al. 1996, Guillette et al. submitted). This technique uses radiolabeling to quantify the amount of unknown antigen and is based on competition between known and unknown amounts of antigen for antibodies specific for the hormone assayed. For testosterone determination, frigatebird plasma (50 |il; all samples were performed in duplicate) was extracted twice with ethyl ether to remove the lipophilic steroids. After drying the sample, ether extracts where filtered with low humidity air and the samples were resuspended with 100 i^l borate buffer (0.5 M, pH 8.0). Androgen antibody (100 |il; final dilution 1:36,000), BSA/borate buffer (100 0.5 M borate buffer, 7.5% BSA), and radiolabeled testosterone (100 |il of 9000 cpm; TRK 402; 102 Ci/mmol; Amersham Life Science Inc., Arlington Heights, IL) were added and the tubes were vortexed and incubated overnight at 4° C. Bound-free separation was accomplished by adding 500 |il of 5% charcoal/0.5% dextran and centrifuging the tubes for 30 min at 2,000 1 The supernatant was decanted, diluted with a scintillation cocktail and counted on a Beckman LS 5801 scintillation counter. Concentrations were estimated by commercially available software (Beckman Instruments). For estradiol determination, 50 i^l of plasma was extracted twice with ethyl ether. Estradiol antisera (E26-47; Endocrine Sciences, Calabasas Hills, CA) was used at a final concentration of 1 :95,000. Cross-reactivities of this antisera to other ligands are as follows: estrone, 1.3%; estriol, 0.6%; 16-keto-estriol, 0.2%; all other ligands < 0.2%. Estradiol label (TRK.587; Amersham International, Arlington Heights, IL) was used at 10,000 cpm per tube. To reduce non-specific binding, bovine serum albumen was added at a final

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53 concentration of 1.5%. Antisera, label, and BSA were diluted in assay buffer (0.5 M borate buffer, pH 8,0 with 10 N NaOH). To determine the presence of the egg inside the female's reproductive tract (uterus) prior to egg laying, I felt for the egg by introducing a gloved finger into the female's cloaca. Data Analvsis Behavioral analvsis. A clear temporal pattern of the presence of the male and female at the display site in every copulating pair and the different duration of nest-building periods per nest precluded my averaging the data on a daily basis or taking the laying of the egg as a reference point. Instead, the data were analyzed by dividing the nest-building period (during nest construction when copulations occurred; see Chapter 1 ) into three equal parts for each pair in the sample (close to Mating, Middle part of the nest-building period and close to Laying). For simplicity I called these: "initial", "middle" and "late". For every nest in each third of the nest-building period, the time spent by the adults at the nest, the number of sticks carried by the male to the female, the time the adults spent together at the nest and the number of copulations and copulation attempts were averaged. I averaged the occurrence of the behavioral categories per nest and then I averaged the means. When copulations and copulation attempts were pooled it is mentioned in the text.

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54 Statistical analysis . I used non-parametric tests (Mann-Whitney U, Spearmann Rank Correlation and Fisher's Exact Probability Test) since samples were small and not normally distributed. I tested specific predictions derived from the hypotheses by using one-tailed statistical tests at a 95% confidence limit. Results The Copulatorv Pattern in the Magnificent Frigatebird: The Descriptive Approach Typically, during the first day of the arrival of the female at the displaying site, the male continued displaying his inflated gular pouch to other females while the female remained at the displaying site in close physical contact with the male. During the second day together, typically males deflate their gular pouch and both adults remained inactive at the displaying site. The displaying site invariably became the nest site. From the third day and until egg laying, the male brought nesting material to the female while the female built the nest. It is during this nest building period at the displaying site that the pair copulated. Once the pair is at the displaying site, the site is always guarded by at least one adult during the whole courtship, nest-building, incubation and brooding period. If the nest is left unattended even for seconds, other males immediately take over the site or the nesting matehal. I observed this dozens of times. Both males and females remained at the nest almost 70% of the time during the first part of the nest-building and copulation period (initial). Then, during the middle and late third (laying) of the nest-building period, the male decreased his time at the nest and started to bring nesting material to the female (Figure 2.1 ). Duhng

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55 the last third of the nest-building period (close to laying) males and females were observed to spend 45 and 60% of the total day-time at the nesting site. Consistent with this figure, males and females remained at the nest together about 40 percent of the time during the "initial" period and then during the "middle" and "late" periods, the time at the nest together decreased dramatically (Figure 2.2). Nest building and copulation behavior. We observed 22 nests from the beginning of the nest building and copulation period to egg laying in 1993-1994 breeding season. Nest construction activities peaked duhng the second third (middle third) of the whole nest-building penod (between 5 and 8 days before the egg laying; Figure 2.3). Males brought an average of 1 .3 sticks per day during the copulation and courtship period (SE=0.22, n=22) and a total of 17.3 sticks during the whole period (SE=3.55, n=22). There was a weak but significant association between the number of sticks brought by the male and the number of copulations (Spearmann Rank correlation r=0.32, p=0.009, n=66). I used here an extensive sample of nests where the number of copulations and the rate of bringing nest material by the male was recorded, but where no egg was necesarily laid. Intra-pair copulation frequency . During the nest-building pehod copulations occurred only during the day, from very early in the morning to dusk. We rarely noticed a copulation at night even when we spent much time marking animals and weighing chicks at night. The average individual nest-building period in this colony lasted 13.2 days (SE=0.89, range=7 to 23, n=22) for the sample of nests where we recorded the beginning of the nest building and the egg-laying date. Copulations occurred only at the nest site duhng the nestbuilding penod. Copulations occurred more frequently during the first and the

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56 second third of the nest-building period and decreased during the last third (Figure 2.4). Even though the clutch size is only one egg, these birds copulated on average16.2 times per clutch (SE=2.2, range=2 to 44 copulations, n=22). Frigatebirds copulated with their mate 1 .3 times per day on average (SE=0.2, range=0 to 10, n=22) and the copulation frequency peaked 6 days before egg laying and decreased dramatically two days before laying (Figure 2.4). Intra-pair copulation attempts occurred on average 3.4 times per clutch (SE=0.79, range=0 to 13 attempts per nest, n=22). Extra-pair copulation frequency . Extra-pair copulations occurred in at least 8% (12/151 ) of the pairs observed. In a restricted sample where we knew the laying date (n=26 nests), the proportion of nests where at least one extrapair copulation occurred was 11% (3 extra-pair copulations in 26 pairs). Extrapair copulations occurred at the nest site and almost all occurred during the second part of the courtship period. Extra-pair copulations occurred 6, 14 and 18 days before egg laying and in no case was the extra-pair copulation the last copulation before laying. Extra-pair copulation attempts occurred at similar frequency to the extra-pair copulation rate (4 in 26 pairs). Experimental Results Control and experimental nests Shots from water guns were a good technique to discourage copulation in experimental nests. Not all copulations were interrupted in experimental nests. We interrupted 88% (388) of all (441 ) copulations recorded in 22 experimental nests. Copulations in control nests were 9 times more frequent than in experimental nests (Figure 2.5). Dunng the nest-building period males stayed at nests with females only for short periods of time if they were not copulating. As

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57 a result, control nests were necessarily shot with water at a lower frequency than experimental nests (Figure 2.5). Water shots did not influence the nest-building behavior and copulatory period of experimental nests, compared with controls. The frequency and rate of sticks brought by the male to the female for nest construction in those nests where the egg was laid (13 experimental and 6 control), did not vary between experimental and control nests (experimental frequency=71.85 sticks, SE=16.16, n=13: controls: frequency=46.33 sticks, SE=8.46, n=6, Mann-Whitney U=33.5, p=0.64 two tailed test; experimental rate=5.63 sticks per day, SE=1.17, n=13; control rate=5.30 sticks per day, SE=1.7, n=6, Mann -Whitney U=36.00, p=0.83; two-tailed test). Fertilization Hypothesis Although we interrupted 88% of copulations in experimental nests, there was a higher proportion of nests with a live chick in March in experimental (8/13) than in control (1/6) nests (Fisher Exact Test, p=0.14, two-tailed test; Table 2.1). This result contradicts the prediction of the Fertilization Hypothesis. Stimulation-Assessment Hypothesis The proportion of females that laid an egg at experimental nests (59%) was not different from the proportion in control nests (75%; Fisher Exact Test, p=0.34). In addition, the copulation rate (copulations in controls or interrupted copulation in experimental nests per day per nest) was not higher in experimental than control nests (Experimental: mean=1.74, SE=0.17, n=13; Control: mean=2.25, SE=0.35, n=6; Mann-Whitney U=29.5, p=0.21, n=13, 6). Also, egg laying was not more delayed in expehmental (mean=12.5 days, SE=0.7, n=13) than in control nests (mean=10.7 days, SE=1.9, n=6; Mann-

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58 Whitney U= 27, p=0.17). These results are inconsistent with the predictions from the Stimulation-Assessment Hypothesis, The Stimulation-Assessment Hypothesis implies that high copulation rates (copulations per day) stimulate egg production in females. There was a significant association between the proportion of nests that produced an egg and high copulation rate in experimental nests (Fisher Exact Test, p=0.04, Table 2.2), but no such association was found in controls (Fisher Exact Test, p=1 .0). I could not test if copulations occurred outside the fertile period of the female as predicted from this hypothesis since no peak of estradiol (indicating the releasing of the mature follicle) occurred during the copulatory pehod in which samples were taken. A more dramatic effect occurred in testosterone where concentrations declined from 1000 to 250 pg/ml on the day of egg laying (Figure 2.6). However, most of the copulations occurred during the first part of the nest-building period. Copulation frequency decreased with the testosterone concentration, but the correlation was not significant (Spearman Rank Correlation r=0.71, p=0.14, n=6, two-tailed test). Estradiol concentrations did not correlate with copulation frequency (Spearman Rank Correlation r=-0.09, p=0.92, n=6, two-tailed test). However, testosterone and estradiol correlated with each other (Spearmann Rank Correlation r=0.69, p=0.016, n=11). The number and rate at which sticks were brought by the male to the female for nest construction did not vary between experimental and control nests (experimentais: frequency=71.8 sticks, SE=16.2, n=13: controls: frequency=46.3 sticks, SE=8.5, n=6, Mann-Whitney U=33,5, p=0.32; experimentais rate=5.6 sticks per day, SE=1.17, n=13; controls: rate=5.3 sticks per day, SE=1.7, n=6, Mann -Whitney U=36.00, p=0.41 ). There was no association between the rate of sticks brought to the nest and the copulation rate in experimental (Spearmann rank correlation r=0.16, p=0.60, n=13; two tailed-test) or control nests

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59 (Spearmann rank correlation r=0.60, p=0.42, n=6; two-tailed test). Also, the incidence of nest failures before egg laying, though larger in experimentals (9/22) did not differ statistically from controls (2/8) (Fisher Exact test=0.29). Taken together, the results contradict the predictions of the Female-StimulationAssessment Hypothesis. Sperm Competition Hypothesis At least one extra-pair copulation occurred in 21% nests. This sample included all the observed nests (22 experimental and 8 controls;n=30). Inconsistent with the predictions of this hypothesis, however, the incidence of extra-pair copulations in experimental nests (3/22) did not differ from control nests (4/8) (Fisher Exact test=0.06). Peak of Copulations Hypothesis In order to explain the peak of copulations 14 days before egg laying, I examined the female for the presence of the egg inside the uterus in a sample of individuals obtained outside the experimental sub-colony. In 13 instances I had both the egg-laying date and whether the egg was present inside the female's reproductive tract. On average the egg was present in the uterus 1 .85 days before laying (SE=0.32). In four instances in which I checked the same female twice I did not find an egg both times. The average time before egg laying where I did not detect an egg (but an egg was eventually produced) was 5.5 days(SE=1.26).

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60 Discussion The copulatory pattern observed in the magnificent frigatebird can be summarized as follows: females invariably laid a single egg per clutch but pairs copulated 16.2 times during an average period of 13 days before the female laid the egg. Pairs initiated copulations up to 22 days before laying and copulation peaks 6 days before laying and then declined to become rare two days (1 .85) before laying. Sticks brought to the female by the male for nest construction showed a weak but significant positive correlation with the copulation frequency. The copulation pattern of frigatebirds (frequency and peak) was similar to other seabirds and to other species of birds laying only a single egg. Species laying only one-egg clutches have high copulation frequencies; most of the reported species copulated 5 to 100 times per clutch (Birkhead et a! 1987). Only a few descriptions of the copulation pattern in seabirds are available but in general, copulations occurred longer before egg laying than in land birds, suggesting that seabirds store sperm for longer periods of time (Birkhead et al. 1987, Simmons 1990, Venierand Robertson 1991, Hunter at al. 1992). Time periods from the last recorded copulation and the egg-laying date range from 8 days in guillemots to 60 days in petrels (see ref. in Birkhead et al. 1987). The copulation pattern in seabirds is unexpected based on available information about egg fertilization. According to the literature, in chickens and other birds, the fertilization window is about 24 hours prior to egg laying (Birkhead and Moller 1992). Therefore, one would expect that only a few copulations one day before egg laying should be sufficient to fertilize the one egg produced by the female. However, frigatebirds copulate about 16 times to fertilize the egg and the peak of copulations occurred during the first two thirds

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61 of the courtship period, 6 days prior to the egg laying, rather than close to egg laying (Figure 2.7). Fertilization and Stimulation Hypotheses Evidence from the experiment does not support neither the Fertilization nor the Stimulation-Assessment Hypotheses. Contrary to the Fertilization Hypothesis, even though I did not record the fertility of eggs and I did not check for the presence of the egg up to hatching, chicks were present one month later in 43% (8 out of 1 3) of experimental nests where an egg was laid as compared with 5% of the control nests (1 out of 6). The higher proportion of experimental nests with a chick suggests that hatching failure may have been even higher in controls than experimental nests. This result implies that only a few copulations are necessary to fertilize the egg. The Stimulation-Assessment Hypothesis was not supported because experimental females were able to produce an egg as frequently as controls and during a similar period of time (copulation and nest construction period). There was, however, an association between high copulation rate (rate of copulation attempts) and the proportion of nests that produced an egg. This result alone does not support the Stimulation-Assessment Hypothesis since it might be that some female assessment occurs but the mechanism is not necessarily stimulation of the female to release the egg from the follicle. In fact, in support of the Assessment Hypothesis (but not the Stimulation Hypothesis) in natural nests observed in the descriptive part of this work, there were a weak but significant association between the number of sticks brought by the male and the number of copulations (see below). I was unable to determine the duration of the female's fertile period in frigatebirds using circulating hormone levels. Estradiol is known to rise some

