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Reproductive biology of a tropical procyonid, the white-nosed coati

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Reproductive biology of a tropical procyonid, the white-nosed coati
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Binczik, Gerald Allen
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vii, 120 leaves : ill. ; 29 cm.

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Animal reproduction ( jstor )
Animals ( jstor )
Female animals ( jstor )
Foraging ( jstor )
Fruits ( jstor )
Invertebrates ( jstor )
Mating behavior ( jstor )
Rainy seasons ( jstor )
Reproduction ( jstor )
Species ( jstor )
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bibliography ( marcgt )
theses ( marcgt )
non-fiction ( marcgt )

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Thesis:
Thesis (Ph. D.)--University of Florida, 2006.
Bibliography:
Includes bibliographical references.
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Printout.
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Vita.
Statement of Responsibility:
by Gerald Allen Binczik.

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University of Florida
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Copyright [name of dissertation author]. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
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REPRODUCTIVE BIOLOGY OF A TROPICAL PROCYONID, THE WHITE-NOSED COATI


By

GERALD ALLEN BINCZIK


















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


2006















I tarried in producing this document, and as a result two of the people I most wanted to share it
with did not live to see its completion. I offer my dissertation in their memory...

My mother, Rosemary Binczik

Professor John F. Eisenberg















ACKNOWLEDGEMENTS

Front and center in my thanks are of course my advisor, Dr. Louis J. Guillette, Jr., the rest

of my academic committee, Dr. Joel H. Brendemuhl, Dr. H. Jane Brockmann, Dr. Colin A.

Chapman and Dr. Melvin E. Sunquist, and Dr. John F. Eisenberg, who was unfortunately unable

to complete his service on my committee. Having always previously worked independently

(some might have instead said I was hard-headed), I learned as much as anything else in the

course of my Ph.D. program to make better use of the expertise and life knowledge I am offered,

and I am grateful to them for all that they shared (and tried to share) with me. Thanks go out, too,

to Dr. Rebecca T. Kimball for helping out on short notice at the end of my program.

The Lincoln Park Zoo Scott Neotropic Fund provided essential funding and the Florida

Museum of Natural History and University of Florida lent necessary equipment and laboratory

access. The field work in Tikal National Park, Guatemala, was permitted by the Consejo

Nacional de Areas Protegidas (CONAP) and the Instituto de Antropologfa e Historia. I am

particularly grateful to Lic. Oscar Lara of CONAP for his efforts over and above the call of his

office. Lorena Calvo and Carlota Monroy were also important allies in getting through the

bureaucratic tangles associated with starting a field project from scratch in a remote part of a

foreign country.

My time in the field was made much more fun by regular assistants Prudencio Tobar,

Fermin Lima and Don Luis Savala. The Universidad de San Carlos kindly loaned the very

capable Carla Ramirez as a six-month student intern. During nesting periods Benjamin Gonzalez

and Jos6 Tobar climbed trees that I as a big, clumsy gringo could not. Jen Boyd, Jason Brueck,

Aaron King, Bob Schuyler and Josh Vinlove were all crazy enough to volunteer for various

periods of time, as well. All of these people deserve much of the credit for the fieldwork's









successful completion. Dr. David Whitacre kindly provided housing to a number of people who

assisted in fieldwork, and he, Mario Jol6n and Haroldo Garcia just as importantly served as

sympathetic ears and apt problem-solvers in helping me to overcome the various obstacles that

inevitably arise in a lengthy field project. Dr. Denise Gross similarly helped by teaching me a

simple and inexpensive method for making blow-darting equipment, a skill which I am sure the

family dog was glad I did not possess in boyhood but which proved essential in the field. Maria

Jos6 Gonzilez was thoughtful enough to drop what she was doing in order to bring me a freshly

road-killed coati, in the process turning what would have been just another senseless animal death

on the national park road into a learning experience and scientific contribution.

Barbara Booth, Randall Harmon and Dan lisser not only provided much-needed visits

from home, but also took upon themselves the not-so-small task of bringing needed equipment

and supplies when I could not leave the field. The occasional postcards and letters that made it

through to me from my family, Rosemary, Anne Marie, David, Joan, Jason and Elizabeth

Binczik, also helped keep me going.

Mae Chisholm, Satish Degala, Jenny Gates, Patricia A. Lewis, Deidre Meiggs, Dr. Don

A. Samuelson, Doris Sartain and Dr. Samuel K. Wasser all provided essential assistance to my

efforts in the laboratory. Of special note in this regard is also Dr. Edward F. Orlando, a fellow

graduate student at the time who refreshed my memory on the ins and outs of steroid

radioimmunoassay, and much more importantly helped keep me sane during some tough times by

offering his friendship and collaboration; both were and are most welcome. Dr. Timothy A.

Pearce kindly applied his malacological expertise to snail identifications.

Last and of course most, my darling wife, Dr. Susan D. Booth-Binczik, not only stood by

me through much more than would the typical devoted spouse, but was also the best part of why

and how this study was completed. I can never fully repay my debt to her nor even fully express

my thanks, but I look forward to trying! I also look forward to finally putting the adjective

"professional" alongside the "collaborators" we have long been.
















TABLE OF CONTENTS
Page

ACKNOW LEDGEM ENTS ..................................................................................................... iii

ABSTRACT ............................................... ........................................................................... vi

CHAPTER

1 BACKGROUND ................................................................................................................... 1

2 REPRODUCTIVE SEASONALITY ......................................... ................ ......................... 4

Introduction ................................................................................................................... 4
M ethods......................................... ................................................................................ 8
Results ........ ........................................................................................................... ........ 15
Discussion .................................................................................................................. 38

3 BIRTH SYNCHRONY ....................................................................................................... 51

Introduction ..................................................................................................................... 51
M ethods........................................................................................................................... 53
Results ............................................................................................................................. 56
Discussion ................................................................................................................ 58

4 RUT.......................................................................................................................................... 64

Introduction ..................................................................................................................... 64
M ethods........................................................................................................................... 67
Results ............................................................................................................................. 74
Discussion ....................................................................................................................... 81

5 SUM M ARY ............................................................................................................................. 96

APPENDIX RAW TESTIS VALUES ................................................................................. 102

REFERENCES........................................................................................................................... 104

BIOGRAPHICAL SKETCH ................................................................................................. 120










v















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

REPRODUCTIVE BIOLOGY OF A TROPICAL PROCYONID, THE WHITE-NOSED COATI

By

Gerald Allen Binczik

May 2006

Chair: Louis J. Guillette, Jr.
Major Department: Zoology

Some 80% of the world's mammals reside in the tropics, but few-and almost no long-

lived-species there have been subjects of reproductive research. This study contributes detailed

information on the reproduction of a long-lived procyonid carnivore, the white-nosed coati

(Nasua narica), in Tikal National Park, Guatemala.

Whereas most tropical mammals display broad reproductive seasonality (e.g., producing

offspring within a six-month period) or reproduce year-round, the coati exhibits extraordinarily

tight timing in reproductive events. In Tikal mating took place within about two weeks in the

middle of the dry season, births occurred in a comparably short period at that season's end, and

young emerged from nests and began foraging alongside adults early in the wet season. When

the timing of parturition was examined in more detail, the interquartile range (i.e., middle 50%)

for females from three social groups spanned only five and six days in consecutive years, and the

mean birthdates in those years differed by only six days. The male coati has responded to reliable

clustering of female receptivity by evolving a rut more akin to that of many ungulate species than

to the pattern of any other carnivore species yet examined.









Coati reproduction is timed such that the young are weaned over an extended period

coincident with the season of greatest food availability. Leaf litter invertebrates and fruits figure

prominently in the coati diet, but the former are evidently most important. Notable among these

are insects, and in Tikal especially the scarab beetle Enema endymion; adults and larvae of this

one species accounted for 8.6% of all invertebrates consumed by coatis over the course of this

study. Communal care and predator swamping were explored as alternative explanations for the

coati's remarkable reproductive pattern, but these hypotheses were rejected.

Exactly how the coati achieves such tight reproductive seasonality remains unknown, but

a prediction based on the hypothesis that sociality plays a role was upheld. Social cues

exchanged among associates are presumably used by the coati to augment the weak

environmental cues (e.g., photoperiod) upon which seasonally reproducing tropical species must

otherwise rely.















CHAPTER 1
BACKGROUND

Although the white-nosed coati (Nasua narica) is a wide-ranging, locally abundant and

readily habituated diurnal carnivore, the most detailed studies to date have been of a single island

population. The majority of what is known and believed about coati ecology and reproduction is

based upon extensive behavioral observations by Kaufmann (1962), Russell (1979) and most

recently Gompper (1994) of a small group of animals on Barro Colorado Island (BCI), Panama.

The species is primarily insectivorous/frugivorous (Kaufmann, 1962), with some small

vertebrates taken opportunistically. Adult females are highly social, living with their immature

offspring in cohesive bands most of the year (except for a brief nesting period encompassing birth

and early lactation), and adult males are chiefly solitary (Kaufmann, 1962; Booth-Binczik, 2001).

Russell (1982; 1983) reviewed various hypotheses put forth to explain female sociality, and

asserted that it functions to protect juveniles from predation, most notably by cannibalistic adult

males (see also Russell, 1981), and ectoparasitism. Gompper (1996), however, concluded that

group living is a way for females to increase their foraging success on patchy resources, whereas

several studies at other sites have provided evidence that group living in coatis is an anti-predator

adaptation (Burger and Gochfeld, 1992; Booth-Binczik, 2001; Hass and Valenzuela, 2002).

The coati has received considerable attention for its unusual social system, but it is even

more notable among tropical mammals for its remarkable degree of reproductive seasonality.

Kaufmann (1962) and Russell (1982) addressed the timing of coati reproduction on BCI. The

species displays a strongly seasonal pattern at this locale, with apparently only one finely timed

birth period per year. The proportion of adult females reproducing can vary dramatically from

year to year; they are capable of delaying their first reproduction (which usually occurs at two









years of age) by one or two years, perhaps due to food availability, but generally reproduce every

year thereafter. Males mature later than females, and most probably do not reproduce until one or

two years after their first opportunity. It is unclear whether reproductive senescence occurs, but

Kaufmann (1962) observed one and Russell (1982) two older females (estimated to be at least

seven years of age) that did not produce young. Animals have lived to be more than 17 years old

in captivity; Poglayen-Neuwall, 1990.

A few reports (e.g., Gilbert, 1973; Hass, 2002 for Arizona; Valenzuela and Ceballos,

2000 for Jalisco, Mexico) suggest that coati reproduction may be patterned similarly at other

locations as well, but these have not been confirmed by thorough study. Moreover, even the

abundant behavioral/spatial ecological data for BCI fall short of satisfying the lack of basic

knowledge about coati reproductive biology. Many questions remain: Does the portrait

described for BCI apply elsewhere in the species' range? Where it is seasonal, is this largely

tropical mammal pursuing an obligate or facultative (i.e., opportunistic) strategy? What

evolutionary pressures drive seasonality, and what environmental cues are used in timing it?

This study addresses these questions by extending beyond prior research in four

important ways. It is the first intensive study of reproductive patterns in any coati population,

focusing on animals at a site that is distant from but ecologically similar to BCI. It is also the first

to examine male reproductive biology at any level. A much greater level of detail is presented on

certain environmental stresses confronting the coati with an eye toward resolving specific issues

left ambiguous by previous workers. Perhaps most important, this research provides the first

information on the reproductive physiology of the species.

The focus of the study is the free-ranging coatis in Tikal National Park, Guatemala. The

Park protects approximately 600 km2 of tropical moist forest in the seasonally dry "Mayan" forest

of northeastern Pet6n, and constitutes the centerpiece of Central America's largest remaining tract

of lowland rainforest (Nations et al., 1988). Unlike BCI (Willis, 1974; Glanz, 1982; Robinson,

1999) where ecological conditions could be considered somewhat artificial (Willis, 1974;






3


Eisenberg et al., 1979; Terborgh and Winter, 1980), Tikal retains a full complement of large

predatory species. The disagreement among studies regarding the adaptive value of coati group

living provides an example of the risks of extrapolating from data obtained on BCI to the species

as a whole. Studies at sites such as Tikal should be more useful for identifying selective

pressures important in coati evolution.















CHAPTER 2
REPRODUCTIVE SEASONALITY

Introduction

Mammals display two basic patterns in the timing of their reproduction (Bronson, 1989):

opportunism, in which they reproduce as often as conditions permit, and obligate seasonality, in

which one or more predictable environmental factors in combination with other life history

aspects compel them to follow a seasonal reproductive schedule. Evolutionarily, these are better

thought of as tendencies than rigid choices, and a single species may employ both strategies under

different conditions (e.g., the purple-faced langur, Presbytis senex; Rudran, 1973).

Obligate seasonality appears to be the strategy adopted by most long-lived mammals (i.e.,

those with lifespans of more than one year) inhabiting seasonal environments, especially species

with a substantial investment per offspring, specialized diet or extreme seasonal survival

mechanism such as migration or hibernation (Bronson, 1989). Ovarian function in such species is

regulated by the appearance of reliable proximate cues-especially photoperiodic changes-thereby

setting a schedule for sexual receptivity, ovulation and/or embryonic development. The most

environmentally sensitive phase of the species' reproductive pattern is timed to coincide with the

most favorable conditions for offspring survival (Lancaster and Lee, 1965; Sadleir, 1969).

Ultimate factors postulated to account for mammalian reproductive seasonality

(summarized in Sadleir, 1969; Bronson, 1989; Di Bitetti and Janson, 2000) include food

availability (both in terms of energy and essential nutrients), rainfall, ambient temperature,

predation pressure and competition. Of these, food availability (most notably energy intake) is

widely believed to be the strongest determinant of seasonality; other factors may modify a pattern

but are considered unlikely to override it (Bronson and Heideman, 1994).









There is an obvious logic to seasonal reproductive patterns among mammals at temperate

latitudes, where annual fluctuations in insolation profoundly affect temperature and the

availability of free water, factors critical at the base of essentially all food chains. But strong

seasonal weather patterns, particularly in rainfall, can also promote reproductive seasonality in

the tropics (Bronson, 1985). Tropical rainfall patterns have pronounced effects on the abundance

of all manner of terrestrial and arboreal food items, and climatic fluctuations could conceivably

also affect competition, predation and/or parasitism pressures on a tropical species.

Unfortunately, despite the fact that some 80% of all mammalian species reside in the tropics,

relatively few species and very few locations in the lower latitudes have thus far been examined

(O'Brien, 1993; Bronson and Heideman, 1994; Dubost et al., 2005).

In this respect, the lowlands of the Panama Canal Zone may have received more attention

than any other tropical site. In his review of the literature, Fleming (1973) found that half of the

species studied at this locality (23 of 45) were known to be seasonal breeders, with a strong

tendency toward birth or weaning occurring at the beginning of the wet season. This pattern is

exemplified by the region's best-studied carnivore, the white-nosed coati (Nasua narica).

Observations by Kaufmann (1962) and Russell (1979; 1982) indicate that coati

reproduction on Barro Colorado Island (BCI), Panama, is strongly seasonal: mating activity there

appears to take place early in the four-month dry season, litters are born late in that same season,

and young emerge from the nest and are gradually weaned beginning early in the eight-month wet

season. Scattered observations suggest reproductive events may also be seasonal at other sites

(e.g., southern Arizona: Gilbert, 1973; Hass and Roback, 2000; Costa Rica: Sienz, 1994).

Fruit and leaf litter invertebrates are the principal foods of coatis on BCI (Kaufmann,

1962; Russell, 1982; Gompper, 1996) and elsewhere (Delibes et al., 1989; Sienz, 1994). Smythe

(1970) examined fruit-fall on BCI in correlation with Kaufmann's (1962) data on coati life

history stages and concluded that the period encompassing parturition and first emergence of

young from their nests matches the time of greatest fruit supply. Russell (1982) compared coati









intake rates of fruit and animals, and concluded that reproduction is timed to allow juveniles to

begin foraging at the onset of a long-lasting peak in the availability of invertebrate prey; he

believed the concurrent availability of a major fruit crop was "perhaps fortuitous" (p. 428).

This discrepancy stems from the fact that on BCI the seasonal peak in size and abundance

of forest floor arthropods (at the onset of the wet season; Levings and Windsor, 1982) overlaps

substantially with one of two annual peaks in fruit availability (Foster, 1982b). Fruit availability

in neotropical forests often peaks at the onset of the wet season (van Schaik et al., 1993; Sakai,

2001). As arthropod abundance in tropical forests commonly varies positively with moisture

levels (Levings and Windsor, 1984; Burgess et al., 1999), such overlap is likely widespread.

Tikal National Park, Guatemala, is similar to BCI in that it is characterized by fairly

uniform temperatures and strongly seasonal rainfall (Fig. 2-1); there is a marked four-month dry

season from January through April and a six-month wet season from June through November,

with May and December being transitional periods. In contrast to BCI, however, the forests of

northern Guatemala are believed to have been significantly altered by the ancient Maya (Lundell,

1937; Puleston, 1982), whose horticultural practices likely favored species which produce

plentiful, nutritious fruit and tend to do so at what would otherwise be times of scarcity. For

example, the highly nutritious Brosimum alicastrum (ram6n, a.k.a. breadnut), a tree which has

been reported to undergo three heavy, evenly-spaced fruit sets per year (February-March, June-

July and October-November; Puleston, 1968; in Coelho et al., 1976), is unusually dense

throughout the region (Lundell, 1937; Puleston, 1982).

Given the above, it was anticipated that coati reproduction in Tikal would be highly

seasonal as it appears to be elsewhere, but that Mayan efforts there might have resulted in

sufficient temporal separation between peaks in fruit and invertebrate abundance to aid in

determining the relative importance of these foods to the timing of coati reproduction. Even if

peak overlap was found to occur in Tikal, it was believed that a more rigorous exploration of









Dry Season Wet Season


250


200


150


100


50


35 -


30 -


25 -


20 -


Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month
Figure 2-1. Mean ( SEM) monthly rainfall and maximum (filled squares) and minimum
(open circles) temperature in Tikal National Park, Guatemala, January 1984 through
April 1998. Number of years contributing to each mean ranges from 10 to 13 depending
on availability of complete month's data from the Instituto de Sismologia, Vulcanologia,
Meteorologia e Hidrologia (Guatemala City, Guatemala).









coati foraging habits accompanied by consideration of nutritional matters might clarify this issue.

The purpose of the present study was therefore twofold:

1. Coati reproductive phenological events were monitored year-round at Tikal to

document-and provide greater detail on-the species' reproductive seasonality at this new tropical

forest site.

2. The abundance and quality of potential coati food items and also coati foraging

behavior and body condition were monitored year-round to clarify the relationship between the

species' reproductive pattern and food availability.

Methods

Free-ranging white-nosed coatis were studied from June 1994 into November 1996 over

an area of approximately 20 km2 at the center of Tikal National Park (17N, 89W). The Park

protects nearly 600 km2 of forest that has at various times been identified as subtropical moist or

tropical semi-deciduous (Schulze and Whitacre, 1999; based on the classification schemes of

Holdridge et al., 1971, and Pennington and Sarukhan, 1968, respectively), tropical dry (Walker

and Cant, 1977; based on Holdridge, 1957), and quasi-rainforest (Lundell, 1937). Total annual

rainfall averages 1285 80 mm (based on the eight complete years of data between 1984 and

1998 available from the Instituto de Sismologia, Vulcanologfa, Meteorologia e Hidrologia,

Guatemala City, Guatemala). Located in the "Mayan" (i.e., ancient Maya-modified; J.F.

Eisenberg, pers. comm.) forest of northeastern Peten, Tikal constitutes the centerpiece of Central

America's largest remaining tract of lowland rainforest and retains a full complement of the

region's wildlife species (Nations et al., 1988).

Rainfall in the park during the study was recorded at a uniform time daily via a

government-operated weather station. From these data monthly totals were calculated for

comparison to various phenological data.

Fifty-five adult female coatis resident to four bands (females of this species live in groups

with their maturing young except to nest, whereas males are largely solitary; Kaufmann, 1962)









were utilized in this study. Animals were initially captured by live-trap or (more often) blowgun

and chemically immobilized by intramuscular injection of approximately 7 mg/kg Telazol (Fort

Dodge Laboratories Inc., Fort Dodge, IA). Anesthetized animals were tattooed and eartagged for

identification, weighed, visually examined to determine general physical condition and measured

as described below. Forty-three of the coatis were additionally fitted with 90 g motion-sensitive

radiocollars (Advanced Telemetry Systems, Isanti, MN) to enable subsequent location and

recapture, and to confirm death if such occurred. Individual females were recaptured by blowgun

(never more often than monthly) for resampling; the average number of immobilizations per

female was 2.6 + 0.2. All animal handling procedures were conducted as per protocol #4084

approved by the University of Florida's Institutional Animal Care and Use Committee.

In order to monitor reproductive state, size indices for the vulva and right anteriormost

teat were obtained during each female's immobilization. For each body part, the longest

dimension (L), the widest perpendicular dimension (W) and the highest dimension above the

surrounding body surface (H) were measured to the nearest 0.1 mm via calipers and then

combined in the formula V= L x W x H to produce an approximation of volume. One person was

responsible for taking these measurements throughout the study. Indications of pregnancy and

lactation were also noted. (Originally serum and fecal reproductive steroids were to be monitored

as well, but samples obtained for this purpose were rendered useless by a catastrophic freezer

failure after fieldwork was completed and before radioimmunoassays could be conducted.)

As a measure of body condition, an index of each coati's body fat level was also

determined at the time of immobilization. Following Hossler et al. (1994), a fold of the animal's

skin (i.e., excluding muscle) was pinched at the back of each rear leg midway between knee and

hip, and calipers were used to measure the thickness of this fold to the nearest 0.1 mm.

Measurements for the left and right thighs were averaged to produce the index reported for that

coati/immobilization. One person took all such measurements throughout the study.









The animals in three coati bands were habituated to the close presence of investigators,

who simply visited the bands frequently over several weeks and briefly baited the coatis at the

beginning of each encounter until the animals allowed themselves to be accompanied (without

additional feeding) for several hours thereafter. By the end of the habituation period it was

possible to follow animals so closely that at times investigators had to be careful not to kick or

step on them, and sometimes the coatis even had to be gently shooed a short distance away to

allow investigators sufficient room to process immobilized animals during captures.

Thereafter, the reproductive activities of habituated females were monitored ad libitum

(Altmann, 1974) one to three times per week (as often as their bands were visited) during the

period of detailed behavioral observations (see below) or as close to daily as possible during

periods of particular interest. Data on six reproductive phenomena were recorded.

Copulation was either directly observed or presumed based on the presence of mating

wounds (see Results for description of latter).

Pregnancy was generally identified by the midpoint of gestation, when an increase in a

female's girth became visually apparent.

Nesting was defined as beginning when a female departed from its band prior to giving

birth, and ending when the infants first accompanied the female down from the nest.

Parturition was determined to have occurred when a female showed a sudden

pronounced reduction in girth followed by continued nesting behavior, and was ultimately

confirmed by observation of young still in the nest or shortly after their emergence from the nest.

Reaggregation was operationally defined as the rejoining of a postpartum female and its

young with at least three other such females and their young.

Nursing was either directly observed or inferred from evidence of lactation noted during

a female's immobilization.

During nesting, 20 nest trees were climbed and nests examined to verify the presence and

count the number of young. Ages at which young were examined varied from approximately one









to five weeks after birth, depending on when nests were initially located and how soon thereafter

opportunities occurred to examine the nests without the females nearby.

Systematic observations of female coati foraging behavior were conducted from August

1995 through September 1996. Observation sessions were scheduled two to three times per

week, and in each case began as soon after first light as the target animals could be located

(typically by 08:30) and continued for several (typically four) hours thereafter. All-day (up to 10

hr) observation sessions were conducted once each month to confirm that activity patterns did not

change such that mornings were no longer appropriate for monitoring normal foraging behavior.

In each session, one 5-minute block of focal animal sampling (Altmann, 1974) was conducted

each quarter hour, rotating through focal animals opportunistically selected for that session;

during the nesting period each session instead focused on a single female (reducing sample sizes

during this period). In the selection of target animals for systematic behavioral observations,

priority was placed on distributing observation effort across females without respect to their band

membership, such that no individual coati served as a focal animal in more than one block per

hour (except in the nesting period), nor in more than one session per week.

During each sampling block, the amounts of time spent by the focal animal foraging in,

under and away from potentially relevant fruiting trees were recorded. Also recorded were the

type and number of food items consumed in each of these three areas, as well as the time spent

consuming the items; foraging time and time of food consumption were mutually exclusive

categories. The identities of animal prey were determined to the lowest taxonomic levels

possible, and fruits eaten were identified to species.

As bases for calculating monthly rates of foraging success, the three foraging areas were

used thus: The leaf litter invertebrate zone was the combination of under and away from fruiting

trees. The fruit zone was the combination of in and under fruiting trees. A given female's

monthly foraging success rates were then calculated as both number of items consumed per

minute foraging and number of seconds spent consuming the items per minute foraging, using









monthly totals for each zone. To eliminate evident outliers caused by undersampling of specific

individuals in specific months, females with fewer than 300 seconds spent foraging in a leaf litter

invertebrate zone or 20 seconds in a fruit zone in a given month were not included in analyses;

the monthly rates for the remaining females were averaged to produce the reported values.

Leaf litter and associated invertebrates were sampled on approximately the 5", 15" and

25h of each month from September 1995 through September 1996. On each collection date 10

samples were obtained. Each sample was collected by placing a bottomless tub, the area of which

was 1 m2, on the forest floor and quickly scooping the litter and invertebrates therein into a bag;

the soil thus cleared was then dug to a depth of three to four inches (as the substrate allowed) and

any additional animals found thereby were added to the bag. Exact sample locations and times

were determined by accompanying a foraging band of coatis for two to four morning hours and

placing the tub at the front edge of the band at random intervals (skipping any preselected times

at which the animals were not foraging).

Each sample bag was weighed fresh and then hand-sifted to harvest visible invertebrates..

Animals thus obtained were identified to the lowest practical taxonomic level and weighed to the

nearest 0.1 g; animals individually weighing less than 0.1 g were grouped by type and the total

weight for the group was used to calculate an average weight per individual. Voucher specimens

were occasionally preserved to aid species identifications, but otherwise invertebrates were

bagged by sample date and then frozen in liquid nitrogen and stored in an ultracold freezer for

subsequent nutritional analyses (see below). Finally, each sample's leaf litter was dried in the sun

for a minimum of two days (or more, as weather dictated) and again weighed to obtain dry litter

mass and litter moisture content. Monthly means were calculated for total invertebrate mass,

litter mass and litter moisture content. The individual contributions of various invertebrate

classes to monthly totals were examined by calculating their monthly numbers and masses on a

percentage basis.









Fruiting tree phenology was monitored from June 1995 through September 1996. Ten 10

m x 50 m plots were established at random intervals along 1 km of (and also at random directions

and distances up to 50 m from) each of three forest paths traversing the entire home range of one

coati band as well as parts of the ranges of three other bands. In each plot, all trees measuring at

least 10 cm diameter at breast height at the onset of data collection were tagged and identified to

species. Every month, each plot was randomly assigned to a group of 10 which was then

surveyed on approximately the 5h, 15th or 25th of that month. During surveys, tagged plants were

checked for the presence and percentage of immature and ripe fruit, and when fruit was present in

a tree it was quantified via the visual count method (Chapman et al., 1992). Samples of ripe

fruits were also collected to aid species identifications and frozen/stored as described for

invertebrates to provide material for later nutritional analyses (see below). One person was

responsible for determining fruit counts and percent ripe fruit in almost all months; a second

person trained under and performed calibration runs with the first person repeatedly throughout

the study before replacing the first person in the final month.

Using the above methodology, data were obtained on many more tree species than

appeared in the coati diet. Only those species which were ultimately seen being eaten by coatis

and/or appeared in their scat on at least 15 separate dates were selected for analysis and

presentation in this paper. The percentage of trees with fruit and the mean number of fruits and

ripe fruits per tree were calculated on a monthly basis for each of these species.

After field work was completed, proximate nutritional analyses were conducted on

monthly (i.e., mixed) leaf litter invertebrate collections and also on individual invertebrate and

fruit species deemed of particular relevance to the coati diet (as described above). Each sample,

consisting of either whole invertebrates or the edible portions of fruits, was first thawed, weighed,

dried for two days at 600C, allowed to equilibrate to room temperature overnight before being

weighed again, then finely ground and homogenized by use of a Wiley Mini-Mill equipped with a

20-mesh Monel screen (both Thomas Scientific, Swedesboro, NJ) prior to additional processing.









Crude fat and energy content were determined in nutrition laboratories of the University

of Florida's Animal Science Department following procedures outlined in Helrich (1990). To

obtain crude fat, samples were weighed, dried 3 hr at 1020C, equilibrated to room temperature

under desiccation and then extracted four times in ethyl ether using a Soxhlet apparatus.

Extracted samples were subsequently dried 12 hr at 1020C before being equilibrated under

desiccation and weighed once more; the amount of fat was calculated as the difference in mass

between pre- and post-extraction samples. Energy content was obtained by bomb calorimetry

using a 1261 Isoperol Calorimeter (Parr Instrument Co., Moline, IL) after samples had been

weighed into crucibles, dried at 650C for 24 hr, equilibrated under desiccation and weighed again.

Crude protein, ash-free neutral detergent fiber (NDFaf) and ash content were determined

in the Forage Evaluation Support Laboratory of the University of Florida's Agronomy

Department. Samples were first weighed, dried for 15 hr at 1050C and weighed again, and then

organic matter was determined by ashing for at least 4 hr at 5000C. Total nitrogen (N), and from

it crude protein (as N x 6.25), was obtained by a modification of the standard Kjeldahl procedure

(Helrich, 1990). Samples were digested using a modification of the aluminum block digestion

procedure by Gallaher et al. (1975); sample weight was 0.25 g, the catalyst used was 1.5 g of 9:1

K2SO4:CuSO4, and digestion was conducted for at least 4 hr at 375C using 6 ml of H2SO4 and 2

ml H202. Digestate nitrogen was then determined by semiautomated colorimetry (Hambleton,

1977) via a Technicon Autoanalyzer (Technicon Instruments Corp., Tarrytown, NY). Neutral

detergent fiber (NDF) was determined by the procedure of Golding et al. (1985), consisting of

boiling 1 g of sample in a neutral detergent solution for I hr, filtering, extracting with acetone and

then drying; NDFaf was obtained by correcting NDF for the amount of ash in the sample.

The moisture content of an initial sample was calculated by combining the results of the

relevant drying steps outlined above. Crude protein, crude fat, NDFaf, ash and energy content

were calculated on a dry matter basis. (It must be noted that the invertebrate and fruit samples

were subjected to the same storage freezer failure as were frozen serum and fecal samples,









although unlike the latter samples they appeared to take little or no harm from it. This topic is

addressed further in the Discussion.)

Sokal and Rohlf (1981) guided all statistical efforts, and SPSS 8.0 (SPSS, Inc., Chicago,

IL) aided computations. Correlational analyses were conducted to examine the relationships

between environmental variables, resource availability and foraging behavior. Pearson

correlations (r) were tested where scatterplots of the data appeared consistent with bivariate

normality, and Spearman rank correlations (p) were instead tested where this assumption

appeared to be violated or where samples were deemed too small for proper visual evaluation.

Because multiple comparisons were involved and there are numerous arguments against the more

elaborate methods that are often employed to adjust for such comparisons (Moran, 2003), a

conservative P, < 0.01 was adopted as the level of significance.

Results

Ordinarily each female underwent only one complete reproductive cycle (i.e., succeeding

at least to the point of rejoining a band with recently born young in tow) each year, but rarely a

female underwent a second cycle if pregnancy, nesting or early emergence was unsuccessful.

Accordingly and unless otherwise indicated, the following data pertain only to females' lone/first

yearly cycles.

Part or all of 11 copulatory events were observed; three of these (in two coati bands)

occurred from 13 to 16 February 1995, and eight (in four bands) from 14 to 28 February 1996.

Another 40 females (in four bands) were presumed to have copulated from 13 to 27 February

1996 based on the appearance of fresh mating wounds (see below).

In each of the three copulatory events observed in entirety, the female initiated mating by

leaving its band foraging on the ground, approaching one of the males perched in the tree canopy

above the foraging band (see Booth-Binczik et al., 2004, for a detailed description of the coati

mating system in Tikal) and standing beside the male with hindquarters oriented toward the male









and tail bent upward and to the side. The male briefly sniffed at and then mounted the female,

clasped its forelegs around the female's midbody and presumably intromitted intromissionn could

not be visually confirmed). In all observed copulatory events, coitus included bouts of rapid,

quivery thrusting alternating with bouts of apparent stillness by the male, accompanied

throughout by soft grunting or panting. It often appeared as if the female was attempting to leave

during the longer moments of copulatory stillness but was held fast by the male. Typically the

female ultimately broke free from the grip of the male's claws during such a bout-leaving long,

deep parallel scratches on the sides of the female's body in the process-then turned on the male

with loud squealing vocalizations and feinted or actual bites and paw swipes (events occurred too

rapidly to confirm the extent of physical contact) before fleeing down or even falling from the

tree and racing back to its band. On one occasion the female was instead simply released by the

male, walked away and then lay down and rested on the tree limb about a meter from where the

male remained perched. Complete copulations lasted 16, 19 and 48 minutes from intromission

until separation, although it should be noted that the first of these was concluded by the male in

coitus being attacked by another male (Booth-Binczik et al., 2004). The eight copulations

already underway when first observed continued for 2-29 minutes thereafter.

Eleven pregnant females (from two bands) were confirmed to have established nests in

1995, and 28 (from four bands) in 1996. In 1995, the first of these females that was observed to

depart its band to begin nesting did so on 12 April and the last did so on 24 April. In 1996 the

onset of nesting among females under observation ranged from 12 April to 30 April.

In almost every case a nest was occupied by a solitary female, but on three occasions it

appeared that pairs of females shared a nest at least temporarily. Nests were usually situated in

large, living trees, either in their crotches or in tangles of lianas hanging free from or lying against

their trunks, at a measured height of 9.8-30.2 m above the ground. They were constructed

primarily of interwoven slender, leafy branches and vines bitten off of living plants. Nests varied

in size and shape; most often they were approximately 0.5-0.7 m-diameter hollow spheres with









one or two entrances just large enough to accommodate a female, but occasionally they were

much more simply constructed open bowls/platforms up to about 1.5 m in diameter. In any event

the nest cavities/floors were lined with approximately 5-20 cm-deep carpets of small loose leaves,

tiny branches and bromeliad tufts into which the infants burrowed.

Females often stayed out of sight in their nests for a few to several days surrounding

parturition, making precise dates of birth seldom identifiable and in turn likely resulting in an

overestimate of birth period duration. Bearing that in mind, the earliest and latest that parturition

could have occurred among nine nesting females (from two bands) in 1995 were 16 April and 29

April, respectively, and 23 females (from two bands) gave birth in 1996 from 22 April to 9 May.

Despite the fact that a substantial effort was made to pinpoint the timing of reproductive events,

copulation and parturition could both be narrowed down to reasonably tight spans of time for

only one female; it gave birth 71 to 74 days after mating. For 18 litters examined while still in

the nest, average litter size was 4.0 0.3.

Late in the nesting period it was common for a female to move its young from one nest to

another, but the infants were not considered to have emerged (and the female to have concluded

nesting) until they followed their dam down to the ground and began foraging; thereafter the

female was rarely seen on foraging excursions without its young alongside. Eight females (from

two bands) brought their young down from the nest 27 May to 4 June 1995, and 15 (from four

bands) did so from 23 May to 19 June 1996. The process of reaggregration began so soon after

emergence that it was possible on only three occasions to determine with certainty how many

young individual females emerged with; these females (the nests of which had not been

examined) brought down four, five and six young.

Complete band reintegration was in some instances a lengthy process even though

females with infants reaggregated into small groups rapidly after nesting. The earliest and latest

points at which any of 14 females (from two bands) reaggregated in 1995 were 5 June and 29

June, respectively, and 20 females (from two bands) reaggregated from 31 May to 19 June 1996.









Nursing was almost never observed, presumably because it most often occurred in

various tree canopy roosts used by the coatis for taking brief siestas during the day and sleeping

at night. Incidences of nursing on the ground (in brush piles) were seen on 4 August 1995 and 27

July 1996. On 13 September 1996 a female was observed evading attempts by an infant to

suckle, and twice on 27 September 1996 (in a single band) infants were observed investigating

but not suckling from females' teats, suggesting that nursing concluded in the middle or last half

of this month.

Three females (in two bands) in 1995 and one in 1996 underwent interrupted

reproductive cycles followed by second, successful cycles; one more female in 1995 was believed

to be in the midst of a second cycle when initially encountered, and another female in 1995 died

while nesting in a second cycle. It was never possible to identify the specific causes) of

reproductive failure, but information on the point at which it was evident may be instructive.

Females returned to their bands (presumably soon) after reproductive failure, and dates on which

this phenomenon was observed were 30 April 1995 (i.e., at the end of the observed parturition

period) for three females, 23 May 1996 (late in the nesting period), and on or shortly after 5 June

1995 (soon after reaggregating with several other females; the exact date could not be identified

because it quickly became unclear which young belonged to which females).

Although much less information was obtained on second cycles, they appeared to

proceed similarly to lone/first cycles. Late mating was not observed. Pregnant females departed

their bands to nest from 30 July to 18 August 1995 and by 7 August 1996. Parturition could be

narrowly attributed for only one female, on or shortly before 12 August 1996; this animal's litter

contained four young when it was examined while still in the nest on 5 September. Females

concluded nesting and rejoined their bands from 3 September to 6 October 1995 and by 20

September 1996. The 1996 female brought to its band all four offspring that had been found in

the nest; three other second-cycling females brought one, one and two young to their bands.









Nursing by females undergoing second cycles was observed on 13 November 1995 and 24

September and 8 November 1996.

Reproductive morphometric changes exhibited by females throughout the study (Fig. 2-2)

were revealing of physiological events underlying the coati reproductive cycle despite the

unfortunate lack of hormonal data (see Methods). Sudden, pronounced vulval swelling-

presumably an estrogenic effect-was observed in immobilized females from 7 February to 19

February, i.e., beginning shortly before the mating period and ending about midway through that

period; a much smaller secondary increase in vulva size occurred in late March to early April,

within a couple of weeks before parturition and roughly coincident with the beginning of a

prolonged increase in teat size. Teat size-presumably reflecting estrogen, progesterone and

prolactin levels in turn-rose fairly rapidly from March through the parturition period to a peak in

late May to early June, then declined more slowly until it again reached baseline around the end

of September, about the same time that lactation/nursing apparently concluded. (Note: The

greatest teat size observed in the study actually occurred on 5 September, but this data point was

unique in that it belonged to a female that was in the midst of a second reproductive cycle and

therefore out of step with its cohorts.)

The amount of leaf litter varied seasonally in strong positive correlation to rainfall (r[i =

0.81, P = 0.001), as did the overall mass of litter invertebrates (Table 2-1), falling from highs at

the onset of sample collection in September 1995 to lows in February and March 1996 before

rising again to moderately elevated levels that essentially held steady from June 1996 until the

conclusion of sample collection in September 1996 (Fig. 2-3). Leaf litter moisture content (Fig.

2-3) varied less from month to month, and although it too resembled the rainfall pattern in some

ways (e.g., rising gradually from a low reached in March 1996), the correlation between these

was not significant (r[I ] = 0.41, P = 0.17). Rainfall over the course of sample collection (Fig. 2-

3) resembled the typical year (Fig. 2-1) except that rains were somewhat heavier than usual in the

middle of the 1995 wet season and unusually light in the middle of the 1996 wet season.












Dry Season Wet Season

5 O
_^ i-
S4 Vulva

o 3

S2 c
1 B -


> 0 rM Eiln g &^iEl a l in 1:1DD ^ifi 1111l ilTTT1

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

S9 C-

| ~ Teat
I -,
26 -


32 .2.


0 'F'FZ' Ti1 "
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Date

Figure 2-2. Annual vulva and teat size profiles exhibited by adult female white-nosed
coatis in Tikal National Park, Guatemala, July 1994 through October 1996. Mating
period (13 Feb 28 Feb) indicated by lightly shaded background and period of parturition
(16 Apr 9 May) more darkly shaded. Based on measurements obtained during 139
immobilizations of 55 animals.








Wet Season Dry Season Wet Season


Rainfall


0
300 -


200-


100 -
-^zo


Litter Invertebrates










Dry Litter






..........


Litter Moisture


Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Month
Figure 2-3. Monthly total rainfall and mean ( SEM) leaf litter characteristics in Tikal
National Park, Guatemala, September 1995 through September 1996. Thirty 1-m2
quadrats sampled each month.










Table 2-1. Correlational statistics for relationships between monthly leaf litter invertebrate data
and rainfall, dry litter weight and litter moisture content in Tikal National Park, Guatemala.
Thirteen consecutive months compared except where otherwise indicated; significant findings
indicated in bold.

Invertebrates Rainfall Litter Weight Litter Moisture


r = 0.91, P< 0.001


r = 0.82, P = 0.001


r = 0.55, P= 0.05


Nutrient Content
water
crude protein
crude fat
energy

Snails and Slugs
number
mass

Earthworms
number
mass

Centipedes
number
mass


Millipedes
number
mass

Arachnids
number
mass

Insects
number
mass


a
ar=
a
r=
a
r=


0.48,
0.54,
0.67,
0.56,


P = 0.08
P = 0.05
P = 0.008
P=0.04


r= 0.52, P = 0.07
r= 0.14, P=0.64


r= 0.65, P= 0.02
r= 0.36, P= 0.23


r = -0.38, P= 0.20
r= 0.47, P=0.10


r= 0.02,
r= -0.10,


P = 0.94
P = 0.75


r= 0.57, P=0.04
r= 0.12, P=0.68


r= 0.68,
r= 0.85,


P = 0.01
P < 0.001


0.36,
0.34,
0.48,
0.36,


P = 0.22
P = 0.26
P = 0.09
P = 0.23


r = 0.66, P = 0.01
r= 0.06, P= 0.83


r= 0.33, P= 0.28
r= 0.12, P = 0.70


r = -0.08, P = 0.80
r= 0.81, P= 0.001


r= 0.14,
r= 0.03,


P = 0.66
P = 0.92


r= 0.59, P=0.03
r= 0.17, P=0.58


r= 0.85,
r = 0.82,


P < 0.001
P = 0.001


r= 0.32,
r= 0.05,
r = -0.05,
r = -0.03,


P = 0.29
P= 0.88
P = 0.87
P = 0.93


r= 0.20, P= 0.50
r= 0.36, P= 0.22


r= 0.64, P=0.02
r= 0.65, P = 0.02


r=-0.25, P = 0.41
r= 0.12, P = 0.69


r= 0.38,
r= 0.23,


P = 0.20
P = 0.45


r= 0.42, P=0.16
r= 0.23, P = 0.46


r= 0.34,
r = 0.25,


P = 0.25
P = 0.42


a based on comparison of 14 consecutive months

Leaf litter invertebrate groups varied considerably from one another in their temporal

patterns of number and mass (with spiders and insects even differing within their own groups), as

reflected in their contributions to monthly totals of these measures of abundance (Figs. 2-4 to 2-

6). Examination of the relationships between invertebrate class numbers and masses (not

proportionate numbers and masses) and environmental variables (Table 2-1) reveals that insects


Total Mass









were principally responsible for the correlations of overall invertebrate abundance with rainfall

and litter mass.

Insects (Fig. 2-6) dominated the leaf litter fauna in overall abundance, but there were a

few monthly exceptions: Earthworms (Fig. 2-4), the second most prevalent group overall, were

slightly more numerous in October and December 1995 and weighed more in July and August

1996. Millipedes (Fig. 2-5) were slightly more numerous in February 1996. Snails and slugs

(Fig. 2-4) were most prevalent by weight in May 1996. Spiders (Fig. 2-6) were always fairly

abundant but never contributed much weight to samples, and were never predominant in either

regard. Centipedes (Fig. 2-5) were generally scarce and contributed negligible weight even when

modestly abundant in March 1996.

Within Insecta (Fig. 2-6), beetles and their grubs were notable in that they were always

among the most abundant orders and contributed substantially more weight than any other order

in every month except April 1996, when orthopterans dominated. The contributions of a single

large scarab beetle species, Enema endymion, figured most prominently. The adults and larvae of

this species were so common in the vicinity of the park that they were known by unique names

(ronrones and gallinas ciegas, respectively) by the local people, and were at certain times of the

year extraordinarily abundant atop or in the leaf litter or at shallow depths in the soil beneath it.

