• TABLE OF CONTENTS
HIDE
 Front Cover
 Copyright
 Abstract
 Table of Contents
 Introduction
 Acknowledgement
 The species setting
 Experimental design and method...
 Definitions and criteria
 Some natural history data...
 Results
 Discussion
 Literature cited
 Back Cover






Group Title: Bulletin of the Florida Museum of Natural History
Title: Reproductive strategies of female Didelphis
CITATION THUMBNAILS PAGE IMAGE ZOOMABLE
Full Citation
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Permanent Link: http://ufdc.ufl.edu/UF00095823/00001
 Material Information
Title: Reproductive strategies of female Didelphis
Series Title: Bulletin - Florida Museum of Natural History ; volume 36, number 4
Physical Description: p. 109-140 : ill. ; 23 cm.
Language: English
Creator: Sunquist, Melvin E
Eisenberg, John Frederick
Florida Museum of Natural History
Publisher: University of Florida
Place of Publication: Gainesville, Fla.
Publication Date: 1993
Copyright Date: 1993
 Subjects
Subject: Didelphis marsupialis -- Reproduction -- Florida   ( lcsh )
Didelphis marsupialis -- Reproduction -- Venezuela   ( lcsh )
Virginia opossum -- Reproduction   ( lcsh )
Genre: bibliography   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
non-fiction   ( marcgt )
 Notes
Bibliography: Includes bibliographical references (p. 137-140).
General Note: Cover title.
General Note: Abstract in English and Spanish.
Statement of Responsibility: Melvin E. Sunquist and John F. Eisenberg.
 Record Information
Bibliographic ID: UF00095823
Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: oclc - 29906789

Table of Contents
    Front Cover
        Page 107
    Copyright
        Page 108
    Abstract
        Page 109
        Page 110
    Table of Contents
        Page 111
    Introduction
        Page 112
    Acknowledgement
        Page 113
    The species setting
        Page 114
        Page 115
    Experimental design and methods
        Page 116
    Definitions and criteria
        Page 117
    Some natural history data for didelphis
        Page 118
    Results
        Page 119
        Page 120
        Page 121
        Page 122
        Page 123
        Page 124
        Page 125
        Page 126
        Page 127
        Page 128
        Page 129
        Page 130
        Page 131
        Page 132
        Page 133
    Discussion
        Page 134
        Page 135
        Page 136
    Literature cited
        Page 137
        Page 138
        Page 139
        Page 140
        Page 141
    Back Cover
        Page 142
Full Text



*KUJEEEU,..


of the




FLORIDA
MUSEUM OF
NATURAL HISTORY


REPRODUCTIVE STRATEGIES
OF FEMALE DIDELPHIS

Melvin E. Sunquist and John F. Eisenberg


Biological Sciences, Volume 36, Number 4, pp. 109-140 199.


UNIVERSITY OF FLORIDA


GAINESVILLE









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REPRODUCTIVE STRATEGIES OF FEMALE DIDELPHIS




Melvin E. Sunquist and John F. Eisenberg*






ABSTRACT



A two-year experimental field study was conducted simultaneously in Venezuela and
Florida to test the hypothesis that in polygynous mammals offspring sex ratio is affected by maternal
capacity for reproductive investment. Female common opossums (Didelphis marsupialis) and
Virginia opossums (D. virginiana) were used as model animals. At each study site three groups of
adult virgin females (10/group/year) were trapped prior to the breeding season, weighed,
radiocollared and released. Females were randomly assigned to Control, Provisioned, or Delayed
Reproductive groups. Provisioned females were located at daytime rest sites and provisioned with
about a 125 gm mixture of sardines and cat food at 2-day intervals from at least three weeks prior to
conception until the end of the breeding season. Delayed Reproductives were those whose embryonic
young were removed repeatedly from the pouch to assess the potential reproductive cost to females
who conceived but lactated for only a brief time. All females were recaptured at monthly intervals for
weighing and to record the sex and size of pouch young or, in the case of Delayed Reproductives, to
remove any new pouch young.
In both Florida and Venezuela, reproduction was highly seasonal and most (> 90%)
females in the population produced two litters per year. The mean litter size (mode=7) for both sites
did not differ significantly between the first and second litters, nor was there any effect of treatment
on litter size. The interval between the birth of the first and second litters was of similar duration for
Provisioned and Control females. Length of lactation was also similar for Provisioned and Control
females, although the length of lactation for the second litter was 1-2 weeks longer in both Florida
and Venezuela. There was no differential investment in male or female offspring during the teat-
attachment phase, but Provisioned females exhibited greater parental investment. The weight at
weaning of young from Provisioned females was significantly higher than young of Control females.
Provisioned females invested disproportionately in males by producing male-biased sex ratios and by
producing a higher percentage of litters that were male biased. Females, whether provisioned or not,
that were in good condition tended to produce more male-biased litters. A drought in Florida in 1985