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62 hours after ovulation in hens (Lance and Callard 1978). However, the only peak found during the copulatory pehod of frigatebirds occurred one day before egg laying, when the egg was detected in the uterus. This peak could be only a late manifestation of ovulation in frigatebirds. I was unable to assay other hormones because of technical limitations. Copulations occurring as early as 22 days before egg laying might support the Stimulation-Assessment Hypothesis since this hypothesis predicts that copulations begin before the fertile period of the females. However, since the fertile period may be extended by the presence of sperm storage structures inside the reproductive tract of most female birds and especially in seabirds the length of the fertilization pehod is uncertain (Birkhead etal. 1987). Sperm Competition Hypothesis I did not obtain unequivocal evidence in favor of the Sperm Competition Hypothesis since a strong ongoing El Nino effect in the Pacific coast affected the survivorship of the chicks included in this expehment and consequently I could not obtain enough blood samples from families for paternity analysis. However, the descriptive study in this colony indicated that conservative amounts of extrapair copulations occur in this population. Extra-pair copulations were detected in 9% of the pairs observed in 1 992-1 993. Since no evidence was found in favor of the Fertilization and only weak support was found for the Stimulation Hypotheses, the Sperm Competition hypothesis is a good candidate to explain the evolution of the copulatory pattern (frequency and peak) in frigatebirds. Several forms of the Sperm Competition Hypothesis could be plausible here but in particular I tested one prediction of the Mate Guarding Hypothesis from the point of view of males. Although extra-pair copulation occurred in 7 out of 30 manipulated nests (experimentals and controls), against this hypothesis

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63 the incidence of extra-pair copulations was not more frequent in experimental than control nests, suggesting that the probability of having an extra-pair copulation does not depend on the number of successful copulations. In other words, copulation frequency does not apparently function as a mate guarding tactic for males. If males are not guarding the female by copulating frequently, the alternative is that males are protecting their paternity by diluting the sperm of other males that previously copulated with the female (Paternity Assurance Hypothesis). This is in fact a viable alternative. On the other hand, if sperm precedence is a possible mechanism promoted by sperm-storage structures in females, by copulating frequently males can increase their likelihood of being the last male copulating with the female, increasing their probabilities of fathering the chick. Both hypotheses predict that, in an experimental situation like that used here, the incidence of false paternity will be higher in experimental than in control nests. Since many of the chicks in the sample disappeared before I took the blood samples from the experimental and control families, these hypotheses remain to be tested. However, since extra-pair copulations occur and if alternative explanations do not explain multiple intra-pair copulations, multiple copulations by the same male is a likely explanation. From the point of view of the female, I tested two alternatives: The MaleGuarding and the Immediate Material Benefits Hypotheses. The results are equivocal. Contrary to the Mate Guarding Hypothesis, there were no more nest failures before laying in experimental than in control nests, suggesting that by copulating less frequently in experimental nests, females were no more likely to lose their mates than in control nests. However, the significant association between high copulation rates (copulation per day) and reduced probability of

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64 nest failure in experimentals suggests that female mate guarding could be one of the functions of the high copulation rates in frigatebirds. Inconsistent with the prediction of the Immediate Material Benefit Hypothesis, males did not bring more nesting material to control nests than to experimental nests. However, in support to the Immediate Material Benefit Hypothesis, manipulated nests (experimental and control nests) had higher copulatory rates and higher delivery rates of nesting material than natural nest from the descriptive part of the study. This result suggests that males, obligated to leave the nest more frequently looked for more nesting material and increased the copulation frequency of the pairs. Additional support for this hypothesis comes from the observation of natural pairs: there was a weak but significant association between copulation frequency and nesting material brought by the male to the female. The Future Material Benefits Hypothesis (Hunter et al. 1993) hardly applies to the fngatebird system. Since obligate male desertion occurs in this species, and desertion seems dependent on the time of the year (Chapter 4), this explanation is unlikely. Females do not gain any extra help from males since the only vahable that counts to explain variability in desertion date of males is how early in the season a pair becomes established (Chapter 3). Peak of Copulation Hypothesis Copulations peaked in frigatebirds about 6 days before egg laying. Hypotheses about a decline in copulation frequency before egg laying (and presumably when the female is still fertile) have been advanced under the assumption that the fertile period extends to the laying date (Birkhead and Moller 1993). The evidence presented here suggests that the decline in copulation frequency occurs about two days before egg laying when the females

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65 are no longer fertile, based on the presence of the egg Inside the female's uterus. This is not unusual since other birds have similar periods of egg retention (birds laying eggs two days apart; Birkhead and M0ller 1992). If the fertilized egg is in the uterus two days before laying, there is no additional benefit for females to continue copulating. In addition, if males are able to detect that the egg is fertilized, there is no additional benefit for the male in continuing to copulate. If frequent copulations involve a cost to both parents of the possible damage to the developing unlaid egg, males and females should stop copulating before the laying of the egg. Water shots were a good method for discouraging copulations in frigatebirds. However, the manipulation had some influence on control and experimental nests (manipulated nests) compared with non-manipulated nests observed from November 1993 to March 1994. Males brought 4 and 2.7 times more nesting material to experimental and control nests respectively than to non-manipulated nests. Nonetheless, copulation frequency (copulation attempts plus copulations) and the copulation period of manipulated nests (control and experimental) were not different from those in unmanipulated nests during 19931994. The comparison suggests that by disrupting copulations I increased the activity of males only, but females still copulated at similar rates and this activity of males did not affect the laying date. Even with this effect on the behavior of males, the results are still valid. High levels of estradiol and moderate levels of testosterone have been associated with female reproductive and copulatory behavior in birds (Lance and Callard 1978, van Tienhoven 1983, Wingfield et al. 1989, Hannon and Wingfieig 1990, Wingfield 1994). Estradiol levels in frigatebirds were comparable to concentrations reported for other birds (e.g. ptarmigans; Hannon and Wingfield 1990) fluctuating from 20 to 200 pg/ml. However, In frigatebirds the circulating

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66 level estradiol declines as the copulation period progresses and estradiol concentrations did not correlate with the copulation rate. There was a better but still non significant correlation between testosterone levels and copulation frequency in frigatebirds suggesting some functional connection. Frigatebird testosterone levels were higher compared with concentrations of this hormone in females but smaller than in males of other species (Wingfield et al 1989, Hannon and Wingfield 1989). There is no information about the hormone levels in frigatebird males but different ratios of male and female testosterone concentrations are different in different mating systems (Wingfield 1983). Male/female testosterone ratio seems to be low in species with slight sexual dimorphism. Since frigatebird females are constantly competing for males, raised testosterone levels may be a sub-product of strong female-female competition (the Challenge Hypothesis, Wingfield et al. 1987). Since changes in plasma testosterone appear to mirror those of the estradiol during the ovulatory cycle of hens (Lance and Callard 1978), it is not surprising that estradiol and testosterone are correlated in frigatebirds. In summary, frigatebirds copulated about 16 times during a period of 13 days. Copulations peaked at 6 days before egg laying and then declined. The experimental manipulation of copulation frequency in the magnificent frigatebird did not support the Fertilization and the Stimulation-Assessment Hypotheses as explanations for the frequent copulation in this bird. Data indicated that only a few copulations are sufficient to fertilize the egg. In addition, like many other birds, copulation frequency was independent of egg laying in these birds. In the context of the Sperm Competition Hypothesis, frequent intra-pair copulations could serve the interest of males and females. By copulating frequently males may be increasing their paternity (Paternity Assurance Hypothesis) and females could be assessing the quality of the mate. The paternity analysis is needed to

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67 demonstrate that the incidence of extra-pair paternity was lower in control than in experimental nests. The presence of the fertilized egg inside the reproductive tract of the female could be associated with the decline in intra-pair copulations. The copulation pattern of males and females in frigatebirds may be the outcome of conflicting reproductive interests of both sexes.

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68 Table 2.1 Reproductive success and nest failure in experimental and control nests. frequency of each treatment variable experimental control Initial sample size 22 8 Egg observed 13/22 (59%) 6/8 (75%) Failure before laying 9/22 (41%) 2/8 (25%) Chick observed 8/13 (61%) 1/6 (12%) Failure after laying 5/13 (38%) 5/6 (63%)

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69 Table 2.2 Copulation rate (interrupted copulations) in experimental nests and the frequency of egg laying. High and low copulation rate are above and below the mean (1.7 copulations per nest per day). frequency of copulation rate egg laying nest failure (no egg laid) high 9 (41%) 2 (9%) low 4 (18%) 7 (32%) One-tailed Fisher Exact test for the entire table, p=0.04

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70 0.8 T Initial Middle Late Nest-building and copulation period (thirds) Figure 2.1 Proportion of time that males and females stayed at the nest (n=22) during the nest-building and copulation period.

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71 c/) 0.45 c 0.4 i_ CD 0.35 ^ 0.3 D) O 0.25 E 0.2 *—> O 0.15 c o 0.1 o 0.05 O < Q. 0 Initial Middle Late Nest-building and copulation period (thirds) Figure 2.2 Proportion of time that males and females stayed together at nest during the nest-building and copulation period (n=22 nests).

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72 2.5 T 2 " 1.5 1 0.5 I f 0 Initial Middle Late Nest-building and copulation period (thirds) Figure 2.3 Rate of stick delivery by the male (mean ± SE) as a function of the nest-building and copulation period (n=22 nests).

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73 0 5 10 15 20 25 Days before egg laying Figure 2.4 Copulation rate (mean ± SE) as a function of the days before egg laying. Day 0 corresponds with egg laying. Numbers near the dots represent sample sizes.

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74 25 T Copulations Interrupted Water shots copulations (outside copualtion) Figure 2.5 Average copulation frequency at experimental and control nests. In experimental nests copulations were interrupted using water shots. In control nests water shots were used outside of the copulation interaction.

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75 1200 n 1000 Testosterone Estradiol E S 800 c o i_ "c (U o o o 0) o E o X 600 400 200 10 I 0 0 2 4 6 8 10 Days before egg laying 12 Figure 2.6 Circulating concentrations of testosterone and estradiol in females as a function of the days before egg laying. Day 0 was the day when the egg was laid. Sample sizes (numbers close to the dots) are the same for dots and squares. For comparison, sticks brought by the male occurred from day 14 to 2 and then declined. Copulations started at day 14, peaked at day 6 and then declined to day 2 before egg laying.

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CHAPTER 3 THE TIMING OF MALE DESERTION IN THE MAGNIFICENT FRIGATEBIRD: A TRADE-OFF BETWEEN CURRENT AND FUTURE REPRODUCTION Introduction Differences in parental care between males and females within a pair have been reported in several species (Ridley 1978). The extreme case of this inequality is mate desertion. Desertion is defined as the termination of offspring attendance by one parent before offspring independence (Fujioka 1989). Desertion by the male is commonly reported in birds (Ezaki 1988) but females desert in some species (Eens and Pinxten 1995). In some other species of birds like kites and little egrets, either sex may desert (ambisexual desertion, Beissinger 1986, 1987a, 1987b, Fujioka 1989, Persson and Ohrstron 1989). Desertion could be flexible, as in polygynous species or inflexible as in frigatebirds in terms of its occurrence, the sex of the deserter (Beissinger 1990), and the time of desertion. In the former case the interesting question could be why individuals desert or stay, but in the second case the desertion time is more interesting. Parental investment is defined as everything that the parent does for the survivorship and future reproduction of the offspring at a cost to the parent in her/his ability to invest in other (current or future) offspring (Trivers 1972). With this definition Trivers put the main prediction of parental investment theory in the 76

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77 context of the trade-off between current and future reproductive success. The main idea here is that individuals are expected to optimize their parental investment to produce the maximum number of offspring with the minimum cost over their lifetime. From this perspective, mate desertion is expected to evolve only when the reproductive advantages to deserters is larger or at least equal to that of non deserters. This theory gives us the framework to generate many hypotheses to explain reproductive patterns observed in the field and, even better, to derive precise predictions and test them in the field. According to Parental Investment Theory (Thvers 1972), we can expect mixed reproductive strategies by males and females of sexual species in order to increase their individual life-time reproductive success (Darwinian fitness). Since males and females are under different selective pressures to maximize reproductive success, conflicts arise over the amount and time of parental investment (Thvers 1972). The recent literature suggests that the diversity of reproductive strategies results from sexual conflict (Trivers 1972, Rodwe et al. 1994; Kempenaers 1995; Gowaty 1996) constrained by the distribution and availability of resources (Orians 1969). Although the concept of Parental Investment has been very useful for the development of models. Parental investment has been rarely used because it is difficult to measure (Evans 1990, Clutton-Brock 1991, Clutton-Brock and Godfray 1991 ). The alternative in the field is to use the concept of Parental Care and Reproductive Success as a substitute for Parental Investment. Parental care is the amount of energy, time and risks incurred by a parent in cahng for the offspring and Reproductive Success is the number of chicks produced to independence (Clutton-Brock 1991 ). In the context of the trade-off between current and future reproduction, the loss of potential mating opportunities represents an additional cost.

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78 Two types of models to explain and predict desertion have been developed, depending on the cost-benefit equation for deserters and non deserters (optimizing and dynamic modeling: Grafen and Sibly 1978, Winkler 1987, Kelly and Kennedy 1993) or the outcome of the conflict between the male and female strategies in the mating pair (frequency-dependent models: Maynard Smith 1977, Lazarus 1990). However, only a few field studies have tested the predictions from the models. Both types of theoretical modeling approaches to mate desertion have indicated that any strategy of stay or leave the offspring by either or both parents could reach an evolutionarily stable state. The outcome depends on three initial conditions: (a) the ability of one parent to complete the rearing of the offspring alone (this factor also depends on the feeding and caring demands of the offspring and the abilities of parents to complete the care of the chicks alone); (b) the opportunity for additional matings after desertion (operational sex ratio, sensu Orians 1969); and (c) paternity certainty (Maynard Smith 1977, Grafen and Sibly 1978, Lazarus 1990, Whittingham et al. 1992, Xia 1992, Houston 1995). Although the factors influencing desertion have been analyzed in some detail (Fujioka 1989, Westneat 1988, 1993, Whittingham and Robertson 1994), little attention has been paid to the main prediction of parental investment theory: the trade-off between current and future reproductive benefits (Kelly and Kennedy 1993). According to the theory, we expect mate desertion to be favored by natural selection when the reproductive benefit of the deserters is higher than the reproductive outcome for non deserters. High reproductive success for nondeserters in the current reproductive season does not rule out the possibility that in the long run, deserters may have a better or at least equal expectation of long-term reproductive success.