By weight, adults constituted 34.2% of the June 1996 invertebrate sample, and larvae amounted

to 60.4% in September, 69.9% in October and 51.3% in November 1995 samples, and 6.3% in

August and 22.0% in September 1996 samples. Adults appeared in the coati diet (more on this

below) or scat or were noted to be abundant in general observations made aside from leaf litter

invertebrate sample collections from 8 June to 16 July 1994, 15 June to 4 July 1995 and 12 May

to 17 July 1996. Larvae were similarly recorded from 17 August 1995 to 13 January 1996 and 17

July to 8 November 1996 (when field work concluded).

Six species of fruiting trees (Fig. 2-7) were selected for detailed examination based on the

coati's reliance upon them over the course of the 16-month survey of tree phenology as well as on









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the species' abundance in forest plots. Aspects of some species' fruiting patterns appeared

seasonal as noted below, but neither of the measures of fruit production (mean number of fruits

per tree and percent of trees in fruit, which mostly but not in all ways varied together) was more

than marginally correlated with rainfall for any species (Table 2-2). Ripe fruit was not observed

in large enough numbers (presumably because coatis and other frugivores were eating it as it

became available) to warrant depicting it in species' graphs.

B. alicastrum fruit (Fig. 2-7) was present and usually abundant in virtually every month

of the survey, with a brief peak in August 1995 and a broad peak centered around February 1996,

i.e., in the middle of those years' wet and dry seasons, respectively. Ripe fruit was recorded

March-September 1996, i.e., from the last half of that year's dry season to the middle of the wet

season. B. alicastrum was seen being eaten by coatis and/or was found in their feces on 94 dates

between 7 March and 30 September 1996, demonstrating significant correlation with ripe fruit

availability (Table 2-2). (It also appeared in the coati diet outside of the survey period three times

from 30 December 1994 to 27 January 1995, and on 3 October and 8 November 1996.)

Manilkara zapota (chico zapote, a.k.a. sapodilla) fruit (Fig. 2-7) was also present and

abundant much of the year, and displayed peaks timed similarly to B. alicastrum. There were

lulls in fruit production in June and July, i.e., early in the wet season, in both 1995 and 1996.

Ripe fruit was recorded only in May 1996, coincident with the normal onset of rains, but

distinguishing ripe from unripe fruit was particularly difficult in this species due to its lack of a

pronounced color change; possibly only the most mature fruit specimens were recognized as ripe.

This likely explains why the correlation between ripe M. zapota availability and the appearance

of the fruit in the coati diet did not achieve significance (Table 2-2). This species was recorded

eaten/defecated by coatis on 52 dates between 11 January and 27 June 1996 (and also 16 dates

between 7 January and 3 May 1995).

Fruit production in Trichilia moschata (cedrillo rosa) (Fig. 2-7) was observed only

during the last four months of the survey, June to September 1996, beginning early in the wet









season and increasing as the season progressed and the survey concluded. Ripe fruit was

recorded only in the last month, September 1996. In contrast, T. moschata appeared in the coati

diet in two bouts: 14 times from 11 April to 2 July 1996, and 10 times from 22 August to 29

September 1996 (and also on 3 and 10 October 1996)-indicating that a survey sample size greater

than the 19 trees available would have been preferred for this species. Accordingly, fruit

consumption was not significantly correlated with ripe fruit availability (Table 2-2).

Blomia prisca (tzol) fruited (Fig. 2-7) twice during the survey: for an indeterminate

period including the first two wet season months examined, June and July 1995, and in April and

May 1996 when rains resumed after that year's dry season. Fruits were very low in number

during the latter of these periods, but ripe fruit was recorded in every month of fruit production

except April 1996, correlating significantly with consumption by coatis (Table 2-2). B. prisca

appeared in the coati diet six times from 2 June to 6 July 1995 and 10 times from 22 April to 18

May 1996 (and also six times from 23 April to 31 May 1995, and on 7 and 8 November 1996).

Pouteria reticulata (zapotillo hojafina) fruit (Fig. 2-7) was present for five months

beginning with the onset of rains in April 1996. Ripe fruit was noted in the last two months of

fruit production, July and August 1996, i.e., toward the middle of the wet season. This species

was recorded in the coati diet on 23 dates from 13 June to 30 July 1996. The correlation between

ripe fruit availability and fruit consumption was marginal (Table 2-2).

Pimenta dioica (pimienta, a.k.a. allspice) fruited (Fig. 2-7) in the same wet season

months as T. moschata, June to September 1996. Unlike the latter species, however, fruit

production in P. dioica peaked early in its appearance and was waning as the survey concluded.

Ripe fruit was recorded in the last two months of the survey, August and September 1996. Fruit

was similarly recorded eaten/defecated by coatis 20 times from 24 August to 29 September 1996

(and also five times from 1 to 10 October 1996), correlating significantly with ripe fruit

availability (Table 2-2).









600


400


200


0

1000

800

600

400

200

0

600


400


200


0


Brosimum alicastrum (N = 69)


Manilkara zapota (N = 26)


Trichilia moschata (N = 19)


60


40


20


0 -

60


40


20 0
4--)

60

60


40


20


0


Jun Aug Oct Dec Feb Apr Jun Aug
Jul Sep Nov Jan Mar May Jul Sep
Month
Figure 2-7. Fruiting phenology of and reliance upon tree species important to white-
nosed coatis in Tikal National Park, Guatemala, June 1995 through September 1996.
Dates fruit seen eaten and/or in feces indicated by Xs. Number of trees surveyed each
month (N) indicated parenthetically after species name.









250

200

150

100


0

350
300
250
200
150
100
0

5000

4000

3000

2000

1000

0


Blomiaprisca (N= 109)


Pouteria reticulata (N = 121)


Pimenta dioica (N= 17)


Jun Aug Oct Dec Feb Apr Jun Aug
Jul Sep Nov Jan Mar May Jul Sep
Month
Figure 2-7 (Continued). Fruiting tree phenology and coati fruit consumption.


60


40


20


0

60





20
40
o m
I-i

20 o








20


0
'-4





40


20


0









Table 2-2. Correlational statistics for relationships between monthly fruit availability and rainfall
and between monthly ripe fruit availability and fruit consumption by white-nosed coatis in Tikal
National Park, Guatemala. Sixteen consecutive months compared; significant findings indicated
in bold.


Fruiting Tree Species

Brosimum alicastrum
number of fruits / ripe fruits per tree
percent of trees in fruit

Manilkara zapota
number of fruits / ripe fruits per tree
percent of trees in fruit

Trichilia moschata
number of fruits / ripe fruits per tree
percent of trees in fruit

Blomia prisca
number of fruits / ripe fruits per tree
percent of trees in fruit

Pouteria reticulata
number of fruits / ripe fruits per tree
percent of trees in fruit

Pimenta dioica
number of fruits / ripe fruits per tree
percent of trees in fruit


Rainfall


p= -0.49, P = 0.05
p = -0.53, P = 0.03


p= -0.40, P= 0.12
p= -0.54, P = 0.03


p= -0.01, P = 0.96
p = -0.03, P= 0.92


p= 0.12, P = 0.65
p= 0.14, P= 0.60


p = 0.26, P = 0.34
p= 0.32, P = 0.23


p= 0.09, P = 0.74
p= 0.03, P= 0.91


Coati Consumption


p = 0.94, P < 0.001



p = 0.48, P = 0.06



p = 0.48, P = 0.06



p= 0.78, P < 0.001



p = 0.50, P = 0.05



p= 1.00, P < 0.001


Considering coati food item nutrient composition (Table 2-3), a few general patterns

were evident.

Among monthly leaf litter invertebrate samples (Table 2-3), protein, fat and energy

content per gram were all highest from September to November 1995, in the latter half of that

year's wet season and during and immediately after the months of highest rainfall recorded in the

sample collection period. All three nutritional measures then dropped to low levels during the

transition into the following dry season in December 1995, rose briefly and modestly as the dry

season progressed, then declined again as rains resumed in April 1996 leading into the next wet

season. All again began rising from August to September 1996, albeit at lower levels overall than









Table 2-3. Proximate nutrient composition of white-nosed coati dietary items in Tikal National
Park, Guatemala. Nutrients other than water reported on a dry matter basis.

Sample Water Crude Crude Ash-Free Ash Energy
(%) Protein Fat (%) Neutral (%) (kcal/g)
(%) Detergent
Fiber (%)

Leaf Litter Invertebrates
August 1995 71.7 35.9 11.2 12.0 7.7 3.33
September 1995 78.3 50.4 19.1 18.6 2.1 4.61
October 1995 75.9 58.6 24.6 17.6 0.5 5.61
November 1995 77.5 61.6 14.9 19.9 1.5 5.02
December 1995 72.4 38.3 11.1 9.6 10.2 3.13
January 1996 74.4 35.3 11.2 11.2 2.5 3.37
February 1996 72.6 40.9 8.7 23.3 3.5 3.52
March 1996 70.5 39.8 12.3 11.9 1.5 3.58
April 1996 64.6 35.0 10.2 15.9 14.5 3.02
May 1996 70.0 35.9 7.1 13.3 12.7 2.89
June 1996 66.3 34.3 8.6 14.6 12.4 2.61
July 1996 74.3 33.1 6.3 10.6 12.5 2.67
August 1996 70.8 30.3 5.4 2.42
September 1996 67.4 40.2 6.6 16.3 10.7 2.57

Enema endymion
larva 88.7 62.3 12.1 30.5 0.5 4.83
adult 62.5 67.5 20.3 51.5 4.1 6.03

Brosimum alicastrum 83.1 11.6 1.8 4.03
Manilkara zapota 80.0 4.0 5.9 61.8 2 4.80
Trichilia moschata 77.1 12.0 25.2 5.27
Pouteria reticulata 86.3 9.7 4.8 4.37
Pimenta dioica 74.6 5.1 2.2 31.6 1.1 4.07


in the previous year. Only fat, however, was significantly correlated with rainfall (Table 2-1), the

other nutrients being at most marginally so. The contributions of E. endymion beetles and

especially grubs (Table 2-3) figured as prominently in the above pattern as they did in leaf litter

invertebrate samples. Adults provided the greatest amount of protein and energy per gram of any

food item analyzed, and the third greatest amount of fat; larvae were particularly high in protein

and energy and less so in fat, and had the highest moisture content of all food items.









No sample of B. prisca fruit was analyzed, but of the other five important fruit species

(Table 2-3), T. moschata was highest in protein, energy and especially fat content; indeed, gram-

for-gram this species achieved the highest fat level of any food item analyzed. The results for

other fruit species were variable except that P. dioica was at or near the bottom of the group in

every category.

All of the invertebrate samples contained higher protein levels than any of the fruit

samples (bearing in mind that the latter consisted only of edible portions, therefore excluding

seeds) (Table 2-3). With the aforementioned notable exception of T. moschata, invertebrates also

typically provided more fat per gram. Fruits equaled or slightly bested the mixed leaf litter

invertebrate samples in terms of energy content, and usually held more moisture as well.

In terms of foraging effort, coatis spent more-generally much more-time foraging in the

leaf litter invertebrate zone than in the fruit zone at all times of year (Fig. 2-8). As noted above,

ripe fruit was essentially unavailable for the five months of September 1995-January 1996, i.e.,

the latter part of the 1995 wet season. However, even during the greatest months of overall ripe

fruit availability, April and May 1996-i.e., at the end of that year's dry season and during the

transition into the following wet season-coatis were never observed to spend more than 6.6% of

their foraging time in the canopy of fruiting trees. The animals searched for food under fruiting

trees somewhat more, spending 22.8% of their foraging time in such areas in April, 24.6% in May

and 24.5% in September 1996, i.e., the early to middle wet season of that year, but these were

areas of overlap in which not only ripe fruits but also leaf litter invertebrates could be found.

Examining invertebrate and fruit foraging success (Figs. 2-9 and 2-10, respectively) more

closely, fewer invertebrates were consumed and fewer seconds were spent consuming them per

minute relevant foraging time than was true for fruits in almost every month in which both food

types were eaten; March and April 1996 were exceptional in that invertebrates and fruits were

consumed at comparably low rates. With respect to time spent consuming items, however, it

should be noted that coatis used some undetermined portion of that time processing fruits of









Brosimum alicastrum, M. zapota, T. moschata and Blomia prisca in order to discard various

presumably inedible or distasteful portions (husks, skins and/or seeds).

Over the 14 months of systematic behavioral observations, the coatis' consumption of

leaf litter invertebrates (Fig. 2-9) displayed a clear pattern in terms of number of invertebrates

consumed and time spent consuming them. Overall, invertebrate consumption decreased from

the beginning of the study in August 1995 through April 1996, i.e., through the last half of the

1995 wet season and all of the 1996 dry season, then rose sharply in May 1996 with the onset of

that year's wet season and peaked a month or two later (depending on the measure under

consideration) before again declining. Neither measure of foraging success was significantly

correlated with total invertebrate mass in monthly samples (number consumed: rp 11 = 0.26, P =

0.39; time spent consuming: r[i ] = 0.38, P = 0.20). In accordance with previously presented data,

beetles and grubs-again, especially E. endymion-predominated. Only 19.4% of the invertebrates

coatis preyed upon during observations could be positively identified (with an obvious bias

favoring larger or more agile species); 96.2% of these were insects, and 81.9% various

Coleoptera. E. endymion alone accounted for 44.4% of identified invertebrate prey, or 8.6%

(6.5% larvae, 2.1% adults) of all invertebrates consumed by coatis over the course of the study.

Fruit consumption (Fig. 2-10) followed a similar pattern (aside from the several months

in which ripe fruit was unavailable, of course). A notable exception resulted from the animals'

early reliance upon M. zapota, the first tree species with ripe fruit in the 1996 dry season, causing

a brief spike in consumption rates in February of that year. That species and also Brosimum

alicastrum, which ripened soon after, continued to be consumed at much lower rates throughout

the remainder of the dry season. Fruit consumption increased again in May 1996 when ripe fruit

of various species appeared with the onset of wet season, as noted previously. It was not possible

to look for correlations between fruit foraging success and total fruit availability because

phenological data were lacking for several of the fruit species which were consumed by coatis.

















Wet Season Dry Season Wet Season


100


Oct


Dec


Feb


Apr


Jun


Sep Nov Jan Mar May


Aug
Jul Sep


Month

Figure 2-8. Mean percentage of time foraging adult female white-nosed coatis spent in
areas where ripe fruit was present and absent in Tikal National Park, Guatemala, August
1995 through September 1996. Based on a total of 76.1 hours observation of foraging by
37 animals.


0 t!
Aug












Wet Season Dry Season Wet Season


Invertebrates Consumed

4 T
- 9 16

17 19

19 1 18 18


Aug


Sep


Oct


Dec


Nov


Feb


Mar


Apr
May


p 1.5-

1.0
Lo
o

0.5

0


12.5 -

S10.0 -

"o 7.5 -
0
5.0-

2.5 -
0i


Jun


Aug


Sep


Aug Oct Dec Feb Apr Jun Aug
Sep Nov Jan Mar May Jul


Sep


Month
Figure 2-9. Mean ( SEM) number of invertebrates consumed and time spent
consuming them by foraging adult female white-nosed coatis in Tikal National Park,
Guatemala, August 1995 through September 1996. Number of females sampled in each
month indicated on bars. Based on a total of 93.7 hours observation of invertebrate
foraging by 32 animals and 73.0 of 29 animals, respectively.


2.0-


Time Spent Consuming


1












Wet Season Dry Season Wet Season


Aug Oct Dec Feb Apr Jun Aug
Sep Nov Jan Mar May Jul Sep


Time
Spent
Consuming


Aug Oct Dec Feb Apr Jun Aug


Sep


Nov


Mar May


Sep


Month
Figure 2-10. Mean (+ SEM) number of fruits consumed and time spent consuming them
by foraging adult female white-nosed coatis in Tikal National Park, Guatemala, August
1995 through September 1996. Number of females sampled in each month indicated on
bars. Based on a total of 10.4 hours observation of fruit foraging by 23 animals.


4.5

.E
--
&o 3.0


1.5


0









Adult female coati body fat profiles (Fig. 2-11), presumably indicative of how well

energy availability met energetic demands, displayed a clear seasonal pattern. Body fat declined

rapidly from its high point at the beginning of the dry season in January to the mating period in

the last half of February, leveled off or slightly rose thereafter until just before the parturition

period began in the last half of April, then resumed its decline through the parturition period and

well into the wet season. Fat stores appeared to reach nadir in the vicinity of July to early August

(a time of sparse data), i.e., shortly before the middle of the wet season, and then rose presumably

steadily (discounting another gap in the dataset from mid-October through November) through

the remainder of the wet season and until the end of the year.

Discussion

Behavioral and morphometric data reveal that coatis in Tikal National Park normally

reproduce only once per year, with relevant events occurring across the population in narrow,

consistent periods: Mating takes place over an approximately two-week period in the middle of

the dry season. Birth occurs over a comparable period at the end of the dry season, about 10

weeks after mating. Solitary nesting, which lasts 1/V2-2 months, begins shortly before birth occurs

and ends with the emergence of young at the beginning of the wet season; the band reunites

within the month following nesting. The young begin foraging alongside their dam as soon as

they are brought down to the ground, but are not fully weaned until months later, in the middle of

the wet season. A second reproductive cycle with similar timing but delayed by approximately

four months may be initiated if the first is unsuccessful, but second cycles rarely occurred in

Tikal and appeared to result in smaller litters. Taking into account seasonal differences in

different parts of the coati's range, the reproductive pattern in Tikal fits well with previously

published information on coatis at other locales.

Based primarily on observations of increased female-male affiliative behavior and male-

male agonism from late January to mid-March 1959 and throughout January 1960, Kaufmann

(1962) identified a month-long period of sexual activity among coatis on BCI; because it appears




















Dry Season Wet Season

0
SO0



o'- o 8 o ooo
- 0 0




o o o
; 0 0 0 00
% 0 O O 0
000@90 0


I I I l l | l l l I I I I l
Jan Feb Mar Apr May Jun Jul

Date


I I I I I I I I II II I I
Aug Sep Oct Nov Dec


Figure 2-11. Annual body fat profile exhibited by adult female white-nosed coatis in
Tikal National Park, Guatemala, July 1994 through October 1996. Mating period
(13 Feb 28 Feb) indicated by lightly shaded background and period of parturition
(16 Apr 9 May) more darkly shaded. Based on measurements obtained during 135
immobilizations of 54 animals.


0




td)









that actual copulation was not observed (see below), however, the mating period could not be

defined. Based on similar observations and the timing of nest emergence, Russell (1979; 1982)

concluded that the coati mating period on BCI lasted one to two weeks in early February, shifting

slightly from year to year. Sunquist and Montgomery (1973) observed a pair of coatis in coitus

on the island on 5 March 1971. Gilbert (1973) believed that the coatis in southern Arizona, at the

northernmost edge of the species' range, mated in March and early April. Hass and Roback

(2000) observed two coati copulations (excluding a possible third; see below) there on 6 April 97

and 5 April 98, and also stated without providing further details that the mating period in their

population lasted from late March to mid-April. Studying captive animals in southern Arizona,

Smith (1980) reported that copulations took place on 28 and 30 March 1976.

Previous detailed descriptions of mating activity among free-ranging coatis include

mounts lasting only a few seconds (Kaufmann, 1962; Gilbert, 1973; Hass and Roback, 2000).

Kaufmann (1962) referred to these as attempted copulations, whereas the later authors considered

them to be copulations. However, Gilbert (1973) also believed that more lengthy periods of

mating activity probably occurred out of sight of observers, when a male and a female would

depart from the band together, and Hass and Roback (2000) additionally observed two

copulations lasting approximately 60 minutes each between coatis who were out of sight of other

band members. The coatis found already engaged in copulation (most similarly to copulations

observed in the current study, in the tree canopy over a foraging band) by Sunquist and

Montgomery (1973) continued for seven minutes after being discovered. Smith described two

copulations among captive coatis: one lasted one minute in total and another continued for 23

minutes after being discovered in progress. The numerous observations of prolonged copulatory

events in the present and earlier studies suggest that Kaufmann (1962) was correct in describing

brief mounts as merely attempted copulations.

Prolonged copulation could be interpreted as an indication that coatis are induced

ovulators, as has been suggested by Hass and Roback (2000), but it may also be a form of mate









guarding by males. Litters examined in Tikal exhibited a high rate of multiple paternity (Booth-

Binczik, 2001), indicating that female coatis commonly mate with more than one male.

Observations in the current study and by Smith (1980) of females attempting to break away from

but being restrained by males suggest that prolonged copulation is more advantageous to the male

than to the female. The closely related raccoon (Procyon lotor) was demonstrated by Sanderson

(1961) to ovulate spontaneously (after initially being reported to be an induced ovulator by

Llewellyn and Enders, 1954-an erroneous finding that unfortunately persists in the literature), but

the review of carnivore ovulation by Lariviere and Ferguson (2003) demonstrates that it is unsafe

to base assumptions in this regard on phylogenetic relationships.

Coatis were not radiocollared for Kaufmann's (1962) BCI study, so he was able to keep

track of only one female during the 1960 nesting period; that animal left its band on 1 April, gave

birth on 10 April and brought its young out of the nest and joined other females with young on 20

May. Without providing any foundation, Russell (1979) stated that coati births occurred on the

island during the second week of April in 1977 and the fourth week of April in 1978, and

(Russell, 1982) that the nesting period there took place in April and May. Russell (1982) also

said that coati bands on BCI reaggregated in late May. Based on animal movements monitored

by radiotelemetry, SAenz (1994) reported that female coatis in the dry forest of Santa Rosa

National Park, Costa Rica, left their bands to nest in April. Also based on telemetry data,

Ratnayeke et al. (1994) reported that females in southern Arizona were solitary for at least a

month before parturition in early July. Gilbert (1973) stated that females there disbanded in the

third week of June, and estimated that all females in the band he was observing gave birth

between 16 and 23 June. Hass (2002) said that females in Arizona left their bands in mid-June

and reaggregated in early August when the young were five to six weeks old.

There are as yet few data available on the length of coati gestation against which to

compare the 71- to 74-day pregnancy seen in a single female in the current study. The most

concrete of these come from Smith's (1980) Arizona captive animal study, in which one female









gave birth 71 days and another 76 days after being observed copulating. Average gestation

lengths can be approximated for the two coati bands from which most data derive for the 1996

mating and parturition periods of the present study, bearing in mind that parturition periods

(which are presented and discussed in greater detail in Chapter 3) were likely overestimated; the

differences between the midpoints in the mating and parturition periods in these bands are 66 and

68 days. Kaufmann (1962) reported that three coati litters were born approximately 70 days after

the period in which he observed heightened sexual activity on BCI. The relative consistency of

these data across divergent locales-as well as the tightness and consistency of the mating period

at the start of the coati reproductive cycle-suggest this species undergoes direct development.

Understandably little information is available concerning coati lactation. Kaufmann

(1962) reported that in 1958 nursing was seen on BCI as late as 16 September. Inexplicably,

Russell (1983) put forth that young there were nearly weaned by the time of reaggregation,

months earlier. Smith (1980) noted that young born to a captive female first began eating solid

food at 45 days of age. Smith also reported that the female began moving away at the approach

of its young when the latter reached 74 days of age, and that the female's teats appeared greatly

reduced in size at that time; she observed no nursing as of 80 days postpartum.

Prior to this study, nesting behavior and parturition outside of the usual narrowly defined

coati nesting season had been observed only in Santa Rosa, where Sienz (1994) found that

females quite commonly underwent second reproductive cycles after losing their first litters to

nest predation by white-faced capuchins (Cebus capuchinus); second litters were born there in

late July or early August. Second litters have also been documented in the procyonid P. lotor in

south Texas after failed reproductive attempts were made during the normal breeding season

(Gehrt and Fritzell, 1996), and the phenomenon has been seen in many other mammals as well.

The data on food availability provide a ready ultimate explanation for coati reproductive

seasonality in Tikal, but leave some details yet to be clarified. In the present study, infants

emerged from their nests at the start of the wet season when (in at least one year) both leaf litter









invertebrates and fruit were increasing in abundance. Are these patterns in food availability

consistent, though? Taken by itself, this ecologically brief study suggests that the invertebrate

pattern may be consistent but the fruit pattern is not; placing the current results into the context of

the literature provides much keener insight into the question of pattern inconsistencyc.

Populations of leaf litter invertebrates in the tropics are strongly dependent on moisture

levels (Levings and Windsor, 1982), as is evidenced by the high correlation between invertebrate

abundance and rainfall in Tikal. As occurred in the present study, overall litter invertebrate

abundance on BCI was lowest during the dry season and highest in the early wet season (Levings

and Windsor, 1982). Nine of thirteen arthropod taxa examined there individually showed

population maxima in the early wet season (Levings and Windsor, 1985). E. endymion adults

congregate around lights at night in huge numbers (pers. obs.), and should therefore be

considered night-flying insects as well as litter insects. Night-flying insect abundance (and large

beetle abundance in particular) also peaked in the early wet season on BCI (Smythe, 1982), and

night-flying insects were most abundant in the late dry season and early wet season at the Cocha

Cashu Biological Station in Peru's Manu National Park (Terborgh et al., 1986; cited in Goldizen

et al., 1988). Moreover, differences in rainfall patterns among years affect litter arthropod

population levels but do not obscure seasonal trends in abundance (Levings and Windsor, 1985).

In contrast, seasonal patterns of tropical fruit production vary greatly from year to year

not just in Tikal but at other sites as well (Foster, 1982a; Bullock and Solis-Magallanes, 1990;

van Schaik et al., 1993; Chapman et al., 2005). None of the tree species that were most important

in the coati diet in Tikal showed the same pattern of fruit availability in June-September 1995 as

in June-September 1996 (at the beginning and end of the phenological survey). Rains were heavy

at the height of the 1995 wet season and even more unusually light in the middle of the 1996 wet

season; leaf litter fall and invertebrate and fruit availability all showed associated patterns. The

climatic fluctuations may have been due to the occurrence of an El Nifio event in 1994 (based on

information from the U.S. National Oceanic and Atmospheric Administration, Washington, DC);









the El Nifio Southern Oscillation tends to create a pattern in which dry sunny years alternate with

wet cloudy years in Central America (Wright et al., 1999). Unusually rainy dry seasons,

particularly following an El Niiio year (Wright et al., 1999), apparently result in failure of the

fruit crop in many species that normally produce fruit in the wet season, including the ordinarily

prolific B. alicastrum (Foster, 1982a). Even in the absence of obvious rainfall anomalies,

however, many tropical tree species exhibit non-annual rhythms in fruit production and/or high

intraspecific variability in phenology (Milton, 1991; Newstrom et al., 1994; Hemingway and

Overdorff, 1999). It has been reported that B. alicastrum trees in Tikal produce fruit three times

per year: February-March, June-July, and October-November (Coelho et al., 1976). The

phenology data in the present study do not support this contention, but do indicate non-

synchronous fruit production by this species, as fruit availability continued and even increased

during a lengthy period of heavy consumption by coatis and other frugivores (pers. obs.).

The data are scant but suggest consistent seasonal patterns exist in food nutrient content

as well as food availability. In the present study virtually all leaf litter invertebrate nutrient levels

rose and fell in parallel to rainfall, although only fat content correlated significantly. Fruit

nutrient levels were examined herein at only a single point in time per species, but Schaefer and

Schmidt (2002) reported that fleshy fruits in Venezuela rose steadily in caloric value throughout

the dry season, and Worman and Chapman (2005) found that the fat content of ripe fruits of a

single tropical species varied tremendously within a year, being much higher during periods of

high rainfall. This is clearly an area of tropical ecology warranting further study.

There is also the matter of the freezer failure and its potential effects on the present

study's nutritional analyses to consider. Few nutritional data are available in the literature that

are useful for comparison, but those are encouraging. Analysis of an unknown species of dung

beetle from Tanzania (Pennino et al., 1991) produced values remarkably similar to those found in

the present study for adult E. endymion for water content (58.3%), fat content (20.6%), NDF

(51.6%) and ash (7.4%), but completely different for protein (7.8% versus 67.5% in the current









study). Previously published values (Coelho et al., 1976) for B. alicastrum fruit (84% water,

15.6% protein, 3.1% fat, 3.50 kcal/g) and M. zapota fruit (75% water, 2.0% protein, 4.4% fat,

3.76 kcal/g) are likewise similar to those obtained in this study.

The relative importance of leaf litter invertebrate versus fruit availability to the timing of

coati reproduction remains uncertain, but the findings of the present study appear to support

Russell's (1982) assertion of the primacy of invertebrates. Tikal's coatis clearly focused their

foraging efforts on invertebrates more than on fruit at all times, though seasonal patterns are

somewhat difficult to assess due to the high degree of interannual variation in fruit availability

during this study. For example, the animals ate no fruit during the second half of the wet season

in 1995 because no fruit was then available, but data from September and anecdotal observations

made in October and November 1996 suggest that foraging patterns late in that year's wet season

might have looked quite different. Coatis spent the highest percentage of their foraging time in

fruit zones at the end of the dry season, but it was still much less than the time they spent foraging

for invertebrates; the time they spent consuming invertebrates was actually higher then than at

any other time, too, suggesting that both fruit and invertebrates were abundant at that time. An

evolutionary argument also exists for invertebrates being more important than fruits as

determinants of coati reproductive timing, namely that consistent annual peaks in invertebrate

availability are much more capable of driving seasonal adaptation than are profoundly less

consistent peaks in fruit availability.

In any event, the present study adds to the growing body of literature demonstrating the

importance of leaf litter invertebrates and their phenology to coatis. Kaufmann (1962) reported

that BCI's coatis spent more than 95% of their active time foraging for invertebrates, and that

fruit was eaten more during the dry season than the wet season. Russell (1982) estimated that

coatis on BCI spent 89% of their foraging time in the wet season and 54% in the dry season

foraging for invertebrates. He also reported that scats he collected consisted mostly of beetle

parts. Contrasting somewhat to the patterns in Tikal and BCI, Sienz (1994) found approximately









equal frequencies of invertebrates and fruit in the scats he collected throughout the year in Costa

Rica; as in Tikal, though, Coleoptera was the dominant invertebrate group in the diet (followed

closely by Orthoptera). A heavy reliance upon beetle prey is clearly a common facet of coati

ecology at a variety of sites, but no previous study has found as strong a relationship between this

procyonid and a single prey species as was evident in Tikal between it and E. endymion.

Coati reproductive seasonality in Tikal appears to be driven not by restrictive effects of

food availability on female physiology (reproductive or otherwise), but rather by its direct effects

on the survival of offspring. Specifically, reproduction there is timed such that gradually weaning

young (arguably the most vulnerable life stage; Russell, 1982) can capitalize on a surfeit of food

resources which first appears at the beginning of the wet season and continues through the first

half of that season. As others have pointed out, predatory species are unlikely to suffer shortages

of particular nutrients (Stephens and Krebs, 1986; Bronson and Heideman, 1994; Galef, 1996), so

when such species are timing reproduction to match food availability they are likely doing so

with regard to more purely energetic constraints. Female coatis do lose energetic stores (i.e., fat)

during nesting and early weaning (the most energetically expensive part of reproduction for many

mammals; Rutberg, 1987) even as males are rapidly rebuilding theirs after the mating period (see

Chapter 4) by relying upon the same foods (Booth-Binczik, 2001), but females apparently have

sufficient reserves to get them through. Unlike on BCI where deferment of reproduction was

common (Kaufmann, 1962; Russell, 1982), virtually all mature females reproduced each year in

Tikal (unpublished data). The fact that some females in Tikal were able to successfully complete

second reproductive cycles after failing in their first provides additional evidence of ample

energetic reserves in these animals. Reviewing reproductive seasonality among neotropical

primates, DiBitetti and Janson (2000) concluded that very small species time reproduction so that

peak food availability coincides with lactation, whereas species large enough to store sufficient

energy reserves-i.e., those similar in size to the coati-time reproduction so that peak food

availability coincides with weaning.









To more fully assess the importance of birth season to offspring survival, it would be

useful to compare survivorship among young born during second cycles to that among young

born at the normal time of year. However, the few litters that were produced during second

cycles in this study do not provide adequate data for such a comparison. One infant that was born

in August 1995 and the four that were born in August 1996 were known to survive to the end of

the study; the fates of the other out-of-season infants were unknown (as is the cause of whatever

difference in litter size exists between first and second litters).

Beyond energy availability, a few related ultimate factors might contribute to the

observed pattern of seasonal reproduction. For example, protein content of invertebrates peaked

in the middle of the wet season, so birth might be timed such that infants are fully weaned when

the most protein is available to support their continued growth. Also, the fact that birth occurs at

the end of the dry season means that juveniles have as much time as possible to grow, learn and

build energetic reserves before they have to deal with the dry-season low in invertebrate

availability (Russell, 1982). The only other factor that appears at all likely to promote strong

coati reproductive seasonality in Tikal is water availability. The region's pronounced dry season

and lack of natural permanent surface water (due to underlying permeable limestone) create the

possibility that lactating females might be restricted in milk production by a shortage of water.

However, this is not likely to be a factor in most parts of the species' range, and the fact that

females in Tikal give birth before the dry season ends suggests that water stress is not relevant to

the timing of their reproduction.

Reproductive seasonality such as the coati displays would not be remarkable in a long-

lived mammal inhabiting the higher latitudes; indeed, such patterns are the norm there (Sadleir,

1969; Bronson, 1989). Despite the paucity of studies on long-lived tropical species, reproductive

seasonality is increasingly known from the lower latitudes, too. The coati is extraordinary among

that latter group, however, in the narrow, consistent timing of its reproductive events. Looking

past species which appear to display no seasonality whatsoever, such as the sun bear (Helarctos









malayanus) in Borneo (Schwarzenberger et al., 2004), seasonal reproductive events among

tropical mammals are better thought of as indistinct statistical phenomena rather than clearly

demarcated ecological events. Spotted hyena (Crocuta crocuta) populations distributed across

very low latitudes reproduce throughout the year, but often with modest population-specific

seasonal peaks (Holekamp and Smale, 2000). Acouchies (Myoprocta exilis), agoutis (Dasyprocta

leporina) and pacas (Agouti paca) at 6N latitude similarly give birth throughout the year, albeit

with apparent seasonal peaks (Dubost et al., 2005). White-lipped peccaries (Tayassu pecari) at

8N latitude and saddle-back tamarins (Saguinusfuscicollis) at 120S latitude both display birth

peaks coincident with greatest food availability in the first half of the wet season, as does the

coati, but the peccary's mating period has been documented to last at least eight months

(Altrichter et al., 2001) and the tamarin's parturition period spans a similar length of time

(Goldizen et al., 1988). A population of the Ethiopian wolf (Canis simensis) times reproduction

somewhat more finely at 7N latitude, displaying a parturition period of about four months

(Sillero-Zubiri et al., 1998). Extremely few studies have as yet been conducted on or in the very

near vicinity of the equator, but at least one species there has already been found to display

seasonal reproduction: mandrills (Mandrillus sphinx) exhibit a 6-month mating period (Abernethy

et al., 2002).

Wherever it is found, reproductive seasonality for most long-lived mammals appears to

be a strategy of optimization. As such, the degree of variation seen in the timing of specific

reproductive events should reflect the selective pressures that favor those events taking place at

the most advantageous times. So why is the same adaptation so often expressed so differently in

the tropics than it is at the higher latitudes?

Two related arguments that have been posited are that optimal conditions occur over a

longer time period or selective pressures favoring seasonality are otherwise weaker in the tropics

than at higher latitudes because of the less variable/more benign climates generally thought to

exist in the former region. However, many (perhaps even most) tropical locales fail to live up to









such rosy expectations (Foster, 1982a; Bronson and Heideman, 1994). Even setting that fact

aside, selective pressures weak or strong are still selective pressures. Given an evolutionary

timeframe, species-or more accurately, their populations-should respond to those pressures as

best they are able.

Bronson and Heideman (1994) have argued persuasively that reproductive seasonality is

generally less well-defined in the tropics because animals residing there have less reliable or

distinct proximate cues upon which to rely. Photoperiod, the most universally relied upon

zeitgeber for long-lived mammalian reproduction (Sadleir, 1969; Bronson, 1989), obviously

diminishes in degree of both annual and daily change as one proceeds from the poles to the

equator. Tropical rains and their innumerable effects on food availability, although often

apparently consistent enough over history to promote the evolution of reproductive seasonality,

generally vary too much from year to year to serve as predictive cues for timing specific

reproductive events. Other possible cues appear even less reliable.

It is unknown at what point photoperiodic changes become too slight for animals to use

them to time or fine-tune the timing of their reproduction (Bronson and Heideman, 1994), but of

course such timing depends on the extent of both the photoperiodic changes themselves and the

genetic variability of the populations subjected to them. One prediction based on this premise in

combination with the assumption that there are no latitudinally based differences in population

genetic variability is that long-lived seasonal species (or even closely related groups of species)

should display a broadening and perhaps ultimately a disappearance of peaks in reproductive

events in populations at increasingly low latitudes, and this has been amply demonstrated to occur

(Bronson, 1985; Di Bitetti and Janson, 2000). Bronson (1989) also suggested that social species

should be able to time their reproduction more finely than would otherwise be possible at low

latitudes by using interactive cues to augment environmental cues, i.e., the reproductive responses

of the most environmentally sensitive individuals in a population could socially trigger like

responses in the population's remainder. In accordance with this prediction, the tropical









mammals that have thus far been found to exhibit relatively narrow reproductive seasonality are

indeed social species (e.g., ring-tailed lemurs, Lemur catta; Jolly, 1967; impalas, Aepyceros

melampus: Murray, 1982; greater spear-nosed bats, Phyllostomus hastatus: Porter and Wilkinson,

2001; red ruffed lemurs, Varecia rubra: Vasey, 2005). The coati may simply be one of the most

extreme examples of such found to date. (This subject is examined in greater detail in Chapter 3).

The discussion does not end there, however. As O'Brien (1993) emphasized, lamentably

few long-lived tropical mammals have so far been examined for the possibility-let alone the

extent-of reproductive photoresponsiveness and, with the exception of Nile grass rats

(Arvicanthis niloticus: Sicard et al., 1992), all of the short-lived tropical species that have so far

demonstrated any photoresponsiveness whatsoever in the laboratory have displayed continuous or

opportunistic reproduction (i.e., free from predictive cues) in the wild. Looking farther abroad

taxonomically, spotted antbirds (Hylophylax n. naevioides) at 90N latitude in Panama show

reproductive physiological responsiveness to the very slight natural changes in daylength found at

that latitude (Hau et al., 1998). If tropical mammals possess similar capabilities, that of course

merely begs the question of why they do not utilize them more often. To the delight of the

curious, scientific endeavors invariably raise more questions than they answer.















CHAPTER 3
BIRTH SYNCHRONY

Introduction

In the absence of extraordinary selective pressures, reproductive seasonality is a strategy

of optimization. As such, it often allows for considerable variation in the timing of specific

reproductive events, even within a single population of an obligate seasonal species. This is

especially true in the tropics, where annual variation in photoperiod is slight and other potential

environmental predictors may be patchy or may shift somewhat from year to year in response to

climatic conditions (e.g., rainfall; Rand and Rand, 1982). For example, as Russell (1982) pointed

out, birth peaks among Panama's seasonally reproducing mammals are largely probabilistic

events; birth periods for most species span at least a few months (summarized in Fleming, 1973).

The white-nosed coati is unusual in this regard, with all parturition on Barro Colorado

Island (BCI), Panama-the only population previously well-studied-seemingly occurring within a

1- to 2-week period each year (largely inferred from observations of first emergence of young

from nests; Kaufmann, 1962; Russell, 1979; 1982). This pattern prompts consideration of

ecological pressures favoring a high degree of birth synchrony in the species. [Note: The terms

reproductive seasonality and synchrony have sometimes been used interchangeably (e.g., Boinski,

1987), leading to confusion about the nature and causes of these phenomena. The author has

adopted Ims' (1990b) definition of reproductive synchrony: "a phenomenon caused by biological

interactions operating to produce a tighter clustering of reproductive events than would have been

imposed by environmental seasonality alone" (p. 135).]

Adult female coatis are also highly social, living in cohesive bands with their young most

of the year and becoming solitary only to nest (Kaufmann, 1962). Russell (1982; 1983)









emphasized the importance of cooperation among adult females to minimize losses of young to

predation and parasitism, and (1982) suggested that a high degree of both intra- and interband

birth synchrony exists to facilitate this strategy. Other possible explanations more generally

offered for birth synchrony include predator swamping (Pianka, 1976), dependence upon an

ephemeral food or other resource (e.g., the need of some desert anurans for breeding ponds), or

utilization of social mechanisms to supplement inadequate environmental predictors (e.g.,

photoperiod at low latitudes) employed in a seasonal reproductive strategy (Bronson, 1989).

None of these explanations has yet been rigorously examined for the coati, nor has birth

synchrony even been established as a general phenomenon in the species (although a handful of

reports suggest that coati reproduction may be patterned similarly at other locations, e.g., in

southern Arizona: Gilbert, 1973; in Costa Rica: Sienz, 1994; in Jalisco, Mexico: Valenzuela and

Ceballos, 2000). It seems reasonable to rule out transitory requirements as an explanation for

birth synchrony in this long-lived, tropical forest-dwelling mammal, however, and no such

requirements were discovered during the extensive observations of BCI's coatis by Kaufmann

(1962), Russell (1979) and Gompper (1994).

Accordingly, this study examines data on the timing of coati reproductive events at Tikal

National Park, Guatemala, to provide details on birth synchrony at this new locale and to test

specific predictions about the phenomenon based on the following hypotheses:

HI: Coati birth synchrony minimizes juvenile mortality by facilitating communal care of

young.

The five- to six-week nesting period (Chapter 2) is the least social time in the lives of

female and juvenile coatis, so communal care cannot become a relevant factor until the animals

have reaggregated into bands after the young have emerged from the nest. Birth synchrony

would be relatively useless for facilitating communal care if subsequent reaggregation is too

asynchronous. It was therefore predicted that within a band of coatis, the variance in the timing

of reaggregation is no greater than in that of parturition.









H2: Birth synchrony minimizes juvenile mortality by predator swamping.

Even the largest bands of coatis do not include more than about a score of reproductive

females in a given year (Booth-Binczik, 2001; Chapter 2), and predators are capable of

consuming an entire litter of newborn coatis in short order (e.g., Rose, 1997). There is also much

home range overlap among neighboring coati bands (Kaufmann, 1962; Gompper, 1997). To

swamp predators rather than merely prompt them to shift their focus from band to band, then,

birth synchrony would have to exist across as well as within bands. Hence it was predicted that

the variance in the timing of parturition between bands is equal to that within bands.

H3: Birth synchrony results from the coati's reliance upon social mechanisms to enhance

reproductive seasonality.

If coatis are relying upon social mechanisms to augment weak environmental cues for

timing reproduction, it is reasonable to assume that this process will result in a greater degree of

birth synchrony within than between bands. In opposition to the prediction of H2, therefore, this

hypothesis generated a prediction that the variance in the timing of parturition between bands is

greater than that within bands.

It should be noted that the aforementioned three hypotheses are in fact independent rather

than mutually exclusive alternatives; more than one may pertain. Further, whereas the first two

hypotheses directly address possible ultimate causes of birth synchrony, the third instead

addresses a proximate mechanism by which the ultimate factor of seasonal food availability (see

Chapter 2) may contribute to the coati's tight clustering of birth.

Methods

From June 1994 through October 1996, various data were collected on a population of

free-ranging white-nosed coatis in Tikal National Park, Guatemala (17N, 890W) as part of a

broad study of the species' reproductive biology. (An overview of the coati's reproductive

pattern at this locale appears in Fig. 3-1.) This chapter specifically examines data on the timing

of parturition in 1995 and 1996, and the reaggregation of parous females after nesting in 1996.





















Dry Season Wet Season


nesting reaggregation
S ----


- *i


Feb


Mar


parturition
I --


Apr
Apr


May


Jun


Jul


Month


Figure 3-1. Timeline of white-nosed coati reproductive phenological events in Tikal
National Park, Guatemala (see Chapter 2).


mating









In all, reproductive events occurring among 28 females from three bands contributed to

the study. Each female was initially captured by live-trap or (more often) blowgun and

chemically immobilized by intramuscular injection of approximately 7 mg/kg Telazol (Fort

Dodge Laboratories Inc., Fort Dodge, IA). Anesthetized animals were tattooed and eartagged for

identification and fitted with 90 g motion-sensitive radiocollars (Advanced Telemetry Systems,

Isanti, MN) to enable monitoring thereafter. The animals were subsequently habituated to the

close presence of observers (as described in Chapter 2), and the status of each female was

checked daily (as possible) during the time periods when parturition and (in 1996) reaggregation

took place. All animal handling procedures were conducted as per protocol #4084 approved by

the University of Florida's Institutional Animal Care and Use Committee.

Parturition was determined to have occurred when a female showed a sudden

pronounced reduction in girth followed by continued nesting behavior, and was ultimately

confirmed by observation of young still in the nest or shortly after emergence from the nest.