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79 The trade-off resulting from the decision to leave or stay and care for the offspnng or the decision about the timing of desertion depends on (1 ) the probability of finding another partner and rearing another brood (this includes the time for breeding recovery), and (2) whether the current offspring are going to survive after desertion with the attention will the mate only. Under this circumstance it is expected that deserters to take into account variables influencing the survival probabilities of the offspring (e.g. female, offspring and own physical condition). If one parent is able to rear the chick alone from the beginning, we can expect that male desertion will occur shortly after copulation or immediately after the female lays the egg. However if the offspring demands more post-zygotic care than one parent can supply or deliver even temporarily, then it can be predicted that the male will delay desertion until such a time when offspring demands decrease to a point where one parent is able to feed (and protect) the chick alone (feeding threshold). Although all models have assumed this trade-off, unfortunately, the systems in which models have been validated have not yet offered information about the current and future reproductive benefits of deserters simultaneously (Beissinger 1987a, b, Fijioka 1989, Kelly and Kennedy 1993). In the specific case in which a model was developed and validated using information coming from several populations of the Cooper's hawk, the key factor influencing desertion was the interaction between the threat to the future reproduction of the deserters (the female in this case) and the nestlings' risk of death. However, the trade-off was not tested since none of the deserter females re-nested after desertion (Kelly and Kennedy 1993). Expenmental manipulation of the deserters is essential to demonstrate the costs and benefits between the current and future reproduction (trade-off), but the manipulation itself could be very difficult and probably uninformative.

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80 since the feeding rates of males and females and the growth rates of the offspring might have coevolved (Clutton-Brock 1991). This means that when the mate is removed, the offspring always dies, thus confounding the effects of desertion and disturbance. To circumvent this problem, we can analyze the timing of desertion in natural populations and look for the reproductive trade-off for early and late deserters. I used this approach to test the main qssumption of parental investment theory and the role of the mate during and after mate desertion, using the male desertion system of the magnificent frigatebird. I derive here a set of predictions taking into account the reproductive biology of this seabird. Frigatebirds are socially monogamous seabirds that rear one altricial chick for 12 to more than 18 months (Chapter 1). Although biparental care seems to be the rule in frigatebirds, in one species, F. magnificens, there is a dramatic division of labor between the sexes in caring for the chick. In this species males and females share the incubation and the first three weeks of brooding equally (see Chapter 1 ). However, when the chick is still small and unable to survive without parental attention (the male stays 1 7 to 50% of the total time that the chick is at the nest and from 7 to 20% if we add the dependence period up to independence), the male deserts the nest leaving the female to feed the chick for a long period of time ranging from 12 to 1 5 months. Obligate male desertion has been consistently reported in the magnificent frigatebird (Diamond 1972, 1973, Nelson 1975, Coello et al 1977, Trivelpiece and Ferraris 1987, Durand 1992). In addition, successful frigatebirds are unable to reproduce again in the same breeding season (this study) and it has been suggested that frigatebirds undergo a 5-month molt between consecutive reproductive periods (Diamond 1972). Furthermore, all breeding colonies of frigatebirds restart reproduction annually. However, it has been speculated that

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81 if males are deserting their chick after 6 months of parental effort (from courtship to chick rearing), even if they molt, they can re-mate again in the next breeding season, whereas females are limited to biennial breeding constrained by feeding of the chick (Diamond 1972). Predictions Derived From the Parental Investment Theory All males leave so this decision is obligate but individuals still have to decide the proper time to leave in terms of the trade-off between the current and future reproduction. Two aspects of this trade-off are (1 ) the survivorship of the current offspring and (2) the probability of recovering and finding another mate. In frigatebirds the best time to leave is affected by the age and condition of the chick: (a) when the chicks are able to survive with the care of the female alone (when the probability of chick survival highest), and (b) the condition of the female caring for the chick, and the condition of the male. A more specific prediction is a negative correlation between the desertion date in terms of chick age and the body condition of the female, chick or the deserting male. Since successful frigatebirds are unable to reproduce again in the same breeding season and because a 5-month recovery period is required in these birds, males only increase their future reproduction in the next breeding season. Thus, the prediction here is that the deserting males will be looking for mates in the next breeding season. Since the proper time for desertion should be a compromise between these two conflicting times, the proper companson is the reproductive success and the remating time between early and late deserters. The individuals deserting very early in the life of their chick are going to sacrifice chick survival. In contrast, those individuals deserting late are going to sacrifice future reproduction.

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82 All this is predicted assuming that females are able to rear the chick alone as soon as the chick is able to remain safely at the nest. The ability of females to care for the chick alone could be because the chick has already passed the peak period of vulnerability to predation or the peak feeding requirement or because the chick is more resistant to periods of starvation or because the female increases her effort to cover the chick's feeding demands. If females are compensating for the absence of males, I expect a significant increase in the feeding rate of females after male desertion. Methods We followed 95 nests that contained chicks for 40 days each after hatching until fledging. In 40 nests at least one parent was marked and in 47 both parents were marked and in seven only chicks were marked. All chicks in the sample were individually marked with numbered wing tags. Chick survivorship was checked once a week and monitored three consecutive days per week during behavioral observations. Chicks were weighed and their culmen and ulna lengths were measured once a week from 40 days of age to fledging. Chicks were handled at night to minimize disturbance. To monitor parental care and chick feeding, we made behavioral observations from 20 February to 21 July 1994 and on an opportunistic basis from 17 November to 27 December 1994 when chicks fledged and from 28 March to 12 April 1995. We recorded chick feeding frequency and the arrivals and departures of adults to and from the nest for three consecutive days per week from 0800 to 1 800 h. We made focal observations on up to 36 nests simultaneously from an observation

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83 site located 30 to 1 50 m from the focal nests. It was possible to observe such a large group of nests because we recorded only a few conspicuous behavioral categories occurring infrequently. In addition to our focal recording methods, we scanned for the presence of parents and chick at every nest every hour. Measurements Male desertion . Since we followed every nest up to chick fledging, male desertion was determined in all successful nests as the last time we recorded the presence of the male at the nest, not necessarily feeding the chick. In unsuccessful nests we scored desertion if the chick survived attended by one parent only and the mate was not seen visiting the nest for more than three consecutive days. We could not distinguish male desertion from nest failure when the death or disappearance of the chick coincided with the time of mate desertion. Laving date estimation and settlement time . Laying dates in every nest were calculated retrospectively from chick age by adding 56 days (incubation period. Chapter 1 ). For analysis, nests in the sample were divided into those established early and those established late in the season. I called them: earlyand late-settled nests. The division between earlyand late-settled nests was the mean laying date in the sample. Chick aoe estimations . Chick age was estimated from the culmen (upper mandible) length the first day we measured it or included the chick in the sample. We measured it by placing a measuring tape (± 0.5 mm) at the base of the bill and following its

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84 curvature. We interpolated the age of the chick from the growth curve fitted in 1991 for this population (Durand 1992). Durand's data were based on a weekly measurements of 13 chicks of known age. Chick feeding rate . Feeding was infrequent in frigatebirds (once each 3 days). I report here the frequency of feedings that occurred during three consecutive days per week as a feeding rate. Since some unknown frequency of feedings occurred at night, I assume here that our chick feeding rates were only estimates of the real feeding rate. Body condition . Body condition of males, females and chicks were estimated from the mass and culmen length measurements. Chick body condition was calculated from measurements taken on the closest date to male desertion. While adult body-condition indexes may not be biased, the chick body condition is correlated with age because of the allometry between mass and culmen length. In the case of the chicks, I estimated body condition from the residuals of the regression between the natural logarithm of the mass"^ (to work in the same dimension) and the natural logarithm of the culmen length. Since residuals give the distance between the average and each chick measurement, this method estimates the individual condition controlling for biases by sex, age and settling time. In the case of adults I estimated condition as the mass/culmen length ratio since there was no correlation between the log mass'^ and log culmen length. For the analyses of chicks, I correlated the residuals of the log mass"' and log culmen length with chick age at the time of male desertion following the predictions

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85 derived from theory (see introduction) and between the mass/culmen length and chick age at the time of male desertion in the case of adults. Statistical Analysis . Comparisons were made using non-parametric tests (Mann-Whitney U, Wilcoxon and Spearmann Rank Correlation tests) because small samples and heterogeneous variances precluded me from using parametric tests (unpaired and paired t-tests and Pearsosn's Correlation). In addition, I used Chi Square tests to analyze frequencies and the Fisher Exact Probability test when some observed values were zero or when sample sizes were small. Statistical tests were one-tailed when I tested directional alternative hypothesis and null hypotheses were rejected at the 95% confidence level. Results Time of Male Desertion The age of the chick when males deserted (age of desertion) was variable, ranging from 18 to 161 days (Figure 3.1). Surprisingly, all males deserted the nest and eventually the colony during a short period of time during the year. Most of the desertions (74%) occurred before May (between March and AphI 1994; Figure 3.2). Differences in male desertion dates was a consequence of variation in the laying date, with early-settled males deserting older chicks and late settlers deserting younger ones (laying date vs. deserting

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86 date; r=-0.78, p=0.0001, n=42). In fact, early-settled males deserted their nest when chicks were 40 days older on average (1 05.3 days, SE=5.4, n=1 8) than late-settled males (65.4 days, SE=4.1, n=14; Mann-Whitney U=15.5, p<0.0001). In spite of the large difference in chick age at the time of desertion between earlyand late-settled males, earlysettled males deserted only 1 0 days before the late-settled males on average considering the desertion dates during the year (early-settled males deserted on 27 March, SE=6.4 days, n=18; late-settlers deserted on 7 April, SE=3.2 days, n=14). The average difference in desertion date during the year was not significant (Mann-Whitney U=79, p=0.08). Male Desertion and Body Condition Contrary to my prediction, the age of the chick at the time of male desertion did not correlate with the female ( r=0.1 , p=0.30, n=32) or male (r=0.003, p=0.49, n=26) body condition. However, in support of my prediction, a negative correlation was found between chick body condition and chick age at desertion (r=-0.47, p=0.003, n=32. Figure 3.3): males deserted chicks in good condition earlier than those in poor condition. No correlation occurred in earlysettled nests (r=0.17, p=0.25, n=18; Figure 3.3), but the same correlation was strong, negative and highly significant for late-settled males (r=-0.78, p=0.0005, n=14; Figure 3.3). Survival Probabilitv of Chicks The importance of the male's contribution to the feeding and care of the chick decreased continuously up to desertion at 100 days of chick age (Figure 3.4). No eggs nor chicks survived when one adult deserted during incubation,

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87 hatching or brooding (from laying to 18 days of chick age, n=36 unsuccessful nests Chapter 1 ). The proportion of dead chicks following male desertion dropped as the chick age increased to 80-100 days (Figure 3.4). Thereafter, no chicks died after male desertion (n=39). There was a negative and significant relationship between the proportion of chicks that died after male desertion and chick age (r=-0.86, p=0.006, n=8). Early-settled nests were more successful at rearing chicks than latesettled nests. Seventy-two percent (21/29) of nests settled early were successful, whereas only 40% (18/48) of late-settled nests successfully fledged a chick (Chi square=6.55, df=1 , p=0.01 ; in 18 cases the laying date was not known). Reproductive Benefit of Desertion to Males Although all males deserted their nest, 45% (15/33) of marked males that produced a fledged chick in the 1993-1994 breeding season (those where the female was able to rear the chick alone after male desertion) returned the next breeding season with a red gular pouch indicating reproductive condition. This return to the breeding place occurred while 18 out of 29 marked females were still feeding flying juveniles. In six cases (25% of the successful pairs where both adults were marked) both adults were seen simultaneously at the breeding place (not necessarily at the same nest site) the next reproductive season. In all cases females were feeding the chick while males were seen in reproductive condition. Similarly, 57% (16/28) of unsuccessful marked males were seen the next breeding season in breeding condition. Successful and unsuccessful males did not differe in their probablity of returning the next breeding season (Chi square=0.43, df=1, p=0.51).

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88 Successful males from late-settled nests returned in the next breeding season less frequently (3/14) than early-settled males (11/16; Fisher Exact Probability test, p=0.012; Table 3.1). Although all males deserted during a short pehod of time (March-April), there was a trend toward slightly early deserters (deserting ten days earlier in average than late deserters) being marginally more able to return in reproductive condition the next breeding season than late deserters (Fisher Exact Probability test= 0.1 ). Male and Female Conthbution to Chick Feeding Females made at least 60% of the feeding trips when males were still present before desertion (Figure 3.5). They compensated for the male's absence by increasing their feeding rate after male desertion: feeding rate after desertion was 32% higher than before desertion (Chapter 4). There were no significant differences between early and late-settled males in the frequency of chick feeding; both early and late males fed the chick at a similarly low rate (early-settled=0.43 feedings per 3 days, late-settled=0.24 feedings per 3 days per week; Mann-Whitney U=8.5, p=0.13, n=6,6). Discussion Consistent with previous observations in F. magnificens (Diamond 1972, Coello et al. 1977, Trivelpiece and Ferraris 1987, Moreno and Carmona 1988, Durand 1992;, males always deserted the nest and we did not record any case in which the chick was fed by the male only. Male desertion occurred when

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89 chicks were as young as 18 days and as old as 161 days. In spite of this variation, male desertion occurred during a narrow time-window in the year: 74% of males deserted during March and April. This suggests a temporal threshold for male desertion. Since most late settled males were not seen the next breeding season, I called this time threshold "the critical date for male desertion". Chick Survival and Male Desertion In spite of the threshold for desertion, males showed some evaluation of the proper time for desertion. Contrary to my expectation from theory, male desertion was not associated with the body condition of the female nor the body condition of the male. However, in support of my prediction, males deserted their chicks earlier when the chicks were in good condition. More interestingly, early-settled males seemed to desert their chicks close to the average condition (Figure 3.3). Late-settled males, in contrast, were in a more difficult situation since the critical date for male desertion was closer, so they apparently took the condition of the chick into account. The contribution of the male to the survival of the chick changed over the breeding season. Males were indispensable during incubation and up to 30 days post-hatching as evidenced by higher chick mortality when desertion occurred at less than 20 days of chick age and by the invariable nest failure when adults left the nest unattended during incubation. After 20 day male importance decreased gradually up to 80-100 days. During this age range (20100 days) desertions occurred but the survivorship of the chick clearly increased when desertions occurred later. Early settled-males were able to attend the chick longer and still desert with time enough to become reproductive the next

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90 breeding season. More evidence that early-settled males are taking the survival of their chicks into account is the fact that these males stayed longer at the nest when they had a daughter at the nest rather than a son (Chapter 5). Daughters seem more expensive since they stay longer at the nest (Chapter 5). In support of my prediction, males returned the next breeding season in reproductive condition. In spite of the fact that most males deserted during a short period of time during the year, not all males did equally well. Early-settled males were more likely to return the following breeding season in breeding condition, advertising for mates, compared to late-settled males. Late-settled males dispersed, died more frequently or were unable to return presumably because they worked intensely and waited up to the last time to desert. Those males may pay one of the costs of the trade-off. Perhaps, late males could not start earlier because they were in poor condition at the beginning of the breeding season. I could not find evidence of poor physical condition in these males but my estimate of this variable could be insensitive to subtle differences. Measures of fat deposits could possibly be a better indicator of condition in adults. Late breeders could be the product of (a) individuals arriving late (maybe as a consequence of being in poor condition), (b) individuals failing during their first reproductive attempt, (c) individuals trying unsuccessfully to attract a mate. Some males were unable to obtain a mate even when they arrived early at the reproductive colony and began to display. I have seen a number of males every season trying unsuccessfully to mate at different displaying sites and during a period of several weeks. These males sometimes engage in extra-pair copulation attempts. In one case we recorded a marked individual displaying in different places for two weeks, he established a nest for 3 days and then after a failure, engaged in an extra-pair copulation and finally left the island. In any

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91 case, because of the high energetic demands of breeding, these three categones may be highly correlated for individuals in poor condition. Deserters in this species seem to fit the predictions from the Parental Investment Theory. There is evidence that early-settled individuals, are evaluating the best time to leave: (a) early-settled males deserted when the survival probabilities of the chick were high, and (b) early-settled males deserted with time enough to migrate, replenish energy or molt (Diamond 1972) and return in reproductive condition looking for a mate during the next breeding season. Additional evidence showing that early-settled individuals are responding to the trade-off is that they stayed longer with the chick even when they could leave earlier. Since no advantage can be seen for deserting a long time before the molt period and since the energy can be better allocated to chick survivorship (chicks deserted younger were more likely to die), early-settled males deserting late in relation to chick age but early during the year are showing their response to the trade-off. Late-settled males, on the other hand, were more constrained in their decisions: they started late, contributed less to chick rearing, their chicks died more frequently, they deserted later during the critical deserting period and they were less able to return in reproductive condition in the next breeding season. Still these late settled males are responding to the condition of their chick to decide the best time to desert when constrained by the critical desertion date. Early-settled individuals are dealing well with the trade-off, but late-settled individuals and their females (see Chapter 4) are just "making the-best-of-a-badjob". Why late-settled individuals are deserting at all even when their chicks may die and when they will probably not be able to return in the next breeding season is not clear. Perhaps, even when deserting late, males may be doing better by recovering and looking for mates in other colonies that begin breeding

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92 a little later than the Isia Isabel colony. It is also possible that in other years, recovery is faster so that, on average, even when late-settled males desert they will have same opportunity to breed again in the following season (even though I did not see this during the year I observed them). Several reproductive colonies of frigatebirds are inside the range of dispersion of the frigatebirds I studied (Chapter 1 ). It may be that male desertion in the magnificent frigatebirdcan be explained, on average, if individuals are doing better by sacrificing the survivorship of a young chick late during the breeding season and trying to become reproductive again and looking for a mate earlier in the next breeding season in another colony. Earlyand late-settling by males can be either a fixed pattern in some individuals or conditional tactics of the same individuals at different periods of their lives. For example, late-settled individuals may be younger and inexperienced than early-settled breeders and paying the cost of becoming an efficient breeder. Since my interpretation is based on strong but correlative information, other interpretations are also possible. The critical desertion date for males could be only the consequence of the females' ability to feed the chicks alone because the feeding conditions improved late during the breeding season. The consequence of this is that males are able to desert after this improvement in feeding conditions. In addition this may explain why late females are increasing their feeding rates. However, since (1 ) chick survival was associated with the age of male desertion and because (2) peak feeding rates of early and latesettled nests did not coincide in time and, in fact since the feeding rate of latesettled nests was always higher, this explanation is unlikely (Chapter 4).

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93 Female Contribution Females always feed their chicks more frequently than males. Deserted females compensated for the absence of the male, increasing their feeding rate up to 30% (see Chapter 4). Perhaps because of their larger size (about 15% larger than males), females may have greater rearing abilities than males. Two explanations can be offered. Size dimorphism could be the result of different sexual roles or, on the other hand, the preexisting sexual differences promoted by sexual selection may set the conditions for male desertion. The magnificent frigatebird has one of the more pronounced dimorphism in the genus, suggesting that the second hypothesis could be more plausible (Nelson 1975). The Trade-off Between Current and Future Reproduction In spite of the apparently rigid desertion pattern (males always desert during a short period of time during the year), clear evidence was found for a trade-off between current and future reproduction for the deserters constrained by a long-lasting molt or recovery period. This seems to explain mate desertion behavior in frigatebirds. There are reproductive conflicts between current and future reproductive incentives for early and late-settled individuals. Early males did better by investing longer in their current reproduction and still leaving plenty of time to recover and become reproductive again. Late-settled individuals invested as long as possible but deserted with time enough to become reproductive again. Figure 3.6 shows a schematic summarizing this trade-off. This diagram shows the apparent desertion time window in this bird and the cost of the trade-off between the current and future reproductive opportunities. The diagram shows a typical chick born in early January. An early hatched chick is

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94 going to be 100 days old when the critical desertion date occurs in April. In this case the male of this hypothesized frigatebird nest is going to be able to attend the chick longer which will reduce the risk of chick death. This is pointed out in the diagram by the intersection between the critical desertion date (vertical line in April) and the first increasing survival curve to the left. In this imaginary earlysettled nest, the male clearly gains more by contributing longer to the chick feeding than by deserting early. By doing so, the male is reducing the death risk of the chick and is still able to desert in plenty of time to recover the energy or molt and become reproductive again at the beginning of the next breeding season. As indicated by the bars in the sketch, most of the desertions occurred around April (see also Figure 3.2). In the case of a nest established later duhng the breeding season, the survival curves are shifted to the right (subsequent ascending curves to the right of the initial one). In these cases the conflict is becoming more difficult and late-settled individuals start to lose in chick survival by deserting when the chick is small or lose future mating opportunities if the male stays longer than the critical time. The intersections between survival curves and the critical desertion time are occurring progressively later when the probability of chick survivorship is becoming smaller. At some point the male should to pass up breeding this year and start earlier in the following year. This is one of the few data sets supporting the predicted trade-off between the current and future reproduction and the kind of costs incurred by deserters in that trade-off. In frigatebirds, in spite of the rigid desertion pattern, deserting time seemed the result of the interaction between the survivorship of the current offspring and the probability of recovering and becoming reproductive again in the next breeding season. Early-settled individuals were more responsive to the current chick's survivorship and late-settled males were

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95 more constrained in their decisions by the condition of the current chick and their future opportunities for reproduction.

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96 Table 3.1 Frequency of early and late-settled marked males seen and not seen in the next breeding season. successful marked males Settling time seen not seen early 1 1 (68%) 5 (31%) late 3 (21%) 1 1 (78%) Fisher Exact Probability test; p=0.012

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97 Desertion date (chick age) igure 3.1 Frequency of male desertion as a function of the age of the chick.

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Figure 3.2 Frequency of male desertion as a function of the date of the year.

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99 4 n X o C £ 2 c q c o o o O 0 early-settled late-settled 20 40 60 80 100 120 140 160 180 Age of the chick at the desertion of the male (days) Figure 3.3 Chick condition index at the time of male desertion as a function of the age of the chick at male desertion. The index represents the residuals of the regression line between the mass"^ and the culmen length of the chicks.

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Figure 3.4 Chick mortality after male desertion. Numbers close to the bars represent the number of males deserting at that chick age.

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101 Figure 3.5 Feeding frequency of males and females as a function of chick age.

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102 Egg laying Hatching o o 0 S E 01 o 3 Fledging New breeding season Only those males deserting before April are able to return Females continue to feed fledglings Nov Jan April July Nov Date of the year Figure 3.6 Schematic representation of the trade-off between current and future reproduction in frigatebirds. The scheme is based on the critical desertion date for males. In this figure, the first ascending curve to the left represents the survival curve of an early-settled nest as a function of chick age. Sequential curves from the left to the right represent individuals nesting later in the season. Bars are the proportion of desertions in that month. Notice that late-settled individuals deserting on the same critical date are sacrificing the survivorship of their chick. Those individuals deserting after the critical desertion date (bars to the right of the critical desertion line) are increasing the survival of their chicks but sacrificing future matings. After April a few nest are established.

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CHAPTER 4 FEMALE TACTICS TO COPE WITH MALE DESERTION IN THE MAGNIFICENT FRIGATEBIRD Introduction Mate desertion, the termination of parental care by one parent before the independence of the offspring, is frequently reported in socially monogamous birds (Beissinger 1987a, 1987b, 1990, Ezaki 1988, Fujioka 1989, Eens and Pinxten 1995) Mate desertion is expected when by doing so, individuals increase their future inclusive fitness (Trivers 1972, Dawkins and Carlisle 1976, Maynard Smith 1977) more than if they were to continue caring for the offspring. Desertion could evolve when conditions for re-mating (and producing more offspring) are available for deserters and when current offspring may survive with the care of the mate only. In monogamy, sources of conflict can arise as soon as some asymmetry in costs or benefits occurs between the male and the female within the pair (Trivers 1972, Grafen and Sibly 1978). Some pre-existing sexual differences could favor or predispose one sex for desertion or some environmental factor could be promoting cost-benefit asymmetries between sexes (Trivers 1972, Gowaty 1994). Genetic relationship (parentage), mating opportunities and rearing abilities of males and females are expected to influence the occurrence and timing of mate desertion (Maynard Smith 1977). Genetic relationship and 103

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104 mating opportunities have been analyzed to some extent (Westneat and Sherman 1993, Whittingham et al. 1992, Xia 1992, Houston 1995), but the effect of differences in rearing ability have been assumed and demonstrated in only a few cases (Owens 1993). The desertion decision as an evolutionary problem has been examined mainly from the point of view of the deserters. However, the role of the deserted individuals is crucial to understand the incidence and timing of desertion (Owens 1993). Models of parental investment assume that deserted individuals are passive and stay with the offspring as the best or the only strategy. A partial increase of parental investment but not total compensation for the reduction of the mate's investment is another general conclusion from models (Houston and Davies 1985, Winkler 1987). The "cruel bind" described by Robert Trivers (1972) is the best example of this thinking. However, even when the alternatives for the deserted individuals are limited, they still have several options after desertion or to prevent desertion. For example: female aggression toward other females inside the territory (Kilpimaa et al. 1995). The alternatives available to deserted individuals have been addressed but only limited options have been considered (Maynard Smith 1977, Grafen and Sibly 1978, Winkler 1987, Kelly and Kennedy 1993). For instance, compensatory feeding of chicks has not been evaluated empirically as a strategy of females to cope with or prevent male desertion. Deschptive information from several species of birds has shown that at the time of desertion, one parent is able to rear the offspring alone (Beissinger 1987a, Fujioka 1989). This could be because the demands of the offspnng are reduced at the time of desertion or because the mate is able to meet the demands of the offspring at his/her own expense or both. In some cases desertion occurs at the final part of the rearing penod, supporting the former

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105 hypothesis (Beissinger 1987, Fujioka 1989) and several studies have demonstrated that some extra effort is expended by the deserted parent to cover the requirements of the offspnng (Fujioka 1989, Dunn and Robertson 1992, Meek and Robertson 1994, Eens and Pinxten 1995), Empirical studies producing short or dramatic male removals have demonstrated that deserted or abandoned females responded with partial compensation as predicted from models but other more specific predictions derived from theory were not evaluated (Bart and Tornes 1989, Johnson et al. 1992). There are only a few experiments handicapping or removing females to see the effect on male caring levels (Markman et al. 1995). In one experiment a weight was attached to the female's tail to reduce her feeding conthbution and males responded to this manipulation by partially compensating for the female's impediment as expected from theory. Evidence of the strategies of both sexes is still scanty in species where one individual in the pair deserts. Response to Desertion The theoretical treatment of mate desertion and parental investment problem has been approached from three different points of view: optimality (Winkler 1987), frequency-dependent models (EES; Maynard Smith 1977, Lazarus 1990) and dynamic modeling (Kelly and Kennedy 1993). Although complementary, these approaches do not integrate in one model the trade-off between current and future reproduction, parental effort, and cost and benefits simultaneously. As a consequence, the predictions from the models while consistent, are resthcted. I discuss here the optimality and the frequencydependent models since the dynamic modeling is a form of the optimality model.

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106 The frequency-dependent model analyzes the pay-off of the alternatives available to both individuals in a pair (stay or desert) assuming that individuals are repeatedly assessing the desertion decisions of the pair duhng the period of parental care (Lazarus 1990), This model is based on a previous model developed by John Maynard Smith (1977), The model assumes that individuals are choosing to desert or stay depending on the decision already adopted by the mate that gives them the greater fitness. This analysis was the first to emphasize the alternatives of action for an individual already deserted (Lazarus 1 990). The model predicts that a deserted individual should re-evaluate the situation after the desertion of the mate and stay or desert depending on the net expected reproductive success (the trade-off between the survivorship of the current offspring and the cost of investing in his/her offspring in the future). This model predicts only whether the deserted individual stays or deserts after the decision of the mate; it assumes no variation in the level of parental investment (timing of desertion). On the other hand, the optimization approach by Winkler (1987) analyzes the investment decisions of the individual as a function of the investment of the partner and offspring production. This is a model of parental investment rather that a model of desertion. However, some general conclusions are applicable to the desertion situation. In this model it is predicted that the best action in response to a partner's decrease in parental care is to increment or decrement the investment as a function of offspring production. This model assumes that offspring production is positively related to parental effort in an s-shape curve. When the expected production of offspring is under a critical value (the inflection point in the curve of offspnng production and parental effort), the best action is to reduce the parental care as a response to the reduced parental care of the mate. If the reduction of the parental care of the mate occurs after the inflection

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107 point in the curve between offspring production and parental effort, the best response is to increase the parental care as a response to the reduction of the mate (Winkler 1987). In this model no changes are assumed in the parental effort-chick production curve, but we can imagine that mortality, chick starvation, chick age and the condition of parents are variables that might influence the form of this curve. Parent-offspring relatedness, age of the offspring and time of the breeding season are also vanables analyzed in this model but only as independent vanables. An integrative analysis is still lacking and it is important to derive more specific predictions to fully understand patterns of parental investment. If we put together the two models we can expect females to vary their parental effort as a response to the time of male desertion; i.e. "if the chicks are small, desert; if large stay and increase the effort". Depending on the condition of females and how early during the life of the chick the male is deserting, more complicated and sometimes counter-intuitive tactics could be adopted by deserted females ranging from extra-compensation for the mate's absence (additional compensation in relation to a female non deserted by the male) to the desertion of the offspring after being deserted by the mate, sacnficing the survivorship of the current offspring. I approach here the mate desertion problem from the point of view of the deserted female in the magnificent frigatebird. Here I combine the assumptions and some conclusions from these two models (frequency-dependent and optimality models) to derive predictions about the role of the female during the desertion of the male. Male desertion is not a flexible strategy in the magnificent frigatebird (Chapter 1 , 3). In this species males always desert the nest during a short period of time during the year (March-April). The variance in the desertion date in terms of chick age is not explained by the condition of the male, the

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108 chick, or the female (Chapter 3), nor by the abundance of potential partners at the colony in the same breeding season (Chapter 1 ). Variance in male desertion is explained by the interaction between the laying date and the critical desertion date (Chapter 3). The critical desertion date occurs prior to the five-month period required by males to become reproductive again in the next breeding season. Because desertion is obligatory and because there is a particular limiting critical date during the year to desert (after this date males are hsking they probability to return next breeding season, Chapter 3), males that settle early are able to feed their chicks for a longer period of time (88 days of chick age in average) than males that settle late. Females of late-settled nests, therefore, have an extra-cost since late males desert when the chicks are still small (43 days of chick age on average). Based on the two models we can expect different strategies from females dealing with male desertion at different ages of the chick. From the optimality model, we can expect that females deserted after the peak demands of the current offspring should not only stay with the chick but compensate for the absence of the mate increasing their effort. In addition, if the male deserts early during the life of the chick, we can expect a large increase in female effort to increase the survival opportunities of the chick. However, if desertion occurs very early during the life of the chick (before the peak of demands), females can desert as a response to the male desertion. In this case, and according to the frequency-dependent model, the cost to the female of increasing her effort could be so high that the best strategy of the female is to desert.