Parturition dates could not usually be pinpointed because the females tended to give birth while

remaining out of sight within their nests for days at a time. In this circumstance the scoring of a

female's parturition was distributed over an appropriate span of time (e.g., one-third of the

female's parturition was ascribed to each of three possible days). Data on females of

indeterminate status for two weeks or longer were not utilized.

For the purpose of this study, reaggregation was deemed to have occurred when a

postpartum female and her young were observed to have reunited with at least three other such

females. In most cases reaggregation dates could not be pinpointed and were scored as described

above for uncertain parturition dates.

Sokal and Rohlf (1981) guided all statistical efforts, and a Pa < 0.05 level of significance

was utilized in all tests. In order to assess whether the variance in the timing of parturition was

greater than or equal to that of reaggregation, i.e., to test the communal care prediction, a one-

tailed test for equality of two variances was conducted for each of the two coati bands that









contributed almost all of these data in 1996; data on a single female from a third band were

included in the descriptive statistics presented for this year. An ANOVA was conducted to

compare the variances in the timing of parturition between and within the two primary bands in

1996, i.e., to test the predictions for predator swamping and social facilitation of reproductive

seasonality. Insufficient data were obtained for the 1995 parturition period to include in such

analyses, and these data were therefore used only for comparison with the 1996 parturition period

via descriptive statistics. To aid in comparing the annual birth pulse of the coati in Tikal to that

seen at other locales and/or in other species, the interquartile range (i.e., middle 50%) was also

calculated for each year's data.

Results

Coati parturition was both narrowly timed within each year and consistent between the

years of the study (Table 3-1). The nine births recorded in 1995 occurred in a slightly flattened

but normally distributed peak of 14 days duration, and the 24 births recorded in 1996 occurred in

a similar peak lasting 18 days. These peaks were centered six days apart late in the dry seasons/at

the beginning of the wet seasons (see Chapter 2) of their respective years.

There was a discernible difference in the timing of parturition between the two primary

bands under observation in 1996 (Fig. 3-2), with Band 1 females giving birth over a 14-day span

that began four days after the start of the 12-day span in which Band 2 females did so. Mean

birthdates in the two normally distributed birth peaks were 2 May and 27 April, respectively. The

variance in the timing of birth between Bands 1 and 2 was significantly greater than that within

the bands (F[1.21 = 24.21, P < 0.001).

Reaggregation in 1996 occurred relatively quickly after females first brought their young

down from their nests between the early and middle wet season (see Chapter 2). Eleven females

with young from Band I found at least three other such families within a 20-day span beginning

31 May, and nine females with young from Band 2 accomplished it in 16 days beginning 4 June.

Comparing parturition to reaggregation within each band: The variance in the timing of






























n nn F


22 23 24 25


26 27 28
April


m= Band 1 (N= 12 females)
hI Band 2 (N = 11 females)


rvd


SL n H n r


29 30 1 2 3 4

Date


5 6
May


7 8 9


Figure 3-2. Timing of births in neighboring white-nosed coati bands in Tikal National
Park, Guatemala, in 1996. Scoring of a female's parturition distributed over appropriate
span of time when date not pinpointed (e.g. 1/3 of female's parturition ascribed to each of
three possible days); mean ( SEM) span for all females 3.9 + 0.6 days, range 1-10 days.


4-

3-

2

1-


S. 1 1...


" I









reaggregation was significantly greater than in that of birth in Band 2 (F[8,0o] = 8.77, P = 0.001).

Band 1 displayed the same tendency, but it was not significant (F[lo. l = 2.28, P = 0.10).

Discussion

The communal care hypothesis for coati birth synchrony assumes that the presence of

multiple females at the same reproductive stage is important to the survival of young. Certainly,

evidence suggests that coati sociality is employed in group defense, including of offspring.

Russell (1983) found that BCI's coati bands adopted a formation that was optimal for protection

of young rather than foraging efficiency when moving through the forest. He further reported

that juveniles spent more time vigilant when unaccompanied by adults, and adults were more

vigilant in smaller groups. This latter finding was also confirmed by Burger and Gochfeld (1992)

in Costa Rica. However, the presence of the band may actually be more important to the survival

of adult females than of juveniles, as mortality rates of females are higher when they are alone

than when they are in groups (Booth-Binczik, 2001; Hass and Valenzuela, 2002) and female

mortality is lower in larger groups, whereas juvenile mortality is not (Hass and Valenzuela,

2002). There are no published data on relative mortality rates of juveniles before and after band

reaggregation, and direct observations of predation are few. During the course of the present

study a pair of crested eagles, Morphnus guianensis, was observed taking five coati infants to its

Table 3-1. Descriptive statistics for observed white-nosed coati birth periods in two years in
Tikal National Park, Guatemala.

Statistic 1995 1996

Number of Females / Bands 9 / 2 24 / 3

Parturition Period 16 29 April 22 April 9 Maya

Mean Birthdate 24 April 29 Aprila

Interquartile Range (days) 5 6

Degree of Kurtosis (- 3) -0.62 -0.69

a calendar dates not strictly comparable because 1996 was a leap year









nest in a couple of weeks' time at about the end of the coati nesting period in Tikal, and other

raptor species were occasionally observed preying upon nestling coatis as well (D.F. Whitacre,

pers. comm.). Rose (1997) documented heavy predation on nestling coatis-principally within

their first few weeks of life-by white-faced capuchins (Cebus capuchinus) in Santa Rosa National

Park, Costa Rica, and Sienz (1994) reported that this resulted in as much as 100% nestling

mortality in some bands. Russell (1982) reported heavy juvenile mortality on BCI in the first

three months following reaggregation, and Hass and Valenzuela (2002) estimated 43-75%

mortality in the first 3-5 months of life in southern Arizona and Jalisco, Mexico. It appears likely

that the risks faced by a young coati do indeed diminish in the company of its band, but the anti-

predation benefits of group living do not depend on females being at the same reproductive stage.

Certain aspects of coati biology and two historical observations of coati behavior (albeit

perhaps of a single animal) prompt special consideration of the adult male as a potential predator

of young. The subject of infanticide by male coatis has been dealt with more fully by Booth-

Binczik (2001), but brief mention in the course of this discussion of birth synchrony and

communal care seems appropriate. Female coatis have been documented to undergo successful

second reproductive cycles shortly after losing litters born at the normal time (Sienz, 1994;

Chapter 2), making sexually selected infanticide a possibility (Bertram, 1975; Hrdy, 1979). The

fact that males are predominantly solitary has also been interpreted as a result of exclusion by

females for the protection of their young (Russell, 1981). In support of his interpretation, Russell

(1981) reported an apparently secondhand observation of an adult male coati on BCI consuming

an infant near a biological laboratory animal feeding station, and another of an adult male

(possibly the same animal) attacking and carrying an infant away from the same site on the

following day. However, in Tikal most coati litters are multiply sired (Booth-Binczik, 2001),

resulting in paternity confusion which would discourage sexually selected infanticide (Wolff and

Macdonald, 2004). Male coatis are also not excluded from bands in Tikal, and in fact they

frequently associate with bands there (Booth-Binczik, 2001) as well as in Arizona (Gilbert, 1973)









and Costa Rica (Sienz, 1994). Moreover, despite several hundred-possibly thousands of-hours

of field observations by several biologists at a few sites, no one other than Russell (1981) has

uncovered any evidence of infanticide in the species. To the contrary, in Tikal adult male coatis

were often seen in the near vicinity of young of all ages with neither the young nor their dams

displaying any alarm or other defensive behavior (Booth-Binczik, 2001).

In addition to cooperative defense, other forms of communal care of offspring have been

documented in the coati. Nest sharing has been observed both in the wild (Russell, 1979; 1983;

Chapter 2) and in captivity (Smith, 1980). In some instances it involved a female that had lost a

litter helping to care for another female's litter (Russell, 1979; Smith, 1980), and in one case two

females pooled their litters and both nursed all infants (Russell, 1979). There have also been

frequent observations of allogrooming by non-parents once bands have reunited after the nesting

period (Russell, 1983; pers. obs.).

As important as communal care of whatever form may ultimately be to coati offspring

survival, however, it does not appear to explain the species' remarkable birth synchrony, as a

rather basic prediction arising from the communal care hypothesis failed testing in the current

study. It is suspected but as yet unknown whether coatis undergo direct development (Chapter 2),

but females are presumably able to exert at least as much control over the timing of reaggregation

as parturition. Nonetheless, births were clustered significantly more than were reaggregation

events. Selective pressures for being in a group are evidently not the driving forces behind coati

birth synchrony.

Considering the aforementioned nest raiding by predators on coatis, the predator

swamping hypothesis might at first look somewhat more attractive. The effectiveness of this

anti-predation strategy, however, is determined not only by the degree of synchronization of a

vulnerable prey stage but also by the nature of the predators and their methods. That is, if

neighboring groups of prey differ somewhat in their timing and their predators are sufficiently

mobile, the predators will simply respond by shifting their focus from group to group accordingly









(Ims, 1990a). Considering the mobility of coati nestling predators (especially raptors) and given

the significantly greater variance in the timing of births between than within bands found in the

present study, shifting predators appear to pose a real threat to coati young. The predator

swamping hypothesis for birth synchrony is unsupported.

At least until new hypotheses and/or evidence are examined to account for coati birth

synchrony, then, the most likely explanation appears to be that this phenomenon is merely an

extreme example of a tropical animal using social cues to supplement the relatively weak

environmental predictors it relies upon for timing reproduction. Some support for this argument

is found in the results of the comparison of intra- and inter-band synchrony mentioned above.

Additional support can be found in a closer consideration of the coati's annual birth

pulse. As mentioned, both the 1995 and 1996 overall peaks in parturition were slightly

platykurtic, perhaps only differing from completely normal curves due to the method used for

estimating uncertain birthdates, i.e., attributing portions of each of these births to more than a

single day. The coati has ample cause in terms of food availability to have developed the

adaptation of reproductive seasonality (Russell, 1982; Chapter 2), which-barring severe climatic

curtailment (e.g., at very high latitudes) or protraction by variable response to weak

environmental cues (e.g., at low latitudes)-should produce a normally distributed biological

response. That is, if the coati's annual birth pulse is driven purely by seasonal considerations, it

should be normally distributed or flattened depending on the environmental predictors available

to the species and its ability to respond to them. Accordingly, most seasonally reproducing

tropical mammals studied to date display long, modestly peaked birth pulses (Fleming, 1973;

Bronson, 1989; Di Bitetti and Janson, 2000; Chapter 2), and the notable exceptions are highly

social species (Chapter 2). In contrast, the evolutionary forces that promote synchrony do so by

acting against either tail of a response curve (e.g., Findlay and Cooke, 1982), creating a

leptokurtic distribution. The coati's normally distributed parturition peaks suggest that birth

synchrony in and of itself is not adaptive in this species.









Given the likelihood of direct development in this species (Chapter 2), it is also possible

that the coati's unusually tight clustering of births is simply the result of selection for mating

synchrony. Synchrony of estrus among females should make it less possible for one male to

monopolize mating access to a group of females (Emlen and Oring, 1977; Gehrt and Fritzell,

1999a). It could therefore be advantageous for females to synchronize their receptivity if it gives

them access to more than a single male, enabling mate choice. However, some studies have

failed to find a relationship between degree of synchrony in female receptivity and degree of

monopolization by males (Poston et al., 1999; Widdig et al., 2004), and it has also been

suggested that synchronized receptivity would limit rather than enhance females' opportunity for

mate choice (Pereira, 1991; Schank, 2001). The nature of the relationship between mating

synchrony and mate monopolization/mate choice undoubtedly depends upon the degree of

overlap among females' periods of receptivity, which is not yet known for the coati.

Of course, it could be argued that to be most useful, the term "birth synchrony" should be

reserved solely for situations in which selective pressures are acting directly on the clustering of

births. From this viewpoint, the tight clustering of births exhibited by the coati would not qualify

as birth synchrony per se if it results from such phenomena as reproductive seasonality and

mating synchrony.

Left wholly unexplored is the question of precisely how the coati achieves such

extraordinarily tight reproductive seasonality. Assuming social facilitation of environmental cues

as appears to be the case, numerous possibilities exist. Among Mammalia social mechanisms for

timing reproduction have primarily been investigated in rodents. Although in most cases the

presence of chemical cues from reproductively active females inhibits ovarian cycling in others

(reviewed in Bronson, 1989), in some situations it has instead been found to trigger (Drickamer

and Hoover, 1979) or synchronize (McClintock, 1978) such cycling. Males have also been

shown to use both chemical and tactile means of initiating and/or synchronizing female

reproductive cycling (Whitten, 1956; Marsden and Bronson, 1964; Bronson and Maruniak, 1975;






63


Carter et al., 1986), and in the case of red deer (Cervus elaphus), even to use auditory signals

(McComb, 1987). On that last bit of information, it is perhaps worth noting that the coati is the

first carnivore to be identified in which males undergo a rut (Chapter 4), and that a hallmark

feature of this male adaptation is an advertising call. With opportunity, this will be a focus of

future research.















CHAPTER 4
RUT

Introduction

Long mistaken for a separate species due to its larger size and markedly different habits

(e.g., Sanderson, 1941), the male white-nosed coati (Nasua narica) has received far less attention

than has the female from researchers. This disparity in scientific effort is perhaps a result of the

chiefly solitary nature of adult males (Kaufmann, 1962; Booth-Binczik, 2001) and the problems it

poses to one wishing to work with these diurnal, semi-arboreal, medium-sized carnivores in their

primarily dense, tropical forest habitat (general ecology reviewed by Gompper, 1995). Previous

discussions of coati reproductive ecology addressed only the timing of reproductive events and

possible benefits of seasonality to females and young (Kaufmann, 1962; Smythe, 1970; Russell,

1982). This paper focuses instead on reproductive patterns displayed by the male of the species.

Environmental influences act on females in determining a species' timing of birth, and

males can be expected to respond to female imperatives or (in some instances) the environment

which shaped them with reproductive adaptations of their own. Males of many species are

opportunists, maintaining full reproductive readiness at all times for whatever mating chances

occur, but many other species have evolved temporal variation in male reproductive capabilities

in ways that reflect patterns of female receptivity. This variation seems designed both to

maximize the males' ability to capitalize on mating opportunities when they exist and to minimize

the costs associated with that ability when they do not. One such temporal pattern seen among

male mammals involves rut.

The term "rut" has often been used to describe a seasonal, principally or wholly

behavioral phenomenon displayed by males of some species or populations (e.g., the "fall rut" of









several high latitude North American ungulates; Spomer, 1996). Sometimes it has even been

used simply as shorthand for the mating period of any seasonally reproducing species (e.g.,

Genovesi et al., 1997). From an evolutionary perspective, however, rut might more properly be

thought of as an attribute of individual males rather than of seasons, species or populations as a

whole. Accordingly, the author defines rut as a brief annual period of dramatically enhanced

male reproductive capability that likely arose in response to tight female reproductive seasonality

in combination with the intense male-male competition such seasonality sometimes fosters, and

that therefore tends toward synchrony within a population. It differs from other forms of male

reproductive seasonality not only in the brevity and magnitude of the changes rutting males

undergo, but also in the nature of those changes. Specifically, males in rut display a fugue of

behavioral, physiological and anatomical characteristics that-despite some seeming maladaptive

at first glance-act in concert to temporarily maximize competitive ability and thus likely

reproductive success.

Besides being interesting in their own right, male reproductive adaptations can also

provide insight into a species' overall reproductive strategy. One example is presented in the case

of mammals in which the males undergo seasonal aspermatogenesis. Of interest in studies of

species displaying seasonal reproduction is whether the pattern is a (relatively) rigid evolutionary

result of historical climatic rhythms or merely an opportunistic response to prevailing conditions,

i.e., whether it is an obligate or facultative strategy (Negus and Berger, 1972; Bronson, 1989).

Because spermatogenesis takes longer to complete than does ovulation after a period of

reproductive quiescence, and because males are evolutionarily impelled to have mature sperm

available whenever females might be ready to receive such, healthy adult male mammals have

generally evolved to produce mature sperm over time periods that more than encompass periods

of female receptivity (Bronson, 1989). Seasonal aspermatogenesis is thus primafacie evidence

that a species has adopted obligate reproductive seasonality, as such an extreme male adaptation









would be expected to arise only where females have a highly predictable pattern of receptivity,

especially where the potential costs of male reproductive capability are great.

The coati certainly fulfills the first part of this evolutionary scenario, being exceptional

among tropical mammals (Fleming, 1973) for its high degree of reproductive seasonality at the

few locales thus far examined (Kaufmann, 1962; Russell, 1982; Chapter 2). The pattern seen in

Tikal National Park, Guatemala, may be typical in this respect. There, virtually all copulation

occurs within an approximately two-week period near the middle of the January-April dry season

and parturition occurs in a similarly brief period beginning shortly before the onset of the rains in

May (Chapter 2).

There is also reason to hypothesize high costs of reproduction for male coatis. Unlike

males, female coatis are highly social, living in cohesive bands with their young most of the year

and becoming solitary only to nest and give birth (Kaufmann, 1962; Chapter 2). Combined with

the species' brief mating period, the result is a temporal and spatial clustering of receptive females

that could be expected to foster intense competition among males. Indeed, anecdotal

observations of male coatis by previous researchers suggest such competition exists. Chapman

(1938) and Kaufmann (1962) noted marked seasonal changes in male body condition. They and

Gilbert (1973) also attributed a seasonal proliferation of serious injuries among males to

intrasexual agonism during the mating period.

This study was undertaken to determine the extent and results of male reproductive

competition in the coati and to evaluate the hypothesis that male coatis have evolved adaptations

to maximize their competitive ability and minimize their associated costs. Specifically, year-

round data on male behavior, physiology and anatomy were collected to test the prediction that

male coatis exhibit periods of enhanced and reduced reproductive capability in a pattern which

reflects that of female receptivity.









Methods

General

As part of a broader study of white-nosed coati reproductive biology in Tikal National

Park, Guatemala (17N, 89W), behavioral, morphometric and endocrinologic data were

collected on 24 free-ranging adult male coatis (plus one found freshly road-killed) from June

1994 through October 1996 (except as noted below). A male was considered adult once it

dispersed from its natal band, which typically took place 1-2 months prior to the mating period in

its second year of life (i.e., at 20-21 months of age).

Each male was initially captured by live-trap or (more often) blowgun and chemically

immobilized by intramuscular injection of approximately 7 mg/kg Telazol (Fort Dodge

Laboratories Inc., Fort Dodge, IA). Anesthetized animals were tattooed and eartagged for

identification, weighed, measured and subjected to blood collection. Each male was also visually

examined to determine general physical condition, giving particular attention to the nature and

abundance of any injuries. Identified injuries were fresh scars, open wounds and missing body

parts. Eighteen of the coatis were additionally fitted with 90 g motion-sensitive radiocollars

(Advanced Telemetry Systems, Isanti, MN) to enable subsequent location and recapture, and to

confirm death if such occurred. Individual males were recaptured by blowgun (never more often

than monthly) for resampling. The research was conducted under Institutional Animal Care and

Use Committee protocol #4084 from the University of Florida. All animal handling procedures

were conducted in accordance with National Institutes of Health standards.

Behavior

Four radiocollared males were habituated to the close presence of observers (see Chapter

2) and then utilized for behavioral data collection from September 1995 through August 1996.

Observation sessions were scheduled twice monthly for each available male (although frequent

radiotransmitter failures often resulted in fewer males being available at any given time), and in

each case began as soon as possible after locating the focal animal in the morning (typically









06:00-09:00) and continued for the next 4-6 h thereafter. Two observers were always present,

one of whom was responsible for monitoring and recording behavior and the other for estimating

the distance traveled by the focal animal via a tally counter as well as assisting in keeping the

animal in sight. The same people performed the same observational tasks throughout the study,

except that on eight occasions substitutes filled in for the second observer after cross-training and

calibration sessions were conducted to ensure uniformity in coati travel distance estimation.

During each observation session, the amount of time spent by the focal male with a coati

band versus alone was recorded, and the nature and duration of all interactions involving the male

were recorded. A male was considered to be with a band if the observer following him could see

any band member, typically less than 30 m distant. The frequency and/or duration of other

behaviors were recorded during the first 5 min of every quarter hour. The following states and

behaviors were utilized in the analyses: Active doing anything other than sitting or lying down.

Interaction two or more animals apparently altering their behavior in response to one another.

Agonism aggressive or defensive interaction. Fight agonistic interaction involving chasing,

knocking each other out of trees, or actual or attempted biting and/or clawing. Approach one

individual orienting toward and moving to within touching distance of another. Scentmark -

briefly (approximately 1 sec) rubbing the genital region against some substrate. Forage bringing

the nose into close proximity or manipulating various substrates in apparent search of

invertebrates or fallen fruit, or similarly investigating fruit-bearing portions of plants. Groom -

manipulating one's own body parts with mouth or paws. Travel moving from one place to

another with the head not oriented toward any substrate, i.e., not apparently foraging. Rut call -

producing a rhythmic, staccato, low-pitched vocalization which appeared to fall into Kaufmann's

(1962) "grunting" (p. 123) classification; distinguishable from similar vocalizations (e.g.,

grunting in alarm) by the combination of its slower cadence, greater loudness and much longer

duration (typically several minutes at a time) as well as by the situation in which it was produced.









Morphometry

Each male's teeth were visually examined for damage (such as broken tips) during each

immobilization, and intact lower canines were measured from gum line to tip with calipers. If

both teeth were undamaged, lengths (to the nearest 0. 1mm) were averaged; otherwise only the

length of the intact tooth was obtained. For comparative purposes, these same data were obtained

for the teeth of females immobilized during a companion study.

An index of each male's body fat level was determined at the time of immobilization.

This was accomplished in the manner of Hossler et al. (1994) by pinching a fold of the animal's

skin at the back of each rear leg midway between knee and hip, and using calipers to measure the

thickness of this fold to the nearest 0.1 mm. Measurements for the left and right thighs were

averaged. One person was responsible for taking these measurements throughout the study.

Testis size was also measured during each immobilization, and from the measurements

an index of testis size was determined. The scrotal skin was pulled taut around each testis and

three axes were measured with calipers to the nearest 0.1 mm: the longest dimension (L), the

widest perpendicular dimension at midlength (Wi), and the midlength dimension perpendicular to

both of these (W2). One person took all measurements. Opportunistic dissections of two freshly

road-killed coatis (one radiocollared, the other previously uncaptured) revealed a layer of fat

surrounding the testes ranging from scarcely visible on 7 June 1995 to as much as 5 mm thick on

9 January 1996. To compensate for this in approximating an animal's actual testis size, a

correction factor Y = 0.77X 2.23 was subtracted from each of the aforementioned dimensions,

with X being the fat level index of the animal at the time of examination. (For this purpose, the

fat level index of one coati for which leg pinch measurements were lacking was approximated

from a regression of all available fat data on time of year.) The above equation represents the line

connecting two points which were obtained by assigning the minimum and maximum fat level

indices recorded in the course of the study Ys of 0 and 10 (i.e., representing fat layers of 0 and 5

mm thick present on each side of a measured testis), respectively. This likely resulted in a









conservative correction of testicular dimensions, as 5 mm may have been a low approximation of

the maximum possible scrotal fat layer. The adjusted testicular dimensions were then plugged

into the formula for calculating the volume of an ellipsoid, V = L x W, x W2 x n/6, and the left

and right testis volumes so obtained were averaged to produce the testis size index reported. (The

raw data on coati testis size are presented in the Appendix.)

Endocrinology

Five to 10 ml of venous blood were drawn from a foreleg of each immobilized coati.

Blood was kept in an ice bath from the time of collection until the serum could be separated by

centrifuge 2-4 h later and then frozen. Fecal samples were also collected whenever possible

during immobilizations, and additional samples were obtained opportunistically from males under

observation. In either case, an entire fecal deposit was collected within 5 min of defecation and

maintained at ambient temperature for 2-6 h, after which it was homogenized and a sample of up

to 10 ml was frozen. All serum and fecal samples were first held in liquid nitrogen and then at

the completion of the fieldwork were transferred to a -700C laboratory ultracold freezer for

storage until they were analyzed en masse by testosterone radioimmunoassay (RIA).

Prior to analysis, a malfunction of the ultracold freezer resulted in all serum and fecal

samples thawing for a period estimated to have been 1-2/2 weeks. The effect of this thawing on

the androgen content of the samples is not known. The endocrinologic data presented herein

should therefore be considered representative of the pattern but not necessarily of the actual

testosterone levels circulating in or excreted by coatis.

Serum Testosterone RIA. Serum testosterone concentrations were determined via an

RIA procedure (Guillette et al., 1996) utilized previously for a wide variety of species and

validated for coati serum. Duplicate 50 ll aliquots of serum were extracted twice with 2.5 ml -

300C ethyl ether, dried under filtered air and reconstituted in 100 tl borate buffer (0.5 M, pH

8.0). To these were added 100 pl bovine serum albumen solution (0.75% BSA in borate buffer),









200 pC testosterone antiserum (T3-125 at a final concentration of 1:18,750; Endocrine Sciences,

Calabasas Hills, CA) and 100 pl [1,2,6,7-3H]-testosterone radiolabel (TRK-921 diluted in borate

buffer to approximately 13,000 cpm/100 pl; Amersham Life Science, Inc., Arlington Heights,

IL). Assay tubes were then vortexed briefly and incubated overnight at 40C. Bound-free

separation was achieved by adding 500 pl 5% charcoal/0.5% dextran in phosphate-buffered saline

and then centrifuging the tubes for 30 min at 2000 g, 4C. The supernatant was decanted, diluted

with 5 ml scintillation cocktail (Scintiverse BD, Fisher Scientific, Fair Lawn, NJ) and counted on

a scintillation counter (Beckman LS 5801, Beckman Coulter, Inc., Fullerton, CA).

Counts-per-minute were averaged for each pair of duplicates, and these were subjected to

Rodbard and Lewald's (1970) logit transformation. Testosterone concentrations were determined

by comparison of transformed data to a logit-log plot of 10 standards, ranging from 3.125 pg to

1600 pg hormone per assay tube, which were also run in duplicate in each assay. Naturally low,

medium and high testosterone concentration serum pools were also run in duplicate in each assay

as a check on inter-assay variance. Final testosterone concentrations were calculated as ng/ml

serum, and are reported without correction for assay accuracy.

Two assays were conducted to analyze samples, and three more to complete validation.

For all sample pairs, the mean ( SEM) duplicate coefficient of variance (CV) was 3.5 0.4%,

and r > 0.99 for the standard curve fit in all assays. Non-specific binding averaged 2.6 0.6%.

Inter-assay CVs in low, medium and high pools of serum were 17%, 7% and 12%, respectively.

The minimum detectable concentration of testosterone, based on the mean 2SD percentage of

bound radiolabel observed in five pairs of charcoal-stripped serum, was 0.04 ng/ml. A standard

curve prepared by spiking charcoal-stripped serum (four pairs at each standard concentration) was

parallel to that made using borate buffer (test for homogeneity of slopes Ff1,6, = 0.14, P > 0.75);

assay accuracy as determined by spike-recovery was 102%. Serial dilutions (one pair each at 30

pl, 50 pl and 70 gll) of low, medium and high pools produced flat lines with CVs of 13%, 8% and









4%, respectively. Intra-assay CVs in low, medium and high pools (five pairs of each pool) were

6%, 6% and 7%, respectively. Cross-reactivities greater than 1% reported by the antiserum's

manufacturer were: dihydrotestosterone 44.0%, 8-1-testosterone 41.0%, 6-1-dihydrotestosterone

18.0%, 5a-androstan-3P,17p-diol 3.0%, 4-androsten-3, 17p-diol 2.5%, 8-4-androstenedione

2.0% and 50-androstan-3p,17p-diol 1.5%.

Fecal Testosterone RIA. Fecal testosterone concentrations were determined much as

described for serum, except fecal steroid extraction was accomplished via a slightly modified

version of the "short method" described in Wasser et al. (1994), and this procedure as well as the

subsequent assay were validated for coati feces. Fecal samples were lyophilized at -550C under

vacuum exceeding 100 x 103 mBar and then ground to fine powder (removing discernible

extraneous material such as seeds, insect parts, etc.). For each sample, 0.1 g of powder was

lightly boiled for 20 min first in 5 ml and subsequently in 2.5 ml of 90% ethanol, and the

supernatant was dried tnder filtered air and reconstituted in 1 ml absolute methanol. The

methanol suspension was diluted 100 pl to 7.4 ml borate buffer, and 100 gl of the resulting

solution were pipetted into duplicate tubes and treated as per reconstituted serum extract in the

RIA described above. The 10 standards utilized in the fecal RIA ranged from 1.5625 pg to 800

pg hormone per assay tube. Final concentrations were calculated as ng/g dried feces, and are

reported without correction for assay accuracy.

Samples were analyzed in two assays, and validation was completed in another four. The

mean CV for sample duplicates was 1.8 0.2%, and r > 0.99 for the standard curve fit in all

assays. Mean non-specific binding was 0.6 0.1%. Inter-assay CVs in low, medium and high

fecal pools were 7%, 9% and 8%, respectively. The minimum detectable concentration of

testosterone, based on the mean 2SD percentage of bound radiolabel observed in six pairs of a

naturally very low testosterone fecal pool, was 17 ng/g. A standard curve prepared by spiking the

very low pool (four pairs at each standard concentration) did not differ statistically from that









made using borate buffer (test for homogeneity of slopes F[,.16] = 0.58, P > 0.5); spike-recovery

accuracy was 111%. Serial dilutions of a medium pool (one pair each at 50 ptl, 75 pll, 100 pl, 125

pl and 150 pl methanol suspension diluted in borate buffer to a total of 7.5 ml solution) produced

a flat line with a CV of 8%. Intra-assay CVs in low, medium and high pools (five pairs of each

pool) were 3%, 6% and 1%, respectively.

Statistical Analyses

Observations obtained in companion studies of female coatis conducted over the entire 2

'/2-year sojourn in Tikal (Booth-Binczik et al., 2004; Chapter 2) were used to delineate three

distinct annual periods to aid in data presentation and analysis:

The non-rutperiod comprised the nearly 11 months of the year that occurred outside of

the pre-mating and mating periods, from 29 February or 1 March (depending on year) through 22

January.

The pre-mating period comprised the three weeks leading up to the mating period

during which multiple male coatis (as opposed to one or none) were regularly detected

accompanying a given band at a given time, from 23 January through 12 February.

The mating period comprised the 16 days during which copulations were noted, from

13 February through 28 February.

In some analyses data for the pre-mating and mating periods were combined into a single

rut period which was then compared to the non-rut period.

Whenever possible, each male was sampled repeatedly within each period every year, but

was in general represented by only a single data point per period in a given statistical test. This

was accomplished by averaging a male's subsamples where collection effort was equal (e.g., in

the case of multiple immobilizations) and adding subsamples where it was not (e.g., in the case of

multiple observation days of varying lengths). The exception was in evaluating the correlation

between serum and fecal testosterone concentrations, in which all sample pairs (i.e., serum and









feces collected from the same animal at the same time) were treated as independent; individual

contributions to this dataset ranged from one to five sample pairs per represented male.

Sokal and Rohlf (1981) guided all statistical efforts, and STATGRAPHICS Plus 5.1

software (Manugistics, Inc., Rockville, MD) aided computations. Datasets for comparing the

three periods first underwent a battery of tests for homoscedasticity and normality (using a

conservative Pa < 0.10 level of rejection), and were subjected to standard transformations if such

were indicated. When raw or transformed data met parametric assumptions, two-way ANOVAs

were conducted treating period and male as main effects (male effects were never found to be

significant and are not discussed further); otherwise the data were analyzed via Kruskal-Wallis

tests. Fisher's Least Significant Difference procedure was used to distinguish among periods

when overall significance was detected. Two-tailed t-tests were conducted instead of ANOVAs

in the few cases where only two groups were compared. A P,, < 0.05 level of significance was

utilized in all reported statistical tests.

Results

Males interacted on 26 (90%) of the 29 occasions when they came within sight of one

another during scheduled observations. All male-male interactions quickly escalated into

relatively brief but intense physical altercations with few or no apparent preliminaries. Male

coatis fought sporadically throughout the year, but the frequency of such contests increased

during the pre-mating period and peaked during the mating period (Fig. 4-1). The frequency of

male-male agonism in the three defined periods of non-rut, pre-mating and mating could not be

statistically distinguished (H14.4.3 = 4.66, P = 0.097). However, focusing instead simply on a

comparison of non-rut to rut (the latter being pre-mating and mating combined) revealed fighting

to be significantly more common during rut (0.41 0.18 fights/hr versus 0.04 0.01 fights/hr

during non-rut; paired tt31 = 3.63, P = 0.036).









0.8
Male-Male Agonism

0.6-


0 0.4


S0.2 -


0
S4
0 '-- T '---------


10 -
Injuries
8 -
6
6 6-

4 -

2-
2 F15
18T
0 1--
Non-Rut Pre-Mating Mating

Figure 4-1. Mean ( SEM) frequency of intrasexual agonistic interactions and injuries
observed among adult male white-nosed coatis in Tikal National Park, Guatemala,
September 1995 September 1996 and June 1994 October 1996, respectively.
Number of males sampled in each of the three defined periods (non-rut: 29 Feb/1 Mar -
22 Jan; pre-mating: 23 Jan 12 Feb; mating: 13 Feb 28 Feb) indicated on bars.









The incidence of injuries noted during immobilizations rose sharply during the mating

period (Fig. 4-1; H18,15,6J = 8.74, P= 0.013). Injuries most often affected the head, chest or

forelimbs and were frequently severe, including badly broken or missing teeth (especially

canines) and missing claws or entire toes, as well as a variety of deep flesh wounds. Remarkably,

none of the examined animals died as a direct consequence of such injuries, but two of the three

natural deaths recorded among radiocollared males during the course of the study occurred in

February 1995, i.e., during rut of that year; the third death occurred in August 1996.

Unfortunately it was not possible to reach the carcasses quickly enough to determine the exact

timing or causes) of death.

A comparison of male and female coati dentition revealed the males' lower canine teeth

to be substantially longer (15.5 0.4 mm for 22 males versus 8.7 0.2 mm for 49 females; t691 =

18.40, P< 0.001).

Males spent significantly more time with bands during the mating period than at other

times of the year (Fig. 4-2; F12.5] = 6.16, P = 0.045). Periods did not differ in terms of males

approaching females either quantitatively (Fig. 4-2; F[2.5] = 0.57, P = 0.618) or qualitatively;

regardless of time of year such approaches were most often rebuffed-sometimes violently.

Occasionally females allowed brief perineal sniffing by males, however, or less often investigated

the males in a similar fashion themselves. Females also sometimes initiated or reciprocated

allogrooming with males. These affiliative behaviors were infrequent and sporadically

distributed throughout the year.

Males scentmarked at a high rate throughout the year against the base of a living or fallen

tree or on a log or some other relatively low-lying feature of the terrain being traversed; they also

occasionally climbed into and traveled through the forest canopy seemingly just to repeatedly

scentmark the large, lower branches along some distance before returning to the ground.

Although scentmarking was highest during the mating period, no time of year could be

statistically distinguished from another (Fig. 4-3; F[2.5] = 2.60, P = 0.168).









80 -


60 -


40-


20-


0

1.2


0.9


0.6


0.3


Male-Band
Association


4


T3


Approaches


Non-Rut Pre-Mating Mating


Figure 4-2. Mean ( SEM) percentage of time adult male white-nosed coatis spent with
bands and frequency with which males approached females in Tikal National Park,
Guatemala, September 1995 September 1996. Number of males sampled in each of the
three defined periods (non-rut: 29 Feb/1 Mar 22 Jan; pre-mating: 23 Jan 12 Feb;
mating: 13 Feb 28 Feb) indicated on bars.


-









50-
Scentmarking
a 40- 3

0 30
ST4 4
20-

S10-

0


12
Calling




S 6 -


3- 4

0
Non-Rut Pre-Mating Mating

Figure 4-3. Mean ( SEM) frequency of scentmarking and percentage of active time
spent calling by adult male white-nosed coatis in Tikal National Park, Guatemala,
September 1995 September 1996. Number of males sampled in each of the three
defined periods (non-rut: 29 Feb/i Mar 22 Jan; pre-mating: 23 Jan 12 Feb; mating:
13 Feb 28 Feb) indicated on bars.









The rut call was heard only during the pre-mating and mating periods (especially the

latter; Fig. 4-3; H[4.4.3] = 6.14, P = 0.046) and elicited close investigation by both females and

males. The area occupied by Tikal's large bands (up to 162 females and maturing young; Booth-

Binczik, 2001)-and thus also the males accompanying them-as the animals moved through the

forest precluded two human observers quantifying many aspects of the mating pattern,

particularly when those observers were concentrating primarily on the behavior of a single focal

animal. However, it was evident that up to several males (at least four could be conclusively

identified in one instance) were calling at the same time from individual perches in the lower

canopy directly or peripherally over a given band foraging on the ground below, changing their

perches as necessary to keep up with the movements of the band. On at least six occasions

individual females were seen leaving their bands and going to calling males, and at least three

times the females stayed with the males to copulate. Calling males usually appeared to ignore

one another, but on at least two occasions individual males were also seen briefly leaving their

calling stations to chase or fight with others calling nearby; most recorded fights occurred when

males were not calling.

Males in Tikal spent significantly less time grooming during the mating period than at

any other time of year (Fig. 4-4; H[4,4,3] = 6.66, P = 0.036). Periods did not differ appreciably in

terms of time males spent foraging or distances males traveled (Fig. 4-4; for foraging H[4.4,3] =

2.64, P = 0.268; for traveling F[2,5] = 3.36, P = 0.119).

Body fat levels measured in immobilized males rose steadily throughout most of the year

but fell sharply at the beginning of the pre-mating period, ultimately reaching a low at the end of

the mating period that was only 20-25% of the peak achieved at the end of the non-rut period

(Fig. 4-5). Fat levels were significantly lower during mating (3.8 0.6 mm versus 7.8 + 0.7 mm

and 7.7 0.8 mm during non-rut and pre-mating, respectively; H[18,15,61 = 11.27, P = 0.004).








Self-Grooming


4


Traveling


4 4


Non-Rut


Pre-Mating


Figure 4-4. Mean ( SEM) percentage of active time adult male white-nosed coatis spent
grooming themselves and foraging, and their rate of travel in Tikal National Park,
Guatemala, September 1995 September 1996. Number of males sampled in each of the
three defined periods (non-rut: 29 Feb/I Mar 22 Jan; pre-mating: 23 Jan 12 Feb;
mating: 13 Feb 28 Feb) indicated on bars.


T3
F __


9

6

3


100


700
600
500
400
300
200
100
0


T3


Mating









The testes of immobilized males increased rapidly in volume with the beginning of the

pre-mating period, peaked late in pre-mating or early in the mating period, decreased nearly as

rapidly throughout the remainder of mating and then continued decreasing more slowly well into

the non-rut period (Fig. 4-6). The males' testes were significantly smaller during non-rut (1.8 +

0.2 x 103 mm3 versus 2.9 0.3 x 103 mm3 and 3.3 0.2 x 103 mm3 during pre-mating and

mating, respectively; F[2.13] = 8.85, P = 0.004). Histological examination of testicular

parenchyma obtained from road-killed males on 7 June 1995 and 9 January 1996 revealed the

presence of all cell types-including mature spermatids-in the seminiferous tubules at both times

of year.

Serum and fecal testosterone concentrations were highly correlated (r = 0.86 for 28

sample pairs from 16 males; t[261 = 8.42, P < 0.001) and displayed a clear circannual pattern (Fig.

4-7). Specifically, testosterone levels rose gradually beginning several months prior to the pre-

mating period, spiked suddenly to a peak near the end of pre-mating and then fell even more

suddenly back down to baseline by the end of the mating period. The three periods of the year

differed significantly whether serum and fecal testosterone values were treated separately or

combined (for combined data in which serum values (TI) were converted to fecal equivalents (Ty)

via the regression formula Ty= 52.97T, + 51.07, non-rut was 172 19 ng/g, pre-mating 549 63

ng/g and mating 358 106 ng/g; H[19,16,8] = 16.66, P < 0.001).

Discussion

Male-Male Agonism

Lacking the showy weaponry seen in many rutting species (such as antlers, horns and

tusks), the male coati nonetheless appears well-equipped for intrasexual combat. Both sexes rely

on their teeth as well as their powerful forelegs and long, sharp claws when fighting, but the

male's dentition may be specially designed for this purpose given the degree of lower canine

tooth sexual dimorphism observed in the present study.



















Wet Season Dry Season
16 0o
O
14 o
S 12 o o
10 o
pi oo o
S008 o

S- 0 0o 0 0
0. 4 o o g) o o


Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun
Date
Figure 4-5. Annual body fat profile exhibited by adult male white-nosed coatis in Tikal
National Park, Guatemala, July 1994 through October 1996. Based on hind leg pinch
thickness measured in 42 immobilizations of 18 animals during non-rut period unshadedd
background; 29 Feb/I Mar 22 Jan), 16 of 15 animals during pre-mating (lightly shaded;
23 Jan 12 Feb) and 6 of 6 animals during mating (more darkly shaded; 13 Feb 28 Feb).




















Wet Season Dry Season

0
0
0

0


0 0 00
o o o o o
S000 0 O O

0 GD CP
0ilililil____ilUnl___l___lilil___l___


Aug Sep Oct Nov Dec


Jan Feb Mar Apr May Jun


Date


Figure 4-6. Annual profile of testicle size exhibited by adult male white-nosed coatis in
Tikal National Park, Guatemala, June 1994 through October 1996. Individual testis
measurements were corrected for the animal's estimated testicular fat layer (see Materials
and Methods) prior to ellipsoid volume calculation. Profile based on 45 immobilizations
of 19 animals during non-rut period unshadedd background; 29 Feb/1 Mar 22 Jan), 16 of
15 animals during pre-mating (lightly shaded; 23 Jan 12 Feb) and 6 of 6 animals during
mating (more darkly shaded; 13 Feb 28 Feb).


0


Jul










S Wet Season Dry Season


Serum T


O]


20

16

12

8

4

0


1500

1200

900

600

300

0


Fecal T


Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun
Date
Figure 4-7. Annual serum and fecal testosterone (T) profiles exhibited by adult male
white-nosed coatis in Tikal National Park, Guatemala, July 1994 through October 1996.
Non-rut period (29 Feb/I Mar 22 Jan) indicated by unshaded background, pre-mating
(23 Jan 12 Feb) lightly shaded and mating (13 Feb 28 Feb) more darkly shaded. Serum
profile based on 42 samples from 18 animals during non-rut, 16 from 15 animals during
pre-mating and 6 from 6 animals during mating; fecal profile based on 70 samples from
13 animals, 8 from 8 animals and 8 from 5 animals, respectively. Twenty-eight paired
samples (i.e. serum and feces collected from same animal at same time) from 16 animals
represented by solid symbols. Curve visually fitted to all combined and smoothed data.


Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun


U









Other than their potential usefulness in combat, no explanation for the male coati's

enlarged canines is apparent. Although Smythe (1970) speculated that males on Barro Colorado

Island (BCI), Panama, might pursue larger prey than females, this idea was not borne out in

subsequent studies at that locale (Gompper, 1996) nor did it appear to pertain in Costa Rica

(SAenz, 1994) or Tikal (Booth-Binczik, 2001). In a comparative analysis of sexual dimorphism in

carnivore dentition, Gittleman and Van Valkenburgh (1997) likewise found that dietary

differences between the sexes were reflected in the size of the carnassials rather than the canines.

Instead, Gittleman and Van Valkenburgh (1997) determined that carnivore canine tooth

dimorphism correlated with mating system, with more polygynous species exhibiting greater

dimorphism. Such species likely experience particularly intense competition among males for

mates (Emlen and Oring, 1977), suggesting the enlarged canines' principal role lies therein. It

may be relevant in this respect to note that the ratio of male:female lower canine size found

among coatis in the present study (1.78) exceeded that displayed by any of the 45 carnivore

species Gittleman and Van Valkenburgh (1997) examined, and that the highest ratio they

discovered (1.62) belonged to Nasua nasua, a South American congener of the white-nosed coati

which has been much less studied but is believed to be similar in many respects (Emmons, 1990).

Based on the frequency with which Tikal's coati males were observed fighting and the

frequency and severity of the injuries they sustained presumably as a result, it appears that males

of this species do indeed face considerable and costly intrasexual competition. All male-male

interactions observed in the present study were agonistic. Most male-male agonism occurs during

the rut and, judging from the data on injuries, is most violent during the mating period.