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109 Methods Methods are the same as those of Chapter 3. We followed the marked chicks and adults of 95 nests with chicks from 40.6 days on average after hatching to fledging. Chick survival was checked once a week and monitored three consecutive days per week during behavioral observations. Chicks were weighed and their culmen and ulna lengths were recorded once a week. Parental care and chick feeding we recorded from 20 February to 21 July 1994 and on an opportunistic basis from 17 November to 27 December 1994 and from 28 March to 12 April 1995. We observed up to 36 focal nests simultaneously from an observation platform located 30 to 150 m from the focal nests. We recorded the chick feeding frequency and the arrivals and departures of adults to and from the nest three consecutive days per week from 0800 to 1800 h. In addition to our focal recording methods, we checked for the presence of parents and chick at each nest every hour (scan sampling). Male desertion was determined in all successful nests (nests where the chick fledged and was seen alive when we left the island) as the last time we recorded the presence of the male at the nest, not necessanly feeding the chick. In unsuccessful nests (those that lost their chick) we scored desertion if the chick survived some period of time when attended by one parent only and the mate was not be seen visiting the nest for more than three consecutive recording days. We could not distinguish male desertion from nest failure when the death or disappearance of the chick coincided with the time of mate desertion.

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110 Laving Date Estimation . Laying dates in every nest were calculated retrospectively from the hatching date by adding 56 days incubation period (Chapter 1). For the analysis, nests in the sample were divided into those established early and those established late in the season (earlyand late-settled nests). The border line between earlyand late-settled nests was the mean laying date in the sample. Chick Age Estimations . Chick age was estimated from the culmen length the first day we measured it or included the chick in the sample. We interpolated the age of the chick from the growth curve fitted in 1991 to this population (Durand 1992). Durand's data were based on a weekly measurements of 1 3 chicks of known age. Chick feeding rate . Feeding was infrequent in frigatebirds (once every 3 days in average; see Chapter 1 ). I report here the frequency of feedings that occur during three consecutive days per week as a feeding rate. Since some unknown frequency of feedings occurred at night, I assume that our chick feeding rates were only estimates of the real feeding rate. This value was used in the statistical comparisons of the feeding rate.

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Ill Chick Growth . Growth rate was fitted to a polynomial function (j^A+Bx+Cx^+Dx^+Ex") for every chick in the sample. Variables were defined in Chapter 1 . Since chicks were not handled before 40 days of age, we used the initial average size (mass and culmen and ulna length) of a small sample (n=3) of hatchlings of known age as the initial size in every curve fitting. The curve fit the growth data well: ranging from r^=0.92 to r^=1 .0. Maximum growth rate (MGR), the age at which the MGR was reached (AMGR) and the maximum chick size (asymptotic growth, AG) were calculated for each chick from the derivative function of the polynomial curve fitted in every case. Curve fittings (polynomial and derivatives) were calculated using Implot software, written by Michael Richie (1992). This software calculates the best curve by iteration. Sexino Fledglings . I was able to sex all fledglings using a discriminant function applied successfully to chicks in this population in 1991 (Durand 1992). This function was based on 18 fledglings of known sex (7 males and 1 1 females; Durand 1992). Sex was estimated from culmen and ulna measurements. The discriminate equation was: y=-40.5199+0.1226(culmen)+0.08955(ulna) where if y>0, then female; if y<0, then the bird was classified as male. Statistical Analysis . For the statistical comparison of growth rates among chicks, I used the MGR, the AMGR and the AG estimated for each chick. Growth rate and

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112 behavioral comparisons were made using non-parametric test (Mann-Whitney U and Wilcoxon tests) when small samples and heterogeneous variances precluded me from using parametric tests (unpaired and paired t-tests). In addition, I used the Chi-Square test to analyze frequencies and the Fisher Exact Probability test when some observed values were zero or sample sizes were small. In the analysis of feeding rates in subsequent time periods (chick age or time of the year), a non normal distribution of the whole sample precluded me from using a Repeated Measurements ANOVA. Intead I used independent ANOVAS for each chick age period or a Two-way ANOVA for feeding rates in different months. When a prediction was evaluated, statistical tests were onetailed and null hypotheses were rejected at 95% confidence level. Results Female Co mpensation For the Male's Absence Frigatebird females contributed at least 60% of the chick feedings when males were still present (Figure 4.1 ). They compensated for the male's absence by increasing their feeding contribution to the chick after male desertion. The feeding rate after the desertion of the male was 32% higher than before desertion (Female Feeding Frequencies, before=0.95 feedings per 3 days per week, SE=0.16, n=20; after=1,26 feedings per 3 days per week, SE=0.16, n=20; paired t-test t=2.23, df=19, p=0.019).

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113 Female Tactics Dealing With the Male's Desertion Females were more than passive actors during male desertion. Latesettled mothers increased their feeding frequency by 50% when compared with early mothers (feeding frequency: early-settled females=1.01 feeds per 3 days per week, SE=0.09, n=19; late-settled females=1.51 feeds per 3 days per week SE=0.14, n=19; Mann-Whitney U=89.0, p=0.008; Figure 4.1). An analysis by age of the chick every four weeks indicated no significant differences in the feeding rate of early and late-settled females for the 42-70 day period, my earliest observation penod (ANOVA F=0.51, p=.49, n=29). However at 71-98 and 99-126 days, late females fed their chicks at a higher rate (71-98 d: F=9.79 p=0.005, n=39; 99-126 d: F=4.41, p=0.046, n=32, Table 4.1). At 127-154, 155182 and 183-210, significant differences were not found (Table 4.1). No significant differences were found in the contribution to feeding by earlyand late-settled males (early-settled=0.43 feedings per 3 days, late-settled=0.24 feedings per 3 days; Mann-Whitney U=8.5, p=0.13, n=6,6), except that latesettled males contributed for a shorter period of time (early chicks=105.3 days, SE=5.4, n=18; late chick=65.4 days, SE=4.11, n=14; Mann-Whitney U=15.5, p<0.0001 ). To test whether the high feeding frequency of late-settled mothers was an increase in their own effort or whether this increase was associated with a late increase in food availability, I compared the total feeding frequencies of earlyand late-settled nests as a function of the time (month) of the year (March to July). Late-settled nesters fed their chicks 45% more frequently than earlysettled nesters on the same days (early-settled nests: mean=0.42 feedings per day, SE=0.4, n=45 recording days; late-settled nests: mean=0.61 feedings per day, SE=0.4, n=45 recording days; ANOVA F=10.29, df=1, p=0.002; Figure 4.2).

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114 I analyzed chick gro\A^h for earlyand late-settled nests using the average laying date as a splitting criterion. Late chicks grew faster than early chicks in terms of maximum growth rate (Early=16,9 g/day, SE=0.08, n=20; late=20.7 g/day, SE=1.4, n=17; Mann-Whitney U=94.5, p=0.02), age of maximum growth rate (early=39.0 days, SE=4.1, n=20; late=29.1 days, SE=4.0, n=16; MannWhitney U=93.0, p=0.03) and the age at which asymptotic mass was reached (early=1 37.48 days, SE=3.7, n=21; late=111.85, SE=7.1, n=17; Mann-Whitney U=50.0, p=0.002, Figure 4.3). The culmen and ulna length data showed the same trend (Figure 4.4, 4.5). In addition, chicks from late-settled nests flew 16 days younger than chicks from early-settled nests (early=184.8 days, SE=3.79, n=18; late=168.6, SE=6.1, n=7; ANOVA F=5.07, df=21, p=0.03). Higher growth rates of the chicks from late-settled females could be due to the female's tactic to reduce the vulnerability of the chick when male desertion occurs or alternatively it could be due to an anticipation of female to cope with the decline of feeding conditions later in the season. Consistent with the former hypothesis is the result that the body mass of the late chicks immediately before male desertion was 30% (SE=5.22%, n=14) greater than the average body mass of same-age, same-sex early chicks (paired t-test=2.71, df=26, p=0.0117). This is the proper comparison since in both cases chicks were raised by both parents at the same age. Also I separated male and female chicks because female chicks are larger than males (See Chapter 5).

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115 Discussion As expected from the optimization hypothesis, females compensate for the absence of the male by increasing their feeding rate (by 32%) after the desertion of the male. Late-settled females increased their feeding rates by 50% as compared with early-settled females and actually increased the growth rate of their chicks above that achieved by chicks from early-settled nests at the same age. Male desertion is more costly for females of late-settled breeders than for early-settled females, so some counter-strategies can be expected from the females of these nests. Increased feeding rates and faster chick growth rate could be a tactic adopted by late females to cope with male desertion early in chick life. I call this possible tactic "extra-compensation" by late-settled females. Faster chick growth may increase the chance of chick survivorship when coming from nests established later during the breeding season by increasing their chance of surviving premature male desertion (the desertion of the male when the chick is still at risk of dying due to the lack of the father's attention). When male desertion occurs, the chick is big enough to survive with the feedings delivered by the female alone. Actually, by feeding the chicks more frequently, late females provided extra-compensation for the absence of males (Figure 4.6). In Figure 4.6, 1 sketch the desertion decision of males and the growth rates of early and late chicks. We can expect some advantage to females from increasing the growth rate of their chicks if the male leaves early. For example, by increasing the chick growth rate by 10%, latesettled females can increase the survival probabilities of the chicks by, say, 10% before a premature male desertion. This tactic could allow the females to increase the chick's chances of survival by 10% when male desertion occurs, as it inevitably does. The benefit

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116 only depends on where the chick survival curve crosses growth curves of a chick from early and late-settled nests and the difference in the probability of chick mortality at the two intersections (Figure 4.6). The data support this hypothesis since the body size of late chicks immediately before the desertion was higher than the body size of the chicks of the early females when most of them were fed by both parents. A possible alternative explanation here is that if food conditions improve later during the breeding season (in frigatebirds, it seems that chick production matches the increase of food availability, Carmona et al. 1995, Chapter 1 ), we can expect that the increase is only a consequence of greater abundance of food. This was not the case in this study. The total amount of feedings by late-settled adults to their chicks was higher than the feeding frequency to early-settled chicks from March to June (Figure 4.2). The assumption in this analysis is that early and late-settled individuals react equally to food abundance. The only way to test unequivocally this hypothesis is by removing the male of early and late-settled nest and observe the modification of feeding rates by females. I do not know why early mothers do not provide additional food to their chicks. However, I can speculate that if there is no benefit from increased growth rate for early chicks (i.e. chicks are not becoming independent early), and if increased chick feeding imposes costs on the mother, a more conservative strategy of early females could be expected. An alternative interpretation is that late-settled females are increasing their feeding rates to the chick to reach a bigger chick size early not as a tactic to cope with premature male absence but simply anticipating the difficult feeding conditions (feeding and fishing) during the rainy season starting in late June at this locality. If they started breeding late during the season, their chicks are going to be younger and more vulnerable when the rainy season starts. In this

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117 case we can expect that females should feed the chick faster from the beginning and feeding should be disconnected from the time of male desertion. The evidence suggests that this is not the case in this species of frigatebird since feeding rates from late-settled females were statistically different (higher) only at 70 to 126 days, when chicks were growing faster and when males were deserting. Feeding rates were no different at the beginning and at the end during the chick-dependence period. In addition, although not evident in the weight and culmen growth rate figures, the ulna growth of iate-settled chicks overcame the growth rate of early-settled individuals at the time of male desertion (Figure 4.5), again suggesting an increase to diminish the impact of male desertion on chick survival. Extra-compensation probably is not the only strategy followed by deserted females in this population. Three sources of evidence suggest that sometimes the females also desert the chick after desertion by the male: (1 ) some dry chick corpses are found every year at their nests eliminating predation as a plausible explanation; (2) half of the dead or disappeared chicks were underweight (with respect to the average weight of a same age chick) the last day before their disappearance (chicks dead or disappeared in 38 out of 78 nests, in nine cases the corpses were found and in 29 cases the chick just disappeared, Chapter 1 ). We did not know the causes of death or disappearance but in 13 cases (43%), the chicks died or disappeared after a continuous mass loss. These 13 chicks were 27% below of the average mass of a surviving chick of the same age (SE=3.91 ). Death of the mother is an unlikely explanation in these cases since although I do not have data on adult mortality, five of the nine females where the dead chick was observed were seen at the colony the next breeding season. (3) There was a negative correlation between chick mortality after male desertion and the age of the chick (Chapter 3). In these cases we were unable to

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118 determine the causes of chick death, but It could be hypothesized that females (especially late ones) are more willing to contribute or complete the chick rearing if the chick is older than if the chick is younger, according to my predictions derived from the models. A large chick represents less future investment. Females should be evaluating their probability of rearing the chick to independence alone. The optimality model suggest the possibility that before the peak demands of the offspring, the best tactic of the individual when responding to a reduction in the parental care by the mate is a reduction of investment. I do not have data indicating that the mortality of the frigatebird chicks after male desertion is due to predation or female desertion but this is indeed a possibility. Finally, perhaps males are the deserting sex in frigatebirds because females may have larger rearing capabilities than males. Three pieces of evidence suggest this interpretation: (1) females are about 15% larger than males, (2) females always contributed more to chick feeding even when the male was present and (3) we did not record any situation in which the female apparently deserted early and the male fed the chick. If these situations occurred, probably males are unable to provide enough food for the chick, and the chick always dies. In summary, the alternatives of action by the females (the deserted sex) in frigatebirds seems to be diverse. Early-settled females compensate for the absence of the male and late-settled females perhaps extra-compensate for the premature absence of the male. In addition, some females may desert after the male's desertion when the size or condition of the chick or the condition of the female is poor. Increased feeding rate by late females and faster growth of late chicks could be a tactic of the female to reduce chick-mortality risks when males desert early during the chick's life. These findings in frigatebirds are consistent

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119 with the theoretical derivations made here: (1 ) females that were deserted when the chick was older, stayed with the chick and compensated for the absence of the male; (2) when males deserted early, females extra-compensated the absence of the male; and finally (3) in those cases where rearing conditions were presumably difficult, females probably deserted their chicks.

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120 Table 4,1 Feeding rates (feedings per 3 day) by females to chicks of early and late-settled nests as a function of chick age. chick age (days) settling time P early-settled late-settled 41-70 0.08 ±.334 (8) 1.18±0.26(12) NS 71-90 0.62 ±0.19 (14) 1.46±0.19 (13) ** 91-126 0.98±0.19 (16) 1.59 ±0.21 (13) * 127-154 1.09 ±0.33 (16) 1.78 ±0.37 (12) NS 155-182 1.24 ±0.23 (15) 1.00 ±0.26 (12) NS 183-210 1.21 ±0.32 (15) 0.33 ±0.75 (3) NS * p=0.05; ** p=0.005 (Two-way ANOVA)

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121 Early-settled nests _ Late-settled nests Chick age (days) Figure 4. 1 Feeding rate (number of feedings per three consecutive days per week) delivered by earlyand late-settled females.

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122 February March April May June July Date of the year (month) Figure 4.2 Total feeding rate (number of feedings per three consecutive days per week) delivered by males and females in earlyand late-settled nests as a function of time of the year. Sample sizes were 19 early and 19 late-settled nests.

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123 Figure 4.3 Growth (weight) of the chicks from earlyand late-settled nests (mean ± SE). Sample sizes dropped at 150 days of age.

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124 Figure 4.4 Growth (culmen length) of the chicks from earlyand late-settled nests (mean ± SE). Sample sizes dropped at 150 days of age.

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125 0 1 1 r 0 50 100 150 200 250 Chick age (days) Figure 4.5 Growth (ulna length) of the chicks from earlyand late-settled nests (mean ± SE). Sample sizes dropped at 150 days of age.

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126 Figure 4.6 Schematic representation of female extra-compensation in terms of chick survival. The scheme shows the growth rate of chicks from early (solid curve a) and late-settled (solid curve b) nests. Dashed lines represent the other growth rate for comparison (i.e., growth curve of chicks from late-settled grew at the same rate as those from early-settled nests). Increasing curves (thin lines) are the survival probability curves after male desertion. The male desertion date is symbolized by the vertical line in April. The arrows show the difference in survival for chicks growth at different rates. Notice that early-settled adults gain nothing by increasing the growth rate of their chicks. In contrast, chicks from late-settled nests have better opportunities for survival by growing faster than early chicks.

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CHAPTER 5 FLEDGING SEX RATIO AND THE COST OF REARING MALES AND FEMALES BY DESERTED FEMALES IN FRIGATEBIRDS Introduction In sexual species, male and female offspring are normally produced in equal numbers (Fisher 1958, Charnov 1982). Since the sex ratio of the offspring could affect the fitness of the parents and because in the long term, the payoff to the sexes is dependent on the sex ratio produced by other individuals in the population, equal investments in the production of male and female offspring should be the evolutionary outcome in natural populations (Charnov 1982, Maynard Smith 1982). However, different costs of producing males and females and differential mortality of sexes during the period of parental care can influence the sex ratio of the offspring at the time of hatching and eventually at independence (Charnov 1982). Under these circumstances, if parents are investing equal amounts of energy in producing male and female offspring, but if males are more expensive to produce than females, the result should be a biased offspring sex ratio in favor of the cheaper sex (Slagsvold et al. 1986, Teather 1987). According to theory, the mating system and the survivorship of offspnng after the end of the parental care period should not influence the 127

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128 expected sex ratio at hatching (Charnov 1982). That means that with any adult sex ratio, it is still stable for parents to invest equal amounts of energy in the production of male and female offspnng. On the other hand, if one sex dies more frequently during the period of parental care, an over-production of the sex having more mortality is expected (Charnov 1982). The evidence from natural populations of birds indicates that differential costs of producing the two sexes and differential mortality are frequently associated (Clutton-Brock et al. 1985, Slagsvold et al. 1986). Different costs of producing male and female offspring have been suggested as factors that influence the offspring sex ratio, especially in sexually size dimorphic species. In such species, the sexual size differences have been associated with different demands for food (amount and dependency period). In addition, different demands for food may induce different mortalities on the sexes. In such a case, the more demanding sex could also be the more susceptible to starvation and in consequence be the most vulnerable to death (Clutton-Brock 1985, Slagsvold et al. 1986). Since the effect of these two costs on the offspring sex ratio are opposite, we can expect only weak sex-ratio biases under these circumstances. Demonstrations of biased offspring sex ratios in birds are frequent in the literature (Clotfelter 1996, Major and Kendal 1996, Telia et al. 1996). However, demonstrations of the differential cost of males and females are rare (Slagsvold et al. 1986, Teather 1987, Telia et al. 1996). This is related to the problem of measuring differences in parental investment. Sexual differences (size dimorphism) do not necessarily mean differential investment from parents

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129 (feeding rates, food amount; leather 1987). Offspring may differ in the rate of fledging or in the efficiency with which they utilize food (Clotfelter 1996). Facultative Sex Ratio At the level of the whole population, a 1 :1 sex ratio is normally the evolutionarily stable strategy. However, at the level of individuals, parents may manipulate the sex ratio of their offspring in ways that maximize fitness (facultative modification of the offspring sex ratio; Trivers and Willard 1973). This may occur (1 ) when there is high variance in the reproductive success of one sex; (2) when sub-adults help at the nest; (3) when differences in dispersion result in competition between parents and the philopatric sex for mates or resources or (4) when relative attractiveness of adults is variable. Rearing conditions (e.g., the condition of the female, food abundance), for example, can affect the sex ratio of offspring produced (Ankney 1982, Cooke and Harmsen 1983, Rayder 1983, Meathrel and Ryder 1987). Females can bias the sex ratio of their offspring at independence by over-producing the sex with the highest reproductive value. If the reproductive value of the offspring is predictable, and if females can alter the condition of their offspring, then females can achieve higher reproductive success by producing an excess of the sex with higher reproductive value (Trivers and Willard 1973). In birds, an alternative to this mechanism is that individuals may manipulate the sex of their offspring according to ecological conditions such as food availability by altenng feeding rates to sons and daughters (differential provisioning). In this way they produce more expensive offspring under conditions of food abundance. Another example

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130 is that females may increase their effort in the production of the sex with high reproductive value according to the female's survival probabilities (Blank and Nolan Jr. 1983), Under ecological situations when it is more difficult to afford expensive offspring, we can expect facultative sex ratio biases. Mechanisms for biasing the sex ratio include: (1 ) non random disthbution of sex gametes (meiotic drive, this mechanism may be especially likely in birds where the heterogametic sex is the female); (2) differential mortality; (3) selective rejection of the offspring; (4) siblicide coupled with a sex-biased laying sequence and (5) sexbiased provisioning (Stamps 1990, Gowaty 1993. Gowaty and Droge 1991). Sex Conflict About the Offsprino Sex-ratios Another interesting idea about sex ratios is that the male and female of a pair do not necessarily agree about the optimal sex-ratio of their offspring. Differential dispersion (or philopatry) of the offspring may increase reproductive costs for one parent over the other and reduce the future value of the offspring if, in the future, the offspring becomes a competitor of the parent for resources or mates (Local Resource or Mate Competition hypothesis; Stamps 1990, Gowaty and Droge 1 991 ). Under these conditions adults can benefit by favoring the over-production of the opposite or dispersing sex. As a result of this sex-ratio conflict, we can expect sex-biased provisioning to the offspring by males and females (Gowaty and Droge 1991, Gowaty 1993). Although this idea has been criticized for its use of the comparative method (Weatherhead and Montgomery 1995), at the level of individual behavior some evidence for differential feeding by males and females to their sons and daughters has been reported in some

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131 species of birds (see review in Gowaty and Droge 1991 , Ciotfelter 1996, but see Weatherhead and Montgomery 1995). Extending this idea, male and female might disagree over the sex of their offspring when they invest differently in offsphng rearing. Because of reverse size dimorphism (Chapter 1), intense male-male competition and the extremely different roles of males and females in caring for the chick and because of the difficult conditions experienced by late-settled females when rearing their chick alone after male desertion, frigatebirds make a good species in which to test current ideas about the function of sex-ratio biases. In the magnificent frigatebird, but not in other species of frigates, males desert the nest when the chick is very small (Chapter 3). Males desert at a particular time during the year, and females feed the chicks alone up to the time of independence. Reproduction in frigatebirds is a very long process. The total cycle for a successful pair takes 14 to 16 months. By deserting early, males are emancipated from the care of their chick after a period of five to six months of parental care. However, females engage in reproduction for more than a year (Chapter 1 and 3). Since the colony starts reproduction every year, deserting males are able to reproduce every year, whereas successful females are only able to reproduce every two years. The consequence of this breeding regime in this species of frigatebirds is that in the successful fraction of the population (pairs that rear their chick successfully to independence), males on average are reproducing more frequently than females. In addition, strong sex biases among fledging individuals have been reported in two populations of the magnificent frigatebird, Fregata magnificens at Barbuda island and in the Galapagos Islands (1.8 female/male ratio, Diamond 1972, 1973; 1.5 female/male ratio, Coello et al.

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132 1977), although no such bias was found at Isia Isabel in the Mexican Pacific (Durand 1992) nor in a population of the great frigatebird, Fregata minor on the Galapagos (Coello et al. 1977). Because the strong bias toward females was found and because of the different reproductive frequencies of males and females, Diamond (1972) speculated that the large female-biased production in some populations is a strategy by parents to compensate for the more frequent reproduction of males. This group selection argument is difficult to sustain on the basis of general theory (and this tactic can be invaded by an alternative selfish strategy, Maynard Smith 1982). The frigatebird offers a good opportunity to evaluate the sex-ratio theory and the costs of rearing males and females. Because of the strong sexual size dimorphism in the magnificent frigatebird (adult males are 15% smaller than females on average, Chapter 1), we can expect different costs of rearing males and females (or differential mortality biased toward the expensive sex). In this case, we can expect the over-production of males (the cheaper sex). In addition, because of male desertion, we can expect difficult chick feeding conditions for females, especially for those females established late during the breeding season (since in this case the male deserts early during the life of the chick, Chapter 1 and 3). In this Chapter I analyze (1) the differential size of male and female chicks and relate these differences to adult feeding frequencies and to growth rates and growth periods of male and female chicks; (2) I analyze the sex ratio of fledglings at independence. Theory predicts the sex ratio of individuals during their lifetime, however, the assumption here is that population level is reflecting the action of individuals. If a particular frigatebird pair is producing one offspring per breeding, from the population sex ratio we can derive the sex ratio of individuals;

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133 (3) I test the prediction that late-settled females, presumably in a more difficult situation for gathering enough food for the chick (since the male deserted early), can not afford the chick's requirements and they will produce a skewed sex ratio to the cheaper sex (males). (4) Finally, I analyze Gowaty and Droge's prediction of differential contribution of adults to male and female offspring. I analyze if male and female parents are feeding male and female offspring differentially and in consequence biasing the sex-mortality of their chick. Methods I studied the sex-ratio and the growth rate of chicks in the magnificent frigatebird at Isia Isabel, 30 km from the Pacific coast of Mexico. The study was conducted from 15 November 1993 to 27 July 1994, and from 10 November to 27 December 1994 and from 20 March to 10 April 1995. Individual Marking and Nest Visits Birds were marked using plastic numbered wing tags. Marking was conducted at the beginning of the breeding season from 17 to 21 November 1993 and from 10 to 27 November 1994. During these periods, we marked 275 and 100 birds respectively. Other birds were marked subsequently as they were captured at their nest.

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134 We visited every nest in the sample once a week to check for the presence of the egg or chick. We monitored the survivorship of every chick up to fledging. We weighed chicks at the nest using a Pesola spring balance (±12.5 g) and measured their culmen and ulna length using a measunng tape (±0.5 mm). Since nest disturbance causes chick loss when they are small (less than 20 days old), we started our weekly visits to the nests after 20 days. More observations during the transition to independence of fledglings were made in the next breeding season from the same observation post. We checked for the presence of the chick or egg at the nest during the behavioral observation sessions (see below). Behavioral Observations We observed and recorded the behavior of adults and chicks at the nest from 20 November 1993 to 21 July 1994. We recorded behavior at each nest three consecutive days per week, from 0800 to 1900 h (from 16 February to 20 July 1994) during the chick rearing period (from 40 days to 6 months chick age). The observing post was located at the top of a building, 30 to 150 m apart from the individual focal nests. Two observers alternated two hours observation sessions from 0800 to 1 800 recording data on up to 36 nests simultaneously. This large number of nests was possible because we recorded only a few specific behavioral categories and because behavioral categories were conspicuous (see below). In addition, every behavioral category was easy to record since frigatebirds are large (adult females are almost 2 m wingspan) and the behavioral patterns occurred infrequently (commonly one feeding per nest

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135 per three consecutive days per week). The behavioral categories were the presence of the adults at the nest, the time of arrival and departures of the adults to and from the nest and the frequency of feedings to the chick. Chick feeding . Chick feedings were recorded when the chick introduced its bill into the open mouth of the parent. In every interaction we recorded the identity (number) and sex of the parent and the chick involved. We scored this interaction even when we did not actually see food passing from the parent's bill to the chick's mouth. Some unknown number of feedings occurred at night so, I assumed that our chick feeding rates were estimates of the real feeding rate. Feedings to chicks younger than 20 days were very difficult to see so, I considered these data inaccurate and I excluded them from the analysis. Observations of Marked Birds. To monitor chick independence, we also observed the presence of marked birds (juveniles and adults) at the breeding site. We recorded these during our regular behavioral observations. In addition, once per week we walked around the island looking for marked frigatebirds. In the next breeding season (from November to December 1994) during our behavioral observations we recorded the presence of marked adults and juveniles.