Kaufmann (1962) reported that all male-male coati encounters he saw while conducting

observations of females on BCI were similarly agonistic, but stated that actual physical contact

was uncommon outside of the mating period, when most fights occurred. Chapman (1938) and

Kaufmann (1962) attributed a seasonal proliferation of injuries among BCI's male coatis to

intrasexual agonism associated with mating, and Gilbert (1973) reported a similar phenomenon









among male coatis in Arizona. Chapman (1938) and Kaufmann (1962) also detailed the severity

of the animals' injuries, noting their prevalence on the heads and forelimbs, and remarked upon

the animals' exceptional recuperative powers. Such healing ability notwithstanding, Chapman

(1938) reported the permanent partial blindness of a semi-tame male under his casual observation

after one such season, and believed the animal's ultimate disappearance two years later may have

been the result of it succumbing to injuries obtained in a subsequent mating period.

Male-male combat is also common-and often results in the injury or death of

combatants-in rutting species. Indeed, it might even be considered a hallmark of this

reproductive pattern. As in the present study, fighting among males of such species generally

spikes shortly before and during their brief annual mating periods (Wilkinson and Shank, 1976;

Clutton-Brock et al., 1982; Komers et al., 1994), and in some cases appears to cause a substantial

proportion of adult male mortality (Leslie and Jenkins, 1985; Hall-Martin, 1987; Poole, 1989). In

contrast, male-male agonism in carnivore species other than the coati tends to be centered on

territory establishment (e.g., tigers, Panthera tigris, Smith, 1993) or acquiring control of a social

group (e.g., lions, Panthera leo, Bygott et al., 1979; Packer and Pusey, 1982) before mating

opportunities arise, and conflicts during the mating period itself are less common.

Male-Female Affiliation

Bands of female coatis were typically the focal points of male-male encounters in Tikal,

and to some extent the greater incidence of fighting among males during the mating period might

simply reflect their increased opportunity to engage in such activity at that time. The present

study revealed that males spend more time in the company of bands during the mating period than

at other times of the year, and the number of males accompanying a given band at a given time

varies accordingly; whereas bands were usually seen with only one (but not necessarily the same

one) or no male in attendance throughout most of the year, during the mating period as many as

nine males have been simultaneously observed with a single band (Booth-Binczik et al., 2004).









Kaufmann (1962) also noted an increase in male-band spatial affinity at about the time of

reproduction among coatis on BCI, but with some differences. He believed that males there only

rarely associated with bands outside of what he considered to be the coatis' month-long mating

period (essentially a combination of the pre-mating and mating periods of the present study), and

that one particular male remained with each band almost constantly throughout that time, perhaps

copulating with all females therein. (It is unclear whether he ever observed successful

copulation; Chapter 2.) Kaufmann (1962) acknowledged, however, that unobtrusive males might

have come and gone undetected because only the bands were habituated to his presence and

served as the foci of his observations. That admonition was later borne out by Gompper et al.

(1997), who found that the males most commonly seen with bands on BCI during the mating

period nonetheless did not sire most of the young subsequently produced by females in those

bands. Booth-Binczik (2001) further demonstrated multiple paternity not only within bands but

also within individual females' litters in Tikal.

One might expect that male coatis would capitalize on their closer association with bands

during the mating period by directly initiating interaction with the females therein more

frequently, but this appeared not to be the case in Tikal. There, males approached females least

during the mating period, and their approaches were generally rebuffed then just as they were at

other times of the year.

This finding contrasts somewhat with Kaufmann's (1962) report that males in association

with bands during the coati mating period on BCI spent much of their time pursuing females, and

were more often amicably received by females then compared to other times of year. He

described almost all close male-female encounters occurring outside of the mating period as

hostile. Intersexual perineal sniffing and allogrooming were reportedly especially common at the

beginning of the mating period. Russell (1981) observed less agonism and more allogrooming

between the sexes not only during BCI's mating period but also for two months prior, which he

called a period of courtship, and reported friendly male-female encounters at other times of year









as well. In Arizona, Gilbert (1973) believed that males required acceptance by bands in a social

context prior to the mating period, simply approached and mounted receptive females during that

period (though it is unclear whether any successful copulations were actually observed; Chapter

2), and remained with bands for months thereafter.

It is well established that males of rutting species spend more time with females while

rutting than at other times of year ungulatess reviewed by Main et al., 1996; Ruckstuhl and

Neuhaus, 2000; African elephants, Loxodonta africana, by Poole, 1987). They are quite variable,

however, in the strategies they employ to secure access to receptive females. Some maintain

harems (Struhsaker, 1967; Clutton-Brock et al., 1982; Lovari and Locati, 1991), others follow

and defend individual females (Lent, 1965; Lott, 1981; Lovari and Appollonio, 1994), and others

defend territories and wait for females to enter (Jarman, 1979; Miura, 1984; Schuster, 1976).

Advertising

At least in Tikal, the male coati appears to depend more on advertising than on directly

pursuing receptive females. Whether its scentmarking behavior exemplifies this strategy remains

as yet unclear. Although the frequency of scentmarking behavior did not vary over the course of

the year, the true significance of this behavior may lie in its quality rather than quantity. An

unusually strong odor was incidentally noted during some male immobilizations and observations

during the mating period. The author therefore believes that scentmarking may yet be found to be

an important component of the male coati's rut.

Lending some support to this contention, Kaufmann (1962) remarked upon male coatis

on BCI "urine-rubbing" (p. 130) at the base of or in trees, especially as the males approached

bands of females during the mating period. Technically speaking, though, it should be noted that

it has not yet been determined whether males of this species employ urine, some other products)

or a combination thereof in scentmarking. Indeed, the procyonids have been studied far less than

some other carnivore families in this regard, but males of the coati's congener N. nasua reportedly









behave similarly (B. Hirsch, pers. comm.) and have sebaceous preputial glands that are believed

capable of producing copious secretary material (Shannon et al., 1995).

Scentmarking is considered ubiquitous among terrestrial mammals (Gosling and Roberts,

2001), but an accentuated form/degree of it may be another hallmark of rut. Typically,

specialized glands suddenly proliferate or activate in the rutting male (e.g., the poll glands of the

camel, Camelus dromedarius, Rai et al., 1996; temporal glands of the Asian elephant, Elephas

maximus, Eisenberg et al., 1971; a variety of glands in cervids, reviewed by Miiller-Schwarze,

1987), and the animal anoints itself and/or various natural signposts with the glands' redolent

products. Urine is similarly used by rutting males of many species (Poole and Moss, 1981;

Clutton-Brock et al., 1982; Miura, 1984), and at least in the case of the fallow deer (Dama dama),

its particularly strong odor appears to be due to the contribution of preputial glands that activate

at that time (Kennaugh et al., 1977).

More readily detected by an observer in Tikal than any coati odor is the male's rut call.

This behavior features prominently in the species' mating pattern there, which has been described

as a kind of mobile lek (Booth-Binczik et al., 2004). Nothing resembling such has yet been

reported for coatis outside of Tikal. However, Kaufmann (1962) noted that males interacting

during BCI's mating period often emitted a "loud, rapid grunting" (p. 125), and on one occasion

during that period he witnessed a male following and similarly vocalizing from a variety of

perches near a band. Hass and Roback (2000) also reported that the male of a copulating pair of

coatis in Arizona made what they interpreted as "alarm grunts" (p. 329) toward an approaching

female. These observations notwithstanding, it seems unlikely that such a flamboyant

phenomenon would have thus far been overlooked, particularly on BCI where so much time has

historically been invested in studying this and other species' behavior. It may be that lekking by

male coatis in Tikal represents a behavioral extreme compared to other populations which have

been examined.









Plasticity in mating patterns may be the rule among ungulates that lek. Fallow deer, for

example, utilize at least seven different mating systems under different ecological conditions

(Langbein and Thirgood, 1989), and topi (Damaliscus korrigum; Gosling, 1991) and blackbuck

(Antilope cervicapra; Isvaran, 2005) show almost equal flexibility.

Advertising calls may be the single characteristic most strongly identified with rutting

mammals. In fact, the word "rut" originates in the Latin rugire, meaning "to roar". Accordingly,

such calls have been widely reported and are evident in all types of mating systems: territoriality

(Estes, 1969; Miura, 1984), harem-holding (Struhsaker, 1967; Lovari and Locati, 1991), and

following (Poole, 1987; Berger and Cunningham, 1991).

It is a matter of debate to what extent either olfactory or auditory signals are directed at

potential mates versus rival males. Most researchers have concluded that both rut calls and

scentmarks serve to notify rivals of a male's physical condition and the attendant risks of

challenging him (e.g., Clutton-Brock and Albon, 1979; Bowyer and Kitchen, 1987; Berger and

Cunningham, 1991). Conversely, Hurst and Rich (1999) argued that the primary function of

scentmarking is to advertise quality to potential mates. There is evidence supporting both points

of view. McElligott and Hayden (1999) found that the vocalization rate of rutting fallow deer

was affected by whether other males were nearby, but not by whether the calling male was about

to copulate or had just done so. In studies of elephants (which display an asynchronous rut

known as musth), however, female African elephants preferred to mate with musth males (Moss,

1983) and apparently used both urine trails and musth rumbles to locate them (Poole and Moss,

1989), and female Asian elephants were able to identify males in musth from the males' urine

(Schulte and Rasmussen, 1999), and the age and musth phase of males from the males' temporal

gland secretions (Greenwood et al., 2005). Additionally, both olfactory (Coblentz, 1976) and

auditory (McComb, 1987) signals from rutting males have been shown to bring females of some

species into estrus. Of course, whether the proximate function is to attract receptive females or

repel competing males (or both), male advertising ultimately functions to increase mating









success; for example, of the many factors considered by McElligott et al. (1999), the amount of

time rutting fallow deer spent groaning was most highly correlated with mating success.

Self-Maintenance Costs

In addition to the risk of injury and death from combat, the male coati may pay a variety

of less apparent costs to support its activities during rut. Coati males in Tikal spend less time

grooming themselves during the mating period than at other times of year. The other relevant

activities monitored in the present study (foraging, traveling) did not differ with time of year, but

year-round male body fat profiles demonstrate a clear negative shift in the animals' energy

balance during the rut. Female coatis display a similar shift at that time (Chapter 2), however,

and the respective roles of reproductive activities and resource availability remain unclear.

No relevant data are available on male coatis at other locales. Profound variation in body

fat or weight is seen in the coati's northern temperate relative, the raccoon (Procyon lotor), but

tends to be more gradual; it is unknown as yet what if any influence mating period may have on

the male raccoon's circannual pattern (Mech et al., 1968; Dunn and Chapman, 1983; Moore and

Kennedy, 1985; Davison, 1993; Gehrt and Fritzell, 1999b).

The indirect costs of rut are well documented in many ungulate species (see the partial

albeit lengthy list of examples provided in Mysterud et al., 2004). Looking at such costs

individually, the effects of rut per se on grooming behavior have not previously been examined,

but Mooring et al. (1996) found that territorial male impalas (Aepyceros melampus) groomed less

while rutting than did females or males that were not holding territories, and the territorial males

hosted more ticks as a result. Typically, rutting males sharply decrease or eliminate foraging

(Mitchell et al., 1976; Miquelle, 1990; Perez-Barberia et al., 1998; Pelletier, 2005) while

increasing their general activity levels (Clutton-Brock et al., 1982; Fint and Krzywinski, 1997).

As a result they experience a sudden decline in body weight and fat levels (Mitchell et al., 1976;

Dunham and Murray, 1982), in some cases even as a season of food scarcity approaches

(Miquelle, 1990; Kolle et al., 1993).









Testicular Activity

The male coati is obviously engaging in a seasonal pattern of reproduction

complementary to that of the female, but how committed is it to that strategy? Changes in

gonadal tissue are clearly involved, as demonstrated by the circannual pattern males displayed in

testis size. The finding that mature sperm are being produced both soon before and several

months after the mating period, however, suggests that at least some level of fertility persists over

a prolonged period if not year-round. Male reproductive capability beyond rut was also

demonstrated by the fact that at least five females that lost their litters not long after parturition

were apparently fertilized again more than three months after rut's conclusion, resulting in them

giving birth to second litters (Chapter 2). Testicular data are lacking for coatis outside of Tikal.

Circannual cycles of testicular regression and recrudescence are normally observed in

rutting species (included in mammalian review by Lincoln, 1989). In most species thus far

examined these cycles include a period of cessation in spermatogenesis and a brief period of

maximal sperm production coincident with rut (Robinson et al., 1965; Lincoln, 1971; Chaplin and

White, 1972; West and Nordan, 1976; Marchlewska-Koj and Kruczek, 1988; Reyes et al., 1997).

In other (typically lower latitude) species the males remain more or less competent year-round

(Abdel-Raouf et al., 1975; Brown et al., 1991; Monfort et al., 1993; Willard and Randel, 2002).

In either case it appears that the rapid testicular proliferation associated with rut serves

mainly to increase androgenesis (see Brown et al., 1991; Reyes et al., 1997), prompting rut

behavior and the development or activation of various structures in its support. The role

androgens play in the social aggression of rutting males has received the most attention

(Jainudeen et al., 1972; Lincoln et al., 1972; Yagil and Etzion, 1980; Mossing and Damber, 1981;

Bouisson, 1983; Poole et al., 1984; Pelletier et al., 2003; Mooring et al., 2004), but these

hormones have also been linked to cutaneous glandular secretion and scentmarking (Jainudeen et

al., 1972; Yagil and Etzion, 1980; Mossing and Damber, 1981; Poole et al., 1984), calling









(Clutton-Brock and Albon, 1979; Yagil and Etzion, 1980; Li et al., 2001) and diminished

foraging (McMillin et al., 1980; Newman et al., 1998) and grooming (Kakuma et al., 2003).

Many if not all of the phenomena displayed by the rutting coati may be under androgenic

control as well. The patterns observed in coati testis size and testosterone level are similar to

those reported for numerous northern temperate ungulate species (Short and Mann, 1966;

Lincoln, 1971; McMillin et al. 1974; West and Nordan, 1976; Schams and Barth, 1982; Asher et

al., 1989; Asher and Peterson, 1991; Ditchkoff et al., 2001; Mooring et al., 2004; Martinez-Pastor

et al., 2005).

In the two procyonids previously studied (also northern temperate species), the raccoon

and ringtail (Bassariscus astutus), testis size also peaked just prior to or early in the species'

annual mating periods, but the processes of recrudescence and regression were more gradual and

(near) maximum size was maintained for several months (Sanderson and Nalbandov, 1973; Dunn

and Chapman, 1983; Poglayen-Neuwall and Shively, 1991; Davison, 1993). Both of these

species also displayed a four- to five-month testicular nadir involving a marked reduction or

cessation in sperm production (Sanderson and Nalbandov, 1973; Dunn and Chapman, 1983;

Poglayen-Neuwall and Shively, 1991). Surprisingly, only scant and unclear endocrinologic data

exist for the male raccoon. Davison (1993) reported only a broad, low peak in testosterone (the

maximum serum concentration recorded was 3.69 ng/ml) roughly centered around the species'

late winter mating period in the southeastern United States, and Kaneko et al. (2005) reported that

testosterone concentrations were highest in the fall (achieving in the vicinity of 80 ng/ml) in feral

animals in Japan; both studies were hampered by small, sporadically obtained samples.

Conclusion

The reproductive pattern displayed by the male coati at Tikal is unusual in two regards:

First, the male coati's rut is more akin to that of many ungulate species than to the pattern

of any other carnivore species examined to date. The highly social nature and strong reproductive

seasonality of female coatis foster intense competition among males. Male coatis have




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REPRODUCTIVE BIOLOGY OF A TROPICAL PROCYONID, THE WHITE-NOSED COA TI By GERALD ALLEN BINCZIK 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 2006

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I tarried in producing this document, and as a result two of the people I most wanted to share it with did not live to see its completion. I offer my dissertation in their memory ... My mother, Rosemary Binczik Professor John F. Eisenberg

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ACKNOWLEDGEMENTS Front and center in my thank s are of course my advisor, Dr. Loui s J Guillett e, Jr., the re s t of my academic committee, Dr. Joel H Brendemuhl Dr. H. J a ne Brockmann, Dr. Colin A. Chapman and Dr. Melvin E. Sunqui s t and Dr. John F. Eisenberg, who was unfortunat e ly unable to complete hi s se r v ice on my committee. Having always pr ev iou s ly worked ind e pendently (so me might h ave in s t ead sa id I was hard-headed), I l ea rn ed as much as anything e l se in th e course of my Ph D. program to make better u se of the expertise and life knowled ge I am offered, and I am grateful t o th e m for all that they s hared (and tri e d to s hare ) with me Th a nk s go out, too to Dr. Rebecca T. Kimball for h e lping out on s hort notic e at the end of my progr a m The Lincoln Park Zoo Scott Neotropic Fund provided essential funding and th e Florida Mu se um of Natural History and University of Florida lent n ecessary equipment and l a b ora tory access. The field work in Tikal National Park, Guatemala was permitted by the Consejo Nacional de Areas Protegida s (C ONAP ) and the ln s tituto de Antropologfa e Hi s torfa I am particularly grateful to Lie Oscar Lara of CONAP for hi s efforts over and above th e call of his office. Lorena Calvo and Carlota Monroy were also important allies in getting throu g h the bureaucratic tangl es associated with starting a field project from scra tch in a remote p a rt of a foreign country. My time in the fi e ld was made much more fun by regular assistants Prud e ncio Tobar Fermin Lima and Don Luis Savala. The Universidad de San Carlo s kindly loaned th e very capable Carla Ramirez as a s ix-month s tud e nt intern. During ne s ting periods Benjamin Gonzalez and Jo se Tobar climbed tr ees that I as a big, clumsy gringo could not. Jen Boyd, Jason Brueck Aaron King Bob Schuyler a nd Josh Vinlove were all crazy enough to volunteer for various period s of tim e, as well. All of the se people deserve much of the credit for the fieldwork's Ill

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successful completion. Dr. David Whitacre kindly provided housing to a number of people who assisted in fieldwork, and he, Mario Jol6n and Haroldo Garcfa just as importantly served as sympathetic ears and apt problem-solvers in helping me to overcome the various obstacles that inevitably arise in a lengthy field project. Dr. Denise Gross similarly helped by teaching me a simple and inexpensive method for making blow-darting equipment, a skill which I am sure the family dog was glad I did not possess in boyhood but which proved essential in the field. Marfa Jose Gonzalez was thoughtful enough to drop what she was doing in order to bring me a freshly road-killed coati, in the process turning what would have been just another senseless animal death on the national park road into a learning experience and scientific contribution. Barbara Booth, Randall Harmon and Dan Flisser not only provided much-needed visits from home, but also took upon themselves the not-so-small task of bringing needed equipment and supplies when I could not leave the field. The occasional postcards and letters that made it through to me from my family, Rosemary, Anne Marie, David, Joan, Jason and Elizabeth Binczik, also helped keep me going. Mae Chisholm, Satish Degala, Jenny Gates, Patricia A. Lewis, Deidre Meiggs, Dr Don A. Samuelson Doris Sartain and Dr. Samuel K. Wasser all provided essential assistance to my efforts in the laboratory. Of special note in this regard is also Dr. Edward F. Orlando, a fellow graduate student at the time who refreshed my memory on the ins and outs of steroid radioimmunoassay, and much more importantly helped keep me sane during some tough times by offering his friendship and collaboration; both were and are most welcome. Dr. Timothy A. Pearce kindly applied his malacological expertise to snail identifications. Last and of course most, my darling wife, Dr. Susan D. Booth-Binczik, not only stood by me through much more than would the typical devoted spouse, but was also the best part of why and how this study was completed. I can never fully repay my debt to her nor even fully express my thanks, but I look forward to trying! I also look forward to finally putting the adjective "professional" alongside the "collaborators" we have long been. IV

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TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .... .. .. . ... ... .. ... . .. .. .... . . . . ... .. . .. .. ...... ... . .... .. .... . .. .. ... .. ... ... ... .. .. iii ABSTRACT ... . . .... .. ... .. .. ...... .... ..... .. ........ .. ... .. .... .. .. ... .. ................ ........... . . .. .. .. ... ........... . vi CHAPTER I BACKGROUND ... .......... .... . .. . . ... .. . .. .... .. .... ..... ........ . . ............... ..... .. . .. ....... ...... ....... 1 2 REPRODUCTIVE SEASONALITY .... ... .... ..... . . ..... ... .. .... .. ... .......... .. .. .... .. . . . .. ..... ... .. .. 4 Introduction ... .. .. ......... ....... .... .. .... ... ...... .. .... ...... ..... .. ... ......... .. ....... .. .. .. .. . .. .... . .. ..... 4 Method s ... .. .. . .. . ... ... .... .............. .... ....... . ..... .. ..... ... ... .. ..... .. ....... ... ... .. .. . ... .... ..... ... 8 Re s ult s .. .. ... ... ... .. .. . ... ... .. .. .. .. . .. .. . ... .. .. .... ... ........ .. ... .. . .. ...... .. .. . ..... .. . . . .. ... .. .. . .. ... 15 Di s cu ss ion .. .. . . ... ... .. .... ..... .... ... .. .. .. .. . .. ......... ... .. . ... . . .. ..... .. ..... .. . .... .... ... . ... ... ... .. 38 3 BIRTH SYNCHRONY ... ....... ... .. ...... ........ ... ... . .. ..... .... .. ... . ...... .... ... ..... .. . . .. ...... .... .. ... 51 Introduction .... . .. .. ...... ... . .. .. ........ . . ...... ... .... .. ..... ... .... ... .. ...... . .. .. ..... .. ...... .. .. .... .. ..... . 51 Method s ... .. . ... ... .... ..... . .. .. ........ ..... ...... ... .... ..... ............. .. .... .. ... ... ...... .. .. ... .... ....... 53 Re s ult s . .. ......... .......... .. ...... .. ... .. . ... . .. .. . .. ..... ..... . .. ... ...... . .. .. .... ... . .... . .. .. . .. . .. .. 56 Di s cu ss ion . .. .... .. . ........... ... .. .. .. ... ..................... .. . .. ........ .. .......... .......... ........ . .. .. 58 4 RUT . . .. ....... ....... .. ..... ... ... .. ...... . ... .. .. .. .... .. .. . .. .. . . .. .. . .. . .. .. ... ... .. .. ... ... .... ... . ... .. ... .. .. ... 64 Introduction ... .... .. ........ . .. .. ......... ............. ................................................................... 64 Methods .......................................................................... .............. ...... ... ................ ....... 67 Result s ....... .... ... .. .. ... .. . . . .. .. .. ... .... .. . .. .. . ... ... .... ....... . .. .. .. ........ ... . ..... .. . . ... . .. ... .. 74 Di s cu ss ion .. .. .... .. . ......... ... .. ... ..... .. . ... .. .... .. ... .. ..... ..... .. ..... .. .... ... ... .. . ......... ...... . ... ..... 81 5 SUMMARY .. ..... .... ... .... . .. .... . . ... ..... .. ... .... .. .. ... . . . .. ...... .. .......... ........................ ... ...... . 96 APPENDIX RAW TESTIS VALUES ... . .. .. ... .. . .. ..... .............................. .. ...... ................. 102 REFERENCES .. .. .. .... .... ... .. ...... . ........... ..... .. ..... . .. .. .... ..... ... . ....... .. .. .. .... .. . . . .. . . .. ... ... . .. 104 BIOGRAPHICAL SKETCH .. . . ..... .. ....... .. ...... ...... ... .. .... .. ... ....... ... . ..... ... .. .. .. .. ..... ... .... .. 120 V

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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 REPRODUCTIVE BIOLOGY OF A TROPICAL PROCYONID, THE WHITE-NOSED COATI By Chair: Louis J. Guillette, Jr. Major Department : Zoology Gerald Allen Binczik May 2006 Some 80 % of the world's mammals re s ide in the tropics but few-and almost no long lived-species there have been s ubjects of reproductive re sea rch. This study contributes detailed information on the reproduction of a l ongli ved procyonid carnivore, the white-nosed coati (Nasua nari ca), in Tika l National Park Guatemala. Whereas mo s t tropical mammal s di s play broad reproductive seaso nality (e.g. producing offspring within a six-month period) or reproduce year-round, the coati exhibits extraordinarily tight timing in reproductive events In Tikal mating took place within about two weeks in the middle of the dry seaso n, births occurred in a comparab l y s hort period at that seaso n's end, and young emerged from ne s t s and began foraging a l ongside adults ea rly in the wet seaso n. When the timing of parturition was examined in more detail, the interquartile range (i.e., middle 50 % ) for females from three soc ial groups spanned on l y five and s ix days in consecutive years, and the mean birthdates in those years differed by on l y s ix day s The male coati has re s ponded to reliable clustering of female receptivity by evolving a rut more akin to that of many ungulate s pecies than to the pattern of any other carnivore species yet examined. YI

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Coati r eprod u ct i o n i s tim e d s uch th a t th e young a r e weane d over a n ex t e nd e d p er iod co incident with th e sea o n of grea t es t food ava il a bilit y Leaf litt e r in ve rt e brate s a nd fruits figur e prominently in the coati di e t but the former a re evidently mo s t important. Notable a mong the se are in sec t s, and in Tik a l es p ec i a lly the sca r a b b ee tl e Enema endymion; adults and lar vae of thi s one spec ie s accounted for 8.6% of all in ve rt e brat es co n s um ed by coati over th e co ur e of thi s tudy. Commun a l ca r e a nd predator swa mpin g were exp l o r ed as a lt e rn a ti ve exp lan a ti on for th e coati's r e markabl e r e produ ct i ve p a tt e rn but th ese h y p o th eses we r e rejected. Exactly how th e coa ti ac hieves s uch tight r e produ c ti ve seaso nality r e main s unknown but a prediction b ase d o n the h ypo th es i s that socia lity plays a ro l e was uph e ld Social c u e exc hanged among a oc i a t e a r e pr es umably u se d b y th e coa ti t o a u g m e nt th e weak e nvironment a l c u e (e.g photoperiod) up o n which easo n a ll y r e produ c in g tropi ca l spec i es mu st otherwise rely VII

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CHAPTER I BACKGROUND Although the white-nosed coati (Nasua narica) i s a wide-ranging, locally abundant and r eadi ly habitu a t ed diurnal ca rni vo re the mo s t detailed st udie s to date have been of a s ingle island population The majority of what is known and believed about coati ecology and reproduction is b ase d upon ex t e n s i ve b e h av ioral observations by Kaufm a nn (1962), Ru sse ll (1979) and most rec e ntly Gompp er ( 1994 ) of a s mall group of animals on Barro Colorado I s land (BCD, Panama. The s peci es i s primarily insectivorous/frugivorous ( Kaufmann 1962), with so me small ve rt e brate s t ake n opport uni s tically. Adult females are hi g hly socia l living with their immature offspring in cohesive band s mo s t of the year (except for a brief nesting period encompassing birth and early lactati o n ), an d adult m a le s are chiefly so litary (Kaufmann, I 962; Booth-Binczik 2001). Ru sse ll ( 198 2; 198 3) r ev i ewed va riou s hypoth eses put forth to explain female sociality, and asse rted that it fun c tion s to prot ec t juveniles from pr e dation mo s t notably by cannibalistic adult m a l es (see also Ru sse ll 1981 ), and ectoparasitism. Gompper ( 1996), however concluded that group living i s a way for female s to increase their foraging success on patchy resources whereas severa l s tudi es at other s ite s have provided evidence that group living in coatis is an anti-predator adaptation (Burger and Gochfeld, I 992; Booth-Binczik, 200 I; Hass and Valenzuela, 2002). The coati ha s r ece i ve d considerable attention for its unusual soc ial system, but it is even more notabl e among tropical mammals for its remarkable d egree of reproductive seaso nality. Kaufmann ( 1962 ) and Ru sse ll ( 1982) addressed the timing of coati reproduction on BCI. The s pecie s di s pl ays a stro ngly seaso nal pattern at this locale, with apparently only one finely timed birth period per year. The proportion of adult females reproducing can vary dramatically from year to year; they a re capable of d e laying their fir s t reproduction (which u s ually occurs at two

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2 years of age) by one or two years, perhap s due to food availability, but generally reproduce every year thereaft e r. Males mature l a ter than female s, and mo s t probably do not reproduce until one or two years after their fir s t opportunity. It is unclear whether reproductive senescence occurs, but Kaufmann ( 1962 ) observed one and Ru sse ll (1982) two older females (estimated to be at lea s t seve n years of age) that did not produce young. Animals have lived to be more than 17 years old in captivity; Poglayen-Neuwall, 1990 A f ew reports (e g., Gilbert, 1973 ; Ha ss, 2002 for Arizona; V a lenzuela and Ceballos, 2000 for Jalisco M exico) s ugg es t that coati reproduction may be patterned s imilarly at other loc a tion s as well, but these h ave not b ee n confirmed by thorough s tudy Moreover, even the abundant beh av ioral/ spa tial eco logical d a ta for BCI fall s hort of satisfying the lack of ba s ic knowledge a b ou t coati reproductive biolo gy Many que s tion s remain: Doe s the portrait described for BCI app ly e l sew h ere in th e s p ec i es' ran ge? Where it i s seaso nal, is thi s l a rgely tropical mammal pursuing a n obligate or facultative (i.e. opportunistic) s trategy? What evo lutionary pressures drive seaso nality and what environmental cues are u se d in timing it ? Thi s s tudy a ddr esses the se que s tion s by extending beyond prior research in four import a nt ways It i s th e first intensive s tudy of reproductive pattern s in any coati population, focusing on animals at a s ite that i s distant from but ecologically similar to BCI. It i s also the first to examine mal e r epro ducti ve biology at any lev e l. A much greater level of detail is pre se nted on certain environmental s tre sses confronting th e coati with an eye toward resolving s pecific i ss ues left ambiguous by pr ev iou s workers. Perhap s most important this re searc h provide s the first information on th e r eprod uctive phy s iology of the s p ec ie s The focus of the s tudy i s the free-ranging coatis in Tikal National Park, Guatemala The Park protect s a pproximately 600 km 2 of tropical moi s t forest in the seaso nally dry "Mayan" forest of northea s tern P e t en, and constitutes the centerpiece of Central America's large s t r e m a ining tract of lowland rainfor es t ( Nation s et al., 1988 ). Unlike BCI (Willis, 1974 ; Gl a nz, 1982; Robin so n, 1999 ) where eco lo g ical conditions could be considered so mewhat artificial (Willis, 1974 ;

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3 Eisenberg et al., 1979 ; Terborgh and Winter 1980) Tikal retains a full complement of large predatory species. The disagreement among studies regarding the adaptive value of coati group living provide s an example of the risks of extrapolating from data obtained on BCI to the species as a whole. Studies at si tes s uch as Tikal s hould be more u se ful for identifying selective pres s ures important in coati evolution.

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CHAPTER2 REPRODUCTIVE SEASONALITY Introduction Mamm a l s di s pl ay two ba s ic pattern s in th e timing of their reproducti o n ( Bron so n 1989 ): opportunism, in which th ey reproduce as often as conditions permit, and obligate seaso n a lity, in which one or mor e pr e dictable environmental factors in combination with other lif e hi s tory aspects compel them to follow a seaso nal r e produ c ti ve sc h e dule. E vo lutionaril y, th ese are better thought of as t e nd e n cies than rigid choices, and a s in g l e species may e mploy both s trat egies under different conditions (e.g., the purple-fac e d langur Pr esby ti s senex; Rudran 197 3) Oblig a t e seaso nality appears to be the s trat egy adopted by mo s t long-liv e d mammal s (i.e., tho se with life spa n s of more than one year) inhabiting seaso nal environments, especially s pecies with a s ub s tanti a l in ves tm e nt p er offspring, s p ecia li ze d diet or extreme seaso nal s urvi va l mechani s m s uch as mi gra tion or hibernation ( Bron so n 1989 ). Ovarian function in s uch s pecie s i s regulated by the appearance of reliable proximate cues-especially photoperiodic changes-thereby setting a schedule for sex ual receptivity, ovulation and/or embryonic development. The mo s t e nvironmentally se n s itiv e pha se of the s pecie s' r e productive pattern i s timed to coincide with the mo s t favorable conditions for offspring s urvival ( Lanca s t e r and Lee 1965; Sadl e ir 1969 ). Ultimate factors po s tulated to account for mammalian reproducti ve seaso n a lity (summarized in S a dl ei r 1969 ; Bronson, 1989 ; Di Bitetti a nd Jan so n 2000) include food availability (both in t e rm s of energy and essential nutrient s), rainfall, ambient t e mperature, predation pre ss ure and competition. Of th ese, food ava ilability (most notably energy intake ) is widely belie ve d to be the s trong es t determinant of seaso nality; other factors may modify a pattern but are considered unlikely to override it ( Bron so n a nd Heideman I 994). 4

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5 There is an obvious logic to seasonal reproductive patterns among mammals at temperate latitudes, where annual fluctuations in insolation profoundly affect temperature and the availability of free water, factors critical at the base of essentially all food chains. But strong seasonal weather patterns, particularly in rainfall, can also promote reproductive seasonality in the tropics (Bronson 1985) Tropical rainfall patterns have pronounced effects on the abundance of all manner of terrestrial and arboreal food items, and climatic fluctuations could conceivably also affect competition, predation and/or parasitism pressures on a tropical species. Unfortunately, despite the fact that some 80 % of all mammalian species reside in the tropics, relatively few species and very few locations in the lower latitudes have thus far been examined (O'Brien, 1993; Bronson and Heideman, 1994; Dubost et al., 2005). In this respect, the lowlands of the Panama Canal Zone may have received more attention than any other tropical site. In his review of the literature Fleming (1973) found that half of the species studied at this locality (23 of 45) were known to be seasonal breeders, with a strong tendency toward birth or weaning occurring at the beginning of the wet season. This pattern is exemplified by the region's best-studied carnivore, the white-nosed coati (Nasua narica). Observations by Kaufmann (l 962) and Russell (1979; 1982) indicate that coati reproduction on Barro Colorado Island (BCI), Panama, is strongly seasonal: mating activity there appears to take place early in the four-month dry season, litters are born late in that same season, and young emerge from the nest and are gradually weaned beginning early in the eight-month wet season. Scattered observations suggest reproductive events may also be seasonal at other sites (e.g., southern Arizona: Gilbert, 1973; Hass and Roback, 2000; Costa Rica: Saenz, 1994) Fruit and leaf litter invertebrates are the principal foods of coatis on BCI (Kaufmann, 1962; Russell, 1982; Gompper, 1996) and elsewhere (Delibes et al., 1989; Saenz, 1994). Smythe (1970) examined fruit-fall on BCI in correlation with Kaufmann's (1962) data on coati life history stages and concluded that the period encompassing parturition and first emergence of young from their nests matches the time of greatest fruit supply. Russell ( 1982) compared coati

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6 int ake ra t es o f f ruit an d a n i m a l s, a nd c o n c lud e d th a t r e p ro du c ti o n i s tim e d t o a ll ow j u ve n i l es t o b eg in fo ra g in g a t th e o n e t o f a l o n gl as tin g p ea k in th e ava il a bili ty o f in ve rt e b ra t e pr ey; h e b e li eve d the c on c urr e nt ava il a bility of a m a jor fruit c rop w as "perhap s fortuitou s ( p. 4 2 8 ). Thj s di sc r e pan cy t e rn s fr o m th e fac t th a t o n BCI th e seaso n al pe ak in s i ze a nd a bundan ce of for es t fl oo r art h ro pod s (a t th e o n se t of th e we t seaso n ; L ev in gs and Wind o r 1 982) ove rl a p s s ub s t a nti a ll y w ith o n e of t wo an nu a l p eaks in f ruit ava il a bilit y (Fos t e r 1 982 b ). F ruit ava il a bilit y in n eo t ro pi ca l fo r e s t s of t e n p eaks a t th e o n se t o f th e we t seaso n (va n S c h a ik et al., 1 993; S akai, 200 I ). A s arthrop o d a bund a n ce in tropi ca l fo r es t s c omm o nl y va ri es po s iti ve l y w ith m o i s ture l eve l s ( L ev in gs a n d Win d o r 1 984; Bur ges e t a l. 1 999), s u c h ove rl a p i s li ke l y w id e pr ea d Tik a l N a ti o n a l P ar k Gu a t e m a l a, i s s imil a r t o B C I in th a t it i s c h arac t e ri ze d b y fai rly uni fo rm t e mp era tur es a nd s t ro n g l y seaso n a l r a in fal l (F i g 21 ); th ere i s a mar k ed fo ur m o nth dry seaso n fr o m Janu a ry throu g h April a nd a s i xm o nth we t seaso n fr o m Jun e th ro u g h N ove mb e r w ith M ay and D ece mb e r b e in g tran s iti o n a l p e riod s In co ntr as t t o BCI h o w eve r th e for es t s of n o rth e rn Gu a t e m a l a are b e li eve d t o h ave b ee n i gn i fica ntl y a lt e r e d b y th e a n c i e nt M aya ( Lund e ll 19 3 7 ; Pul es t o n 1 982) w h o e h o rti c ultur a l p rac ti ces lik e ly favo r e d s p ec i es w hi c h produ ce pl e ntiful nutriti o u fru j t a nd t e nd t o d o so a t w h a t wo uld o th e r w i se b e tim es of scarc it y. Fo r exa mpl e, th e hi g hl y nutritiou s Br os imum a l icas t r um ( ram on, a. k. a. br ea dnut ), a tr ee w hi c h ha s b ee n r e port e d to und e r g o thr ee h eav y eve nl y-s p ace d fruit se t s p e r y ear ( F e bruar yM arc h June Jul y a nd O c t o b e r -Nove mb e r ; Pul es t o n 1 968; in C oe lh o e t a l ., 1 9 76 ), i s unu s u al l y d e n se throu g h o ut th e r eg i o n ( Lund e ll 1 93 7 ; Pul es t o n 1 982). Gi ve n th e a b ove, it was an ti c ip a t e d th a t coa ti r e produ c ti o n in Tik a l wo uld be hi g hly seaso n a l as it a pp ears t o be e l se wh e r e, but th a t M aya n e ff o rt s th e r e mi g ht h ave r es ult e d in s uffi c i e nt temp ora l se p ara ti o n b e t wee n pe ak s in fruit an d in ve rt e brat e a bundan ce t o aj d in d e t e rrrunin g th e re l a ti ve imp o rt a n ce o f th ese fo o d s t o th e timin g o f coa ti r e produ ctio n Eve n i f p eak ove rl a p was fo und t o occ ur in Tik a l it was b e li eve d th a t a m o r e ri goro u ex pl o r a t io n of

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,,-._ 8 8 ..._., 0 ...... cd ...... 0. 0
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8 coati foraging habit s accompanied by consideration of nutritional matter s might clarify this issue The purpose of the pre se nt study was therefore twofold : 1. Coati reproductive phenological events were monitored year-round at Tikal to document-and provide greater detail on-the species' reproductive seasonality at this new tropical forest s ite 2. The abundance and quality of potential coati food items and also coati foraging behavior and body condition were monitored year-round to clarify the r e lation s hip between the species' reproductive pattern and food availability. Methods Free-ranging white-nosed coatis were s tudi e d from June 1994 into November 1996 over an area of approximately 20 km 2 at the center of Tikal National Park ( 17 N, 89 W ) The Park protects nearly 600 km 2 of forest that has at various times been identified as s ubtropical moist or tropical semi-deciduous (Schulze and Whitacre 1999; based on the classification schemes of Holdridge et al., 1971, and Pennington and Sarukhan, 1968 respectively), tropical dry (Walker and Cant, 1977 ; ba sed on Holdridge, 1957), and quasi-rainfore s t (Lundell, 1937 ). Total annual rainfall averages 1285 80 mm (based on the eight complete years of data between 1984 and 1998 available from the Instituto de Sismologfa Vulcanologfa, Meteorologfa e Hidrologfa, Guatemala City, Guatemala) Located in the "Mayan" (i.e., ancient Maya-modified ; J .F. Eisenberg per s. comm.) forest of northea s tern Peten Tikal constitutes the centerpiece of Central America's large s t remaining tract of lowland rainforest and retains a full complement of the region's wildlife species (Nations et al., 1988). Rainfall in the park during the study was recorded at a uniform time daily via a government-operated weather s tation From these data monthly total s were calculated for comparison to various phenological data. Fifty-five adult female coatis resident to four bands (females of thi s s pecie s live in groups with their maturing young except to nest, whereas male s are largely so litary; Kaufmann 1962)

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9 were utilized in this study. Animals were initially captured by live-trap or (more often) blowgun and chemically immobilized by intramuscular injection of approximately 7 mg/kg Telazol (Fort Dodge Laboratories Inc., Fort Dodge, IA). Anesthetized animals were tattooed and eartagged for identification, weighed, visually examined to determine general physical condition and measured as described below. Forty-three of the coatis were additionally fitted with 90 g motion-sensitive radiocollars (Advanced Telemetry Systems, Isanti, MN) to enable subsequent location and recapture, and to confirm death if such occurred. Individual females were recaptured by blowgun (never more often than monthly) for resampling; the average number of immobilizations per female was 2.6 0.2. All animal handling procedures were conducted as per protocol #4084 approved by the University of Florida's Institutional Animal Care and Use Committee. In order to monitor reproductive state, size indices for the vulva and right anteriormost teat were obtained during each female's immobilization. For each body part, the longest dimension (L), the widest perpendicular dimension (W) and the highest dimension above the surrounding body surface (H) were measured to the nearest 0.1 mm via calipers and then combined in the formula V = L x W x H to produce an approximation of volume. One person was responsible for taking these measurements throughout the study. Indications of pregnancy and lactation were also noted. (Originally serum and fecal reproductive steroids were to be monitored as well, but samples obtained for this purpose were rendered useless by a catastrophic freezer failure after fieldwork was completed and before radioimmunoassays could be conducted.) As a measure of body condition, an index of each coati's body fat level was also determined at the time of immobilization. Following Hossler et al. ( 1994), a fold of the animal's skin (i.e. excluding muscle) was pinched at the back of each rear leg midway between knee and hip, and calipers were used to measure the thickness of this fold to the nearest 0.1 mm. Measurements for the left and right thighs were averaged to produce the index reported for that coati/immobilization. One person took all such measurements throughout the study.