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136 Data Analysis Chick age estimations . Since we recorded chick growth after 40 days, the precise age of chicks in our sample was unknown. We estimated the age of the chicks in the sample by interpolation from the culmen length growth curve fitted to chicks of this population in 1991 (Durand 1992). The average estimated age of the chicks in the sample was 40.6 days (SE=2.28, n=43). Sexing the chicks. Female chicks are larger than males at fledging. Sexing a chick was possible from culmen and ulna lengths of fledglings fitted into a discriminant function calculated for fledglings in these population in 1991 (Durand 1992). Discriminant function was validated using the culmen and ulna length of 16 chicks of known sex (8 females and 8 males, Durand 1992). The function was: y=-40.5199+0.12260(culmen length)+0.08955(ulna length); (p<0.0001) where if y>0; then female; if y<0; then male (Durand 1992). Chick growth . Growth rate was estimated for each chick in the sample from a polynomial function of the form: y=A+Bx+Cx^+Dx^+Ex'* (see variables in Chapter 1 ). Since chicks were not handled before 40.6 days of age on average, we used the initial average size of a small sample of hatchlings as initial size in each fitted curve (mass mean=81.25 g, culmen length mean=23 mm, ulna length mean=31.7 mm, n=3). Quality of curve fitting (r^) was high, ranging from 0.82 to 0.98 in the case

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137 of the mass (mean=0.92. SE=0.007, n=39); from 0.97 to 0.99 in the case of the culmen (mean=0.99. SE=0.0008, n=39) and from 0.97 to 1.0 in the case of the ulna length (mean=0.99. SE=0.0008, n=39). Maximum Growth Rate, the Age of Maximum Growth Rate and Minimum Growth Rate as an estimation of the asymptotic size were calculated for each chick in the sample from the derivative function of the polynomial fitted function. Maximum Growth Rate was the value of the maximum slope of the derivative curve, Age of Maximum Growth was the age at the maximum slope and the Age of the Minimum Growth was the age at the slope closest to zero or actually zero. Statistical comparisons of Maximum Growth Rate, Age of Maximum Growth Rate and Age at Minimum Growth Rate were made comparing the estimated values calculated for each chick from the fitted curve. Statistical comparisons of growth rate and sex were done using two way-ANOVA models. Behavioral Analysis Feeding frequencies for males and females to male and female chicks were averaged for each nest (feedings per three consecutive days per week) in blocks of 23 days for early and late settled nests. Two factors were analyzed simultaneously the sex of the offspring and the time of female settlement. Because of male desertion, the sample was too small to analyze statistically but a figure is added when appropriate as a reference. I used non-parametric tests (Mann-Whitney U, Wilcoxon test and Chi square and Fisher exact probability test) because of small sample sizes, nonnormal distributions, or because the assumption of homocedasticity precluded

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138 me from using the parametric versions (t test, one and two way ANOVA and Pearson's correlation). Results Chick Feeding Chick feeding was extremely infrequent. Chicks received on average 0.87 feedings per 3 day pehod (SE=0.095, n=28). At this rate each chick was expected to feed on average 0.29 times per day. There were no differences in the frequency of feedings delivered by the female to male or female chicks. Although females received 7% more feedings than males during the whole rearing period, this difference was not significant (Table 5.1; Figure 5.1). I could not analyze the feeding frequency of males to male and female chicks at the same time periods as females because the desertion dropped the sample size. Instead, I compared the feeding rate delivered by males during the period of 5884 days of chick age. For this period of time the sample was more extensive. In the comparison I included one average value per nest. There were no differences of the male feeding rate to sons and daughters (sons: mean=0.37 feeds per 3 days, SE=0.14, n=13; daughters: mean=0.60, 0.18, n=14; Mann Whitney U test T=1 3, p=0.51 ; Figure 5.2). There was a significant difference, however, in the chick age at which males deserted sons and daughters: early settled males deserted the nests with male chicks earlier (94 days of age,

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139 SE=6.44, n=8) than nests with female chicks (114 days old, SE=8.00, n=10 ; F=31 .84, df=28, p=0.00005). In late-settled nests, on the other hand, there was no such difference: males deserted the nest with male or female chick at the same chick age and when chicks were younger {males=66 days old, SE=6.21 , n=8; females=64 days old, SE=7.58, n=6). Chick growth and chick fledging Chicks grew slowly. The average growth curves for male and female chicks (mass, and culmen and ulna length) during the reahng period are shown in Figures 2.3 to 2.5. Sexual size dimorphism was apparent at 60 days and increased until chick fledging. Actually, near fledging, female chicks were 1 1 .7% heavier, 9.8% larger in culmen length, and 5.7% larger in ulna length than male chicks (Table 5.2). However, surprisingly, there were no significant differences in the maximum growth rate, age of maximum growth rate and asymptotic age of males and females regarding the body mass, and culmen and ulna length (Table 2.3). The only significant difference showed that female chicks reached the asymptotic size of the bill earlier than males (Table 2.3). Even though males flew 10 days earlier than females, the difference was not significant (males: mean=175.6, SE=5.1, n=12; females: mean=185.0, SE=4.6, n=13; MannWhitney U=52.0, p=0.17). Fledging sex ratio The sex ratio of fledglings in our sample did not vary from the 1:1 expected ratio (23 males: 17 females; Chi square=0.9, df=1, p=0.34). Another sample of 33 fledglings taken during the same fledging period was again not

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140 different from 1:1 ratio (20 males and 13 females; Chi square=1.49, df=1, p=0.22). In the whole sample of nests including 33 nests where the chicks were measured and 40 chicks in my original sample, the sex ratio was not different from the 1:1 ratio (43 males: 30 females: Chi square=2.31, df=1, p=0.13), although males were more abundant. The sex ratio from nests established early in the breeding season (in which males contributed longer to chick rearing), was not different from 1:1 ratio (10 males: 1 1 females; Chi square test=0.05, df=1, p=0.83). However, females from nests where the male deserted early produced a trend to a skewed ratio toward males. The sex ratio of these nests established late during the breeding season (where males deserted early because of the time-dependent desertion. Chapter 3) was 13 males to 6 females. However, this ratio did not differ significantly from a 1 :1 sex ratio (Chi square test=2.58, df=1 , p=0.11). Chick Independence Chick independence is a long process in frigatebirds. After fledging chicks continue to return to the nesting area to be fed by their mother. We recorded 22 (56%) out of 39 fledglings marked in July 1994 that were still present near their nesting area in November 1994; 18 (46%) were recorded present in December 1994. We recorded 13 (59%) and 8 (34%) of these chicks being fed exclusively by their mothers in November and December respectively, when my observations were more extensive. In March and April, 12 and 9 (31 and 23% respectively) were present. From these samples the sex ratio of males to females were: 23: 1 7 in July when the chicks fledged; 1 5:7 in November; 1 3:5

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141 in December: 7:5 in March: and 5:4 in April. None of these rations was significant (Chi square=0.9, df=1, p=0.34: Chi square=2.9, df=1, =p0.09: Chi square=3.56, df=1, p=0.06: Chi square=0.33, df=1, p=0.56: Chi square=0.73, df=1, p=0.11 respectively). Discussion The Cost of Reannq Males or Females In spite of the strong reversed sexual size dimorphism in the magnificent frigatebird (adult females are 11. 7% larger than males), there was only poor evidence that females were more expensive to produce than male offspring. Males and females reached their maximum and minimum growth rate at the same age. Although female chicks took longer to initiate flight than males, this was not statistically different. However, since females reached a larger size than males at fledging, they actually had to gow at a somewhat faster rate. Female chicks were also fed at the same rate as male chicks. If we assume that the quality and quantity of feedings per bout is equivalent, two interpretations exist for the lack of difference in feeding rate to male and female chicks: (1 ) males and females are using the same amount of energy in different ways or (2) females are more costly but my methods were not accurate enough to detect differences. Because of (a) my small sample sizes, (b) the consistent trends of females toward staying longer at the nest and (c) because females grew faster to

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142 reach a larger size in the same time, the second explanation seems more likely. In addition, food amount and food quality were not evaluated here but differences might exist. For example, females may be more costly since adult males that settled early during the breeding period deserted their sons 20 days younger on average than their daughters. Late-settled males shov^^ed no such effect. Consistent with the idea of no differential cost of rearing males and females, the sex ratio of fledglings was not statistically different from the expected 1:1 ratio (see also Durand 1992). If females had been slightly more expensive to produce than males, there should have been a bias toward the cheaper sex. A slight but non significant bias to the over-production of the cheaper sex (males) at fledging was consistent with the expected result from theoretical considerations. It is important to consider that the power of the statistical test to reject the null hypothesis with such a small sample is only about 20% and the power of the global test is still low (approximately 38%). With this low power it is likely that I am accepting a false null hypothesis (Toft and Shea 1983, Cohen 1969). A strong female-biased sex ratio at fledging was found in one population of the magnificent frigatebird in the Caribbean Sea (1 .8 female to male ratio, n=110; Diamond 1972) and a similar bias was found in a population on the Galapagos islands (1 .5 female to male ratio, n=1 03; Coello et al. 1 977). I did not find such a female-bias ratio in my sample (1:1, n=73), nor this bias was found in this population three years ago (1:1, n=158; Durand 1992). The reason for the extra-production of fledged female chicks in other populations is not understood but it has been speculated that this strategy is connected with the

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143 different breeding rates of males and females in this species of frigatebirds (Diamond 1972). The rationale for this explanation was that if males are reproducing more frequently than females, it could be advantageous for individuals to produce more females (Diamond 1972). There are two problems with this explanation. First, the reproductive value of (the expectation of success through) son and daughter production is, on average, equal, since each offspring has one father and one mother (Fisher 1958). Second, the reproductive success associated with son or daughter production is frequency dependent. Furthermore, if the sexes have a different cost of production it is expected that individuals are going to over-produce the cheaper sex. Assuming that the larger sex is also the more expensive one, we can expect that frigatebirds pairs will over-produce males not females. It is possible that the bias could be explained by condition-dependent effects however (see below). One possible explanation for inter-population differences in the sex ratio could be related to the sexing method used in the different studies. Diamond used the culmen lengths to validate a plumage difference between males and females. According to Diamond (1972, 1973) females in the magnificent fngatebird in the Barbuda population have white wing bars. This correlation has not been confirmed to date in other populations (Coello et al. 1977, Durand 1992, this study). In the Galapagos population, only the culmen length was used to differentiate the sexes (Coello et al. 1977), but some overlapping individuals were discarded from the sample. At Isia Isabel, this and a previous study (Durand 1972) used the culmen and ulna length of chicks simultaneously to determine the sex of fledglings. Durand (1 992) validated this method statistically by using the culmen and ulna measurements from 16 individuals of

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144 known sex (determined by dissection). In addition, Durand (1992) sexed the chicks using a highly significant statistical technique. Another possible problem could be the overlapping of generations. An abundance of juveniles from previous years is common at the breeding sites. In Durand's study and in this one, we were always certain that the chicks we measured were fledglings from the same breeding season. Furthermore, if there is any bias in mortality after fledging or a tendency for juveniles from one sex to remain at the breeding site (differential philopatric tendency of males and females), or if the fledglings were chosen only on the basis of plumage (juvenile individuals have white-heads) there could be a bias in estimating the sex ratio. Biases in sexing the chicks and biases in choosing chicks from the proper cohort could contribute to the differences among studies in the estimation of sex ratio. The Condition Dependent Sex-bias Hvpothesis The Condition-Dependent Sex-Bias Hypothesis suggests that under predictable circumstances, females can manipulate the sex ratio of their offspring to their benefit. In the original form, this hypothesis suggests that if there are differences in the reproductive value of male and female offspring, and if the condition of females can influence the future reproductive value of the sex with the higher variance, females would be expected to bias the sex ratio, i.e. to over-produce the sex with the higher variance, when in good condition but preferentially produce the sex with smaller variance when conditions are poor (Trivers and Wiilard 1973). Another view of the same theory is to over-produce the cheaper sex when the rearing conditions are difficult and produce the more

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145 expensive sex when rearing conditions are favorable. In the magnificent frigatebird, because of the obligatory desertion of the male duhng a narrow period of time in the year, males from early-settled nests contributed longer to chick rearing (Chapter 3). On the other hand, males from nests established late during the breeding season contributed less to chick rearing. In this study I also show that the survivorship of the chick is negatively correlated with the age of the chick when male desertion occurs (Chapter 3). According to this information, late-settled nests are the more difficult condition for chick rearing. Since female chicks may be particularly expensive in periods of food shortage, there should be incentive for late-settled females to bias the sex ratio of their chicks in favor of the cheaper sex. Under these difficult circumstances, adult females may be unable to afford the requirements of the larger female chicks. As a consequence a biased sex ratio of late-settled pairs toward sons is expected. My results show a trend toward over-production of males in late-settled nests. Since globally the sex ratio of the whole population is not likely to be different from 1:1 ratio, this could explain the over-production of females by early-settled females. It might also explain the observed differences between populations, if the various studies differentially sampled individuals from late-settled nests and if there were an overproduction of males by late-settled females or if data were collected after the sons had already left. No significant differences were found but if the trend were validated, two mechanisms may exist for the over-production of males. First, late-settled females are producing an excess of males at fertilization. I do not have evidence of the sex ratio at fertilization in frigatebirds but these biases have been reported in other birds (Telia et al. 1996). The second mechanism is that

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146 female chicks are dying more frequently. I do not have evidence for differential mortality of male and female frigatebird chicks, nor evidence for the differences between lateand early-settled nests. However, there is some circumstantial evidence: I dissected 5 corpses of chicks found at the nesting site, three of them were females and two were males; the three male chicks were found early (10, 26 February, 6 March) during the breeding season and the three females were found late (20, 22 March, 16 June). Female chicks from late-settled nests could have died more frequently because male adults in these nest are deserting early. From early-settled nests we know that males are leaving later when they have daughters, suggesting that daughters require more attention. Adult Male and Female Conflict About the Offsprino Sex-ratio Males preferentially feeding one sex and females preferentially feeding the opposite sex could be considered a division of labor. However, when the value of the sexes is affected by this feeding pattern, a conflict may arise in the optimal sex-ratio for male and female parents. The argument here is that selective pressures differentially influence the fitness of males and females. In the case of frigatebirds, it can be expected that both sexes differ in their optimal sex-ratio (the sex-ratio of offspring that maximizes the reproductive success of the parent) simply because males are investing less in rearing the offspring. This conflict could be even more critical for late-settled nests. The trend to over-production of males in late-settled nests can not be considered evidence of the conflict since (1 ) mothers were egalitarian in feeding sons and daughters

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147 and (2) if the male bias was related to daughter's mortality, that mortality might be the by-product of the early desertion of males. Finally, it is difficult to interpret these results as favoring the Local Resource and Mate Competition Hypotheses since there is no information available about offspring dispersion in frigatebirds. The conditions for local competition are stringent (and very special) and unlikely in this species (see Chapter 1). In the magnificent frigatebird, in spite of the reversed sexual-size dimorphism, little evidence exists for differential costs of reahng males and females. Males and females were fed equally and they grew at the same rate initially but eventually females grew faster since they reached a large final size. However, early-settled males stayed longer with daughters than with sons before deserting. The global sex ratio of a sample of fledglings was not statistically different from the expected 1.1 ratio. Nevertheless, a non-significant bias in the over-production of males was found especially in late-settled nests where males desert at a young chick age. There was a trend in late-settled nests to overproduce males at fledging. Differential mortality of female chicks late in the breeding season could account for the possible bias, but other explanations are also possible. In particular, females may increase their future reproductive success by laying female chicks in early-settled nests and male offspring in latesettled nests.

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148 Table 5. 1 Comparisons of the average number of feedings delivered by the mother to sons and daughters. chick age (days) feeding frequency (3 days per week) sons daughters F-value (df) P 40-65 0 79 (+0 32) 1 2R 1+0 '?P,\ 1.31 (16) 0.27 66-90 1.15 (±±0,20) 0.94 (±0.18) 0.61 (23) 0.44 91-115 1.43 (±0.21) 1.14 (±0.20) 1.05 (25) 0.32 116-140 1.35 (±0.36) 1.52 (±0.34) 0.11 (25) 0.74 141-155 1.05 (±0.24) 1.20 (±0.25) 0.10 (23) 0.74 156-180 0.62 (±0.65) 0.92 (±0.49) 0.13 (14) 0.72

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149 Table 5.2 Mean (±SE) of the asymptotic size at fledging of 23 male and 17 female chicks. variable males females t-value (df) p mass{g) 1290.20±33.64 1441.20+23.87 3.41 (38) 0.0016 culmen length (mm) 124.70±1.38 136.94±0.95 6.79 (38) <0.00001 ulna length (mm) 256.52±4.57 271.12±1.08 2.70(38) 0.01

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150 Table 5.3 The growth rate of 23 male and 17 female chicks. mean (±SE) of variable male female F-value (df) p maximum gro\A4h rate mass (g/day) 16.68 (±4.43) 19.85 (±3.00) 2.63 (35) 0.11 culmen length (mm/day) 1.52 (±0.15) 1.40 (±0.17) 0.69 (35) 0.41 ulna length (mm/day) 2.59 (±0.35) 2.98 (±0.24) 3.49 (35) 0.07 age of maximum growth rate (days) mass 48.04 (±17.44) 31.98 (±17.31) 0.00 (35) 0.99 culmen 6.95 (±0.38) 9.34 (±7.45) 0.15(35) 0.70 ulna 50.49 (±21.04) 55,81 (±5.96) 0.10 (35) 0.75 age of minimum growth rate (days) mass 137.15 (±17.02) AAA cr\ 1 14.50 (±10.59) 0.29 (35) 0.59 culmen 182.38 (±20.95) 150.31 (±11.68) 4.14(35) 0.05* ulna 150.22 (±15.37) 136.11 (±12.78) 0.00 (35) 0.99 * significant value

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151 Figure 5. 1 Feedings (mean ± SE) by the female to sons and daughters.

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152 Figure 5.2 Feedings (mean ± SE) by the male to sons and daughters.

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153 Figure 5 .3 Growth (mean ± SE) of male and female chicks.

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154 160 -1 140 0 50 100 150 Age (days) Figure 5.4 Growth (mean ± SE) of male and female chicks.

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155 300 -1 0 50 100 150 Age (days) Figure 5.5 Growth (mean ± SE) of male and female chicks.

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CHAPTERS CONCLUSIONS: MAIN REMARKS AND FUTURE RESEARCH The unusual breeding behavior of frigatebirds has been suggested as an adaptation to food scarcity (Nelson 1975). Long reproductive periods, single egg clutches, slow chick growth, long periods at the nest when the mate is away, extremely low feeding frequencies to chicks, and high chick resistance to starvation, all are characteristics that have been associated with a very specialized diet, and complicated feeding technique (Nelson 1975). However, among the five species of frigatebirds, the magnificent frigatebird is clearly the most divergent (Chapter 1 ). The hypothesis here is that the disparate rearing roles of adults and male desertion in this species is associated with differences in their feeding ecology: magnificent frigatebirds feed in coastal areas while other species of frigatebirds breed and presumably feed in pelagic waters. If the magnificent frigatebird has more access to opportunistic food availability associated with humans, such as human fisheries or the availability of other food items close to the shore, rearing abilities of adults may increase and males may do better by deserting and looking for another partner in the next breeding season than by continuing to care for the present chick. After this study, the breeding biology of the magnificent frigatebird is well known but more detailed information from other species of frigatebirds is still needed. For example, we need to confirm the reproductive frequencies of males and females in the other species and the roles of males and females in rearing the offspnng. Are males 156

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157 in the other species sometimes deserting? Are the feeding rates to chicks really higher in the magnificent frigatebird when compared with other frigatebird species? Comparative work using the same or similar methodologies in different populations or different species in the same habitat and information about foraging times, foraging success, diet and foraging area are necessary to establish whether differences in feeding behavior correlate with feeding ecology. The copulation pattern of the magnificent frigatebird did not function exclusively to fertilize the egg. Instead paternity assurance in the context of the Sperm Competition Hypothesis seems to be the more likely explanation of the multiple intra-pair copulations in frigatebirds since some extra-pair copulations were detected (Chapter 2). Extra-pair copulations were probably underestimated in this population since only in a limited sample of pairs were both adults marked. Information about paternity is crucial to really test the influence of copulation frequency in the presence of extra-pair copulations. Almost 80% of the pairs that initially formed separated before egg laying. Since no observations of egg or adult predation associated with nest failure rates were detected at the study site, this high failure rate is intriguing. Probably some mate evaluation and some sperm competition is occurring during the nestbuilding and copulation period. Since the paternity technique has not been developed in this species, this speculation remains unexplored at this time. The theory of parental investment and mate desertion has been developed in some detail (Maynard Smith 1977, Grafen and Sibly 1978, Lazarus 1990). However empirical support is still scarce (Fujioka 1989). Researchers have looked for trade-off in kites (Beissinger 1987a, 1987b, 1990), warblers (Ezaki 1988) and Cooper's Hawks (Kelly and Kennedy 1993) but no trade-offs

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158 have been found. In frigatebirds early-settled males were able to obtain the best trade-off (Chapter 3). The male desertion system of frigatebirds is one of the few demonstrations of the trade-off between the current and future reproductive benefits of desertion. Since all males deserted the nest during a short period of time during the year; early-settled males deserted when their offspring were more likely to survive (with the attention from the female only) and they still had plenty of time to migrate and become reproductive again in the next breeding season. These individuals apparently are maximizing the trade-off between current and future reproductive success. Late-settled males, however, were constrained to a more difficult decision. Although they deserted their chicks at a younger age, late-settled males deserted later during the year (after the critical desertion date) and were unable to become reproductive again in the next breeding season. Why did these individuals not stay and care for their chick longer if they were not likely to return the next breeding season? One possible explanation for this pattern may be the consequence of an involuntary bias in the sample. If the chicks of very late-settled individuals are still very small when the critical desertion date for males is coming, we can expect those individuals to be sacrificing the survivorship of the chick by becoming reproductive again the next breeding season. Since these individuals are losing their chicks immediately after desertion, it will be very difficult to discriminate in the field between male desertion and chick predation. This means that very late-settled individuals are not well represented in the sample analyzed. Some support can be found for this idea since those individuals failing to reproduce in one season were equally likely to be present in the next breeding season (Chapter 3). Intermediate individuals were those that sacrificed future breeding opportunities by staying

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159 longer with the chick. Detailed records of chick mortalities and radio-tracking techniques can be used to analyze this possibility. It is still not clear why all male frigatebirds evolved to desert the nest at a particular time of the year. It can be speculated that if the molt is a very energy demanding process and takes a long time to achieve (5 to 6 months), males may reduce their effort and migrate to richer areas to feed and recover just with enough time to become reproductive again in the next breeding season. That may explain why deserters leave in late March and early April. Only 50% of the marked deserters returned to the breeding site the next breeding season. I do not have information about dispersion and survival of these individuals but several reproductive colonies exist in the range of dispersion reported for this population (Chapter 1 ), It is still possible that latesettled males that deserted slightly later during the year went to other colonies that initiated breeding later in the season. The lack of information suggests that in this widely dispersing species, my observations on the local breeding population are only a limited view. It is now important to work on this system at a larger scale, following individual movements for longer periods of time and at a larger spatial scale. Benefits, costs and constraints on male desertion and the role of females in caring for the chicks in frigatebirds are summarized in Figure 6.1 . In this figure the distribution of desertions is represented as a function of the critical desertion date for males, the survivorship probability of the chick and the growth rate of the chick for early and late-settled males. However, this schematic representation is only the first step to more specific and quantitative predictions about, for example, the timing of male desertion, the cost to males in chick

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160 mortality after desertion and the cost in future breeding opportunities for deserters. The next step is to calculate the probabilities of each curve in the scheme using data from natural populations and in the same common currency. This seems difficult but it is possible by transforming frequencies into probabilities and proportions and re-drawing the scheme to predict accurately when desertion or staying is expected in any year or under particular manipulations. Extra-compensation by the late-settled female to cope with premature male desertion is a new outcome not predicted by models of parental investment (Wrinkler 1987; Lazarus 1990). Clearly one effect of this extra-compensation is the increase in the size of the offspring at the time of premature male desertion increasing the survival probabilities of the offsphng (Figure 6.1 ). An alternative view is that late-settled females are not really paying attention to the desertion date of males since males do not really contribute to the chicks of late-settled nests, and they feed the chick more frequently to fledge the chick before the rainy season starts. The two explanations are not mutually exclusive. Only an experimental manipulation can differentiate the two alternatives. Extra-compensation is a tactic of the deserted individual, but some other strategies may occur in this population that are difficult to observe. Desertion by the female after the desertion of male and desertion of the female before the desertion of male are strategies predicted for some models (Lazarus 1990). These strategies, if occurring early during the chick's life, could be difficult to distinguish from other sources of mortality. Only by following individuals (radiotracking) for extensive periods of time and recording sources of mortality can we evaluate other alternatives.

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161 Another step forward in understanding desertion is to use the lessons from frigatebirds to model the role of deserted individuals in affecting the timing of male desertion. This model should integrate a more complex array of tactics by the deserted mate, taking into account the effect of the actions of parents on the survivorship of the offspring. In the theoretical framework used here, I merged the predictions of two models looking for some theoretical support for the extra-compensation by females (Maynard Smith 1977; Grafen and Sibly 1978: Lazarus 1990). My conclusion is that even though much theoretical work has been done on desertion, models are still simplistic when compared with the array of actions that organisms show in the field. Dynamic game modeling could be the proper tool to model the effect of simultaneous changes in several variables with time and, with different decisions of the two adults in the pair and with changing environmental conditions. One attempt using dynamic modeling of desertion has been recently developed for Cooper's hawks (Kelly and Kennedy 1993), but the decisions of the deserted mate as a function of the time of desertion were not specifically taken into account. Once male desertion has evolved, more consequences are expected. Different reproductive frequencies of males and females, more sexual competition, intense sexual selection, increased sexual dimorphism and possibly more differences in the cost of producing males and females are possible. This opens the possibility of biased sex ratios and the opportunity for adaptive sex ratio bias during difficult rearing periods. This is the suggestion implicit in the analysis of the cost of sons and daughters in Chapter 5. Data are consistent with this interpretation but there are several important pieces of information that we need in order to test this idea. It will be necessary to evaluate the sex ratio

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162 at the time of fertilization or at least during the egg stage and then determine the sources of chick mortality as a function of sex, the sex ratio at fledging and finally the sex ratio at independence. In addition, more accurate measurements on the costs of rearing by males and females and especially, a large sample size are needed. Methods are now available to accomplish all these tasks. In summary, frigatebirds have shov^n that in spite of a time constraint, males are evaluating carefully the best time to desert, taking into account the survivorship of the current offspring and their future reproductive opportunities. Females are compensating for the absence of the males and even providing extra-compensation when male care terminates early because of desertion. Male desertion may be more common in the magnificent frigatebird than in other members of the genus because greater food availability that allows female to care for the young alone.

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163 Figure 6. 1 Schematic representation of the trade-off between current and future reproduction in frigatebirds and female extra-compensation in terms of chick survival. The scheme is based on the critical desertion date for males. Chick growth from early(curve a) and late-settled (curve b) nests, survival curves (thin curves), proportion of males deserting (bars), critical desertion date (vertical line on April), probability curves after male desertion and growth curves for comparison (dashed lines). The arrows show the difference in survival for chicks that grow at different rates. Notice that early-settled adults gain nothing by increasing the growth rate of their chicks. In contrast, chicks from late-settled nests have better opportunities for survival by growing faster than chicks from early-settled nests.

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BIOGRAPHICAL SKETCH Jose Luis J. Osorno Cepeda was born in Mexico City in 1957. He obtained his bachelor's degree in biology at the Facultad de Ciencias of the National University of Mexico (Universidad Nacional Autonoma de Mexico, U.N. A.M.) in 1982. Then he worked as a research assistant at the Animal Behavior lab at the Centre de Ecologia under the direction of Dr. Hugh Drummond. During his time at this lab he studied for the Master in Science in Biology, again at the Facultad de Ciencias, U.N.A.M from 1989 to 1992. He worked on aspects of the reproductive biology of boobies for his bachelor's and master's theses. During 1987 to 1992 he lectured as teaching assistant and then as lecturer for Behavioral Ecology undergraduate courses at the Facultad de Ciencias, U.N.A.M. During these activities and as a laboratory for this lecture, he became involved in the biology of frigatebirds and hermit crabs, both biological systems that the author is still working on. He came to the University of Florida financially supported by the U.N.A.M. in 1992 to do his Ph.D. under the direction of Dr. H. Jane Brockmann, He worked on this dissertation with the magnificent frigatebird. He is married to Guadalupe Hernandez and has 2 children: Rodrigo (14) and Alejandro (11). He probably will be working at the Centre de Ecologia, U.N.A.M. at Mexico City, and as always, at Isia Isabel. 173

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I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philpsophy. y^/^^ in^Jane BrockmaKn, Chair Professor of Zoology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy.^ Louis J. Guillette Professor of Zoology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy. 1^ Richard A. Kiltie Associate Professor of Zoology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy. Associate Professor of Zoology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully ad^uat^, in scope and quality, as a dissertation for the degree of /Docto; Donald A. Dewsbury Professor of Psychology

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This dissertation was submitted to the Graduate Faculty of the Department of Zoology in the College of Liberal Arts and Sciences and to the Graduate School and was accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy. August 1 996 Dean, Graduate School