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JO The animals in thr ee coati bands were habituated to the close presence of inve s tigator s, who s imply visited the band s frequently over seve ral weeks and briefly baited the coatis at the beginning of each encounter until the animals allowed them se lves to be accompanied (without additional feeding) for severa l hour s thereafter. By the end of the habituation period it was po ss ible to follow animals so closely that at time s inve s tigator s had to be careful not to kick or step on them and sometimes th e coatis even had to be gently s hoo e d a s hort di s tance away to allow inve s tigator s s uffi c ient room to proc ess immobilized a nim a l s during captures. Thereafter the r eprod uctive activities of habituated females were monitored ad libitum (Altmann, 1974 ) one to three tim es per week (as often as th e ir band s were visited) during the p er iod of det a il e d b e h aviora l observations (see below ) or as c l ose to daily as po ssi bl e during p e riod s of particular int e re s t. Data on six reproductive phenom e na were recorded Copulation was e ith e r directly observed or pre s um ed b ased on the pre se nce of mating wounds (see Re s ult s for de scri ption of latter ). Pregnancy was generally identified by the midpoint of gestation, when an increase in a female's girth b eca me visually apparent. Nesting was defined as beginning when a female d e parted from it s band prior to giving birth and ending when the infants first accompanied the female down from the ne st. Parturition was determined to have occurred when a female s howed a s udden pronounced reduction in girth followed by continued ne s ting behavior and wa s ultimately confirmed by observation of young s till in the ne s t or s hortly after their emergence from the ne s t. Reaggregation was operationally defined as the rejoining of a postpartum female and its young with at l eas t three other s uch females and their young. Nursing was ei ther directly observed or inferred from evidence of lactation noted during a female's immobilization During ne sti ng 2 0 ne s t trees were climbed and ne s t s examined to ve rify the presence and count the number of young. Ages at which young were examined varied from approximately one

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11 to five weeks afte r birth, depending on when ne sts were initially locat ed and how soo n thereafter op portunitie s occurred to exa mine the ne s ts without the females nearby Systematic observations of female coati foraging b e havior were conducted from August 1995 through September 1996. Ob serva tion sess ion s were sc heduled two to three times per week, and in each case began as soo n after fir s t light as th e target animals could be located ( t yp ic a lly by 08:30) and continued for severa l (typically four) hour s ther eafter All-day (up to I 0 hr ) observation sess ion s were conducted once each month to confirm that activity p a ttern s did not change suc h that mornings were no longer appropriate for monitoring normal foraging behavior. In eac h sess ion, one 5-minute block of focal animal sa mplin g (A ltmann 1974 ) was conducted eac h qu a rter hour, rotating through focal animals opportunistically se lect ed for that sess ion ; during the n es ting period eac h sess ion in s tead focused on a s ingl e female ( r e ducing sa mple s ize s during thi s period ). In the se lection of target animals for sys t e matic beha v ioral observations, priority was placed on di s tributing observation effort aero s f e m a les without respect to their band membership, suc h that no individual coati se rved as a focal a nim a l in more than one block per hour (except in the ne s ting period), nor in more than one sess ion per week. During eac h sam pling block the amounts of time s pent by the focal animal foraging in under and away from potentially relevant fruiting trees were recorded. Also recorded were the type and number of food item s consumed in each of th ese three areas, as well as the time s pent co n s uming the item s; foraging time and time of food consumption were mutually exclusive categories. The identitie s of animal prey were determined to the lowe st taxonomic level s possible, and fruits eaten were identified to s pecies As ba ses for calculating monthly rates of foraging s ucce ss, the three foraging areas were u se d thu s: The l eaf litter invertebrate zone was the combination of under and away from fruiting tree s The fruit zone was the combination of in and und e r fruiting tr ees. A given female's monthly foraging s ucce ss rates were then calculated as both number of item s consumed per minut e foraging a nd number of seco nd s s pent consuming the items per minute foraging, u si ng

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1 2 m o nthl y t o t a l s fo r eac h zo n e. T o e limin a t e ev id e nt o utli e r s ca u se d b y und e r s amplin g o f s p ec ifi c indi v idu a l s in s p ec i fic m o nth s, fe m a l es with few e r th a n 3 00 seco nd s s p e nt fo ra g in g in a l eaf litt e r in ve rt e brat e zo n e o r 2 0 seco nd s in a fruit zone in a g i ve n m o nth w e r e not includ e d in an a ly ses; th e m o nthly ra t es fo r th e r e m a inin g female s wer e ave rag e d t o produ ce th e r e port e d va lu es. L eaf litt e r a nd assoc i a t e d in ve rt e brat es w e r e sa mpl e d o n a ppro x im a t e l y th e 5 th 1 5 th a nd 25 th of eac h m o nth fro m Se pt e mb e r 19 9 5 throu g h S e pt e mb e r 1 996. On eac h co ll ec ti o n d a t e 10 sa mpl es we r e o bt a in e d Eac h sa mpl e was co ll ec t e d b y pl ac in g a b o tt o ml ess tub th e a r ea of w hi c h was I m 2 o n th e fo r es t fl oo r a nd qui c kl y s co o pin g th e litt e r a nd i n ve rt e b ra t es th e r e in int o a b ag; th e so il thu s cl ea r e d was th e n du g t o a d e pth of thr ee t o four in c h es (as th e s ub s t ra t e a ll o w e d ) a nd a n y a dditi o n a l a nim a l s fo und th e r e b y w e r e a dd e d t o th e b ag. Exac t sa mpl e l oca ti o n s a nd tim es we r e d e t e rmin e d b y acco mp a n y in g a fora g in g b a nd of coa ti s fo r t wo t o fo ur m o rnin g h o ur s a nd pl ac in g th e tub a t th e fr o nt e d ge o f th e band a t rand o m int e r va l s (s kippin g an y pr ese l ec t e d tim es a t w hi c h th e an im a l s we r e n o t forag in g) Eac h sa m p l e b ag was we i g h e d fr es h a nd th e n h an d -s ift e d t o h arves t v i s ibl e in ve rt e brat es . Anim a l s thu s o bt a in e d we r e id e ntifi e d to th e low es t p rac ti ca l t axo n o mi c l eve l a nd we i g h e d to th e n eares t 0 1 g; a nim a l s indi v idu a ll y we i g hin g l ess th a n 0 1 g we r e g roup e d by t y p e a nd th e t o t a l we i g ht fo r th e g roup was u se d t o ca lculate a n avera ge we i g ht p e r indi v idu a l. V o u c h e r s p ec im e n s we r e occas i o n a ll y p r ese r ve d t o a id s p ec i es id e ntifi ca ti o n s, but o th e r w i se in ve rt e b ra t es we r e b agge d b y sa mpl e d a t e a nd th e n fr oze n in liquid nitro ge n a nd s t o r e d in an ult raco ld fr eeze r fo r s ub se qu e nt nutriti o n a l a n a l yses (see b e l o w ). Fin a ll y, eac h sa mpl e's l eaf litt e r w as dri e d i n th e s un fo r a minimum o f t wo d ays ( or m o r e, as w ea th e r di c t a t e d ) and aga in we i g h e d to o bt ai n dr y litt e r m ass a nd litt e r m o i s tur e co nt e nt. M o nthly m e an s w e r e ca lcul a t e d fo r t o t a l in ve rt e brat e m ass, litt e r m ass an d litt e r m ois tur e co nt e nt. Th e indi v idu a l co ntribut io n s o f vario u s in ve rt e b ra t e c l asses t o m o nthl y t o t a l s we r e exa min e d by ca lcul a tin g th e ir m o nthl y numb e r s a nd m asses o n a p e r ce nt age b as i s.

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13 Fruiting tr ee phenology was monitored from June 1995 through September 1996 Ten 10 m x 50 m plot s were es tabli s hed at random interval s along I km of (and also at random directions and distance s up to 50 m from) each of three forest paths traversing the entire home range of one coati band as well as parts of the ranges of three other bands In each plot, all tree s measuring at l eas t IO cm diameter a t breast height at the onset of data collection were tagged and identified to s peci es. Every month eac h plot was randomly assigned to a group of 10 which was th e n s urv eye d on approximately th e 5 th I 5 th or 25 th of th a t month During s urv eys, tagged plants were checked for th e pr e s e nc e and percentage of immature and ripe fruit and when fruit was present in a tree it was quantified v ia th e visual count m et hod (Chapman et al., 1992 ). Sampl es of ripe fruits were also collected t o ai d spec ie s id e ntification s and frozen/ s tored as de scribed for inv e rt e brate s to provide mat e rial for later nutrition a l a naly ses (see below ). One person was re s pon s ible for d e t ermi ning fruit counts and perc e nt ripe fruit in almost all month s; a seco nd per so n trained under a nd performed calibration run s with the fir s t person repeatedly throughout the s tudy befor e r ep l aci ng th e first per so n in the final month Using th e above methodology, data were obtained on many more tree spec i es than appeared in the coati diet. Only those s pecie s which were ultimately see n being eaten by coatis and/or appeared in th e ir sca t on at lea s t 15 separate dates were selected for analysis and pre se ntation in thi s paper. The p e rcentage of tree s with fruit and the mean number of fruits and ripe fruits per tr ee were calculated on a monthly ba s i s for each of the se species After field work was completed, proximate nutritional analyses were conducted on monthly (i.e. mix ed) l eaf litter invertebrate collections and also on individual in ve rtebrate and fruit s pecie s deemed of particular relevance to th e coati diet (as de sc ribed above). Each sa mple, consisting of e ith e r whole in verte brates or the edible portions of fruits, was first thawed weighed, dried for two day s at 60 C, allowed to equilibrate to room temperature overnight before being weighed again, th en finely ground and homo ge niz e d by u se of a Wiley Mini-Mill equipped with a 20-mesh Monet scree n ( both Thoma s Scientific, Swede s boro NJ ) prior to additional processing.

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14 Crude fat and e n ergy content were d e t e rmin e d in nutrition laboratori es of th e University of Florida's Animal Science D e partment following pro ce dur es outlined in H e lri c h (J 990). To obtain crude fat, sa mpl es were weighed dri e d 3 hr at 102 C equilibrated to room temperature under de s icc a ti o n and then ex tracted four time s in e thyl e ther u s ing a Soxhlet a ppar a tu s Extracted sa mpl es were s ub seq u e ntly dri e d 12 hr a t I 02 C before being e quilibrat e d und e r d es icc a ti o n and we i g h ed o n ce m o r e; th e a m o unt of fat was calculated as th e diff ere n ce in ma ss b e tw ee n prea nd post-extraction sa mpl es Energy co nt e nt was obtained by bomb ca l o rim e try u s in g a 1 26 1 I so p ero l Calorimeter ( Parr In s trum e nt Co ., Moline, lL ) after sa mpl es h a d b ee n weighed int o c ru cib l es, dried a t 65 C for 24 hr e quilibrat e d under de s icc at ion a nd weighed agai n Crude protein, as h-fr ee n e utral d ete r ge nt fiber (NDFat) and ash co nt e nt were d e t e rmined in the Forage Evaluation Support Laborat ory o f th e University of Florid a's Agronomy D e partm e nt. Samples we r e fir s t weighed, dri e d for 15 hr at 105 C and weighed again, and then organic matt e r was determined by ashing for a t l eas t 4 hr a t 500 C. Tot a l nitrog e n ( N ), and from it c rud e protein (as N x 6 25), was o bt a in e d by a modific a tion of the s tandard Kj e ld a hl procedure ( H e lrich 1990 ) Samples were di ges t e d u s in g a m o dific a tion of the aluminum blo c k dige s tion proc e dur e by G a llah er et al (J 975); sa mpl e weight was 0. 2 5 g, the catalyst u se d was 1.5 g of 9: I K 2 SO 4 :C uSO 4 and di ges tion was conducted for at l eas t 4 hr at 375 C u si ng 6 ml of H 2 SO 4 and 2 ml H 2 O 2 Di ges t a t e nitro ge n was th e n d e t er min e d by se miautomated colorimetry ( Hambleton 1977 ) v i a a T ec hni co n Autoanalyzer ( T ec hnic o n In s trum e nt s Corp. Tarrytown NY ). N e utral detergent fib e r (NDF) was d e t er min e d by th e pro ce dur e of Golding et a l. ( I 985), consisting of boiling 1 g of sa mpl e in a n e utral d e terg e nt so lution for I hr filtering, extracting with acetone and th e n dryin g; NDF af was obtained by correcting NDF for the amount of ash in th e sa mple The moi s tur e co nt e nt of an initi a l sa mple was calculated by combining the re s ult s of the r e l eva nt dryin g steps o utlin e d a bo ve. Crude prot e in crude fat, NDFaf as h a nd e n ergy content were calculated o n a dry m a tt er b as i s ( It mu s t b e not e d th a t the invert e brat e a nd fruit sa mple s were s ubj ec t e d t o th e same s t orage fre eze r failure as were frozen se rum and fecal sa mpl es,

PAGE 22

15 a lthou g h unlik e th e l a tt e r s ampl es they a pp ea r e d to t a k e littl e or no harm fr o m it. Thi s topic i s addr esse d furth e r in th e Di sc u ss i o n. ) Sok a l a nd R o hlf (1981 ) guided a ll s t a ti s tic a l e ffort s, and SPSS 8 0 ( SPSS Inc ., Chicago IL ) a id e d comput a tion s Corr e l a tion a l an a ly ses w e r e condu c t e d to examin e th e r e lation s hips b e t wee n e n v ironm e nt a l v ari a bl es r es our ce ava il a bility a nd foraging b e h av ior. P e ar s on co rr e l a tion s (r) we r e t es t e d w h e r e sca tt e rpl o t s o f th e d a t a a pp e ar e d co n s i s t e nt with bi va riat e n o rm a lit y, a nd Sp ea rm a n rank co rr e lati o n s ( p ) w e r e in s t ea d t es t e d w h e r e thi s ass umption a pp ea r e d to b e v i o l a t e d o r wh e r e s ampl es w e r e d ee m e d t o o s mall for prop e r vi s u a l eva lu a tion B eca u se multipl e co mp a ri so n s we r e in vo l ve d a nd th e r e a r e num e rou s ar gum e nt s aga in s t the more e l a b ora t e m e th o d s th a t a r e o ft e n e mpl oye d t o a dju s t for s u c h co mpari so n s ( M o r a n 2 00 3), a co n se r va ti ve P a ~ 0 0 I was a d o pt e d as th e l eve l o f s i g nifi ca n ce Results Ordin a rily eac h f e m a l e und e rw e nt o nl y o n e co mpl e t e r e produ c ti ve cy cl e (i e., s ucceeding a t l eas t t o th e p o int o f r e j o inin g a b a nd w ith r ece ntly b o rn yo ung in t o w ) eac h y e ar but rar e ly a f e m a l e und e r we nt a seco nd c ycl e if pr eg n a nc y, n es tin g o r e arl y e m e r ge nc e was un s ucc ess ful. Accordin g l y a nd unl ess o th e rwi se indi c at e d th e followin g dat a pertain only to fem a l es' lone/frr s t ye a rl y cycl es P a rt o r a ll o f 11 co pul a t o ry ev e nt s w e r e ob se r ve d ; thr e e of th ese ( in t w o co a ti band s) o c c urr e d fr o m 1 3 t o 1 6 F e bru a r y 1995 a nd e i g ht ( in four band s) fr o m 14 to 2 8 F e bruary 1996 An o th e r 40 fe m a l es ( in fo ur b a nd s) w e r e pr es um e d t o h ave co pul a t e d from 1 3 to 2 7 F e bruary 1996 b as ed o n th e a pp ea ran ce o f fr es h matin g w o und s (see b e low ). In ea ch o f th e thr ee c o pul a t o ry eve nt s ob se rv e d in e ntir e ty th e femal e initiat e d mating by l eav in g it s b a nd fora g in g on th e gro und appro ac hin g on e of the m a l es p e rch e d in the tr e e canopy a b ove the fora g in g b a nd (see Bo o th-Bin cz ik e t al. 2 004 for a det a il e d de s cripti o n of the coati m a tin g sys t e m in Tik a l ) a nd s tanding be s id e th e m a l e with hindqu a rt e r s ori e nt e d toward the m a le

PAGE 23

16 and tail bent upward and to the side. The male briefly sniffed at and then mounted the female, clasped its forelegs around the female's midbody and presumably intrornitted (intrornission could not be visually confirmed). In all observed copulatory events, coitus included bouts of rapid, quivery thrusting alternating with bouts of apparent stillness by the male, accompanied throughout by soft grunting or panting. It often appeared as if the female was attempting to leave during the longer moments of copulatory stillness but was held fast by the male. Typically the female ultimately broke free from the grip of the male s claws during such a bout-leaving long, deep parallel scratches on the sides of the female's body in the process-then turned on the male with loud squealing vocalizations and feinted or actual bites and paw swipes (events occurred too rapidly to confirm the extent of phy s ical contact) before fleeing down or even falling from the tree and racing back to its band. On one occasion the female was instead simply released by the male, walked away and then lay down and rested on the tree limb about a meter from where the male remained perched. Complete copulations lasted 16 19 and 48 minutes from intrornission until separation, although it should be noted that the first of these was concluded by the male in coitus being attacked by another male (Booth-Binczik e t al 2004) The eight copulations already underway when first observed continued for 2-29 minutes thereafter. Eleven pregnant females (from two bands) were confirmed to have established nests in 1995, and 28 (from four bands) in I 996. In 1995, the first of these females that was observed to depart its band to begin nesting did so on 12 April and the last did so on 24 April. In 1996 the onset of nesting among females under observation ranged from 12 April to 30 April. In almost every case a nest was occupied by a solitary female, but on three occasions it appeared that pairs of females shared a nest at least temporarily Nests were usually situated in large, living trees, either in their crotches or in tangles of lianas hanging free from or lying against their trunks, at a measured height of 9.8-30.2 m above the ground. They were constructed primarily of interwoven slender, leafy branches and vines bitten off of living plants. Nests varied in size and shape ; most often they were approximately 0 5-0.7 m-diameter hollow spheres with

PAGE 24

17 one or two entrances just lar ge enough to accommodate a female, but occasionally they were much more simply constructed open bowl s /platform s up to about 1.5 min diameter. In any event the nest cavities/floors were lined with approximately 5-20 cm-deep carpets of s mall loose leaves, tiny branches and bromeliad tuft s into which the infant s burrowed Females often s t ayed out of s ight in th e ir ne s t s for a few to severa l day s s urrounding parturition, making pr ecise dates of birth se ldom id e ntifiabl e and in turn lik e ly r es ulting in an overestimate of birth period duration. B ear ing that in mind the ea rli es t a nd l a te s t that parturition could have occurred among nine n es ting females (from two bands ) in 1995 were 16 April and 29 April, r es pectively, and 23 females (fro m two band s) gave birth in 1996 from 22 April to 9 May D es pite the fact that a s ub s tanti a l effort was mad e to pinpoint th e timin g of r eprod uctive events, copulation and parturition could both b e narrowed down to re aso n ab ly ti g ht s pan s of time for only one female ; it gave birth 71 to 74 day s after mating. For 18 litter s exa mined while s till in the ne s t average litter s ize was 4.0 0 .3. Late in the ne s ting period it was common for a female to mov e its young from one ne s t to another, but the infant s were not co n s ider e d to have e mer ged (a nd the female to have concluded ne s ting) until they followed their dam down to the ground and began foraging; thereafter the female was rarely see n on foraging excursions without its young alongside. Eight females (from two bands) brought their young down from the n es t 27 May to 4 June 1995, a nd 15 (from four band s) did so from 23 May to 19 Jun e 1996. The pro cess of r eagg regration beg a n so soo n after emergence that it was po ssi ble on o nly three occasions to determine with certainty how many young individual females emerged with; the se females (the n ests of which had not been examined) brought down four, five and s ix young. Complete band reintegration was in some in s tance s a lengthy proce ss even though females with infant s rea ggrega t ed into s mall groups rapidly after ne s ting The earliest and late s t points at which any of 14 females (from two band s) reaggregat ed in 1995 were 5 June and 29 June respecti ve ly a nd 20 females ( from two band s) reaggregated from 3 I May to I 9 June 1996.

PAGE 25

18 Nursing was almost never observed, presumably because it most often occurred in various tree canopy roosts used by the coatis for taking brief siestas during the day and sleeping at night. Incidences of nursing on the ground (in brush piles) were seen on 4 August 1995 and 27 July 1996. On 13 September 1996 a female was observed evading attempts by an infant to suckle, and twice on 27 September 1996 (in a single band) infants were observed investigating but not suckling from females' teats, suggesting that nursing concluded in the middle or last half of this month. Three females (in two bands) in 1995 and one in 1996 underwent interrupted reproductive cycles followed by second, successful cycles; one more female in 1995 was believed to be in the midst of a second cycle when initially encountered, and another female in 1995 died while nesting in a second cycle. It was never possible to identify the specific cause(s) of reproductive failure, but information on the point at which it was evident may be instructive. Females returned to their bands (presumably soon) after reproductive failure, and dates on which this phenomenon was observed were 30 April 1995 (i.e., at the end of the observed parturition period) for three females, 23 May 1996 (late in the nesting period), and on or shortly after 5 June 1995 (soon after reaggregating with several other females; the exact date could not be identified because it quickly became unclear which young belonged to which females). Although much less information was obtained on second cycles, they appeared to proceed similarly to lone/first cycles. Late mating was not observed. Pregnant females departed their bands to nest from 30 July to 18 August 1995 and by 7 August 1996 Parturition could be narrowly attributed for only one female, on or shortly before 12 August 1996; this animal's litter contained four young when it was examined while still in the nest on 5 September. Females concluded nesting and rejoined their bands from 3 September to 6 October 1995 and by 20 September I 996. The 1996 female brought to its band all four offspring that had been found in the nest; three other second-cycling females brought one, one and two young to their bands.

PAGE 26

19 Nursing by females undergoing second cycles was observed on 13 November 1995 and 24 September and 8 November 1996. Reproductive morphometric changes exhibited by females throughout the study (Fig. 2-2) were revealing of physiological events underlying the coati reproductive cycle despite the unfortunate lack of hormonal data (see Methods). Sudden, pronounced vulval swelling presumably an estrogenic effect-was observed in immobilized females from 7 February to 19 February, i.e ., beginning shortly before the mating period and ending about midway through that period; a much smaller secondary increase in vulva size occurred in late March to early April, within a couple of weeks before parturition and roughly coincident with the beginning of a prolonged increase in teat size. Teat size-presumably reflecting estrogen, progesterone and prolactin levels in tum-rose fairly rapidly from March through the parturition period to a peak in late May to early June, then declined more slowly until it again reached baseline around the end of September, about the same time that lactation/nursing apparently concluded. (Note: The greatest teat size observed in the study actually occurred on 5 September but this data point was unique in that it belonged to a female that was in the midst of a s econd reproductive cycle and therefore out of step with its cohorts.) The amount of leaf litter varied seasonally in strong positive correlation to rainfall (r[I 11 = 0.81, P = 0.001 ), as did the overall mass of litter invertebrates (Table 2-1 ), falling from highs at the onset of sample collection in September 1995 to lows in February and March 1996 before rising again to moderately elevated levels that essentially held steady from June 1996 until the conclusion of sample collection in September 1996 (Fig. 2-3) Leaf litter moisture content (Fig. 2-3) varied less from month to month, and although it too resembled the rainfall pattern in some ways (e g. rising gradually from a low reached in March 1996), the correlation between these was not significant (r 1111 = 0.41, P = 0.17). Rainfall over the course of sample collection (Fig 23) resembled the typical year (Fig. 2-1) except that rains were somewhat heavier than usual in the middle of the 1995 wet season and unusually light in the middle of the 1996 wet season

PAGE 27

20 Dry Season Wet Season 5 ,-..._ M 8 4 Vulva 8 M 3 0 >< ..._., 2 Q) 8 agJ ;l 1 0 > 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec ,-..._ 9 0 M 0 8 0 Teat 8 0 0 M 6 0 8 0 0 0 00% 0 >< ..._., 0 0 Q) 3 00 00 8 (]) ;l 0 0 0 > 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Date Figure 2-2 Annual vulva and teat size profiles exhibited by adult female white-nosed coatis in Tikal National Park Guatemala, July 1994 through October 1996. Mating period (13 Feb 28 Feb) indicated by lightly shaded background and period of parturition (16 Apr9 May ) mor e darkly shaded. Based on measurements obtain e d during 139 immobilizations of 55 animals

PAGE 28

300 ,_ 200 100 '-" N" 0 4 3 2 0 300 200 on '-" .d) 100 0 100 75 '-" 5 50 i:::: 0 U 25 0 21 Wet Season Dry Season Wet Season Rainfall Litter Invertebrates Dry Litter Litter Moisture Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Month Figure 2-3 Monthly total rainfall and mean( SEM) leaf litter characteristics in Tikal National Park Guatemala September 1995 through September 1996 Thirty l-m 2 quadrats sampled each month.

PAGE 29

22 Table 21. Correlation a l s tati s tic s for relation s hip s b e tw ee n monthl y l eaf litt e r in ve rtebrate data and rainfall dry litter weight and litter moi s ture content in Tikal National Park Guatemala. Thirteen con sec utiv e month s compared except wh e re otherwise indi ca ted ; s ignificant finding s indicated in bold In vertebrate s Rainfall Litt er W e ight Litter Moisture Total Mass r = 0.91, P < 0.001 r = 0.82, P = 0.001 r = 0 .5 5 P= 0 05 Nutrient Content water a r= 0.48, P= 0.08 r = 0.36 P = 0 22 r = 0 .32 P = 0 29 crude protein a r= 0 .54, P = 0.05 r = 0.34 P= 0.26 r= 0 05 P= 0.88 crude fat 3 r = 0.67 P = 0.008 r = 0.48 P= 0 09 r = -0.05, P = 0 .8 7 energy a r= 0.56 P = 0 04 r = 0. 36, P= 0.23 r = -0.03, P= 0 .93 Snai l s and Slug s number r= 0 52, P= 0 07 r = 0.66, P = 0.01 r = 0.20 P= 0 50 ma ss r = 0 14, P= 0 64 r = 0.06 P= 0.83 r = 0 .36, P = 0 22 Earthworms number r= 0 .65, P= 0.02 r= 0 .33 P= 0.28 r= 0 .64 P = 0 02 ma ss r = 0 36, P= 0.23 r= 0 1 2, P = 0 70 r= 0 65, P = 0 .02 Centipedes number r = -0.38, P=0.20 r = -0 08, P = 0.80 r = -0 .25, P = 0.41 ma ss r = 0.47 P= 0 10 r = 0.81 P = 0.001 r= 0 12 P = 0 .69 Millipede s number r = 0 02 P= 0 94 r= 0 14 P = 0.66 r = 0.38 P= 0 20 ma ss r = -0. lO P= 0 75 r = 0 03 P = 0.92 r = 0.2 3, P=0.45 Arachnids number r = 0 .5 7, P= 0.04 r = 0 .59, P = 0.03 r = 0.42 P = 0.16 ma ss r= 0.12, P= 0.68 r= 0.17 P = 0.58 r = 0. 23, P = 0.46 In sec t s number r = 0.68, P = 0.01 r = 0.85 P < 0.001 r= 0.34 P = 0.25 ma ss r = 0.85, P < 0.001 r = 0.82 P = 0.001 r= 0 25 P = 0.42 a based on comparison of 14 consecutive month s Leaf litter invertebrate groups varied considerably from one a nother in their t e mporal pattern s of number a nd ma ss (with spiders and in sec t s even differin g within their own groups) as refl ec ted in their contributions to monthly total s of the se m eas ur es of a bund a nc e (F ig s 2-4 to 26). Examination of the relation s hip s between inv e rtebrate cla ss numb e r s and ma sses ( not proportionate numb e r s and ma sses) and environmental variab l es ( T a ble 2 -1 ) r evea l s that in sec t s

PAGE 30

23 were principally re s ponsible for the correlations of overall invertebrate abundance with rainfall and litter mass. Insects (Fig. 2-6) dominated the leaf litter fauna in overall abundance, but there were a few monthly exceptions: Earthworms (Fig. 2-4), the second most prevalent group overall, were slightly more numerous in October and December 1995 and weighed more in July and August 1996. Millipede s (F ig. 2-5) were slightly more numerou s in February 1996. Snail s and s lugs (Fig. 2-4) were mo st prevaJent by weight in May 1996. Spiders (F ig. 2-6) were always fairly abundant but never contributed much weight to samples, and were never predominant in either regard. Centipede s (Fig. 2-5) were generally sca rce and contributed negligible weight even when modestly abundant in March 1996. Within Insecta (Fig. 2-6), beetles and their grubs were notable in that they were aJways among the mo s t abundant orders and contributed substantially more weight than any other order in every month except April 1996, when orthopterans dominated. The contributions of a s ingle large scarab beetle spec ies Enema endymion, figured mo s t prominently. The adults and larvae of this species were so common in the vicinity of the park that they were known by unique names (ronrones and gallinas ciegas, respectively) by the local people and were at certain time s of the year extraordinarily abundant atop or in the leaf litter or at shallow depths in the soil beneath it. By weight, adults constituted 34.2% of the June 1996 invertebrate sample, and larvae amounted to 60.4 % in September, 69.9 % in October and 51.3 % in November 1995 sa mples, and 6.3% in August and 22.0% in September 1996 samples. Adults appeared in the coati diet (more on this below) or scat or were noted to be abundant in general observations made aside from leaf litter invertebrate sample collections from 8 June to 16 July 1994, 15 June to 4 July 1995 and 12 May to 17 July 1996 Larvae were similarly recorded from 17 August 1995 to 13 January 1996 and 17 July to 8 November 1996 (when field work concluded). Six species of fruiting trees (Fig. 2-7) were selected for detailed examination based on the coati' s reliance upon them over the course of the 16-month s urvey of tree phenology as well as on

PAGE 31

Mollusca: Gastropoda Mesogastropoda D Neritopsina D Stylommatophora D Other CJ Number Weight = Sep Nov Jan Mar May Jul Sep Oct Dec Feb Apr Jun Aug Month 60% 40% 20% 0% 90% 60% 30% 0% Annelida: Oligochaeta Number Weight Sep Nov Jan Mar May Jul Sep Oct Dec Feb Apr Jun Aug Month Figure 2-4 Monthly number and weight of mollusks and annelids as percentage of all leaflitter invertebrates sampled in Tikal National Park, Guatemala, September 1995 through September 1996. Based on 30 l-m 2 leaf litter samples per month. N -""

PAGE 32

Arthropoda: Chilopoda Number Weight Sep Nov Jan Mar May Jul Sep Oct Dec Feb Apr Jun Aug Month 60% 40% 20% 0% 90% 60% 30% 0% Number D c:::::::J iiiiiiiii Weight Arthropoda: Diplopoda Polydesmida D Other ~Do Sep Nov Jan Mar May Jul Sep Oct Dec Feb Apr Jun Aug Month Figure 2-5. Monthly number and weight of centipedes and millipedes as percentage of all leaf litter invertebrates sampled in Tikal National Park, Guatemala, September 1995 through September 1996 Based on 30 l-m 2 leaf litter samples per month. N V,

PAGE 33

Arthropoda: Arachnida Araneae D Other Number Weight Sep Nov Jan Mar May Jul Sep Oct Dec Feb Apr Jun Aug Month 60% 40% 20% 0% 90% 7 I I 60% 30% 0% Number Arthropoda: Insecta Blattaria Homoptera Weight D Coleoptera D Hymenopt era Dermaptera lm:J Lepidoptera l rl~ l:ffiffll H emi pt era D Orthopt era m 1111 Oth e r Sep Nov Jan Mar May Jul Sep Oct Dec Feb Apr Jun Aug Month Figure 2-6. Monthly number and weight of arachnids and insects as percentage of all leaf litter invertebrates sampled in Tikal National Park, Guatemala, Sept e mber 1995 through September 1996. Based on 30 1 m 2 leaf litter samples per month N

PAGE 34

27 the species' abundance in forest plots. Aspects of some species' fruiting patterns appeared seasonal as noted below, but neither of the measure s of fruit production (mean number of fruits per tree and percent of trees in fruit, which mostly but not in all ways varied together) was more than marginally correlated with rainfall for any species (Table 2-2). Ripe fruit was not observed in large enough numbers (presumably because coatis and other frugivores were eating it as it became available) to warrant depicting it in species graphs. B. alicastrum fruit (Fig 2-7) was present and usually abundant in virtually every month of the survey, with a brief peak in August 1995 and a broad peak centered around February 1996, i.e., in the middle of those years' wet and dry seasons, respectively. Ripe fruit was recorded March-September 1996, i.e., from the last half of that year s dry season to the middle of the wet season. B. alicastrum was seen being eaten by coatis and/or was found in their feces on 94 dates between 7 March and 30 September 1996, demonstrating significant correlation with ripe fruit availability (Table 2-2). (It also appeared in the coati diet outside of the survey period three times from 30 December 1994 to 27 January 1995, and on 3 October and 8 November 1996 ) Manilkara z apota (chico z apote a.k.a. sapodilla) fruit (Fig. 2-7) was also present and abundant much of the year, and displayed peaks timed similarly to B. alicastrum. There were lulls in fruit production in June and July, i.e., early in the wet season, in both 1995 and 1996 Ripe fruit was recorded only in May 1996, coincident with the normal onset of rains, but distinguishing ripe from unripe fruit was particularly difficult in this species due to its lack of a pronounced color change; possibly only the most mature fruit specimens were recognized as ripe. This likely explains why the correlation between ripe M. z apota availability and the appearance of the fruit in the coati diet did not achieve significance (Table 2-2). This species was recorded eaten/defecated by coatis on 52 dates between 11 January and 27 June 1996 (and also 16 dates between 7 January and 3 May l 995). Fruit production in Trichilia moschata (cedrillo rosa) (Fig. 27) was observed only during the last four months of the survey, June to September 1996, beginning early in the wet

PAGE 35

28 seaso n and increa s ing as the seaso n progre sse d and the s urv ey concluded. Ripe fruit was recorded only in the la s t month September 1996. In contrast, T. moscfuita ap pear e d in the coati diet in two bout s: 14 time s from 11 April to 2 July 1996 and 10 time s from 22 August to 29 September 1996 (and also on 3 and 10 October 1996)-indicating that a s urvey sa mple s ize greater than the 19 tree s available would have been preferred for this species. Accordingly, fruit consumption was not s ignific a ntly correlated with rip e fruit ava ilability (Table 2-2). Blomia prisca (tzol) fruited (Fig. 2-7) twice during th e s urvey : for a n ind e t e rminate period including the first two wet season month s examjned, June and July 1995 and in April and M ay 1996 when rain s r es um e d after that year's dry seaso n. Fruits were very low in numb e r during the l a tt e r of the se period s, but ripe fruit was recorded in every month of fruit production except April 1996, correlating sign ificantly with consumption by coatis (Tab le 2-2). B. prisca appeared in the coati diet s ix time s from 2 Jun e to 6 July 1995 and 10 time s from 22 April to 18 May 1996 (and also six time s from 23 April to 31 May 1995 and on 7 and 8 November J 996). Pout eria reticulata (zapoti llo hojafina) fruit (Fig. 2-7) was pre se nt for fi ve month s beginning with the onset of rains in April 1996. Ripe fruit was noted in th e la s t two month s of fruit production July and August 1996, i.e., toward the middle of the wet seaso n. Thi s spec ie s was recorded in the coati diet on 23 dates from 13 June to 30 July 1996. The correlation between ripe fruit avaj)ability and fruit consumption was marginal (Table 2-2). Pim enta dioica (pimienta, a.k.a. allspice) fruited (F ig. 2-7) in the sa me wet seaso n month s as T. moschata, June to September 1996. Unlike the latter s pecie s, however fruit production in P. dioica p eaked early in it s appearance and was waning as the s urvey concluded. Ripe fruit was r eco rded in the la s t two month s of the s urvey Augu s t and September l 996. Fruit was s imilarly recorded eaten/defecated by coatis 20 time s from 24 August to 29 September 1996 (a nd also five tim es from I to IO October 1996), correlating s ignificantly with ripe fruit availability (Table 2-2).

PAGE 36

29 600 Brosimum alicastrum (N = 69) 60 400 40 200 20 Q) Q) ;.... 0 0 ;.... Manilkara zapota (N = 26) Q) 1000 60 0. rJ'J 800 2 40 600 0 ;.... 400 Q) 20 8 ;:=j 200 z 0 0 c,:j Q) Trichilia moschata (N = 19) 600 60 D 400 40 200 20 0 0 Jun Aug Oct Dec Feb Apr Jun Aug Jul Sep Nov Jan Mar May Jul Sep Month Figure 27. Fruiting phenology of and reliance upon tree species important to white nosed coatis in Tikal National Park Guatemala, June 1995 through September 1996. Dates fruit seen eaten and/or in feces indicated by Xs. Number of trees surveyed each month (N) indicated parenthetically after species name 2 ..c: rJ'J Q) Q) ;.... 0 Q) u ;.... Q) I

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30 250 Blomia prisca (N = 109) 60 200 40 150 20 100 a) a) $-4 0 0 -,+.j $-4 Pouteria reticulata (N = 121) 2 a) 350 60 rJ) ..c: -,+.j 300 -,+.j 2 250 40 rJ) C,H a) a) 0 200 $-4 $-4 a) C,H 150 20 0 -,+.j ;::s 100 $::l z a) u $::l 0 0 $-4 a) a) Pimenta dioica (N = 17) 5000 60 I D 4000 40 3000 2000 20 1000 0 0 Jun Aug Oct Dec Feb Apr Jun Aug Jul Sep Nov Jan Mar May Jul Sep Month Figure 27 (Continued). Fruiting tree phenology and coati fruit consumption.

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31 Table 2-2. Correlational statistics for relation s hips between monthly fruit availability and rainfall and between monthly ripe fruit availability and fruit consumption by white-nosed coatis in Tikal National Park, Guatemala. Sixteen consecutive months compared; significant findings indicated in bold Fruiting Tree Species Brosimum alicastrum number of fruits/ ripe fruits per tree percent of trees in fruit Manilkara zapota number of fruits/ ripe fruits per tree percent of trees in fruit Tri chilia moschata number of fruits I ripe fruits per tree percent of trees in fruit Blomia prisca number of fruits / ripe fruits per tree percent of trees in fruit Pout e ria reticulata number of fruits I ripe fruits per tree percent of trees in fruit Pimenta dioica number of fruits I ripe fruits per tree percent of trees in fruit Rainfall p = 0.49, P = 0 05 p = -0.53, P = 0 03 p= -0.40, P = 0.12 p = -0.54, P = 0.03 p= -0.01, P = 0.96 p = -0.03, P = 0.92 p= 0.12, P = 0.65 p= 0 14 P=0.60 p = 0.26, P = 0.34 p = 0.32, P = 0.23 p= 0 09, P = 0.74 p = 0.03, P = 0.91 Coati Consumption p = 0.94, P < 0.001 p= 0.48, P = 0.06 p= 0.48, P = 0.06 p= 0.78, P < 0.001 p = 0 .5 0, P = 0.05 p = 1.00, P < 0.001 Considering coati food item nutrient composition (Table 2-3), a few general patterns were evident. Among monthly leaf litter invertebrate samples (Table 2-3), protein fat and energy content per gram were all highe s t from September to November 1995 in the latter half of that year's wet season and during and immediately after the month s of highe s t rainfall recorded in the sample collection period. All three nutritional measures then dropped to low levels during the transition into the following dry season in December 1995, rose briefly and modestly as the dry seaso n progressed, then declined again as rains resumed in April 1996 leading into the next wet seaso n All again began ri s ing from August to September 1996 albeit at lower levels overall than

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32 Table 2-3. Proximate nutrient composition of white-nosed coati di e tary item s in Tikal National Park Guatemal a. Nutrient s other than water report e d on a dry matter ba s i s. Sample W a t e r Crude Crud e Ash-Free Ash Energy ( % ) Protein Fat( %) Neutral (%) (kcal/g) (%) Detergent Fiber( %) Leaf Litter Invertebrate s August 1995 71.7 35.9 11.2 12 .0 7.7 3.33 Sept e mber 1995 78.3 50.4 19.1 18 6 2.1 4.61 October 1995 75 9 58.6 24 6 17.6 0.5 5.61 November 1995 77.5 61.6 14.9 19.9 1.5 5.02 Decemb e r 1995 72.4 38.3 I 1.1 9.6 10.2 3.13 January 1996 74.4 35 .3 11.2 11.2 2.5 3.37 February 1996 72.6 40.9 8.7 23.3 3.5 3.52 March 1996 70.5 39.8 12 .3 11.9 1.5 3.58 April 1996 64 6 35 0 10 2 15.9 14 .5 3.02 May 1996 70.0 35.9 7 1 1 3.3 12 7 2.89 June 1996 66.3 34.3 8 6 14 6 12.4 2.61 July 1996 74.3 33 1 6.3 10.6 12 5 2.67 August 1996 70 .8 30.3 5.4 2.42 September 1996 67.4 40.2 6 .6 16 .3 10 7 2.57 Enema e nd ymion larva 88. 7 62.3 12 1 30.5 0 5 4.83 a dult 62.5 67.5 20.3 51.5 4.1 6 03 Bro simum alicastrum 83.1 11.6 1.8 4.03 Manilkara za pota 80.0 4 0 5 .9 61.8 2 4 .8 0 Tri c hilia mo schata 77 1 12 0 25.2 5.27 P oute ria reticulata 86.3 9 7 4.8 4 37 Pim e nta dioica 74 .6 5 1 2.2 31.6 1.1 4 07 in the previou s year. Only fat, however was s ignificantly correlated with rainfalJ (Table 2-1), the other nutrient s b e in g a t mo s t m a r g inally so The contributions of E. endymio n beetle s and especially grubs ( T a bl e 2-3) figur e d as prominently in the above pattern as they did in leaf litter invert e brate sa mple s Adults provided the greatest amount of protein a nd energy per gram of any food it e m a n a lyzed and th e third greatest amount of fat; larv ae were particularly high in protein and e nergy a nd l ess so in fat, and had th e highe s t moi s ture content of all food it e m s.

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33 No sample of B. prisca fruit was analyzed, but of the other five important fruit species (Table 2-3), T. moschata was highest in protein, energy and especially fat content; indeed, gram for-gram this species achieved the highest fat level of any food item analyzed. The results for other fruit species were variable except that P. dioica was at or near the bottom of the group in every category. All of the invertebrate samples contained higher protein levels than any of the fruit samples (bearing in mjnd that the latter consisted only of edible portions, therefore excluding seeds) (Table 2-3). With the aforementioned notable exception of T. moschata, invertebrates also typically provided more fat per gram. Fruits equaled or slightly bested the mixed leaf litter invertebrate samples in terms of energy content, and usually held more moisture as well. In terms of foraging effort, coatis spent more-generally much more-time foraging in the leaf litter invertebrate zone than in the fruit zone at all times of year (Fig. 2-8). As noted above, ripe fruit was essentially unavailable for the five months of September 1995-January I 996 i.e. the latter part of the 1995 wet season. However, even during the greatest months of overall ripe fruit availability, April and May 1996-i.e., at the end of that year's dry season and during the transition into the following wet season----<:oatis were never observed to spend more than 6.6% of their foraging time in the canopy of fruiting trees. The animals searched for food under frujtjng trees somewhat more, spending 22 8% of their foraging time in such areas in April, 24.6% in May and 24.5% in September 1996, i.e., the early to middle wet season of that year, but these were areas of overlap in which not only ripe fruits but also leaf litter invertebrates could be found. Examining invertebrate and fruit foraging success (Figs. 2-9 and 2-10 respectively) more closely, fewer invertebrates were consumed and fewer seconds were spent consuming them per minute relevant foraging time than was true for fruits in almost every month in which both food types were eaten; March and April 1996 were exceptional in that invertebrates and fruits were consumed at comparably low rates. With respect to time spent consuming items, however, it should be noted that coatis used some undetermined portion of that time processing fruits of

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34 Brosimum alicastrum, M. zapota, T. moschata and Blomia prisca in order to discard various presumably inedible or distasteful portions (husks, skins and/or seeds). Over the 14 months of sys tematic behavioral observations, the coatis' consumption of leaf litter invertebrates (Fig. 2-9) displayed a clear pattern in terms of number of invertebrates consumed and time spent consuming them. Overall, invertebrate consumption decreased from the beginning of the study in August 1995 through April 1996 i.e., through the la s t half of the 1995 wet season and all of the 1996 dry season, then ro se s harply in May 1996 with the onset of that year's wet season and peak e d a month or two later (depending on the measure under consideration) before again declining. Neither measure of foraging success was s ignificantly correlated with total invertebrate mas s in monthly samples (number consumed: r[ 111 = 0 .26, P = 0 .39; time s pent consuming: rr 111 = 0.38, P = 0.20) In accordance with previously presented data beetles and grubs-again, especially E. endymionpredominated. Only 19.4 % of the invertebrates coatis preyed upon during observations could be positively identified (with an obvious bias favoring larger or more agile spec ie s); 96.2% of these were insect s and 81.9% various Coleoptera. E. endymion alone accounted for 44.4% of identified invertebrate prey, or 8.6% (6.5% larvae, 2.1 % adults) of all invertebrates consumed by coatis over the course of the study. Fruit consumption (Fig. 2-10) followed a similar pattern (aside from the several months in which ripe fruit was unavailable, of course). A notable exception resulted from the animals early reliance upon M. z apota, the first tree s pecies with ripe fruit in the 1996 dry season, causing a brief spike in consumption rates in February of that year. That species and also Brosimum alicastrum, which ripened soo n after, continued to be consumed at much lower rates throughout the remainder of the dry seaso n Fruit consumption increased again in May 1996 when ripe fruit of various species appeared with the onset of wet season, as noted previously. It was not possible to look for correlations between fruit foraging success and total fruit availability because phenological data were lacking for severa l of the fruit species which were consumed by coatis.

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cu s bl) $:::::1 bl) ;.... 0 0 100 80 60 40 20 0 Aug 35 Wet Season Wet Season [Z] A way from fruiting trees Oct Dec Feb Apr Jun Aug Sep Nov Jan Mar May Jul Sep Month Figure 2-8. Mean percentage of time foraging adult female white-nosed coatis spent in areas where ripe fruit was present and absent in Tikal National Park, Guatemala August 1995 through September 1996. Based on a total of 76 l hours observation of foraging by 37 animals

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2.0 0 a 1.5 OJ) i::::: ...... OJ) 1.0 0 i::::: 0.5 0 12.5 0 a 10.0 36 Wet Season Dry Season Wet Season Invertebrates Consumed 19 4 9 16 12 11 19 19 15 19 18 18 15 Aug Oct Dec Feb Apr Jun Aug Sep Nov Jan Mar May Jul Sep Time Spent Consuming 8 3 12 8 18 14 16 15 13 7 13 15 15 17 Aug Oct Dec Feb Apr Jun Aug Sep Nov Jan Mar May Jul Sep Month Figure 2-9 Mean( SEM) number of invertebrates consumed and time spent consuming them by foraging adult female white-nosed coatis in Tikal National Park, Guatemala August 1995 through September 1996. Number of females sampled in each month indicated on bars. Based on a total of 93. 7 hours observation of invertebrate foraging by 32 animals and 73.0 of 29 animals, respectively.

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37 Wet Season Dry Season Wet Season 4.5 0 Fruits s Consumed ...... E-15 oI) 3.0 16 i::: 3 15 ...... oI) 13 ro 9 1-, 0 3 .. 1.5 i::: ...... --::i:t:: 0 Aug Oct Dec Feb Apr Jun Aug Sep Nov Jan Mar May Jul Sep 28 0 Time s ...... E-21 Spent oI) i::: Consuming ...... 3 oI) 16 ro 14 15 1-, 0 9 .. 15 i::: ...... 7 3 13 --10 u 0 VJ 0 Aug Oct Dec Feb Apr Jun Aug Sep Nov Jan Mar May Jul Sep Month Figure 2-10 Mean( SEM) number of fruits consumed and time spent consuming them by foraging adult female white-nosed coatis in Tikal National Park Guatemala August 1995 through September 1996. Number of females sampled in each month indicated on bars Based on a total of l 0.4 hours observation of fruit foraging by 23 animals.

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38 Adult female coati body fat profiles (Fig. 2-11), pr es umably indicative of how well energy availability met e nergetic demand s, display e d a cl ear seaso nal pattern. Body fat declined rapidly from its high point at the beginning of the dry season in January to the mating period in the last half of February, leveled off or slightly ro se thereafter until just before the parturition period began in the la s t half of April then resumed it s decline through the parturition period and well into the wet season. Fat s tore s appeared to reach nadir in the vicinity of July to early August (a time of s par se data ), i.e s hortly before the middle of th e wet seaso n and then ro se pr es umably s teadily (discounting another gap in the data se t from mid-October through November) through the remainder of th e wet seaso n a nd until the end of the year. Discussion Behavioral and morphometric data reveal that coatis in Tikal National Park normally reproduce only once p e r year, with relevant events occurring across the popul a tion in narrow consistent period s: Mating take s place over an approximately two-w ee k period in the middle of the dry seaso n. Birth occurs over a comparable period at the end of the dry seaso n about l 0 weeks after mating Solitary ne s ting, which la s t s 1 -2 month s, begin s s hortly before birth occurs and ends with the emergence of young at the beginning of the wet seas on; the band reunjtes within the month following ne s ting The young begin foraging alongside their dam as soo n as they are brought down to the ground, but are not fully weaned until months later in the middle of the wet seaso n. A seco nd reproductive cycle with s imjlar timing but delayed by approximately four months may b e initiated if the first i s un s ucce ss ful, but seco nd cycles rarely occurred in Tikal and appeared to result in s maller litter s Taking into acco unt seaso nal difference s in different parts of the coati's range, the reproductive pattern in Tikal fit s well with previou s ly publi s hed information on coatis at other locale s. Ba se d primarily on observations of incre ase d female-male affiliative behavior and male male agonism from l a te January to mid-March 1959 and throughout January 1960, Kaufmann ( 1962 ) identified a month-long period of sex ual activity a mong coatis on BCI; becau se it appears

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39 Dry Season Wet Season ,,,-.._ 16 8 0 14 0 8 0 0 0 "-"' 8 0 0 12 ...c= 8 0 u 0 l 00 r 10 0 %Co 8 ,, o 0 cf!) ,s> ooo 01) 8 o'(o ~g' 'Ill ., (l) 80 0o 6 cto 0 0 'i:::) &;) 2P 0 0 0 4 0 0 OOo 0 2 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Date Figure 2-11. Annual body fat profile exhibited by adult female white-nosed coatis in Tikal National Park, Guatemala July 1994 through October 1996 Mating period (13 Feb 28 Feb) indicated by lightly shaded background and period of parturition (16 Apr 9 May) more darkly shaded Based on measurements obtained during 135 immobilizations of 54 animals.

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40 that actual copulation was not observed (see below), however, the mating period could not be defined. Based on similar observations and the timing of nest emergence, Russell (1979; 1982) concluded that the coati mating period on BCI lasted one to two weeks in early February, shifting slightly from year to year. Sunquist and Montgomery ( 1973) observed a pair of coatis in coitus on the island on 5 March 1971. Gilbert (1973) believed that the coatis in southern Arizona, at the northernmost edge of the species' range, mated in March and early April. Hass and Roback (2000) observed two coati copulations (excluding a possible third; see below) there on 6 April 97 and 5 April 98, and also stated without providing further details that the mating period in their population lasted from late March to mid-April. Studying captive animals in southern Arizona, Smith ( 1980) reported that copulations took place on 28 and 30 March 1976. Previous detailed descriptions of mating activity among free-ranging coatis include mounts lasting only a few seconds (Kaufmann, 1962; Gilbert, 1973; Hass and Roback, 2000) Kaufmann ( 1962) referred to these as attempted copulations, whereas the later authors considered them to be copulations. However, Gilbert ( 1973) also believed that more lengthy periods of mating activity probably occurred out of sight of observers, when a male and a female would depart from the band together, and Hass and Roback (2000) additionaUy observed two copulations lasting approximately 60 minutes each between coatis who were out of sight of other band members. The coatis found already engaged in copulation (most similarly to copulations observed in the current study, in the tree canopy over a foraging band) by Sunquist and Montgomery ( 1973) continued for seven minutes after being discovered. Smith described two copulations among captive coatis: one lasted one minute in total and another continued for 23 minutes after being discovered in progress. The numerous observations of prolonged copulatory events in the present and earlier studies suggest that Kaufmann (1962) was correct in describing brief mounts as merely attempted copulations. Prolonged copulation could be interpreted as an indication that coatis are induced ovulators, as has been suggested by Hass and Roback (2000), but it may also be a form of mate

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4 1 guar din g b y m a l e Litt e r s exa min e d in Tik a l ex hibit e d a hi g h rat e of multipl e p a t e rnit y ( Bo o th Bin cz ik 2 001 ), indi ca tin g th a t fe male c oa ti s co mm o nl y m a t e w ith mor e th an o n e m a l e Ob se rv a tion s in th e curr e nt s tudy and by Smith ( 1980) of female s attempting to br e ak aw a y from but b e in g r es tr a in e d b y mal e s u gges t th a t prol o n ge d co pul a ti o n i s m o re a dv a nt ageo u s to th e m a le th a n to th e fe m a l e Th e c l o e ly r e l a t e d ra cco on ( P rocyon l o t o r ) was d e mon s trat e d b y Sand e r s on ( 1 96 1 ) t o ovu l a t e p o nt a n eo u s l y (af t e r initi a ll y b e in g r e p o rt e d t o b e a n indu ce d ov ul a t o r b y Ll ewe ll y n a nd E nd e r 1 954-a n e rr o n eo u s findin g th a t un fo rtun a t e ly p e r s i s t s in th e lit era tur e), but th e r ev i e w o f c arni vo r e o vul a ti o n b y Larivi e r e a nd F e r guso n (2 003 ) d e m o n trat es th a t it i s un s afe t o b ase ass umpti o n s in thi s r ega rd o n ph y l oge n e ti c r e l a ti o n hip s C oa ti s we r e n o t ra di oco llar e d for K a ufm a nn 's (1 962) BCI tudy so h e wa a bl e t o k ee p tr ac k o f o nl y o n e fe m a l e dur i n g th e 1960 n es tin g p e ri o d ; th a t an im a l l ef t it b a nd o n I A pril gave birth o n IO A pril a nd brou g ht it s yo un g o ut o f th e n es t a nd j o in e d oth e r fe m a l es w ith yo un g on 2 0 M a y With o ut pro v idin g a n y fo und a tion Ru sse ll ( 197 9) s t a t e d th a t c oa ti birth s occ urr e d o n the i s l a nd durin g th e seco nd wee k o f April in 1977 a nd th e fo urth wee k o f A pril in 1 978, a nd ( Ru se ll 19 82) th a t th e n e tin g p e riod th e r e to o k pl ace in A pril a nd M ay. Ru s e ll ( 1 982) a l so sa id th a t coa ti b an d s o n BCI r eaggrega t e d in l a t e M ay B ase d o n anim a l m ove m e nt s m o nit o r e d by radiotelem e try S ae nz ( 1994 ) r e ported th a t fem a l e coa ti s in the dry for e t of S a nt a Ro sa N a ti o nal P ar k C os t a Ri ca, l e ft th e ir band s to n es t in April. Al s o b ase d on t e l e m e tr y d a t a, R a tn aye k e e t a l ( 1 994) r e p o rt e d th a t f e m a l es in o uth e m A ri zo n a we r e so lit a r y fo r a t l eas t a m o nth b e for e p a rturiti o n in ear l y July Gilb e rt ( 197 3) s t a t e d th a t f e m a l es th e r e di s b an d e d in th e third wee k o f Jun e, a nd es tim a t e d th a t all fe m a l es in th e b a nd h e was o b se r v in g gave birth b e tw ee n 16 a nd 23 Jun e. H ass (2 00 2) s aid th a t f e mal es in Ari z ona l e ft th e ir b a nd in mid-June and r eagg r ega t e d in ear l y Au gus t w h e n th e y oun g w e r e fi ve t o s i x w ee k s o ld. Th e r e a r e as ye t few d a t a ava j} a bl e o n th e l e n gt h o f coa ti ges t a ti o n aga in s t w hi c h to co mp are th e 71 t o 74d ay pr eg n a n cy see n in a s in g l e fe m a l e in th e c urr e nt s tud y Th e m os t co n c r e t e o f th ese co m e fro m Smith 's (1 98 0 ) Ari zo n a ca pti ve a nim al s tud y, in whj c h o n e f e m a l e

PAGE 49

42 gave birth 71 day s and another 76 days after being observed copulating. Average gestation length s can be approximated for the two coati band s from which mo s t data d e ri ve for the 1996 mating and parturition periods of the present s tudy, bearing in mind that parturition periods (which a re pre se nted and di sc u sse d in greater detail in Chapter 3) were likely overestimated; the difference s b e twe e n the midpoint s in the mating and parturition period s in th ese band s are 66 and 68 day s. K a ufm a nn ( 1962 ) r e ported that three coati litter s were born approximately 70 day s after the p e riod in which h e observed heightened sex ual activity on BCI. The relati ve consistency of the se data across divergent locale s-as well as the tightne ss and consistency of the mating period at th e s tart of th e coati r epro ductive cycle-suggest thi s s pecies undergoe s dir ec t d eve lopment. Understandably littl e information i s available concerning coati l ac tati o n. Kaufm a nn ( 1962 ) r epo rt e d that in 1958 nur si ng was see n on BCI as late as 16 September. In ex plicably Ru sse ll ( 1983 ) put forth th a t young there were ne a rly weaned by the tim e of reaggregation month s earlier. Smith (1980) noted that young born to a captive female fir s t b ega n eating solid food at 45 day s of age. Smith also report e d that the female began moving away at the approach of it s young when th e latter reached 74 day s of age, and that the female's teats appea r e d greatly reduc e d in size at that time ; s he observed no nur s ing as of 80 days po s tpartum. Prior to thi s s tudy, ne s ting behavior and parturition outside of the u s ual narrowly defined coati ne s ting seaso n had been observed only in Santa Rosa, where Saenz ( 1994 ) found that females quite commonly underwent seco nd reproductive cycles after lo s ing th e ir first litter s to ne s t predation by white-faced capuchins (Cebus capuc hinus); seco nd litt ers were born there in late July or ear ly August. Second litter s have also been documented in the procyonid P. lotor in so uth Texas after failed reproductive attempts were made during the normal br ee ding seaso n (Gehrt and Fritzell, 1996 ), and the phenomenon has been see n in many other mammals as well. The data on food availability pro v ide a ready ultimate explanation for coati reproductive seaso n a lity in Tikal, but l eave so me detail s yet to be clarified. In the pre se nt s tudy infant s e merg e d from their ne sts at the sta rt of the wet seaso n when ( in at lea s t one year) both leaf litter

PAGE 50

43 in ve rt e brat es and fruit were increa s ing in abundance. Are the se pattern s in food availability consistent though ? Taken by it se lf thi s ecologically brief s tudy s ugg es t s that the invert e brate pattern may be consistent but the fruit pattern is not; placing the current re s ult s into the context of the literature provides much keener in s ight into the question of pattern (in)consistency. Population s of leaf litt e r inv e rtebrate s in the tropic s are s trongly d epe ndent on moi s ture lev e l s (Lev in gs and Windsor, 1982 ), as i s ev id e nc e d by the high correlation betw ee n invertebrate a bund a nce a nd rainfall in Tik a l. As occurred in the pre se nt s tudy overall litter inv e rtebrate a bundance on BCI was lowe st during the dry seaso n and highe s t in the early wet seaso n (Levings a nd Wind so r 1982 ). Nine of thirt ee n arthropod taxa examined there individuaJly s howed popul a ti o n maxima in the ear ly wet seaso n (Levings and Windsor, 1985 ). endymion a dult s co n g r ega t e aro und li g ht s at ni g ht in hu ge number s (pers. obs.), and s hould therefore be considered ni g ht-flyin g in sec t s as well as litter in sec t s. Night-flying insect abundance (an d large b ee tl e a bund a nc e in particular) also peak e d in the ear ly wet seaso n on BCI (S mythe 1982 ), and ni g ht-flyin g insects were mo s t a bundant in the late dry seaso n and ear ly wet seaso n at the Cocha Cashu Biolo g ical Station in P e ru 's Manu National Park (Terborgh e t al., 1986; cited in Goldizen et al., 1988 ). Moreov er, differ e nc es in rainfall patterns among years affect litter arthropod population lev e l s but do not obscure seasonal trends in abundance (Levings and Windsor 1985). In contrast, seaso nal patt e rn s of tropical fruit production vary greatly from year to year not just in Tikal but at o ther s ite s as well (Fos ter 1982a; Bullock and Solf s -M aga llane s, 1990; van Schaik et al., 199 3; Chapman et a l., 2005). None of the tree s pecie s th a t were mo s t important in the coati di e t in Tikal s howed th e sa me pattern of fruit availability in June-September 1995 as in June-S ep t e mb e r 1996 (a t the b eg inning and end of the ph e nological s urvey ). Rain s were heavy at th e height of the 1995 wet seaso n and even more unusually light in the middle of the 1996 wet seaso n ; l eaf litter fall and in ve rt ebra te a nd fruit availability all s how e d associated pattern s. The climatic fluctu a tion s may ha ve b ee n due to the occurrence of an El Nino event in 1994 ( ba se d on information from th e U.S National O cea nic and Atmospheric Administration, Wa s hington, DC);

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44 the El Nino Southern Oscillation tends to create a pattern in which dry sunny years alternate with wet cloudy years in Central America (Wright et al., 1999). Unusually rainy dry seasons, particularly following an EI Nino year (Wright et al. 1999), apparently result in failure of the fruit crop in many species that normally produce fruit in the wet season, including the ordinarily prolific B. alicastrum (Foster, 1982a). Even in the absence of obvious rainfall anomalies, however, many tropical tree species exhibit non-annual rhythms in fruit production and/or high intraspecific variability in phenology (Milton 1991; Newstrom et al., 1994; Hemingway and Overdorff, 1999). It has been reported that B alicastrum trees in Tikal produce fruit three times per year : February-March, June-July, and October-November (Coelho et al., I 976). The phenology data in the present study do not support this contention, but do indicate non synchronous fruit production by this species, as fruit availability continued and even increased during a lengthy period of heavy consumption by coatis and other frugivores (pers. obs.). The data are scant but suggest consistent seasonal patterns exist in food nutrient content as well as food availability In the present study virtually all leaf litter invertebrate nutrient levels rose and fell in parallel to rainfall although only fat content correlated significantly. Fruit nutrient levels were examined herein at only a single point in time per species, but Schaefer and Schmidt (2002) reported that fleshy fruits in Venezuela rose steadily in caloric value throughout the dry season, and Worman and Chapman (2005) found that the fat content of ripe fruits of a single tropical species varied tremendously within a year, being much higher during periods of high rainfall. This is clearly an area of tropical ecology warranting further study. There is also the matter of the freezer failure and its potential effects on the present study's nutritional analyses to consider. Few nutritional data are available in the literature that are useful for comparison, but those are encouraging. Analysis of an unknown species of dung beetle from Tanzania (Pennino et al., 199 I) produced values remarkably similar to those found in the present study for adult. endymion for water content (58.3 % ), fat content (20.6 % ), NDF (51 6 % ) and ash (7.4 % ), but completely different for protein (7 8 % versus 67 5 % in the current

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45 study). Previously published values (Coelho et al., 1976) for B. alicastrum fruit (84% water, 15 6 % protein, 3.1 % fat, 3.50 kcal/g) and M. zapota fruit (75 % water 2 0 % protein, 4.4% fat, 3.76 kcal/g) are likewise similar to those obtained in this study. The relative importance of leaf litter invertebrate versus fruit availability to the timing of coati reproduction remains uncertain, but the findings of the present study appear to support Russell s (1982) assertion of the primacy of invertebrates. Tikal s coatis clearly focused their foraging efforts on invertebrates more than on fruit at all times, though seasonal patterns are somewhat difficult to assess due to the high degree of interannual variation in fruit availability during this study. For example, the animals ate no fruit during the second half of the wet season in 1995 because no fruit was then available but data from September and anecdotal observations made in October and November 1996 suggest that foraging patterns late in that year's wet season might have looked quite different. Coatis spent the highest percentage of their foraging time in fruit zones at the end of the dry season, but it was still much less than the time they spent foraging for invertebrates; the time they s pent consuming invertebrates was actually higher then than at any other time, too suggesting that both fruit and invertebrates were abundant at that time. An evolutionary argument also exists for invertebrates being more important than fruits as determinants of coati reproductive timing, namely that consistent annual peaks in invertebrate availability are much more capable of driving seasonal adaptation than are profoundly less consistent peaks in fruit availability. In any event, the present study adds to the growing body of literature demonstrating the importance of leaf litter invertebrates and their phenology to coatis. Kaufmann (1962) reported that BCI's coatis spent more than 95% of their active time foraging for invertebrates, and that fruit was eaten more during the dry season than the wet season. Russell ( 1982) estimated that coatis on BCI spent 89 % of their foraging time in the wet season and 54 % in the dry season foraging for invertebrates. He also reported that scats he collected consisted mostly of beetle parts. Contrasting somewhat to the patterns in Tikal and BCI, Saenz (1994) found approximately

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46 equal frequencies of invert e brates and fruit in the scats he collected throughout the year in Costa Rica; as in Tikal, though, Coleoptera was the dominant invertebrate group in the diet (followed closely by Orthoptera) A heavy reliance upon beetle prey i s clearly a common facet of coati ecology at a variety of sites, but no previous study ha s found as s trong a relationship between this procyonid and a s ingle prey s pecies as was evident in Tikal between it and E. endymion. Coati reproductive seaso nality in Tikal appears to be dri ve n not by re s trictive effects of food availability on female phy s iology (reproductive or otherwise), but rather by its direct effects on the survival of offspring. Specifically, reproduction there i s timed s uch that gradually weaning young (arguably th e mo s t vulnerable life s tage ; Rus se ll, 1982 ) can capitalize on a s urfeit of food re so urces which fir s t appears at the beginning of the wet seaso n and continues through the first half of that season. As others have pointed out, predatory s pecie s are unlikely to s uffer s hortages of particular nutrient s (Stephens and Krebs, 1986; Bron so n and Heideman, 1994; Galef, 1996), so when such species are timing r e production to match food availability they are likely doing so with regard to more purely energetic constraints. Female coatis do lose energetic s tores (i.e., fat) during nesting and early weaning (the most energetically expensive part of reproduction for many mammals ; Rutberg 1987) even as males are rapidly rebuilding theirs after the mating period (see Chapter 4) by relying upon the sa me foods (Booth-Binczik 2001), but females apparently have sufficient reserves to get them through. Unlike on BCI where deferment of reproduction was common (Kaufmann, 1962; Ru sse ll, 1982), virtually all m a ture females reproduced each year in Tikal (unpublished data ) Th e fact that s ome female s in Tikal were able to s ucce ss fully complete sec ond reproductive cycles after failing in their fir s t provides additional evidence of ample energetic reserves in the se animals. Reviewing reproductive seasonality among neotropical primates, DiBitetti and Jan so n (2000) concluded that very s mall s pecies time reproduction so that peak food availability coincides with lactation, whereas s pecies large enough to s tore s ufficient energy reserves-i .e., tho se s imilar in s ize to the coati-time reproduction so that peak food availability coincide s with weaning.

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47 To mor e fully assess th e importance of birth seaso n to offspring s urvival it would be u se ful to compare s urvivor s hip among young born durin g seco nd cycles to that among young born at the normal time of year. However, the few litt e r s that were produced during seco nd cycles in this s tudy do not provide adequate data for s uch a comparison. One infant that was born in August I 995 and the four th a t were born in August 1996 were known to s ur v ive to the end of the s tudy ; the fates of th e o th er out-of-season infant s were unkn ow n (as is the cause of whatever difference in litt e r size ex i s t s betw ee n fir s t and seco nd litt ers) Beyond energy ava ilability a few r e lated ultim a t e factors might contribute to the observed pattern of seasona l r e production For exa mpl e, prot ei n content of invert e brate s peaked in the middle of th e wet easo n so birth mi g ht b e tim ed s u c h th a t infant s are fully weaned when the mo s t protein is available to s upport th e ir continued grow th Also, th e fact th a t birth occurs at the end of the dry seaso n m e an s that juv e nile s hav e as mu c h tim e as possible to grow, learn and build energetic reserves b efo r e they have to deal with th e dry -seaso n low in invertebrate availability (Russell 1982 ) The only other factor that ap p ea r s at aJI lik e ly to promote s trong coati reproductive seaso n a lity in Tikal i s water availability. The r eg ion 's pronounced dry seaso n and lack of natural p e rm a nent s urface water (due to und e rlying permeable lime s ton e) create the possibility that lactating females might be re s tricted in milk production by a s hortage of water. However thi s i s not likely to be a factor in mo s t part s of the s pecie s' ran ge, and the fact that females in Tikal give birth befor e th e dry seaso n e nd s s u gges t s that water s tre ss i s not relevant to the timing of their r e production. Reproductive seaso nality s uch as the coati di s play s would not be rem a rkable in a long lived mammal inhabitin g the hi g her latitude s; inde e d, s uch patt e rns are the norm th e re (Sadleir, 1969 ; Bron so n, 1989 ) D es pite the paucity of s tudi es on long-li ve d tropical s p ecies, reproductive seaso nality is increa si ngly known from the low e r latitude s, too. The coati i s extraordinary among that latter group how eve r in th e narrow consistent timing of it s reproductive eve nt s. Looking pa s t species which appear to di s play no seaso nality whatsoever, s uch as the s un b ea r ( H e larctos

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48 malayanus) in Borneo (Schwarzenberger et al 2004) seasonal reproductive events among tropical mammals are better thought of as indistinct statistical phenomena rather than clearly demarcated ecological events. Spotted hyena (Crocuta crocuta) populations distributed across very low latitudes reproduce throughout the year, but often with modest population-specific seasonal peaks (Holekarnp and Smale 2000). Acouchies (Myoprocta exilis), agoutis (Das y procta leporina) and pacas (Agouti paca) at 6 N latitude similarly give birth throughout the year, albeit with apparent seasonal peaks (Dubost et al., 2005) White-lipped peccaries (Taya s su p e cari) at 8 N latitude and saddle-back tamarins (Saguinus fus c i c ollis) at l 2 S latitude both display birth peaks coincident with greatest food availability in the first half of the wet season, as does the coati, but the peccary's mating period has been documented to last at least eight months (Altrichter et al., 200 I) and the tamarin's parturition period spans a similar length of time (Goldizen et al., 1988). A population of the Ethiopian wolf (Canis simensis) times reproduction somewhat more finely at 7 N latitude, displaying a parturition period of about four months (Sillero-Zubiri et al., 1998). Extremely few studies have as yet been conducted on or in the very near vicinity of the equator, but at least one species there has already been found to display seasonal reproduction: mandrills (Mandril/us sphinx) exhibit a 6-month mating period (Abernethy et al., 2002). Wherever it is found, reproductive seasonality for most long-lived mammals appears to be a strategy of optimization. As such, the degree of variation seen in the timing of specific reproductive events should reflect the selective pressures that favor those events taking place at the most advantageous times. So why is the same adaptation so often expressed so differently in the tropics than it is at the higher latitudes? Two related arguments that have been posited are that optimal conditions occur over a longer time period or selective pressures favoring seasonality are otherwise weaker in the tropics than at higher latitudes because of the less variable/more benign climates generally thought to exist in the former region. However, many (perhaps even most) tropical locales fail to live up to

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49 such rosy expectations (Foster, 1982a; Bronson and Heideman, 1994). Even setting that fact aside, selective pressures weak or strong are still selective pressures. Given an evolutionary timeframe, species-or more accurately, their populations-should respond to those pressures as best they are able. Bronson and Heideman (1994) have argued persuasively that reproductive seasonality is generally less well-defined in the tropics because animals residing there have less reliable or distinct proximate cues upon which to rely Photoperiod, the most universally relied upon zeitgeber for long-lived mammalian reproduction (Sadleir, 1969; Bronson, 1989), obviously diminishes in degree of both annual and daily change as one proceeds from the poles to the equator. Tropical rains and their innumerable effects on food availability, although often apparently consistent enough over history to promote the evolution of reproductive seasonality, generally vary too much from year to year to serve as predictive cues for timing specific reproductive events. Other possible cues appear even less reliable. It is unknown at what point photoperiodic changes become too slight for animals to use them to time or fine-tune the timing of their reproduction (Bronson and Heideman, 1994), but of course such timing depends on the extent of both the photoperiodic changes themselves and the genetic variability of the populations subjected to them. One prediction based on this premise in combination with the assumption that there are no latitudinally based differences in population genetic variability is that long-lived seasonal species (or even closely related groups of species) should display a broadening and perhaps ultimately a disappearance of peaks in reproductive events in populations at increasingly low latitudes, and this has been amply demonstrated to occur (Bronson, 1985; Di Bitetti and Janson, 2000). Bronson (] 989) also suggested that social species should be able to time their reproduction more finely than would otherwise be possible at low latitudes by using interactive cues to augment environmental cues, i.e the reproductive responses of the most environmentally sensitive individuals in a population could socially trigger like responses in the population's remainder. In accordance with this prediction, the tropical

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50 mammals that have thu s far been found to ex hibit relatively narrow reproductive seaso nality are indeed soc ial s pecie s (e.g., ring-tailed lemur s, L emu r ca tta ; Jolly 1967; impala s, Aepyceros melampus: Murray, 1982; greater spear-nosed bat s, Phyllostomus hastatus: Porter a nd Wilkinson, 2001; red ruffed lemurs Varecia rubra: Va sey, 2005). The coati may s imply be one of the most extreme examples of s uch found to date. (This s ubject i s exa mined in greater detail in Chapter 3). The di sc u ss ion doe s not end there, how eve r. As O Brien ( 1993 ) e mpha s i ze d lamentably few long-liv e d tropic a l mammal s have so far b ee n exa mined for the po ss ibility l e t a lon e the extent-of r e productive photore s ponsivene ss and, with the exception of Nile grass rats (Arvicanthis niloticus: Sicard et al., 1992 ), all of th e s hort-lived tropical spec i es that ha ve so far demon s trated any ph oto re s pon s i ve ne ss whatsoever in the laborator y h ave di s pl ayed continuous or opportunistic r e production (i.e., free from pr e dictive cues) in the wild. Looking farther abroad taxonomically, s potted antbirds (Hylophylax n. na evioides) at 9 N latitud e in P a nam a s how reproductive phy s iolo g ical re s pon s ivenes s to the very s light natural changes in d ay l e ngth found at that latitude ( H a u e:t al., 1998 ). If tropical mammal s po ssess s imilar capabilities, that of course merely beg s the qu es tion of why they do not utili ze them mor e often. To th e d e li g ht of the curious, scientific e ndeavors invariably raise more questions than th ey answer.

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CHAPTER3 BIRTH SYNCHRONY Introduction In the absence of ex traordinary se lective pr ess ure s, r eprod uctive seaso nality is a s trategy of optimization. As s uch, it often allows for considerable variation in the timing of s pecific reproductive events, even within a s ingle population of an obligate seaso nal s peci es This is especially true in the tropics, where annual variation in photoperiod is s light and other potential environmental predictors m ay b e patchy or may s hift so m ew hat from year to year in r espo n se to climatic conditions (e.g., rainfall; Rand and Rand 1982) For example, as Ru sse ll ( 1982 ) pointed out, birth peak s among Panama' s seaso nally r e producing mammal s are largely prob a bili s tic events; birth period s for mo st s pecie s span at lea s t a few month s (summarized in Fleming, 1973). The white-nosed coati is unu s ual in thi s regard, with a JI parturition on Barro Colorado I s land (BCI), Pan a m a-t h e only population previou s ly well-studied-seemingly occurring within a 1to 2-week period each year (largely inferred from observations of first emergence of young from nests; Kaufmann 1962; Ru sse ll, 1979; 1982) Thi s pattern prompts consideration of ecological pre ss ure s favoring a high degree of birth sy nchrony in the s pecie s. [Note: The terms reproductive seasona lity and sy nchrony have so metim es been u se d interchangeably (e g., Boinski 1987), leading to confusion about the nature and causes of the se phenomena. The author ha s adopted Ims (1990b) definition of reproductive sy nchrony: "a phenomenon caused by biological interactions operating to produce a tighter clustering of reproductive events than would have been impo se d by environmental seaso nality alone" (p. 135) ] Adult female coatis are also highly soc ial, living in cohesive band s with their young most of the year and becoming so litary only to ne s t (Kaufmann, 1962 ). Ru sse ll ( 1982 ; 1983 ) 51

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52 e mpha s ized th e importance of cooperation a mon g adult females to minimi ze lo sses of young to predation and para s iti s m, and ( 1982) s ugge s t e d that a hi g h degree of both intraand interband birth sy nchrony exists to facilitate this strategy. Other po ss ible explanations more generally offered for birth sy nchrony include predator swa mping (Pianka, 1976 ), dependence upon an ephemeral food or other re so urce (e.g., the n ee d of so me de se rt anurans for breedin g pond s), or utilization of socia l m ec hani s m s to s upplement inad e qu a t e e nvironment a l predictor s (e.g., photoperiod at low latitude s) e mployed in a seaso nal reproductive s trategy ( Bron so n 1989 ) Non e of th ese explanations ha s yet b ee n rigorou s ly examined for the coati, nor ha s birth sy nchrony even b ee n established as a general phen o menon in the s pecie s (a lthou g h a handful of r e port s s ugg es t th a t coati r e production may b e patterned s imilarly at other loc a tion s, e g., in so uthern Arizona: Gilb e rt 1973 ; in Costa Ric a: Saenz, 1994 ; in Jalisco, M ex ico : Val e nzuela and Ceballos 2000). It see m s reasonable to rule out tran s itory requirements as an ex planation for birth sy nchrony in thi s long-lived tropical forest-dwelling mammal however and no s uch requirements were di scove red during the extensive observations of BCI' s coatis by Kaufmann ( 1962 ), Ru sse ll ( 1979 ) and Gompper ( 1994 ). Accordingly thi s s tudy examines data on the timing of coati reproducti ve eve nt s at Tikal National Park, Guatemala to provide detail s on birth synchrony at thi s new locale and to test s pecific prediction s about the phenomenon ba se d on the following hypothe ses: H 1 : Coati birth synchrony minimi z es ju ven il e mortality by facilitating communa l ca re of young. The fiveto six-wee k ne s ting period (Chapter 2) i s the lea s t soc ial tim e in the live s of female and juvenile coatis, s o communal care cannot become a relevant factor until the animals ha ve reaggregated into bands after the young hav e emerged from the ne s t. Birth sy nchrony would be relatively u se le ss for facilitating communal care if s ub se quent re agg r ega tion is too asynchronous. It was th e refore pr e dicted that within a band of coatis the variance in the timing of reaggregation i s no greater than in that of parturition

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5 3 H 2 : Bir t h sy n c hr o n y minimi zes ju ve nil e m o r ta li ty b y pr eda t o r swa mpin g E ve n th e lar ges t band s of co a ti s do not in c lud e mor e th a n a bout a sco r e o f r e producti v e female s in a g i ve n y e ar ( Booth-Binczik, 2001 ; Chapter 2), and pr e dator s a r e c a p a ble of con s uming a n e ntir e litt e r of newborn coati s in s h o rt ord e r (e g Ro s e 1997 ) Th e re i s al s o much hom e rang e ove rl a p a mon g n e ighboring co a ti band s ( K a ufmann 196 2; G o mpp e r 1 9 97 ). T o swa mp pr e d a t o r s rath e r than m e r e l y prompt th e m t o s hift th e ir fo c u s fr o m b a nd t o b a nd th e n birth sy n c hrony w ould h ave to ex i s t acro ss as w e ll as w ithin b a nd s. H e n ce it was pr e di c t e d that th e va ri a nc e in th e timin g of parturition b e tw ee n b a nd s i s e qual to th a t within b a nd s. H 3 : Bir t h sync hr o n y r esu l ts fr o m th e coat i 's r e li a n ce up o n socia l mec h a ni s m s t o e nhan ce r e pr oduct i ve seaso n a li ty. If c oa ti s are r e lying up o n soc ial m ec hani s m s t o a u g m e nt wea k e n v i ro nm e nt a l c u es for timin g r e produ c ti o n it i s r eas on a bl e to a ss um e th a t thi s proc ess will r es ult in a grea t e r d e gr e e of birth sy n c hrony within than b e tw ee n b a nd s. In opp os iti o n t o th e pr e di c tion o f H 2 th e r e for e, thi s hyp o th es i s ge n e rat e d a pr e diction th a t th e va ri a n ce in th e timin g o f p a rturiti o n be t wee n band s i s g r ea t e r th a n th a t w ithin b a nd s. It s h o uld b e not e d th a t th e afor e m e nti o n e d thr ee h y poth eses ar e in fac t ind e p e nd e nt rath e r th a n mutually ex clu s i ve a lt e rnati v e s; more than on e m a y pertain Furth e r wh e r eas the fir s t two h y p o th eses dir ec tly a ddr ess po ss ibl e ultimat e ca u ses o f birth sy nchrony th e third in s te a d a ddr esses a pro x im a t e m ec hani s m b y w hi c h th e ultim a t e fac t o r o f seaso n a l foo d ava il a bility (s ee Ch a pt e r 2) m ay co ntribut e t o th e c o a ti s ti g ht c lu s t e rin g o f birth Methods From Jun e I 994 throu g h Octob e r 1996 v a ri o u s d a ta w e r e coll ec t e d o n a p o pulati o n of fr ee -rangin g whit en ose d coa ti s in Tik a l Nati o n a l Park Gu a t e m a l a (17 N 8 9 W ) as part of a b roa d s tudy o f th e s p ec i es' r e produ c ti v e biol og y. (A n ove r v i ew o f th e c oa ti s r e p ro ducti ve p a tt e rn a t thi s l oca l e a pp ea r s in F ig. 3-1 .) Thi s c h a pt e r s p ec ifi ca lly exa min es d a t a o n th e timin g of parturition in 1 9 95 a nd 1996 a nd th e r eagg r ega ti o n o f p aro u s fe m a l es a ft e r n es tin g in 1996

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54 Dry Season Wet Season mating nesting reaggregation parturition Feb Mar Apr May Jun Jul Month Figure 3-1. Timeline of white-nosed coati reproductive phenological events in Tikal National Park, Guatemala (see Chapter 2)

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55 In all, reproductive events occurring among 28 females from three bands contributed to the study. Each female was initially captured by live-trap or (more often) blowgun and chemically immobilized by intramuscular injection of approximately 7 mg/kg Telazol (Fort Dodge Laboratories Inc., Fort Dodge, IA). Anesthetized animals were tattooed and eartagged for identification and fitted with 90 g motion-sensitive radiocollars (Advanced Telemetry Systems, Isanti, MN) to enable monitoring thereafter. The animals were subsequently habituated to the close presence of observers (as described in Chapter 2), and the status of each female was checked daily (as possible) during the time periods when parturition and (in 1996) reaggregation took place. All animal handling procedures were conducted as per protocol #4084 approved by the University of Florida's Institutional Animal Care and Use Committee. Parturition was determined to have occurred when a female showed a sudden pronounced reduction in girth followed by continued nesting behavior, and was ultimately confirmed by observation of young still in the nest or shortly after emergence from the nest. Parturition dates could not usually be pinpointed because the females tended to give birth while remaining out of sight within their nests for days at a time. In this circumstance the scoring of a female's parturition was distributed over an appropriate span of time (e.g., one-third of the female's parturition was ascribed to each of three possible days). Data on females of indeterminate status for two weeks or longer were not utilized. For the purpose of this study, reaggregation was deemed to have occurred when a postpartum female and her young were observed to have reunited with at least three other such females. In most cases reaggregation dates could not be pinpointed and were scored as described above for uncertain parturition dates. Sokal and Rohlf ( 1981) guided all statistical efforts, and a Pa.~ 0.05 level of significance was utilized in all tests. In order to assess whether the variance in the timing of parturition was greater than or equal to that of reaggregation, i.e., to test the communal care prediction, a one tailed test for equality of two variances was conducted for each of the two coati bands that

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56 contributed almost all of the se data in 1996; data on a s ingle female from a third band were includ e d in the d esc riptive s t at i s tic s pre se nted for this year. An ANOV A was conducted to compare the variances in the timing of parturition between and within the two primary bands in 1996, i. e to te s t the prediction s for predator swa mping and soc ial facilitation of reproductive seaso nality. In s ufficient data were obtained for the 1995 parturition period to include in s uch a n a l yses, a nd the se data were th e r efo re u se d only for comparison with th e 1996 parturition period v i a d esc ripti ve s tati s tic s. To a id in comparing the annual birth pul se of the coati in Tik a l to that see n at other locale s a nd/or in other s peci es, the interquartile range ( i e. middle 50 %) wa s also ca lcul a t ed for eac h year's dat a. Results Coati parturition was both narrowly timed within eac h year and consistent between the years of the s tudy (Ta ble 3-1 ) The nin e birth s recorded in 1995 occurred in a s lightly flattened but normally di st ributed peak of 14 day s duration and the 24 birth s r eco rd e d in 1996 occurred in a s imilar peak l as tin g 18 day s. Th ese p ea k s were centered s ix day s a p a rt l a t e in the dry seaso n s /at th e be gi nnin g of th e wet seaso n s (see Chapter 2) of their re s pective years. Th e re was a di s cernibl e difference in the timing of parturition b e tw ee n the two primary band s under observation in 1996 (F ig 3-2), with Band l females giving birth over a 14-day span that began four day s after the s tart of the 12 day span in which Band 2 females did so. Mean birthd ates in the two normally di s tributed birth peaks were 2 May a nd 2 7 April, re s pectively The variance in the timing of birth b e tw ee n Band s J and 2 was s ignificantly g reater than th a t within the band s (Fli. 2 11 = 24.21, P < 0.001). Reaggregation in 1996 occurred relatively quickly after females fir s t brought their young down from th e ir n es t s between th e early and middle wet seaso n (see Chapter 2). Eleven females with young from Band 1 found at lea s t three other s uch families within a 20-day s pan beginning 31 May and nine females with young from Band 2 accomplished it in 16 day s beginning 4 June Comparing parturition to r eaggrega tion within eac h band : The variance in the timing of

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5 4 3 2 1 0 57 c=J Band 1 (N = 12 females) c=J B and 2 (N = 11 females) 22 23 24 25 26 27 28 29 30 1 2 3 4 5 6 7 8 9 April D ate May Figure 3-2 Timing of births in neighboring white-nosed coati bands in Tikal National Park Guatemala in 1996. Scoring of a female's parturition distributed over appropriate span of time when date not pinpointed ( e.g 1/3 of female's parturition ascribed to each of three possible days); mean( SEM) span for all females 3.9 0.6 days, range 1-10 days.

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58 reaggregation was s ignificantly greater than in that of birth in Band 2 (F[ s, 101 = 8.77, P = 0.001). Band I di s played the sa me tendency, but it was not significant (F 110 111 = 2.28, P = 0 10). Discussion The communal care hypothe s is for coati birth synchrony assumes that the presence of multiple females at the same reproductive stage is important to the survival of young Certainly, evidence suggests that coati soc iality is employed in group defen se, including of offspring. Ru sse ll (1983 ) found that BCI' s coati band s adopted a formation that was optimal for protection of young rather than foraging efficiency when moving through the forest. He further reported that juveniles s pent more tim e vigilant when unaccompanied by adults, and adults were more vigilant in smaller groups. Thi s latter finding was also confirmed by Burger and Gochfeld ( 1992) in Costa Rica. However, the presence of the band may actually be more important to the survival of adult females than of juvenil es, as mortality rates of females are higher when they are alone than when they are in groups (Booth-Binczik, 2001; Hass and Valenzuela, 2002) and female mortality is lower in larger groups, whereas juvenile mortality is not (Hass and Valenzuela, 2002) There are no published data on relative mortality rates of juveniles before and after band reaggregation, and direct observations of predation are few. During the course of the present study a pair of crested eagles, Morphnus guianensis, was observed taking five coati infants to its Table 3-1. Descriptive statistics for observed white-nosed coati birth periods in two years in Tikal National Park, Guatemala. Stati s tic 1995 1996 Number of Females/ Band s 9/2 24/ 3 Parturition Period 1629 April 22 April 9 May Mean Birthdate 24 April 29 Aprit3 Interquartile Range (day ) 5 6 Degree of Kurtosis (3) -0 62 -0.69 calendar dates not s trictly comparable becau se 1996 was a leap year

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59 ne s t in a couple of weeks' time at about the end of the coati ne s ting period in Tikal and other raptor species were occasionally observed preying upon ne s tling coatis as well (D.F. Whitacre, per s. comm.). Ro se ( 1997) documented heavy predation on ne s tling coatis-principaJJy within their first few weeks of life by white-faced capuchins (Cebus ca pu c hinus) in Santa Rosa National Park, Costa Rica, and Saenz ( 1994) reported that this re s ulted in as much as 100 % ne s tling mortality in so me b a nd s Ru sse ll ( 1982) reported heavy juv e nile mortality on BCI in the first thr ee month s following r eagg r ega tion and H ass and Valenzuela (2 002) estimated 43-75 % mortality in the fir s t 3-5 month s of life in so uthern Arizona and Jalisco Mexico. It appears likely that the ri s k s faced b y a young coa ti do indeed dimini s h in th e company of it s band, but the anti pr e dation benefit s o f group livin g do not depend on female s being at the sa me reproductive s tage. Certain aspects of coa ti biology and two historical observations of coati behavior (albeit perhap s of a s ingl e animal) prompt s pecial consideration of the adult male as a potential predator of young. The s ubj ec t of infanticide by male coatis ha s been dealt with more fully by Booth Binczik (2 00 I ), but brief m e ntion in the course of this di sc u ss ion of birth sy nchrony and communal care see m s appropriate. Female coatis have been documented to undergo successful seco nd reproductiv e cycles s hortly after lo s ing litters born at the normal time (Saenz, 1994; Chapter 2), making sex ually se lected infanticide a possibility (Bertram, 1975; Hrdy, 1979). The fact that male s are pr e dominantly so litary has also been interpreted as a result of exclusion by f e male s for the protection of th e ir young (Russell, 1981 ) In s upport of his interpretation Russell ( 1981) reported an apparently seco ndhand observation of an adult male coati on BCI consuming an infant near a biological laboratory animal feeding s tation, and another of an adult male (possibly the sa me animal) attacking and carrying an infant away from the sa me s ite on the following day. How eve r in Tikal mo s t coati litters are multiply s ired (Booth-Binczik, 2001), re s ulting in paternity confusion which would discourage sex ually se lected infanticide (Wolff and Macdonald 2004). Male coatis are also not excluded from bands in Tikal, and in fact they frequ e ntly associate with band s ther e (Booth-Binczik, 200 I) as well as in Arizona (Gilbert, 1973 )

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60 and Costa Rica (Saenz, 1994) Moreover, despite severa l hundred-po ss ibly thousands of-hours of field observations by severa l biologi s ts at a few s it es, no one other than Ru sse ll ( 1981) has uncovered any evidence of infanticide in the species. To the contrary, in Tikal adult male coatis were often seen in the near vicinity of young of all ages with neither the young nor their dams displaying any alarm or other defensive behavior (Booth-Binczik, 2001). In addition to cooperative defen se, other forms of communal care of offspring have been documented in the coati. N es t s haring ha s been observed both in the wild (Russell, 1979; 1983; Chapter 2) and in captivity (Smith, 1980). In so me in s tanc es it involved a female that had lost a litter helping to care for a nother female's litter (Russell, 1979 ; Smjth 1980 ), and in one case two females pool e d th e ir litt ers and both nur se d all infant s ( Ru sse ll 1979 ). There have also been frequent observations of allogroomjng by non-parent s once band s have reunited after the ne s ting period (Russell, 1983 ; per s. obs.). As important as communal care of whatever form may ultimately be to coati offspring s urvival, howe ve r it does not appear to explain the s p ec i es' remarkable birth sy nchrony, as a rather ba s ic prediction arising from the communal care hypoth es i s failed testing in the current s tudy. It is suspected but as yet unknown whether coatis undergo direct development (Chapter 2), but females are pre s umably able to exert at lea s t as much control over the timing of reaggregation as parturition. Noneth e l ess, births were clustered s ignificantly more than were reaggregation events. Selectiv e pr ess ur es for being in a group are evidently not the driving forces behind coati birth sy nchrony. Con s idering the aforementioned ne s t rruding by pr e dators on coatis, the predator swa mping hypothe s i s might at fir s t look somewhat more attractive. The effectiveness of this anti-predation s trat egy, however, is determined not only by the degree of synchronization of a vulnerable pr ey s t age but also by the nature of the predator s and their method s. That is, if neighboring groups of prey differ so mewhat in their timing and their predator s are s ufficiently mobile, the predators will s imply re s pond by s hifting their focus from group to group accordingly

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61 (lms, 1990a). Consid e ring the mobility of coati ne s tling predators (especially raptors) and given the significantly greater variance in the timing of birth s between than within bands found in the present study, s hifting predators appear to pose a real threat to coati young. The predator swamping hypothe s i s for birth s ynchrony is un s upported At lea s t until new hypotheses and/or evidence are examined to account for coati birth synchrony, then the mo s t likely explanation appears to be that this phenomenon i s merely an extreme example of a tropical a nimal using soc ial cues to s upplement the relatively weak environmental pr e dictor s it relie s upon for timing r e produ c tion Some support for thi s argument is found in th e r es ult s of the comparison of intraand inter-band sy nchrony mentioned above. Addition a l s upport can b e found in a closer co n s id e ration of the coati' s annual birth pulse As mentioned, both the 1995 and 1996 overall peak s in parturition were s lightly platykurtic p e rhap s o nly diff e ring from completely normal curves due to the method u se d for e s timating unc e rtain birthdate s, i. e., attributing portion s of eac h of the se births to more than a single day. The coati ha s ample cause in term s of food availability to have developed the adaptation of r e produ c ti ve seaso nality (Russell, 1982 ; Chapter 2), which-barring seve re climatic curtailment (e.g., at very high latitudes) or protraction by variable re s ponse to weak environmental cues (e.g., at low latitudes)s hould produce a normally di s tributed biological re s ponse. Th a t i s, if th e coati's annual birth pul se i s driven purely by seas onal considerations, it should be normally di s tributed or flattened depending on the environmental predictors available to the species and it s ability to re s pond to them. Accordingly mo s t seaso nally reproducing tropical mammal s s tudied to date display long, mode s tly peaked birth pul ses ( Fleming, 1973; Bronson 1989 ; Di Bit e tti and Jan so n, 2000 ; Chapter 2), and the notable exceptions are highly social s pecie s (Chapter 2). In contrast, the evolutionary forces that promote sy nchrony do so by acting against either tail of a re s ponse curve (e.g., Findlay and Cooke 1982) creating a leptokurtic di s tribution The coati's normally di s tributed parturition peaks s ugge s t that birth synchrony in and of it se lf i s not adaptive in thi s s p ec ie s

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62 Given th e likelihood of direct dev e lopm e nt in thi s spec ies (C hapter 2), it i s also pos s ible that the coati's unu s ually ti g ht clu s tering of birth s i s s imply the re s ult of se l ec tion for mating synchrony. Synchrony of estrus among females s hould make it less po ss ible for one male to monopolize matin g access to a group of females (Emlen a nd Oring, 1977 ; Gehrt and Fritzell, 1999a). It could th erefo re be advantageous for females to sy nchronize th ei r receptivity if it gives them access to mor e than a s in g le m a le, e nablin g mate c hoic e. Howev e r so me s tudi es have failed to find a relationship betwe e n d eg r ee of sy nchrony in female r ecept i v ity a nd d egree of monopolization by male s ( Po s ton e t al 1999 ; Widdig e t a l. 2004), and it ha s also be e n s ugge s t e d th a t sy nchronized r ece pti v ity wou l d limit rather than e nhanc e females opportunity for mate choice ( P e r e ira 1991 ; Schank, 200 I) Th e nature of th e r e lation s hip b e tw ee n mating sy nchrony and mat e monopolization/m a t e choice undoubt ed ly dep e nd s upon the d eg r ee of overlap among females' period s of rec e ptivity which i s not yet known for th e coati. Of course, it could be argued that to b e mo s t u se ful, th e term birth sy nchrony s hould be re se r ve d so lely for s ituation s in which se l ec tiv e pre ss ur es are acting dir ec tly on the clustering of births. From thi s viewpoint, the tight clu s tering of birth s ex hibited by the coati would not qualify as birth sy nchrony per se if it re s ult s from s uch phenomen a as reprodu c ti ve seaso n a lity and mating synchrony Left wholly unexplored i s the que st ion of preci se ly how the coati achieves s uch extraordinarily tight reproductive seaso nality Assuming socia l facilitation of environmental cues as appears to be the case, numerou s pos s ibilitie s exist. Among Mammalia soc ial m ec hani s m s for timing reproduction have primarily been inv es ti ga ted in rodents. Although in mo s t cases the pre se nce of chemical cue s from reproductively active female s inhibit s ovarian cycling in others (reviewed in Bron so n, 1989), in so me s itu a tion s it ha s in s t ea d b ee n found to trigger (Drickamer and Hoover 1979 ) or sy nchronize ( McClintock 1978) s uch cycling. Male s have also b ee n s hown to u se both chemical and tactile mean s of initiating and/or sy nchronizing female reproductive cycling ( Whitt e n 1956 ; M a r s d e n and Bron so n 1964 ; Bron so n and Maruniak, 1975 ;

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63 Carter et al., 1986), and in the case of red deer (Cervus elaphus), even to use auditory signals (McComb, 1987). On that last bit of information, it is perhaps worth noting that the coati is the first carnivore to be identified in which males undergo a rut (Chapter 4), and that a hallmark feature of this male adaptation is an advertising call. With opportunity, this will be a focus of future research.

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CHAPT E R4 R U T Introduction L o n g m i s t ake n fo r a e p ara t e s p ec i es du e t o it s l arge r s ize a nd m a r ke dl y d iffe r e nt h a bit s (e g ., S a nd e r so n 1 94 1 ), th e m a l e w hit en ose d coa ti ( N as u a na ri ca) h as r ece i ve d fa r l ess a tt e ntion th a n h as th e f e m a l e fr o m r esea r c h e r s Thi s di s p a rit y in sc i e ntifi c e ff o rt i s p e rh a p s a r es ult o f th e c hi e fl y so lit a r y n at ur e of a dult m a l es ( K a u f m a nn 1 962; B oo th Bin cz ik 200 1 ) a nd th e p ro bl e m s i t p o s es t o o n e w i hin g t o wo rk w ith th ese diurn a l se mi -a rb o r ea l m e dium i ze d ca rni vo r es in th e ir prim a r i l y d e n se, t ro pi cal fo r e s t h a bit a t (ge n era l eco l ogy r ev i ewe d b y G o mpp e r 1 995). Pr ev i o u s di sc u ss i o n s o f c o a ti r e produ c ti ve eco l ogy a ddr esse d o nly th e timin g o f r e produ c ti ve eve nt s and p as ibl e b e n efi t s o f easo n a lit y t o fe m a l es a nd yo un g ( K a ufm a nn 1 962; Sm yt h e, 1 9 70 ; Ru sse ll 1 982) Thi s p a p e r foc u ses in s t ea d o n r e p ro du c ti ve p a tt e rn s di s pl aye d b y th e m a l e o f th e pec i es. E n v i ro nm e nt a l influ e n ces ac t o n f e m a l es in d e t e rminin g a s p ec i e 'timin g of birth an d m a l es ca n be ex p ec t e d t o r es p o nd t o f e m a l e imp e rati ves o r ( in so m e in s t ances) th e e n v ironm e nt whi c h s h a ped th e m w ith r e produ c ti ve a d a pt a tion s of th e ir o wn M a l es of m a ny p ec i es ar e o pp o rtuni s t s, m ai nt ai nin g full r e p ro du c ti ve r ea din ess a t a ll tim es fo r w h a t eve r m a tin g c han ces occ ur but m a n y o th e r s p ec i es h ave evo l ve d t e mp o ral va ri a ti o n i n m a l e r e pr od u c ti ve ca p a biliti es in ways th a t r e fl ec t p a tt e rn s of fe m a l e r ece pti v ity Thi s va ri a ti o n see m d es i g n e d b o th t o m ax imi ze th e m a l e 'a bilit y t o ca pitali ze o n m a tin g o pp o rtuniti es w h e n th ey ex i t a nd t o minimi ze th e co s t s a ss o c i a t e d w ith th a t a bilit y wh e n th e y do n o t. On e s u c h t e mp o r a l p a tt e rn ee n a mong m a l e m a mm a l s in vo l ve rut. Th e t e rm "ru t h as o ft e n b ee n u se d t o d esc rib e a sea a n a l prin c ip a ll y o r w h o ll y b e h av i o r a l ph e n o m e n o n di s pl aye d b y m a l es o f so m e s p ec i e o r p o pul a ti o n s (e.g. th e "fa ll rut o f 6 4

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65 seve ral high l a titud e N o rth Am e ri c an ungul a t es; Spom e r 1996 ). S o m e tim es it h as eve n b ee n u se d s imply as s h o rth a nd fo r th e m a tin g p e riod of a ny seaso n a lly r e produ c in g p ec i es (e g., G e nov e si e t al 1997 ). From a n e volutionary per s pective however rut mi g ht more properly be thou g ht of a s an attribut e of indi v idual mal es rath e r than of seaso n s, s p ec i es or popul a tion a s a whol e. Ac c ordin g ly the a uth o r d e fin es rut as a bri e f annu a l p e ri o d o f dram a tic a lly e nhanc e d m a l e r e produ c ti ve ca p a bilit y th a t lik e l y a ro se in r es p o n se t o ti g ht fe m a l e r e produ c ti ve easo nalit y in c ombin a ti o n w ith th e int e n se m a l e -m a l e co mp e tition s u c h seaso n a lit y so m e tim e fo s t e r s, and th a t ther e fore t e nd s tow ar d sy n c hrony within a popul a tion. It diff e r s from o th e r form s of mal e r e produ c ti ve sea o n a lity n o t o nl y in th e br ev it y a nd m agn itud e o f th e c h a n ge ruttin g m a l es und e r g o but a l s o in th e n a tur e of th ose c h a n ges. Sp ec ifi ca ll y, m a l es in rut di s pl ay a fu gue o f b e h av i ora l ph ys i o l og i ca l a nd a n a t o mi ca l c h arac t e ri s ti cs th a t-d es p i t e so m e ee min g m a l a d a pti ve a t fir s t g l a nc e ac t in co n ce rt t o t e mp o rarily m ax imi ze co mp e titi ve a bilit y a nd thu s lik e l y r e producti ve s ucc ess B es id es b e in g int e r es tin g in th e ir own ri g ht m a l e r e produ c ti ve a d a pt a ti o n s can also pro v id e in s i g ht int o a p ec i es overa ll r e produ c ti ve s trat egy. On e exa mpl e i s pr ese nt e d in th e c ase of m a mm a l s in w hi c h th e m a l es und e r g o seaso n a l as perm a t oge n es i s Of int e r es t in tudi es o f s p e ci es di s pl a yin g sea anal r e production i s wh e th e r th e p a tt e rn i s a ( r e l a ti ve l y) rigid ev olutionary r es ult of hi s t o ri ca l clim a ti c rh y thm s or m e r e ly an opportuni s ti c r es p o n se to pr eva ilin g c ondition s, i .e wh e th e r it i s a n o bli ga t e o r fac ult a ti ve s t ra t egy ( N egu a nd B e r ge r 1 972; B ro n o n J 9 8 9 ) B eca u se s p er m a t oge n es i s t a k es l o n ge r t o co mpl e t e th a n d oes ovu l a ti o n a ft e r a p e ri o d o f r e producti ve qui e ce n ce, a nd b eca u se m a l es a r e evo luti o n a ril y imp e lled t o h ave m a tur e s perm ava il a ble wh e n eve r fe m a l es mi g ht b e r e ady to r ece i ve s u c h h e alth y a dult m a l e m a mm a l s ha v e ge n era lly evo l ve d t o produ ce m a tur e s p e rm o ve r tim e p e ri o d s th a t m o r e th a n e n co mp a s p e riod s o f fe m a l e r ece pti v i ty ( Bron o n 1 98 9 ). S easo n a l as perm a t oge n es i s i s thu s p ri mafacie ev id e nc e th a t a s peci es h as a d o pt e d o bli ga t e r e produ c ti ve easo n a lit y, as s u c h a n ex tr e m e m a l e a d a pt a tion

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66 would be expected to arise only where females have a highly predictable pattern of receptivity, especially where the potential costs of male reproductive capability are great. The coati certainly fulfills the first part of this evolutionary scenario, being exceptional among tropical mammals (Fleming, 1973) for its high degree of reproductive seasonality at the few locales thus far examined (Kaufmann, 1962; Russell, 1982; Chapter 2). The pattern seen in Tikal National Park Guatemala may be typical in this re s pect. There, virtually all copulation occurs within an approximately two-week period near the middle of the January-April dry season and parturition occurs in a simjlarly brief period beginning shortly before the onset of the rains in May (Chapter 2). There is also reason to hypothesize high costs of reproduction for male coatis Unlike males, female coatis are highly social living in cohesive bands with their young most of the year and becoming solitary only to nest and give birth (Kaufmann, 1962; Chapter 2). Combined with the species' brief mating period, the result is a temporal and spatial clustering of receptive females that could be expected to fo s ter intense competition among males. Indeed, anecdotal observations of male coatis by previous researchers suggest such competition exists. Chapman ( 1938) and Kaufmann ( 1962) noted marked seasonal changes in male body condition. They and Gilbert (1973) also attributed a seasonal proliferation of serious injuries among males to intrasexual agonism during the mating period. This study was undertaken to determjne the extent and results of male reproductive competition in the coati and to evaluate the hypothesis that male coatis have evolved adaptations to maximize their competitive ability and minimize their as s ociated costs. Specifically, year round data on male behavior, physiology and anatomy were collected to test the prediction that male coatis exhibit periods of enhanced and reduced reproductive capability in a pattern which reflects that of female receptivity

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67 Methods General As part of a broader study of white-nosed coati reproductive biology in Tikal National Park Guatemala ( 17 N, 89 W), behavioral, morphometric and endocrinologic data were collected on 24 free-ranging adult male coatis (plus one found freshly road-killed) from June 1994 through Octob e r 1996 (exce pt as noted below) A mal e was considered adult once it di s persed from its natal b a nd which typically took pla ce 1 -2 months prior to the mating period in it s seco nd year of life (i.e., at 20-21 month s of age). Each male wa initially captured by live trap or (more often) blowgun and chemically immobilized by intramu sc ular injection of approximately 7 mg/kg Telazol (Fort Dodge Laboratories Inc. Fort Dodge IA). Anesthetized animals were tattooed and eartagged for identification weighed, mea ured and subjected to blood collection. Each male was al o visually examined to determine general physical condition, giving particular attention to the nature and abundance of any injurie s. Identified injuries were fresh car open wounds and mi ing body parts. Eighteen of the coati were additionally fitted with 90 g motionse n s itive radiocollars (Advanced Telemetry Sy s tem I san ti, MN) to enable s ub se quent location and recapture, and to confirm death if uch occurred. Individual males were recaptured by blowgun (never more often than monthly) for r esa mpling The research was conducted under Institutional Animal Care and Use Committee protocol #4084 from the Univer ity of Florida. All animal handling procedures were conducted in accordance with National Institutes of H ea lth standards. Behavior Four radiocollared males were habituated to the close presence of observers (see Chapter 2) and then utilized for behavioral data collection from September 1995 through Augu t 1996. Ob se rvation sessions were scheduled twice monthly for each available male (a lthough frequent radiotransmitter failure often resulted in fewer male s being available at any given time ), and in each case began as soo n as po s ible after locating the focal animal in the morning (typically

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68 0 6: 00 0 9: 00 ) a nd co n t inu e d fo r th e n ex t 46 h th e r ea ft er. Two o b se r ve r s we r e a l ways pr ese nt o n e o f w h o m was r e p o n s ibl e fo r m o nitorin g a nd r eco rdin g b e h avio r a nd th e o th e r fo r es tim a tin g th e di s tance tra ve l e d by th e fo ca l animal vi a a t a lly co unt e r as w e ll as ass i s tin g in k ee pin g th e a nim a l in s i g ht. Th e ame p eo pl e p e rform e d th e a m e o b se r va ti o nal ta s k s throu g h o ut th e tudy exce pt th a t o n e i g ht occasio n s s ub s titute s fill e d in fo r th e seco nd o b se r ve r af t e r cro s -t ra ining and ca lib ra ti o n sess i o n we r e co ndu c t e d t o e n s ur e uni fo rm i t y in coa ti t rave l di t ance e tim at i o n Durin g eac h o b e r va ti o n sess ion th e a m o unt of t i m e s p e nt b y th e f oca l m a l e w ith a coa ti b a nd ve r s u s a l o n e was r eco rd e d and the n a tur e a nd du ra ti o n o f all int e r ac ti o n s in vo l v in g th e m a l e we r e r eco rd e d A m a l e wa co n id e r e d to b e w ith a b a nd i f th e o b se r ve r fo ll ow in g h i m co uld see a n y b a nd m e mb e r t y pi ca ll y l ess th a n 30 m di s t a nt. Th e fr e qu e n cy a nd /o r durati o n o f o th e r b e h av i o r s we r e r eco r de d durin g th e fir s t 5 min of eve r y qu a rt e r h o ur. Th e fo ll ow in g t a t es a nd b e h av i o r s w e r e utili ze d in th e a n a l yses: A c ti ve d o in g a n y thin g o th e r th a n s ittin g o r l y in g d ow n Int erac ti o n t wo o r m o r e an im a l s a ppar e ntl y a lt e rin g th e ir b e h av i o r in r es p o n se t o o n e a n o th e r. Ago n is m agg r e i ve o r d e f e n ive int erac ti o n Fi g ht ago ni s ti c int erac ti o n in vo l v in g c h as in g, k n oc kin g eac h o th e r o ut o f tr ees, o r ac tual o r a tt e mpt e d bitin g a nd/ o r cl aw in g. App roac h o n e indi vi du al o ri e ntin g t owar d a nd m ov in g to w ithin t o u c hin g di s t ance of ano th e r. S ce ntm ar k bri e fly (a ppro x im a t e ly I ec) rubbing the ge nital r eg i o n aga in s t so me s ub s t ra t e. Fora ge bringin g th e n ose into cl ose pro x imit y o r manipul a tin g va ri o u s s ub t ra t es in a pp are nt searc h o f in ve rt e b ra t es o r fa ll e n f ruit o r s imilarly in ves ti ga tin g fruit b ea rin g p o rti o n s of pl a nt G roo m m a nipul a t i n g o n e's ow n b o d y p a rt s w ith mouth o r p aws T rave l m ov in g fr o m o n e pl ace t o a n o th e r w ith th e h ea d n o t o ri e nt e d t ow ard any s ub tr a t e, i e., n o t a pp are ntl y fo r agi n g. Rut ca JI produ c in g a rh y thmi c, s t acca t o, lo wpitch e d voca li za ti o n w hi c h a pp ea r e d t o fall int o K a ufmann 's ( 1 9 6 2) gruntin g" (p. 1 23) c l ass ifi ca ti o n ; di s tin gu i s h a bl e fr o m s imilar voca li za ti o n s (e.g., g runtin g in a l a rm ) b y th e co mbin a ti o n of it s s l owe r ca d e n ce, g r ea t e r l o udn ess a nd mu c h l o n ge r d ur a ti o n ( t y pi ca ll y seve r al m inut es a t a tim e) as we ll as b y th e s itu a ti o n in w h ic h i t was pr od uc e d

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69 Morphometry Each male's teeth were visually examined for damage (such as broken tips) during each immobilization, and intact lower canines were measured from gum line to tip with calipers. If both teeth were undamaged, lengths (to the nearest 0.1 mm) were averaged; otherwise only the length of the intact tooth was obtained. For comparative purposes, these same data were obtained for the teeth of females immobilized during a companion study An ind e x of each male's body fat level was determined at the time of immobilization. This was accomplished in the manner of Hossler et al ( 1994) by pinching a fold of the animal's skin at the back of each rear leg midway between knee and hip, and using calipers to measure the thickne ss of thi s fold to the nearest 0 1 mm. Measurements for the left and right thighs were averaged. One person wa s responsible for taking these mea s urements throughout the study. Testis s ize was also measured during each immobilization, and from the measurements an index of te s tis size was determined. The scrotal skin was pulled taut around each testis and three axes were measured with calipers to the nearest 0.1 mm: the longest dimension (L), the wide s t perpendicular dimension at midlength (W 1 ), and the midlength dimension perpendicular to both of these ( W 2 ). One person took all measurements. Opportunistic dissections of two freshly road-killed coatis (one radiocollared, the other previously uncaptured) revealed a layer of fat surrounding the testes ranging from scarcely visible on 7 June 1995 to as much as 5 mm thick on 9 January 1996 To compensate for this in approximating an animal's actual testis size, a correction factor Y = 0 77X 2 23 was subtracted from each of the aforementioned dimensions with X being the fat level index of the animal at the time of examination. (For this purpose, the fat level index of one coati for which leg pinch measurements were lacking was approximated from a regression of all available fat data on time of year.) The above equation represents the line connecting two points which were obtained by assigning the minimum and maximum fat level indices recorded in the course of the study Ys of O and l O (i.e., representing fat layers of O and 5 mm thick pre s ent on each side of a measured testis), respectively. This likely resulted in a

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70 con e rv a ti ve correction of te ticular dimen s ion s, as 5 mm may have been a low a pproximation of the m ax imum possible scro tal fat layer. The adjusted t e ticular dimen s ions were then plugged into the formula for calculating the volume of an ellipsoid, V = L x W 1 x W 2 x rr16 and the left and ri g ht te s ti s volumes o obtained were averaged to produce the testis s ize ind ex reported. (The raw data on coati t es ti s s i ze are pre ented in the Appendix.) Endocrinology Five to 10 ml of venous blood were drawn from a foreleg of each immobili ze d coati. Blood was kept in an ic e bath from the tim e of collection until the se rum could be eparated by centrifuge 2-4 h lat er and then froz e n. Fecal sa mple s were also collected whenever possible durin g immobilizations, and additional sa mpl es were obtained opportunistically from male s under ob erva ti o n In e ith er ca e, an e ntir e fecal depo s it was collected within 5 min of defecation and maintain e d at ambient t e mperature for 2-6 h, after which it was homogeniz e d and a ample of up to IO ml was fr oze n All eru m and fecal sa mpl es were first held in liquid nitrogen and then at the completion of th e fieldwork were tran s ferred to a -70 C laboratory ultracold freezer for s tora ge until th ey were a n a ly zed en masse byte to terone radioimmunoa say ( RIA ) Prior to analy is, a malfunction of the ultracold freezer re s ulted in all e rum and fecal sa mpl es thawing for a period estimated to have been 1-2 1/2 weeks The effect of thi s thawing on the androgen content of the amples is not known The endocrinologic data pr ese nted herein s hould therefore be con id e red repre se ntative of the pattern but not nece ssari ly of the actual t e to s t ero ne l eve l s c irculating in or excreted by coatis. Serum Testosterone RIA. Serum te to s t ero ne concentrations were determined via an RIA procedure (Guillette e t al., 1996) utilized pr ev iou s ly for a wide variety of p ec ies and validated for coati se rum. Duplicate 50 I aliquots of se rum were extracted twice with 2.5 ml 30 C e thyl ether, dried und e r filt e r e d air and reconstituted in I 00 I borate buff e r ( 0.5 M, pH 8.0). To the se were added 100 I bovine se rum albumen so lution (0.75% BSA in borate buffer)

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71 200 l te s tosterone antiserum (T3-125 at a final concentration of 1:18,750; Endocrine Sciences, Calaba sas Hill s, CA ) and I 00 I [ l ,2,6,73 H]-te s to s terone radiolabel (TRK-921 diluted in borate buffer to approximately 1 3,000 cpm/100 I; Amersham Life Science, Inc ., Arlington Heights, IL) A ssa y tub es were then vortexed briefly and incubated overnight at 4 C. Bound-free se par a tion was achieved by adding 500 I 5% c h arcoal/0.5% dextran in pho phate-buffered sa]jne and th e n centrifuging th e tube for 30 mjn a t 2000 g, 4 C. The s upernatant was d eca nted diluted with 5 ml sc intillation cocktail (Scintiverse BD, Fi s her Scientific Fair Lawn, NJ ) and counted on a sc inti II at ion counter ( B ec kman LS 580 I, Beckman Coulter Inc., Fullerton, CA) Count sper-minute were ave raged for eac h pair of duplicate s, and the se were s ubjected to Rod b a rd and L ewa ld s ( 1970 ) l o g it tran sfo rmation T es to s t e rone concentration were det e rrruned by comparison of tran sfo rm e d d a t a to a l ogit-log plot of IO s tandard s, ranging from 3.125 pg to 1600 pg h ormone p e r assay tube whic h were a l so run in duplicate in each assay. Naturally low, m e dium and hi g h te s to s t e rone concen trati on se rum pool s were also run in duplicate in each assay as a c h ec k on int e rassay va ri a nc e. Final t es to s terone concentrations were calcu l ated a ng/ml se rum and are r e port e d without correction for assay acc uracy Two assays were conducted to ana l yze sa mple s, and three more to complete validation. For all samp le pairs th e mean( SEM) duplicate coefficient of variance (CV) was 3 5 0.4 % and r > 0 99 for the s tandard curve fit in a ll assays. Non-specific binding averaged 2.6 0 6 % Int e r-a ssay CV s in low m e dium and high pool s of se rum were 17 %, 7 % and 1 2%, re s pectively. The mjnimum detectable concentration of t es tosterone, ba se d on the mean 2SD percentage of bound radiolabel observed in fiv e pairs of charcoal-stripped se rum, wa s 0.04 ng/ml. A s tandard curve prepared by s pikin g charcoal-stripped seru m (fou r pair s at each standard concentration) was parallel to that made u s ing borat e buffer (test for homogeneity of s lop es F[l 161 = 0.14, P > 0.75) ; assay accuracy as det e rmin e d by s pike-reco ve ry wa s I 02 % S e rial dilutions ( one pair each at 30 I, 50 I and 70 l) of l ow, medium and high pool s produced flat lin es with CVs of 13 %, 8 % and

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72 4 % r es p ec ti ve ly. Intra-a ssa y CV s in l o w m e dium and hi g h pool s ( fi ve p a ir s of e a ch pool) were 6 % 6 % and 7 %, r es p ec tiv e l y Cro ss -r eac ti v iti es gr e ater th a n 1 % r e p o rt e d by the anti se rum s manufactur e r w e re : dihydrot es to s teron e 44 0 % 8-1-te s to s t e rone 41.0 % o-1-dihydrote s to s terone 1 8 .0 % 5a-andro s t a n3 ~ 17~ di o l 3 .0 % 4 -a ndro s ten-3~, 17~-di o l 2 .5 % o-4-andro s tenedione 2.0 % a nd 5~-andro s t a n-3~ 17~ diol 1.5 % Fecal Testosterone RIA. Feca l t es to s t e ron e co n ce ntrati o n s we r e d e t e rmin e d mu c h as d esc rib e d for se rum e x ce pt feca l s t e roid ex tra c tion wa s ac c o mpli s h e d v i a a s lightly modified ve r s i o n o f th e s h o rt m e th o d d esc rib e d in W asse r e t al ( 1994 ), a nd thi s proc e dure a s well a s the s ub s e qu e nt assa y we r e va lid a t e d fo r coa ti feces F e c a l s ampl es we r e l yo phjli ze d a t -55 C und e r va cuum excee din g I 00 x I 03 mB a r a nd th e n g round to fin e powd e r ( r e m o ving di s c e rnible ex t ra n eo u s m a t e ri a l s u c h as s ee d s, in s e ct part s, e t c ). F o r eac h sa mpl e, 0.1 g o f powd e r w as li g htly b o il e d for 20 min fir s t in 5 ml and s ub se qu e ntly in 2 .5 ml o f 90 % e thanol and the s up e rn a t a nt was dri e d und e r filt e r e d a ir a nd r eco n s titut e d in I ml a b so lut e m e thanol. The m e th a n o l s u s p e n s i o n w as dilut e d 100 I t o 7.4 ml borat e buff e r and 100 I o f the r es ulting so lution w e r e pipett e d int o dupli ca t e tub es a nd tr ea t e d as p e r r eco n s titut e d se rum e xtract in the RIA d esc rib e d a b ove. Th e 10 s t a ndard s utiliz e d in the fe ca l RIA ran ge d from 1.5625 p g to 800 p g hormone p e r a ssa y tub e Fin a l conc e ntration s were calculat e d a s ng/ g dri e d fece s, and are r e p o rt e d with o ut co rr ec ti o n fo r assa y ac cura cy Sampl es w e r e an a l yze d in two a ssays, a nd v alidation was c ompl e t e d in anoth e r four Th e m ea n CV for sa mpl e duplic a t es w as 1 8 0 2 % a nd r > 0 99 for th e s tandard cur ve fit in all assays. M ea n n o ns p e cific bindin g wa s 0 6 0 1 %. Int e rassa y CV s in lo w, medium and high f eca l pool s w e r e 7 %, 9 % a nd 8 % r es p e cti ve ly. Th e mjnimum d e t e ct a bl e concentration of t es t os t e ron e, b ase d o n th e m ea n 2 SD p e r ce nta ge o f bound ra diol a b e l ob se r ve d in s ix p a ir s of a n a turally ve r y low t es to s t e ron e fe cal pool w as 17 ng/g. A s t a nd a rd curv e pr e par e d by s piking the ve ry lo w p oo l ( four p a ir s a t eac h s tandard co n ce ntration ) did not diff e r s t a ti s tically from th a t

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7 3 m a d e u s ing borat e buff e r ( t es t for h o mo ge n e it y of s lope s F l 1 161 = 0 5 8, P > 0 5 ); s pik ere c overy acc ura cy was 111 < S e ri a l diluti o n s o f a m e dium pool ( o n e p a ir eac h a t 5 0 75 I 00 1 2 5 I and 150 I m e thanol s u s p e n s i o n di lut e d in borate buff e r to a total of 7 .5 ml s olution ) produced a fl a t lin e with a CV o f 8%. Intr a-assa y CV s in l o w m e dium an d hi g h p oo l s ( fi v e pair s of e ach po o l ) w e re 3 %, 6 % a nd I %, r es p ec ti ve ly Statistical Analyses Ob se rv a ti o n o bt a in e d in co mp a ni o n s tudi es o f f e m a l e coa ti co ndu c t e d o ve r th e e ntire 2 y ea r s ojourn in Tik a l ( B oo th Bin cz ik e t al ., 2 004 ; Ch a pt e r 2) we r e u se d t o d e line a t e thr ee di tin c t a nnu a l p e ri o d t o a id in d a t a pr ese nt a ti o n a nd a n a l y i : Th e non-rut period co mpri se d th e n ea rly 11 month s of th e yea r th a t occurr e d out s ide of th e pr e -m a tin g a nd m a tin g p e ri o d fr o m 29 Fe bru a r y o r I M a r c h ( d e p e ndin g o n yea r ) through 2 2 Janu a ry Th e pre-mating p e riod co mpri se d th e thr ee w ee k s l ea din g up t o th e m a tin g p e riod durin g w hi c h multipl e m a l e coa ti s (as o pp ose d t o o n e o r n o n e) we r e r egu l a rly d e t e ct e d a cc o mp a nyin g a g i ve n b a nd a t a g i ve n tim e, fr o m 23 Janu a r y throu g h 1 2 F e bruary. Th e mating period co mpri se d th e 1 6 d ays durin g w hi c h co pul a ti o n s we r e n o t e d from 1 3 F e bru a ry throu g h 2 8 F e bru a ry In so m e a n a l yses d a t a fo r th e pr e -m a tin g and m a tin g p e ri o d s we r e co mbined into a ingle rut peri o d w hi c h was th e n co mp a r e d to th e n o n rut p e ri o d. Wh e n eve r p oss ibl e, eac h m a l e w as sa mpl e d r e p ea t e dl y w ithin eac h period eve ry y e ar, but was in ge n e ral r e pr ese nt e d b y o nl y a s in g l e d a t a p o int p e r pe ri o d in a g i ve n t a ti s ti ca l t e t. Thi s wa s a ccompli s h e d by a ve ra g in g a m a l e s s ub sa mpl es wh e r e c oll e ction e ff o rt w a s e qu a l (e g., in th e case o f multipl e imm o bili za ti o n s) a nd a ddin g s ub sa mpl es w h e r e it wa n o t (e.g in th e ca s e of multipl e ob se r va ti o n da ys o f va r y in g l e n g th s) Th e exce pti o n was in eva lu a ting th e c o rr e l a tion b e tw ee n se rum and feca l t es to s t e ron e c o nc e ntr a tion s, in whi c h a ll sa mpl e p a ir s ( i .e., e rum and

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74 feces co ll ec t e d fr o m th e sa m e a n i m a l a t th e sa m e tim e) we r e tr ea t e d as ind epe nd e nt ; indi v idu a l co ntribution s t o thi s d a t a s e t r a n ge d fr o m o n e t o fi ve s ampl e pa ir s pe r r ep r ese nt e d m a l e. Sok a l and R o hlf ( 19 8 1 ) g uid e d a ll s tati s tic a l e ffort s, a nd STATGRAPHICS Plu s 5.1 sof t ware (Manu g i s t ics In c ., R ockv ill e, MD ) ai d e d co mp u t a ti o n D a t a e t s fo r co mp a rin g th e thr ee p e riod s fir s t und e r we nt a b a tt ery o f t es t s fo r h o m osce d a ti ci t y a nd n o rm a lity ( u s in g a co n e r va ti ve P a $ 0 1 0 l eve l of r e jec ti o n ), a nd we r e s ubj ec t e d t o s t an d a rd t ra n sfo rm at i o n i f s u c h we r e indic a t e d. Wh e n raw o r t ra n fo rm e d d a t a m e t p arame tr ic a s sum pti o n t wo way AN OV A s we r e co ndu c t e d tr ea tin g p e ri o d a nd m a l e a m a in e ff ec t s ( m a l e e ff ec t s we r e n eve r found t o b e i g nifi ca nt an d are n o t d isc u ss ed furth e r ); o th e r wise th e da t a we r e a n a l yze d v i a Kru k a l W a lli s t e t s Fi s h e r 's L eas t S i g nifi ca nt Diff e r e n ce pro ce dur e wa s u s e d t o di tin g ui s h a m o n g p e ri o d w h e n ove r a ll s i g ni ficance wa s d e t ec t e d Twot a il e d /t e s t s w e r e co ndu c t e d in s t ea d o f AN OV A s in th e fe w c ase s w h e r e o nl y t wo gro up s we r e co mp a r e d. A P 0 $ 0.05 l eve l o f s i g nifi ca n ce w as ut i li ze d in all r e p o rt e d s t a ti s ti ca l t e t s Results Mal es int erac t e d o n 26 (9 0 % ) o f th e 2 9 occas i o n s w h e n th ey ca m e w ithin s i g ht o f o n e a n o th e r durin g sc h e dul e d o b e r va t io n s. A ll m a l em a l e int e r ac ti o n s qui c kl y esca l a t e d int o r e l a ti ve ly bri e f but int e n se ph ys i ca l a lt e r ca ti o n s w ith fe w o r n o a ppar e nt pr e liminari es M a l e coa ti s fought s p ora di ca ll y th ro u g h o ut th e yea r but th e fr e qu e n cy o f s u c h co nt es t s in c r ea e d durin g th e pr em a tin g p e ri o d a nd p eake d durin g th e m a tin g pe ri o d (F i g. 41 ) Th e fr e qu e n cy o f m a l emale a go ni s m in th e thr ee d e fin e d p e ri o d s o f non-rut pr em a tin g a nd m a tin g co uld n o t be s t a ti ti c all y di s tin gu i s h e d ( H [ H 3 1 = 4. 66 P = 0 0 97). H oweve r foc u s in g in s t ea d s impl y o n a c omp a rison o f n o n rut to rut ( th e l a tt e r b e in g pr em a tin g a nd m a tin g c ombin e d ) r evea l e d fi g hting t o b e s i g nifi ca ntl y m o r e co mm o n durin g rut ( 0 .4 1 0 1 8 fi g ht / hr ve r u 0 0 4 0 0 I fi g ht /hr durin g non-rut ; p a ir e d t l 3 l = 3.63, P = 0 0 36).

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75 0.8 -MaleMale Agonism 0.6 -----C/'J 3 Q) -0.4 ;:j 0 (.) 4 =+t:: 0.2 ~4 0 I I 10 Injuries 8 6 2 18 15 0 Non-Rut Pre-Mating Mating Figure 4-1. Mean( SEM) frequency of intrasexual agonistic interactions and injuries observed among adult male white-nosed coatis in Tikal National Park, Guatemala, September 1995 September 1996 and June 1994 October 1996, respectively. Number of males sampled in each of the three defined periods (non-rut: 29 Feb / I Mar 22 Jan; pre-mating: 23 Jan 12 Feb; mating: 13 Feb 28 Feb) indicated on bars.

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76 The incid e nc e of injurie s noted during immobilization s rose s harply during the mating period (Fig. 4-1; H [ 1 8 1 5 6 1 = 8.74, P = 0.013). Injurie s mo s t often affec ted the head, chest or forelimbs and were frequently seve re including badly broken or missing teeth (especially canines) and mi ss ing claw s or entire toes as well as a variety of deep fle s h wounds. Remarkably none of the examined animals died as a direct consequence of s uch injuries, but two of the thr ee natural death s recorded among radiocollared male s durin g the course of the s tudy occurred in February 1995, i.e., during rut of that year; the third death occurred in August 1996. Unfortunately it was not po ss ible to reach the carcasses quickly e nough to determine the exact timing or cause(s) of de a th A comparison of male and f e male coati d e ntition revealed the male s' lower canine teeth to be s ub s tantially lon ge r (15 5 0.4 mm for 22 male s versus 8.7 0.2 mm for 49 females; t [ 6 9 1 = 18.40 P < 0.001). Males s pent s ignificantly more time with band s during the m a ting period than at other times of the year (Fig. 4-2 ; F( 2 51 = 6.16, P = 0 045 ). P e riod s did not differ in term s of male s approaching females either quantitatively (Fig 4-2; F[ 2 5 1 = 0 .5 7, P = 0 618) or qu a litativel y; regardless of time of year such approaches were mo s t often rebuff e dso metime s violently. Occasionally females allowed brief perinea! sniffing by males, however or le ss often inve s tigated the males in a similar fashion them se lve s. Females also so metime s initiated or reciprocated allogrooming with males. The se affiliative behaviors were infrequ e nt and s poradically distributed throughout the year. Males scentmarked a t a high rate throughout the year against the ba se of a living or fallen tree or on a log or some other relatively low-lying feature of the terrain being traver se d; they also occasionally climbed into and traveled through the forest canopy see mingly ju s t to r e peatedly scentmark the large lower branches along some di s tance before returning to the ground. Although scentmarking was highe s t during the mating period, no time of year could be statistically di s tingui s hed from another (Fig. 4-3; Fl 2 5 1 = 2.60, P = 0 .168).

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77 80 rJJ 60 ro Male-Band T3 Association -co 0) 40 8 4 T4 0 20 0 1.2 rJJ -Approaches 0.9 co T2 4 $-; 0.6 ......._ -~ rJJ 0) 3 ro 8 0.3 0) =+t 0 Non-Rut Pre-Mating Mating Figure 4-2 Mean( SEM) percentage of time adult male white-nosed coatis spent with bands and frequency with which males approached females in Tikal National Park, Guatemala, September 1995 September 1996. Number of males sampled in each of the three defined periods (non-rut: 29 Feb / 1 Mar 22 Jan; pre-mating: 23 Jan 12 Feb ; mating : 13 Feb 28 F e b) indicated on bars.

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50 (I) a 40 30 (I) > +,.I u < 20 ;.... ::r= ---::t:f_: 10 0 12 (I) a 9 (I) > -~ 6 u < 0 3 0 78 Scentmarking 3 -~ T4 4 Calling -3 -4 4 Non-Rut Pre-Mating Mating Figu r e 4-3. Mean( SEM) frequency of scentma r king and percentage of active t ime spent calling by adult male w hi te nose d coatis in Tikal National P ark, Guatemala, September 1 995 September 1996. Num b er of males sample d in each of the three defined periods (non-rut: 29 Feb/1 Mar 22 Jan; pre-mating: 23 Jan 12 Feb; mating: 13 Feb 28 Feb) indicated on bars.

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79 The rut call was heard only during the pre-m a ting and mating p e riods (es pecially the latter; Fig. 4-3; H 14 4 3 1 = 6 14, P = 0.046) and elicited clo se inve s tigation by both females and males The area occupied by Tikal's large bands (up to 162 females and maturing young; Booth Binczik, 2001)-and thus also the males accompanying them-as the animals moved through the forest precluded two human observers quantifying many aspects of the mating pattern particularly when those observers were concentrating primarily on the behavior of a single focal animal. However it was evident that up to severa l males (at least four could be conclusively identified in one in s tance) were calling at the sa me time from individual perches in the lower canopy directly or peripherally over a given band foraging on the ground below, changing their perches as neces sary to keep up with the movement s of the band. On at lea s t s ix occasions individual females were see n leaving their bands and going to calling male s, and at lea s t three times the females s tayed with the males to copulate Calling males usually appeared to ignore one another, but on at lea s t two occasions individual males were also see n briefly le av ing their calling stations to chase or fight with others calling nearby ; mo s t recorded fights occurred when males were not calling. Males in Tikal s pent significantly less time grooming during the mating period than at any other time of year (Fig. 4-4; H 14 ,4 3 1 = 6.66, P = 0.036). Periods did not differ appreciably in terms of time males spent foraging or distances males traveled (Fig. 4-4; for foraging H 14 4 31 = 2.64, P = 0.268 ; for traveling F 12 51 = 3.36, P = 0.119). Body fat levels measured in immobilized males rose s teadily throughout mo s t of the year but fell sharply at the beginning of the pre-mating period, ultimately reaching a low at the end of the mating period that was only 20-25 % of the peak achieved at the end of the non-rut period (Fig. 4-5) Fat levels were significantly lower during mating (3.8 0.6 mm versus 7 8 0.7 mm and 7.7 0.8 mm during non-rut and pre-mating, re s pectively; H[l 8 1 5 61 = l 1.27, P = 0 004)

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80 12 (I.) 4 Self-Grooming 8 9 ..... (I.) > ..... 6 ...... u 4 -,4 -..... ...... u 40
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81 The testes of immobilized males increa sed rapidly in volume with the beginning of the pre-mating period, peaked late in pre-mating or early in the mating period, decr ease d nearly as rapidly throughout the remainder of mating and then continued decreasing more s lowly well into the non-rut period (Fig 4-6). The males' testes were significantly smaller during non-rut ( 1.8 0.2 x 10 3 mm 3 versus 2 9 0.3 x 10 3 mm 3 and 3.3 0.2 x 10 3 mm 3 during pre mating and mating, re spec ti ve ly ; F 1 2 1 3 1 = 8.85, P = 0 004) Hi s tolo g i ca l examination of testicular parenchyma obtained from road-killed males on 7 June 1995 and 9 January 1996 rev ea led the presence of all cell type s-i ncluding mature spermatids-in the se miniferou s tubule s a t both times of year. Serum and fecal te stos terone concentrations were highly correlated (r = 0.86 for 28 sa mple pair s from 16 male s; t 1 2 61 = 8.42, P < 0 .00 I) and di s played a c lear circannual pattern (Fig. 4-7). Specifically te s tosterone levels rose gradually beginning seve ral month s prior to the pre mating period, s piked s uddenly to a peak near the e nd of pre-mating and then fell even more s uddenly back down to ba se line by the end of the m a ting p er iod The three p erio d s of the year differed significantly whether se rum and fecal t es to s t ero ne va lu es were treat ed separa t e ly or combined (for combined data in which serum values (T ) were converted to fecal equivalents (T 1 ) via the regression formula T 1 = 52.97T + 51.07 non rut was 172 J 9 ng/g pre mating 549 63 ng/g and mating 358 106 ng/g; H 11 9 16 8 1 = 16.66 P < 0.001). Discussion Male-Male Agonism Lacking the s howy weaponry seen in many rutting s pecie s (such as antlers, horns and tusks), the male coati nonethele ss appears well-equipped for intra sex u a l combat. Both sexes rely on their teeth as well as their powerful forelegs and long, s harp claw s when fighting, but the male's dentition may be s pecially de s igned for this purpose given the degre e of lower canine tooth sex ual dimorphi s m observed in the present s tudy

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----16 s s 14 '-" ..c:: 12 0 10 01) 8 Q) 6 '"d 4 ::r: 2 82 Wet Season Dry Season ooo 0 mO Coe 0 0 0 0 '2> 0 0 0 0 0) 00 0 ~o 0 t)O 000 0 o crP c9o 0 0 0 'e)O 0 ([) Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Date Figure 4-5. Annual body fat profile exhibited by adult male white-nosed coatis in Tikal National Park, Guatemala, July 1994 through October 1996. Based on hind leg pinch thickness measured in 42 immobilizations of 18 animals during non-rut period (unshaded background; 29 Feb / I Mar 22 Jan), 16 of 15 animals during pre-mating (lightly shaded; 23 Jan 12 Feb) and 6 of6 animals during mating (more darkly shaded ; 13 Feb28 Feb)

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6 0 Wet Season 0 0 0 d)O 0 0 83 Dry Season 0 0 0 0 i~o~g ~o 0 0 0 0 aj) 00 cf)o 0 0 oo 0 0 Q) Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Date Figure 4-6. Annual profile of testicle size exhibited by adult male white-nosed coatis in Tikal National Park, Guatemala, June 1994 through October 1996. Individual testis measurements were corrected for the animal's estimated testicular fat layer (see Materials and Methods) prior to ellipsoid volume calculation. Profile based on 45 immobilizations of 19 animals during non-rut period (unshaded background; 29 Feb / l Mar-22 Jan) 16 of 15 animals during pre-mating (lightly shaded; 23 Jan l 2 Feb) and 6 of 6 animals during mating (more darkly shaded; 13 Feb 28 Feb).

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20 16 12 8 4 0 1500 1200 900 600 300 0 84 Wet Season Dry Season Serum T Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Fecal T 0 0 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Date Figure 4-7. Annual serum and fecal testosterone (T) profiles exhibited by adult male white-nosed coatis in Tikal National Park, Guatemala July l 994 through October 1996. Non-rut period (29 Feb / 1 Mar 22 Jan) indicated by unshaded background pre-mating (23 Jan 12 Feb) lightly shaded and mating (13 Feb 28 Feb) more darkly shaded. Serum profile based on 42 samples from 18 animals during non-rut, 16 from l 5 animals during pre-mating and 6 from 6 animals during mating; fecal profile based on 70 samples from 13 animals, 8 from 8 animals and 8 from 5 animals respectively. Twenty-eight paired samples (i e. serum and feces collected from same animal at same time) from 16 animals represented by solid symbols Curve visually fitted to all combined and smoothed data.

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85 Oth e r than th ei r potential u se fulne ss in combat, no explanation for the m a le coati's enlarged canines i s a pparent. Although Smythe ( 1970) s peculat e d that male s on Barro Colorado I s land (BCI), Panama, might pursue larger prey than females, this idea was not borne out in s ubsequ e nt s tudie s at that locale (Gompper, 1996) nor did it appear to pertain in Costa Rica (Saenz, I 994) or Tikal (Booth-Binczik, 200 I) In a comparative analysis of sex ual dimorphi s m in carnivore dentition, Gittleman and Van Val ken bur g h ( 1997) likewi se found that dietary difference s b e twe e n the sexes were reflect e d in the s i ze of the carnassials rather th a n th e ca nine s. In s tead Gittleman and Van Valkenburgh (1997) determined that carnivore canine tooth dimorphi sm correlated with mating sys tem with more polygynous s peci es ex hibitin g greater dimorphi sm Such spec i es lik e ly experience particularly inten se competition a m o n g m a l es for mate s (E mlen and Oring, 1977 ), s ugge s ting the e nlar ge d canines' princip a l role I i es th erei n It may be r e levant in thi s re s pect to note that the ratio of male:female lower canine s iz e found among coatis in the present study ( 1 78) exceeded that displayed by any of th e 45 carnivore s pecie s Gittlem a n and Van Valkenburgh ( 1997 ) exa mined and that the hi g h es t ra tio they di scove red ( 1 62) b e longed to Nasua nasua, a South American congener of th e white-nosed coati which ha s been much le ss s tudied but is believed to be s imilar in many re s pect s (E mmon s, 1990 ). Ba se d on the frequency with which Tikal's coati males were observed fighting and the frequency and severi ty of the injuries they s u s tained pre s umably as a re s ult it appears that males of this s pecie s do indeed face considerable and costly intra sex ual competition. All male-male interaction s observed in the pre se nt s tudy were agonistic. Mo s t male-mal e agonism occurs during the rut and, judging from the data on injurie s, is mo s t violent during the mating period. Kaufmann (1962) reported that all male-male coati encounters he saw while conducting observations of females on BCI were similarly agonistic, but s tated that actual ph ys ical contact was uncommon outside of the mating period, when mo s t fight s occurred. Chapman ( 19 38) and Kaufmann ( 1962 ) attributed a seasona l proliferation of injurie s among BCI' s male coatis to intra sex ual agonism assoc i a ted with mating a nd Gilb e rt ( 1973) reported a s imilar ph e nomenon

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86 among male coatis in Arizona. Chapman ( 1938 ) a nd K a ufmann ( 196 2) a l so d eta il e d the seve rity of the animals' injuri es, noting their prev a l e nce on the head s and forelimbs, and remarked upon the animals' exceptional recuperative powers. Such healing ability notwith s tanding Chapman ( 1938 ) reported the permanent partial blindne ss of a se mi-tame male under hi s casual observation after one s uch seaso n and believed the animal's ultimate di sa ppearance two years l a t e r may have b ee n the re s ult of it s uccumbing to injuri es obtained in a s ub se qu e nt m a tin g p e riod. Male-male combat i s also common-and often re s ult s in the injury or d ea th of combatants-in rutting s pecie s. Indeed it might eve n be considered a hallmark of thi s reproducti ve patt e rn. As in th e pre se nt s tudy, fighting a mong male s of s u c h spec i es ge n e rally sp ik es s hortly b efore an d during th e ir bri ef annual mating p e riod s ( Wilkin so n and Shank, 1976; Clutton-Brock et al., 1982 ; Komer s e t a l. 1994), and in so me cases appears to cause a su b s tantial proportion of adult male mortality (Leslie and Jenkin s, 1985 ; Hall-Martin 1987 ; Pool e, 1989 ). In contrast, male-male agonism in carnivore s pecie s other than the coati tend s to b e centered on territory es tabli s hm e nt (e.g., tiger s, Panth era ti gr i s, Smith, 1993 ) or acquiring control of a socia l group (e.g., lion s, Panth era Leo, Bygott et al., 1979 ; Packer and Pu sey, 198 2) before mating opportunities arise, and conflicts during the mating period it se lf are le ss common. Male-Female Affiliation Band s of female coatis were typically the focal point s of male-male e ncounter s in Tikal, and to so me extent the greater incidence of fighting among males during the mating p er iod might s imply reflect their incr eased opportunity to engage in s uch activity at that time The pre se nt s tudy revealed that male s s pend more time in the company of band s during the mating period than at other time s of the year, and the number of males accompanying a given band at a given time varies accordingly; whereas band s were u s ually seen with only one ( but not n ecessar ily the sa me one) or no male in attendance throughout most of the year, during the mating p e riod as many as nine male s have been s imultan eo u s ly observed with a s ingle band ( Booth-Binczik et al., 2004).

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87 Kaufmann (1962) also noted an increase in male-band spatial affinity at about the time of reproduction among coatis on BCI, but with some differences. He believed that males there only rarely associated with bands outside of what he considered to be the coatis' month-long mating period (essentially a combination of the pre-mating and mating periods of the present study), and that one particular male remained with each band almost constantly throughout that time, perhaps copulating with all females therein. (It is unclear whether he ever observed successful copulation; Chapter 2.) Kaufmann ( 1962) acknowledged, however, that unobtrusive males might have come and gone undetected because only the bands were habituated to his presence and served as the foci of his observations That admonition was later borne out by Gompper et al. ( 1997), who found that the males most commonly seen with bands on BCI during the mating period nonetheless did not sire most of the young subsequently produced by females in those bands. Booth-Binczik (200 I) further demonstrated multiple paternity not only within bands but also within individual females' litters in Tikal. One might expect that male coatis would capitalize on their closer association with bands during the mating period by directly initiating interaction with the females therein more frequently but this appeared not to be the case in Tikal. There, males approached females least during the mating period, and their approaches were generally rebuffed then just as they were at other times of the year. This finding contrasts somewhat with Kaufmann's (1962) report that males in association with bands during the coati mating period on BCI spent much of their time pursuing females, and were more often amicably received by females then compared to other times of year. He described almost all close male-female encounters occurring outside of the mating period as hostile. lntersexual perinea) sniffing and allogrooming were reportedly especially common at the beginning of the mating period. Russell ( 1981) observed less agonism and more allogrooming between the sexes not only during BCI's mating period but also for two months prior, which he caJled a period of courtship and reported friendly male-female encounters at other times of year

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88 as well. In Arizona Gilbert ( 1973) believed that males required acceptance by bands in a social context prior to the mating period, simply approached and mounted receptive females during that period (though it is unclear whether any successful copulations were actually observed; Chapter 2), and remained with bands for months thereafter. It is well established that males of rutting species spend more time with females while rutting than at other times of year (ungulates reviewed by Main et al. 1996; Ruckstuhl and Neuhaus, 2000; African elephants, Loxodonta africana, by Poole, J 987). They are quite variable, however, in the strategies they employ to secure access to receptive females. Some maintain harems (Struhsaker 1967; Clutton-Brock et al 1982; Lovari and Locati, 1991 ), others follow and defend individual females (Lent, 1965; Lott, 1981; Lovari and Appollonio, J 994 ), and others defend territories and wait for females to enter (Jarman 1979; Miura, 1984; Schuster, 1976) Advertising At least in Tikal, the male coati appears to depend more on advertising than on directly pursuing receptive females. Whether its s centmarking behavior exemplifies this strategy remains as yet unclear. Although the frequency of scentmarking behavior did not vary over the course of the year, the true significance of this behavior may lie in its quality rather than quantity. An unusually strong odor was incidentally noted during some male immobilizations and observations during the mating period. The author therefore believes that scentmarking may yet be found to be an important component of the male coati's rut. Lending some support to this contention, Kaufmann ( 1962) remarked upon male coatis on BCI "urine-rubbing" (p 130) at the base of or in trees, especially as the males approached bands of females during the mating period. TechnicaJly speaking, though, it should be noted that it has not yet been determined whether males of this species employ urine, some other product(s) or a combination thereof in scentmarking. Indeed, the procyonids have been studied far less than some other carnivore families in this regard, but males of the coati's congener N. nasua reportedly

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89 behave similarly (B Hirsch, pers. comm.) and have sebaceous preputial glands that are believed capable of producing copious s ecretory material (Shannon et al ., 1995). Scentmarking is considered ubiquitous among terrestrial mammals (Gosling and Roberts, 2001), but an accentuated form/degree of it may be another hallmark of rut. Typically, specialized glands suddenly proliferate or activate in the rutting male (e.g. the poll glands of the camel, Camelus drom e darius, Rai et al., 1996; temporal glands of the Asian elephant Elephas maximus, Eisenberg e t al., 1971; a variety of glands in cervids, reviewed by Mi.Hier-Schwarze, 1987), and the animal anoints itself and/or various natural s ignposts with the glands' redolent products Urine is simjlarly u s ed by rutting males of many s pecies (Poole and Moss 1981; Clutton-Brock e t al. 1982 ; Miura, 1984) and at lea s t in the ca s e of the fallow deer (Dama dama ) its particularly strong odor appears to be due to the contribution of preputial glands that activate at that time (Kennaugh et al. 1977). More readily detected by an observer in Tikal than any coati odor is the male's rut call. This behavior feature s prominently in the species' mating pattern there, which has been described as a kjnd of mobile lek (Booth-Binczik et al. 2004) Nothing resembling such has yet been reported for coatis outside of Tikal. However, Kaufmann ( 1962) noted that males interacting during BCI' s mating period often emitted a "loud, rapid grunting" (p. 125), and on one occasion during that period he witne ss ed a male following and similarly vocalizing from a variety of perches near a band Has s and Roback (2000) also reported that the male of a copulating pair of coatis in Arizona made what they interpreted as "alarm grunts (p. 329) toward an approaching female. These observations notwithstanding, it seems unlikely that such a flamboyant phenomenon would have thus far been overlooked, particularly on BCI where so much time has historically been inve s ted in s tudying this and other species' behavior. It may be that telling by male coatis in Tikal repre s ent s a behavioral extreme compared to other populations which have been examined.

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9 0 Pl as ti c it y i n m at in g pa tt e rn s m ay b e th e rul e a m o n g un gu l a t es th a t l e k Fa ll ow d eer, fo r exa mpl e, utili ze a t l eas t seve n di ffe r e nt m a tin g sys t e m s und e r d i ffe r e nt eco l ogica l co ndi t i o n s ( L a n g b e in a nd Thir goo d 1 989) an d topi ( D a m a li scus k or ri gum; G os lin g, 1991 ) and bl ac kbuck (A nt i / ope cervicapra; I svaran, 2 00 5) s h ow a lm os t e qu a l fl ex ibil i t y. Ad ve rti s in g ca ll s m ay b e th e s in g l e c h arac t e ri s ti c m os t s t ro n g l y id e ntifi e d wi th rutt i n g m a mm a l s. In fac t th e wo rd rut o ri g in a t es in th e L a tin ru g i re m ea n i n g t o roa r Acco rdin g l y, s u c h ca ll s h ave b een wi d e l y r e p o rt e d a nd a r e ev id e nt in a ll t ypes o f m a t i n g sys t e m s : t e rrit o ri a lit y (Es t es, 1969 ; Miu ra, 1 984), h a r e m h o ldin g ( Struh s ak e r 1 96 7 ; L ova ri a nd Lo ca ti 1991 ), a nd fo ll ow in g ( P oo l e 1 987 ; B e r ger a n d Cunnin g h a m 1 99 1 ) It i s a m a tt e r o f d e b a t e to w h a t ex t e nt e ith er o l fac t o r y o r a udit ory s i g n a l s a r e dir ec t e d a t p o t e nti a l m a t es ve r s u s ri va l m a l es Mos t r esea r c h e r s h ave co nclud e d th a t b o th rut ca ll s a nd sce ntm ar k s serve t o n o ti fy ri va l s o f a m a l e s ph ys i ca l co n d iti o n a nd th e a tt e nd an t ri s k s of c h a ll e n g in g him (e.g C lutt o n-B roc k a nd Alb o n 1 9 7 9; B owyer a nd Kit c h e n 1 98 7 ; B erge r a nd Cunn i n g ham 1 99 1 ) Co n ve r se l y, Hur s t a nd Ri c h (1999) a r gued th a t t h e prim ary fun ct i o n of sce ntm a rkin g i s t o a d ve rti se qu a lit y t o p o t e nti a l m a t es. Th e r e i s ev id e n ce s upportin g b o th p o int s of v i ew M cE lli go tt an d H ay d e n ( 1 999) fo und th a t th e voca li za ti o n ra t e of ruttin g fa ll ow d ee r was a ff ec t e d by w h e th e r o th e r m a l es we r e n ear b y, but n o t b y w h e th er th e c a llin g m a l e was a bout t o co pul a t e o r h a d ju s t d o n e so In s tudi es o f e l e ph a nt s (w hi c h di s pl ay an asy n c hron o u s rut kn ow n as mu s th ) h owever, fe m a l e A fri ca n e l e ph a nt s p refe rr e d t o m a t e w ith mu s th m a l es ( M oss, 19 83) a nd a pp a r e ntl y u se d b o th urin e tr ai l s a nd mu s th rumbl es t o l oca t e th e m ( P oo l e an d M oss, 1 989), a nd fe m a l e As i a n e l e ph a nt s we r e a bl e t o id e nti fy m a l es in mu s th fr o m th e m a l es' urin e ( S c hult e a nd R as mu sse n 1 999), an d th e age a nd mu s th ph ase of m a l es fro m th e m a l es' t e mp o r a l g l a nd sec r e ti o n s ( G ree n woo d et a l ., 2 005 ). A dditi o n a ll y, b o th o l fac t o r y ( C o bl e nt z, 1 9 7 6) a nd a udit o r y ( M cCo mb 1 98 7 ) s i g n a l s fro m ruttin g m a l es h ave b ee n s h ow n t o brin g fe m a l es of so m e s p ec i es int o es tru s. O f co ur se, w h et h e r th e p rox im a t e fun c ti o n i s t o a tt rac t r ece pti ve f e m a l es o r r e p e l co mp e tin g m a l es (o r b o th ) m a l e a d ve rti s in g ultim a t e l y fun c ti o n s t o in c r ease m a tin g

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91 success; for example, of the many factors considered by McElligott et al. ( 1999), the amount of time rutting fallow deer s pent groaning was most highly correlated with mating success. Self-Maintenance Costs In addition to the risk of injury and death from combat, the male coati may pay a variety of less apparent costs to support its activities during rut. Coati male s in Tikal spend less time grooming them se lve s during the mating period than at other time s of year. The other relevant activities monitored in the pre se nt study (foraging, traveling) did not differ with time of year, but year-round male body fat profiles demonstrate a clear negative shift in the animals' energy balance during the rut. Female coatis display a s imilar s hift at that time (Chapter 2), how eve r, and the respective roles of reproductive activities and resource availability remain unclear. No relevant data are available on male coatis at other locales. Profound variation in body fat or weight is see n in the coati's northern temperate relative, the raccoon (Procyon lotor) but tends to be more gradual; it i s unknown as yet what if any influence mating period may have on the male raccoon's circannual pattern (Mech et al., 1968; Dunn and Chapman 1983 ; Moore and Kennedy, 1985; Da viso n, 1993; Gehrt and Fritzell, 1999b ). The indirect costs of rut are well documented in many ungulate species (see the partial albeit lengthy list of examples provided in Mysterud et al., 2004). Looking at such costs individually, the effects of rut per se on grooming behavior have not previou s ly been examined, but Mooring et al. (1996) found that territorial male impalas (Aepyceros melampus) groomed less while rutting than did females or males that were not holding territorie s, and the territorial males hosted more ticks as a result. Typically, rutting males s harply decrea se or eliminate foraging (Mitchell et al., 1976 ; Miquelle, 1990; Perez Barberia et al., 1998; Pelletier, 2005) while increasing their general activity levels (Clutton-Brock et al., 1982; Flint and Krzywin s ki, 1997). As a result they experience a s udden decline in body weight and fat levels ( Mitchell et al., 1976; Dunham and Murray, 1982 ), in some cases even as a season of food scarcity approaches (Miquelle, 1990; Kolle et al., 1993).

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92 Testicular Activity The male coati is obviously engaging in a seaso nal pattern of reproduction complementary to that of the female, but how committed is it to that strategy? Change s in gonadal tissue are clearly involved, as demon s trated by the circannual pattern males displayed in testis size. The finding that mature sperm are being produced both soon before and seve ral months after the mating period, however, s ug ges ts that at lea s t so me level of fertility persists over a prolonged period if not year-round. Male reproductive capability beyond rut was also demonstrated by the fact that at lea s t five females that lo s t their litters not long after parturition were apparently fertilized again more than thr ee month s after rut 's conclusion, re s ulting in them giving birth to seco nd litters (Chapter 2). Te s ticular data are lacking for coatis outside of Tikal. Circannual cycles of te s ticular regre ss ion and r ec rude sce nce are normally observed in rutting s pecie s (included in mammalian revi ew by Lincoln, 1989). In mo s t s pecie s thus far examined these cycles include a period of cessation in s permatogene sis and a brief period of maximal s perm production coincident with rut (Robinson et al., I 965 ; Lincoln, 1971; Chaplin and White 1972; We s t and Nordan, 1976; Marchlew s ka-Koj and Kruczek, 1988; Reye s et al., 1997). In other (typically lower latitude) s pecies the males remain more or less competent year-round (Abdel-Raouf et al., I 975; Brown et al., 1991; Monfort et al., 1993; Willard and Randel, 2002). In either case it appears that the rapid te s ticular proliferation associated with rut serves mainly to increa se androgenesis (see Brown e t al., 1991; Reyes et al., I 997), prompting rut behavior and the development or activation of various s tructures in its s upport The role androgens play in the socia l aggression of rutting male s has received the mo s t attention (Jainudeen et al., 1972; Lincoln et al., 1972 ; Yagi I and Etzion, 1980; Mossing and Damber, 1981 ; Boui sso n, I 983 ; Poole et al., 1984; Pelletier e t al., 2003; Mooring et al., 2004), but the se hormones have also been linked to cutaneous glandular secretion and sce ntmarking (Jainudeen et al., 1972; Yagil and Etzion, 1980; Mossing and Damber, 1981; Poole e t al., 1984), calling

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93 (Clutton-Brock and Albon 1979 ; Yagil and Etzion, 1980 ; Li et al., 2001) and dimini s hed foraging ( McMillin et al., 1980 ; Newman et al., 1998) and grooming ( Kakuma e t al., 2003). Many if not all of the phenomena di s played by the rutting coati may be under androgenic control as well. The patterns observed in coati te s tis s ize and te s to s terone le ve l are s imilar to tho se reported for numerous northern temperate ungulate s pecie s (Short and Mann 1966 ; Lincoln 1971 ; McMillin et a l. 1974 ; We s t a nd Nordan 1976 ; Sch a m s and Barth 198 2; Asher et al., 1989 ; Asher and P e t e r so n 1991 ; Ditchkoff e t a l ., 2 00 I ; Mooring et al., 2004; M a rtinez-Pa s tor e t al., 2005). In th e two procyonids pr ev iou s ly s tudi e d (also north e rn temp erate s p ec i es), th e raccoon and ringtail ( Ba ssa ri sc u s astutus), te s ti s s i ze also p ea k e d ju s t prior to or ea rly in the s p ec ie s' annual matin g p e riod s but the proce sses of r ec rude sce nc e a nd r egress ion were mor e gra dual and ( n ear) maximum s i ze was maintained for severa l month s (San der so n a nd Nalbandov, 1973 ; Dunn and Chapman 1983 ; Poglayen-Neuwall and Shively, 1991 ; Davi so n, 1993 ) Both of th ese s p ec i es a l so di s pl aye d a fourto fi vemonth t es ticular n a dir invol v ing a mark e d reduction or cessation in s p e rm production (Sanderson and Nalbandov 1973 ; Dunn and Chapm a n 1983; Po g layen-Neuw a ll and Shively 1991). Surpri s ingly, only scan t and unclear e nd ocr inologic data exist for the male raccoon. Davi so n (1993) r e ported only a broad low peak in te s to s terone ( the maximum se rum concentration recorded was 3 69 ng/rnl) roughly centered around the s pecies late winter m a ting period in the so uthea s t e rn United Stat es a nd Kaneko et al. (2 005) reported that te s to s t e rone concentrations were highe s t in the fall (achieving in the vicinity of 80 ng/rnl ) in feral a nim a l s in Japan; both s tudie s were hamper e d by small, s poradically obtained sa mple s. Conclusion The r e productive patt e rn di s played by the male coati at Tikal is unu s ual in two r egar ds : Fir s t th e mal e coati's rut i s more a kin to that of m a ny ungulat e s p ec i es than to the pattern of any other carnivore s pecie s exa mined to date The highly socia l n a ture and s trong reproductive seaso nality of female coatis foster inten se competition among male s. Male coatis have

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94 co rr es pondin g ly evo l ve d a variety of phy s ical and behavioral adaptations t o incr ease their competitive a bility, as well as rather narrow t e mporal limit s on the di s play of th ese adaptations to limjt their associated costs. Phy s iologically circannual changes in androgen le ve ls are s trongly implicated in controlling the appearance and di sa ppearance of the se adaptations Second ju st as female coatis are exceptional a mong tropical m a mm a l s in th e ir r epro ducti ve seaso n a lity (C hapt e r 2), mal e coatis are exce ptional in the sy n c hrony of their rut. Rut i s a mor e or l ess a nnual phenom e non for individual s of affected s p ec i es wherever they re s ide, but the d eg r ee of sy nchrony within a population tends to vary greatly with latitude. At high l a titud es all th e m a l es in a popul a tion typically rut at the sa me time wherea s int e r-male sy n c hrony weakens a nd in so me cases eve n di sa pp ea r s at low l a titud es ( G oss, I 983; Bron so n 19 85; Bran a n and Marchinton, 1987 ; Loudon and Curlewi s, 1988 ); as with th e coati, male p a ttern s ge n era lly r e flect female pattern s in thi s r egar d. It s hould be not ed, how eve r that lam e ntably few fr ee-ra nging tropical mammal s have thu s far been s tudi e d. How m a le coa ti s achieve s uch tight sy nchrony in rut is a t pre se nt unknown. Photoperiodic e ntrainm e nt of a n endogenous circannual rhythm in hypoth a larruc-pituitary go nadal activity h as b ee n d e mon s trated in severa l rutting s p ec ie s ( Snyd er et al 1983 ; Lincoln e t al., 1984 ; A s her and Peter s on 1991; Sempere et al., 1992) and see ms mo s t likely in the coati as well. However changes in the light:dark cycle a:t very low latitudes have tr a ditionally been th o ught to be too s li g ht by them se lv es for finely tirrung r e producti ve eve nt s ( Go ss et al., 1974; Bron so n 1989 ) The soc i a lity of female coatis i s beli eve d to aid them in so utilizing s uch changes ( Chapt er 2), but the so litary habits of male s in th e preparatory month s before rut would see m to preclude thi s s trat egy. Of course, it may be that soc ial cues which appear as part of or are coincident with rut 's onset prompt sy nchronization at th a t point. It may also be that tropical spec ie s h ave s imply b ee n und e re st imated with re s p ec t to their re s pon s iv e n ess to photoperiodic changes; for example, H a u et al. ( 1998) found th a t s pott e d antbirds ( H y lophylax naevioides naevioides) from 9 N r es pond e d to as little as 17 min variation in the light:d a rk cycle in a

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95 l a b ora t ory se ttin g As sc i e n t i s t s h ave b ee n n o tin g fo r ove r 2 0 years (e.g. G oss, 1 983; Mo n fo rt et a l ., 1 993), thi s area c l ea rl y offers fe rtil e gro und fo r futur e r esearc h Th e pl as ti c it y in m a tin g sys t e m di s pl aye d by m a l es o f so m e ruttin g s p e ci es, a ppar e ntly i n cl udin g th e coa ti also i n v it es fu rt h e r sc i e ntifi c inqu ir y. Mu c h a tt e nti o n h as b ee n d evo t e d to th e eco l og i ca l fac t o r s th a t influ e n ce c h o i ce o f sys t e m (e g., L a n g b e in and T h i r goo d 19 8 9 ; G os ling 1 99 1 ; Isvara n 2005) but in fo rm a ti o n i s l ac kin g o n th e und e rl y in g ph ys i o l ogica l m ec h a n is m s. Win gf i e ld ( 1 984) fo und th a t ex p e rim e nt a ll y in c r eas in g t es t os t ero n e l eve l s in m a l es o f t wo s p a rr ow s p ec i es s hi f t e d th e ir b e h av i o r fr o m m o n oga my to p o l ygy n y; mi g ht a s imil a r h o rm o n a l m ec h a n is m ex pl a in th e di ffe r e n ces b e t wee n m a l es in l ekki n g an d n on -l ekk in g p op ul a ti o n s of fa ll ow d ee r (La n g b e in a nd T hir goo d 1 989) o r b e t wee n t e rrit o ri a l an d n o n t e rrit o ri a l m a l es in a s i ka deer (Cervus nippon) p o pul a ti o n ( Miu ra, 1 98 4 )? Th e m a l es' fl exi bilit y can a l so ex t e nd b eyo nd c h o i ce of m a tin g sys t e m t o h ow l o n g o r eve n w h e th e r t o p art i c ip a t e in rut a t a ll. P os p ub e rt a l but soc i a ll y imm a tur e m a l e A fri ca n e l e ph a nt s s h o rt e n o r r e fr a in fro m e nt e rin g mu s th in th e pr ese n ce of m a t ure m a l es ( P oo l e, 1 98 7 ; 1 989; Sl o t ow et a l ., 2000), fo r exa mpl e, a nd a dult m a l e r e d d eer (Cervus e l ap h us) a t a n y l eve l o f m a turity s udd e nl y cease ruttin g af t e r s u s t a in i n g a di sa blin g injur y ( Clutt o n-B roc k et a l ., 1 982). Th e e ndo c rin o l ogy o f s u c h s hi f t s in b e h av i o r r e m a in s un c l ea r.

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CHAPTER 5 SUMMARY This investigation focuses on a most unusual and instructive aspect of white-nosed coati reproductive biology: the remarkably tight temporal clu s tering of reproductive events di s played by this tropical s pecie s. It provides support for the idea that the species' reproductive seasonality results from se lection to wean young at the time of year when food availability i s mo s t consistently high, a nd reveals that the species' extreme birth sy nchrony may s imply be a result of the mechani s m by which reproductive seasonality i s achieved rather than an adaptation in and of it se lf. It also r evea l s that male coatis have adapted to the tight clustering of receptive females by evolving a rut, a pattern commonly seen in ungulate species but unlike that of any other carnivore s pecies yet examined. The se di scove ries highlight the need for information on reproductive pattern s in additional long-lived tropical mammal species as well as a deeper understanding of the phy s iological mechani s m s involved in the timing of reproduction in s uch spec ie s. Data from Tikal National Park Guatemala, confirm the highly seasonal nature of white nosed coati reproduction and provide much greater detail on the reproductive pattern than has previously been available The pattern documented there fits well with previous observations from other sites. Coatis mate during approximately two weeks early in the dry seaso n. Females become solitary to ne s t and give birth late in the dry season. They bring the young down from the ne s ts at approximately five weeks of age early in the wet season. Females with young join together in small groups rather quickly but it takes a few weeks for bands to become fully reaggregated. The young begin foraging immediately after emergence but are not completely weaned until approximately midway through the wet seaso n. 96

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97 lf a f e mal e's regular annual reproductiv e attempt is un s ucce ss ful the a nimal may undergo a seco nd reproductive cycle in which mating apparently occur s a t approximately the time when the regular cohort of young i s brought down from the ne s ts The proportion of females in a population th a t goes throu g h a seco nd cycle undoubtedly depend s upon resource availability and n es tlin g mort a lity. When resources a re sca rc e, females may not be able to maintain a dequate b o dy condition to successfu lly complete a seco nd reproductive cycle. Hi g h lev e l s of pr e dation on ne s tling coatis create se l ec tiv e pre ss ure on femal es to make repeated reproductive attempts, within limit s impo sed by the s p ec ie s' reproductive seaso nality. The timin g of coa ti r eprod ucti o n appears to have evo lved to allow the young to begin foraging at th e s tart of an ex t e nd e d period of p ea k food availability. Both l eaf litt e r invertebrates a nd fruit t e nd to be a bund a nt durin g the fir s t h a lf of th e wet seaso n in Tikal, as in many other n eo tropical s ite s. H oweve r int era nnual variation in rainfall patterns can dramatically alter fruiting phenolo gy, a nd many tropical tree s p ec i es do not seem to follow annual fruiting cycles even in seaso n a l e n v ironm e nt s. The timing of peaks in insect abundance i s mor e consistent, although th e a mplitud e depends on rainfall le ve l s. Thu s, coatis likely depend primarily on a seaso nal abundance of inv e rtebrate s to get the young through the weaning pha se. Comparable data are not available for other neotropical in sec tivore s /omnivores, but a si milar relationship between weaning and peak food availability ha s been observed for large-bodied neotropical primat e s peci es ( DiBit e tti and Jan so n 2000). In addition to being highly seaso n a l, coati reproduction i s extremely sy nchronou s Their m a ting and birth period s are an order of magnitude s hort e r than tho se of mo s t tropical mammals with seaso nal reproduction. Adaptive explanations for s uch tight sy nchrony are not s upported by data from Tikal. For example, birth s are more sy nchronized than reaggregation even when the formation of s m a ll groups i s p e rmi ss iv e ly considered reaggregation indicating that facilitation of communal care is not the driving force behind the sy nchrony Birth s are a l so more sy nchronized within band s than b etwee n neighboring band s, indicating that predator swa mping i s not an

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98 adequate explanation for coati reproductive synchrony and suggesting that social interactions may be important in facilitating the synchrony. The most likely explanation is that the coati's tight birth synchrony is simply a byproduct of the animals' use of social cues to help them achieve seasonally timed reproduction. That is, while the females in a band that are most sensitive to environmental cues may rely on those cues to time reproduction, their associates instead likely rely on some form of social interaction for the same purpose. Although the use of social cues to time reproductive events has been experimentally demonstrated in rodents (see Chapter 3) and suspected in other carnivore species (Rood, 1975), it has not been demonstrated in the wild. The tight, consistent seasonality of sexual receptivity in female coatis, coupled with the large size of coati bands in Tikal, creates intense male intrasexual competition for mating opportunities Accordingly, males undergo their own form of pronounced reproductive seasonality Androgen levels rise with the approach of the mating period, peaking at or before its onset and then declining precipitously back to baseline over the course of that brief period. In mirror-image, testis size spikes just prior to the mating period before declining more gradually. During and/or for a short time before the mating period, males exhibit increased intrasexual agonism (including considerable physical combat), reduced foraging and courtship displays unique to that time of the year. As a result, their body condition drops dramatically and they frequently suffer severe wounds from fighting. The brevity of the male coati's period of enhanced competitive/reproductive capability, which lasts about one month in total, presumably evolved to minimize such costs It is appropriate to refer to this phenomenon as a rut, as the male coati undergoes all of the changes exhibited by species more commonly associated with that term. Rut was previously unknown among the Carnivora. Although basic information indicating coati reproductive seasonality had been previously reported from Barro Colorado Island, Panama, some major aspects of coati reproduction in Tikal, such as replacement litter production by females and rut by males, had not been observed during three intensive long-term studies of coatis on BCI (Kaufmann, l 962; Russell, 1979; Gompper,

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99 1994 ). Thi s illu s tr a t es th e ri sks in vo l ve d in ex trapolatin g to an e ntire s p ecies from observations of a s in g le popul a tion M o r eover, eco lo g i ca l pr ess ur es a ff ec ting th e BCI coati popul a tion may diff er dramatically from tho se a t more natural s ite s, as BCI i s a 15 km 2 i s l a nd that is lacking large predators ( Gl a nz 19 82; Robin so n 1999 ) Such eco lo gica l diff e r e n ces ca n a nd a pp a r e ntly do h ave r e percu ss i o n s for r e productive bi o l ogy. For exa mpl e, coat i band s i zes a r e a n o rd e r of m ag nitud e lar ge r in Tikal th a n on BCI due t o diff e r e nc es in pr eda ti o n pr ess ur e a nd/ or food ava il a bility ( Booth-Binc zik, 2 001 ), and as a re s ult r ece ptive f e m a l es are eve n mor e c lu s t e r e d in s pac e and time in Tikal than th ey pre s umably are on BCI se tting the s t age fo r ex tr eme l y int e n se co mp e tition a m o n g Tik a l 's m a l es. The si tu a tion on BCI, with o nl y a few ad ult females in eac h band ( K a ufm a nn 196 2; Ru sse ll 1979 ; G o mpper, 1997 ), c r eates a m o r e eve n di st ributi o n of m a tin g opportunities for m a l es Among mamm a l s in ge n era l th e s p a ti a l di s tributi o n a nd soc ial organization of females r e fl ec t the di s tributi on of food resources, whereas th e s p a ti a l di s tribution and mating s trategies of mal es r e fl ec t the di s tributi o n of fe mal es (C lutton-Brock and H a r vey 1978 ) Thi s s tudy s ugge s t s that the timin g of r eprod u c ti on follows s imil a r rul es; in th e coa ti the female pattern is b ase d on food availability, whereas the m a l e p a tt e rn i s b ase d on the availability of r ece ptiv e females. Such ge n e raliti es notwith s tanding th e combination of the coati's ecological niche and soc ial structure appears to b e unique to thi s s p ec i es and p e rh a p s a l so it s South American co n ge n e r Nasua nasua. Most o th er procyonids are much l ess well s tudi e d but they are neither diurnal n o r n ear ly as socia l as th e coati. Among carnivores as a whole, th e group-living, diurnal, in sec tivorou s h e rpe s tid s s u c h as meerkats (Suricata suricatta) and band e d mon gooses ( Mun gos mungo) ( Rood 19 86) see m to ha ve th e mo s t in common with coatis, although th e forest-dwelling, fru g ivorou s as p ec t s of the coat i 's life s tyl e are m o r e prim atelike The coati's soc i a l s tructure of gro up-li v ing females a nd chiefly so litary m a l es, on th e ot h e r h a nd i s mo s t si milar to tho se of African e leph a nt s (Loxodonta afr i cana) and s p e rm whales ( Ph y sete r catodon) ( di sc u sse d in Booth-Binczik 2001) spec i es with few eco logical s imilariti es to th e coati. This combination of

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100 soc ial and ecological factors ha s r es ult e d in reproductive ada ptation s that are unu s ual among tropical mammal s and unique a mong carnivores. This study ha s clarified many points with regard to coati reproduction but a number of que s tion s remain unan swere d: Perhaps mo st notably h ormo nal cycles underlying the female pattern remain undocumented. Ind ee d, this points to a s urpri s in g ly lar ge ga p in o ur current understanding of the Procyonidae particularly g iv e n th a t severa l s p ec ie s are common in va riou s part s of North America and one s p ec i es, the raccoon, i s widespread and a bundant throu g hout mo s t of the United States. So far as can be determined, aside from thi s s tudy no e ndocrinolo g ical information i s currently available for any procyonid s p ec i es exce pt th e raccoon; D aviso n ( 1993 ) r e port e d a few proge s t ero ne values for females, a nd Da v i so n ( 199 3) a nd Kan e ko et al. (2005) provid e d only s li g htly more te s to s t ero n e data for m a l es With re s p ec t to th e mal e p a tt e rn, it i s unknown whether m a le ejac ulate qu a lity exhibits seaso n a l changes Th e d a t a ob tain e d in thi s s tudy s u gges t that m a l es produc e s p e rm throughout the year, but s p e rm production m ay b e low e r at so me tim es of yea r than a t others. Seasonal fluctuations in s permato ge n es i s ha ve been docum e nt e d in many s peci es, and although male s of many temperate species display an annual period of complete aspermatogenesis, male s of tropical s pecies are more lik e ly to r e t a in so me reproductive capability throughout the year (discussed in Chapt e r 4). The n a tur e of the proximate c u e(s) upon which th e coati relies for its r e markable r e productive p a tt e rn awa it s e lu c id a tion as well. It see m s mo s t likely th a t olfactory cues s hared among associates a u g m e nt photop e riodic changes, but tactil e and auditory sig nal s may play a role in addition to or in s t ea d of olfaction. As di sc u sse d in Chapter 3, all s uch soc ial cues and in so me cases combinations th e r eof ha ve b ee n found to a id various m a mm a l s in timing their r e production. The bulk of the work in thi s area ha s focused o n rodents, h oweve r and not only procyonid s but carnivores in ge n era l r e m a in esse nti a lly un s tudied.

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IOI Also as mentioned in Chapter 3, the degree of overlap among the estrous periods of individual females within a coati band has not been assessed. There is so me evidence that overlapping periods of receptivity lead to female coatis having difficulty gaining access to preferred mates (Booth-Binczik, 2001). Statistically asynchronous estrous periods within a tightly seasonal mating period have been de sc ribed for ring-tailed lemurs (Pereira, 1991), presumably as an adaptation to avoid s uch competition. Finally, another s ubject warranting further study i s the s p ec ie s' potential for delayed/deferred reproduction and the cause(s) of its expression. Most females on BCI first reproduce in their second year, but at time s up to 80% apparently wait until their third or even fourth year (Kaufmann 1962 Ru sse ll 1979 1982). Becau se thi s finding i s ba se d so lely upon observations of females engaged in nesting behavior or later accompanied by young, when delay s occur it is unknown whether pub e rty it se lf is deferred or whether the female s cycle but are un s uccessful in being fertilized and/or completing pregnancy Ru sse ll (1982) believed that the animals' "decision" to forego reproduction was nutritionally-ba se d a nd pointed out that s uch a strategy would be mo s t appropriate for animals with the m ajo rity of their reproducti ve opportunities still ahead of them. Prolonged shortages in fruit (Foster 1982a) and/or leaf litter arthropods (Levings and Wind so r 1982) are not uncommon on BCI and on rare occasions are severe enough to cause widespread animal s tarvation (Foster 1982a). The pre se nt study found that year-to-year variance in coati food availability occurs in Tikal as well, but perhap s not to the extent necessary to delay maturation or prompt deferral of r e production in a mature animal. Additional studies on BCI or elsewhere may therefore be required to examine the relation s hip between female body condition and reproductive delay/deferral. Should s u c h a relation s hip exist, as seems likely, it will be anoth e r example of reproductive timing in female coatis being dependent on food availability.

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APPENDIX RAW TESTIS VALVES Raw te s tis size indices for white-nosed coatis in Tikal National Park Guatemala. Volumes ( x 10 3 mm 3 ) calculated a s V = L x W 1 x W 2 x rr/6 using mea s urement s unadjusted for surrounding fat layer, then averag e d for left and right testis. Male# Date Testi s Vol. Male# Date Testis Vol. Non-Rut : 29 February/I March 22 January 01 22-Jun-94 2.22 32 05-Mar-95 3.19 01 07-Sep-94 3.63 32 13-Apr-95 3.79 01 2 l-Jan-95 5.06 32 I 8-Jan-96 6.57 01 l l-Mar-95 3 10 32 30-Sep-96 3.78 01 07 Jun-95 3.56 34 l 1-Sep-96 4.33 03 23-Jul-94 2 63 34 I 1-Oct-96 4.76 03 0J-Apr-95 2.11 40 29-Mar-95 3.60 03 31-Aug-95 2 57 40 18-May-95 3 59 03 22-Jan-96 3.67 40 13-Jun 95 3 36 03 13-Aug-96 1.50 43 05-Mar-95 2 37 03 14-Oct-96 3.30 43 02-Apr-95 2 67 09 27-Aug-94 2 74 43 07-May-95 2 53 15 23-Oct-94 2.62 43 20-Jun-95 2 94 15 10-Mar-95 3 54 43 10-Oct-96 4.02 18 17-Jan-95 1.9 I 45 14-Mar-95 3 18 20 27-Mar-95 3.15 50 15-Apr-95 3 79 20 12-Jan-96 4.30 50 I 8-Jun-95 3 64 28 I 7-Mar-95 3.29 51 26-Apr-95 3 50 28 17-Apr-95 3.47 53 17-May-95 3.75 28 30-May-95 4 08 71 24-Aug-96 3 16 28 09-Jan-96 6.11 91 10-Aug-96 3 14 28 05-Oct-96 4.27 99 09-Jan-96 4 02 29 14-Apr-95 3.35 Rut, Pre-Mating: 23 January 12 February 01 12-F e b-95 5 29 22 27-Jan-95 5.44 03 30-Jan-95 3 98 25 28-Jan 95 2.49 20 25-Jan-95 4 04 28 3 l-Jan-95 4 29 ( continued ) 102

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103 Raw te s tis s ize indic es for white-nosed coatis in Tika l National Park Guat e mala (continued). Male# Date Testis Vol. MaJe# Date Te s tis Vol. Rut, Pre-Mating: 23 January 12 February (continued) 29 05-Feb-95 6 50 87 27-Jan-96 5.47 32 07-Feb-95 5 58 88 30-Jan-96 5 05 32 02-Feb-96 5.65 89 03-Feb-96 5.31 34 27-Ja n-96 5 51 90 04-F eb-96 6.6 43 26Jan -96 5.73 91 08-Feb-96 5 32 Rut, Mating: 13 February 28 February 03 23 -Feb-95 2.62 34 14-Feb-95 4.35 20 22-Fe b-95 3 16 40 26-Feb-95 3.55 28 22-Fe b-95 3.48 51 18-F eb-96 5 05

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BIOGRAPHICAL SKETCH Gerald Allen Binczik was born on 9 December 1960 in St. Cloud Minne so ta. He attended Willard and Ascension Elementary Schools in Minn ea poli s a nd Nelson Elementary, Central Junior High and Columbia Height s High School s in Columbia Heights, Minnesota, graduating from the latter in 1978. He attended Northland College in Ashland, Wisconsin, and Arizona State University in Temp e, Arizona, receiving a Bachelor of Science degree in zoology from the latter in August 1984 In June 1993 he obtained a Master of Science degree in wildlife conservation from the University of Minne so ta in St. Paul Minnesota; the title of hi s the s i s was R eproductive Biolo gy of Asian Small-Clawed Otters. 120

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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 Philosophy. Distinguished 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 dissertation for the degree of Doctor of Philosophy. ] Professor of Animal Sciences 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 /,?4-~hH. Jane Brockmann 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. Colin A. Chapman 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 sco e and qualit s a dissertation for the degree of Doctor of Philosophy. Melvin E Sunquist Professor of Wildlife Ecology and Conservation 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. May 2006 Dean, Graduate School

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