Dr. Sunquist is a Rcscarch Scientist in the Dcpartment of Wildlife and Range Sciences, School of Forestry, University of Florida,
Gainesville FL 32611-2035 USA. Dr. Eisenberg holds the Ordway Chair of Conervation through the Florida Museum of Natural History
and the School of Foretry, University of Florida Gaincsville FL 32611-2035 USA.



SUNQUIST, M.E., and J.F. EISENBERG. 1993. Reproductive strategies of female Didelphis.
Bull. Florida Mus. Nat. Hist., Biol. Sci. 36(4):109-140.







BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


disrupted the feeding program, consequently few females received their dietary supplement and a
small percentage of litters were male biased. In Venezuela, male offspring of Provisioned females
were recaptured post-weaning significantly more often than males of Control females, although the
comparison was not significant for the Florida data. Females who were denied the stress of lactation
tended to survive longer, the difference in survivorship approached significance in Venezuela. The
extended survivorship of Delayed Reproductives was not biologically significant as few lived more
than two years, and mean longevity for all groups was less than two years. Opossums of both species
appear to be geared to perform a maximum reproductive effort in the year following their birth.


RESUME


Con el objeto de someter a prueba la hip6tesis de que en mamifferos poliginicos la
proporci6n de sexos es influenciada por la capacidad de inversion reproductive de la madre, se realize
durante dos afios un studio de campo experimental en Venezuela y Florida. Se utilizaron como
animals modelo hembras de rabipelado (Didelphis marsupialis) y hembras de Virginia opossum (D.
virginiana). En ambos sitios de studio y previo al comienzo de la temporada reproductive, se
capturaron tres grupos de hembras virgenes (10/grupo/afio), con el objeto de pesarlas y colocarles
radiocollares. Las hembras fueron asignadas al azar en tres grupos: Control, Abastecidas y de
Reproducci6n Retrasada. Las hembras Abastecidas fueron localizadas en sus lugares de descanso
diurno, ofreci6ndoseles 125g de una mezcla de sardines y alimento pars gatos cada dos dias, desde al
menos tres semanas antes de la concepci6n y hasta el fin de la temporada reproductive. Las hembras
de Reproducci6n atrasada sufrieron la remoci6n repetida de las crias alojadas en el marsupio, con el
objeto de evaluar el costo reproductive potential en hembras que, adln cuando concivieron, s6lo
lactaron por un corto period. Todas las hembras fueron mensualmente pesadas y determinados el
tamafio y sexo de las crias en el marsupio, removiendo ademrs las crias de las hembras de
Reproducci6n atrasada.
Tanto en Florida como en Venezuela la reproducci6n fue altamente estacional y la mayoria
de las hembras (>90%) produjeron dos camadas al afio. Para ambos sitios de studio, el tamafio
medio de camada (moda=7) no difiri6 significativamente entire la primers y segunda camada ni entire
diferentes tratamientos. El intervalo entire el nacimiento de la primer y segunda camada fue similar
para hembras Abastecidas y Control. Aunque la lactancia de la segunda camada fue una a dos
semanas mas larga que la lactancia de la primer camada en Florida y Venezuela, 6sta fue similar
entire hembras Abastecidas y Control. Crfas machos o hembras no recivieron una inversion diferente
durante la fase de adherencia al pez6n, aunque las hembras Abastecidas mostraron mayor inversi6n
materna, siendo sus crias mis pesadas al destete que crias de hembras Control. Las hembras
Abastecidas invirtieron mas en crias machos al producer camadas con una proporci6n de sexos
sesgada hacia los machos, y al producer una mayor proporci6n de camadas con este sesgo. La
tendencia de producer mas camadas sesgadas hacia crias macho fue observada en hembras en buena
condici6n tanto Abastecidas como Control. En Florida, una sequoia caus6 la interrupci6n de el
program de abastecimiento en 1985 y s61o algunas hembras recibieron su suplemento dietario,
disminuyendo el porcentaje de camadas sesgadas hacia crfas macho. Despu6s del destete, una mayor
proporci6n de machos hijos de madres Abastecidas fueron recapturados en comparaci6n con machos
hijos de madres Control. Esta diferencia fue significativa en Venezuela, pero no en Florida. Las
hembras en las que se suprimi6 el estrts de la lactancia tendieron a vivir mis y esta diferencia fue casi
significativa en Venezuela. La mayor sobrevivencia de hembras de Reproducci6n Retrasada no fue
biologicamente significativa ya que pocas vivieron mas de dos afios, y la longevidad media pars todos
los grupos fue menor que dos afios. Las hembras de ambas species parecen estar predispuestas a
desarrollar un esfuerzo reproductive miximo durante el afo que sigue a su nacimiento.





SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


TABLE OF CONTENTS


Introduction ...................................................................... 111
Acknowledgements................................................................... 113
The Species Setting ................................................................... 114
The Environmental Setting......................................................... 114
Experimental Design and Methods ................................................ 116
Definitions and Criteria................................................ 117
Some Natural History Data for Didelphis ............................ 118
R results .................................................................................. 119
Discussion .................................................. .......................... 134
Literature Cited....................................................................... 137


INTRODUCTION


In the last several decades, the evolution of life histories has been a major
theoretical focus (reviewed by Stearns 1976, 1977, 1992). Despite the
proliferation of theory in recent years, life history evolution remains poorly
understood, chiefly because field data bearing on theory, or even on the sampling
assumptions of the theory, are scarce. A crucial variable in many life history
models considers how reproductive energy should be allotted between the sexes,
and how this allocation should change with age and physical condition (Fisher
1930; Williams 1979; Trivers and Willard 1973; Charnov 1982).
Assuming there is a specific amount of reproductive effort available, how
should it be allocated among male and female offspring? Darwin (1871) briefly
considered this question, but the first real analysis was by Fisher (1930). He
concluded that, because the total reproductive value of males equaled the total
reproductive value of females in diploid organisms, parental expenditure should be
equally divided between the sexes. Fisher was vague about what parental
expenditure was, but it could be restated that total reproductive effort should be
equally divided between males and females. Fisher's conclusions have since been
more formally defined (Shaw and Mohler 1953; MacArthur 1965; Charnov 1975;
Maynard Smith 1978).
It should be emphasized that Fisher's (1930) conclusions do not predict a
one-to-one adult population sex ratio. If the reproductive effort to produce a
single male differs from the reproductive effort to a produce a female, then the
overall sex ratio at birth will be inversely related to their relative cost, preserving
equal sexual expenditure. Furthermore, Fisher's conclusions do not make
predictions about what individual parents would do (Williams 1979). It is a
population prediction which might be fulfilled equally well if half the population






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


invested only in males and the other half only in females, or if each parent
invested equally in males and females (Crow and Kimura 1970; Williams 1979).
A particularly interesting extension of Fisher's (1930) conclusions
considers the effects of maternal condition (Trivers and Willard 1973; Reiter et al.
1978; Williams 1979) on sexual investment. Trivers and Willard (1973), using a
polygynous mammal as their model animal, argued that if amount of parental
investment affected the expected reproductive success of individual offspring, then
females in good condition should tend to have sons whereas those in poor
condition would tend to have daughters. Their reasoning was that because
variance in male reproductive success is higher than female variance in
polygynous species, the reproductive gain to a parent able to invest more than
average would be greater if the offspring were male; while a parent able to invest
less than average would maximize its benefits if its offspring were female.
Alternatively, offspring sex ratios at birth could be equal but with greater
investment in males than females (Reiter et al. 1978), or parental investment may
be managed by altering litter size itself (Myers 1978). Even so, Williams (1979)
demonstrated graphically that selection should favor mothers in poor condition
who produce female-biased litters and females in good condition who produce
male-biased litters.
In spite of abundant evidence supporting adaptive adjustment of sex ratios
in invertebrates (Hamilton 1967; Charnov et al. 1981; Green et al. 1982), data are
scant, inconclusive, and often contradictory for mammals. There is ample
evidence that investment is greater in sons in many (Short 1970; Nordan et al.
1970; Glucksman 1974; Reiter et al. 1978; Clutton-Brock et al. 1981; Gosling
1986; Rutberg 1986; McFarland Symington 1987; van Schaik et al. 1989) but not
all (Altmann 1980; Silk et al. 1981; Simpson and Simpson 1982; Silk 1983; van
Schaik and Hrdy 1991) polygynous mammals. However, few mammalian species
have shown significant deviation from either an adult sex ratio of parity, or litter
sex ratios statistically distinguishable from a binomial distribution (Williams
1979; Charnov 1982; Clutton-Brock and Albon 1982). Williams (1979) found no
support for any theory of adaptive sex ratio and concluded sex ratio was just
another Mendelian character. However, most adaptive sex ratio theory says
nothing about adult population-wide sex ratios. Furthermore, sex ratio at birth is
immaterial to most theories, as sex ratio at independence is the important datum,
especially in mammals where there is usually considerable parental care. More
importantly, at least some mammals do seem to modify their sex ratios in response
to changes in physical state or age. Maternal age and nutritional state have been
correlated with both increasing and decreasing sex ratios in a variety of mammals
(reviewed in Clutton-Brock and lason 1986). In coypu (Myocastor coypu), for
example, young females in superior body condition abort small, female-biased
litters, whereas large litters and small, predominantly male litters are retained
(Gosling 1986). Maternal stress has produced female biases in birth sex ratios in
laboratory rats (Lane and Hyde 1973), mice (Geiringer 1961; Rivers and
Crawford 1974), and golden hamsters (Labov et al. 1986). McClure (1981)







SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


demonstrated that female wood rats, when food-stressed, discriminated against
male offspring, thereby producing female-biased litters at weaning. In cervids,
however, Verme (1969) reported male-biased sex ratios among fawns born to
nutritionally deprived white-tailed deer (Odocioleus virginianus), whereas
well-fed does produced more female fawns (Verme 1983). McGinley (1984)
interpreted Verme's (1969) results to be consistent with the hypothesis of Trivers
and Willard (1973), because small litter size increases a female's ability to invest
more per individual offspring (but see Caley and Nudds 1987). In
semidomesticated reindeer, females that were heavier at conception produced more
sons (Kojola and Eloranta 1989). There are also several avian examples that
support the theory of facultative manipulation of sex ratios (reviewed by Gowaty
1991).
While many recent papers report a tendency toward adjustments of
offspring sex rations, no one has to our knowledge performed food
supplementation experiments on free-ranging mammals to specifically examine
sexual investment theory. While doing research on other mammalian species in
Venezuela and Florida, we noted that "old-looking" female opossums tended to
produce female-biased litters. We thus set out to analyze the effects of maternal
age and resource availability on the distribution of sexual investment from birth
until independence in the common (Didelphis marsupialis) and Virginian (D.
virginiana) opossum. The initial results from Venezuela supported the theory
(Austad and Sunquist 1986), but there were many details of the Venezuelan study,
and none of the findings from the parallel study in Florida, that were published.


ACKNOWLEDGEMENTS


We thank Sr. Tomas Blohm for allowing us to work on Hato Masaguaral, for his
generosity and continuous cooperation and support, and for assisting with logistical problems. We
also want to thank Dennis Daneke and his assistants Brent Mitchell and David Manry for performing
most of the field work in Venezuela. The efforts of D. Daneke were extraordinary. Thanks also to
Steve Austad, Fiona Sunquist, Debbie Wright, Veronika Kiklevich, Mark Ludlow, and Theresa Pope
for their contribution to the work in Venezuela.
In Florida, we want to especially thank Debbie Wright and Fiona Sunquist for all their
efforts. We also want to thank Ken Myer, Dan Pearson, Janine Russ, John Hendricks, Margaret
Johnstone, Sheri Allway, and Rob Roy McGinnis for their help with the field work.
We thank Barbara Stanton for ably handling the administrative details and Tia Cordier and
Sylvia Finch for typing the manuscript. John Smallwood was a great help with the statistical analyses.
We would also like to thank Steve Austad for all his input to the development and initiation
of this work. He and John Harder also provided many helpful comments on the manuscript; their
constructive criticism is greatly appreciated. The research in Venezuela was supported by NSF grant
BSR-8315125, awarded to M. E. Sunquist and J. F. Eisenberg, and in Florida by the Ordway Chair
of Ecosystem Conservation.







BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


THE SPECIES SETTING


While the New World Didelphidae may be broken into three major extant
lineages (Reig et al. 1987), we are concerned with the Didelphini, and in
particular the species of the genus Didelphis, specifically the reproductive
strategies of just two species, D. virginiana and D. marsupialis. When relevant,
we will discuss data from studies of D. albiventris. Reviews of marsupial
reproduction may be found in Collins (1973), Hunsaker (1977), Lee and
Cockburn (1985), Tyndale-Biscoe and Renfree (1987), and Eisenberg (1988).
Russell (1982) has reviewed the patterns of parental investment in marsupials.
Reviews on the biology of D. virginiana are included in Gardner (1982) and
Seidensticker et al. (1987).
Didelphis virginiana is distributed from upper New York State to central
Costa Rica. D. marsupialis ranges from eastern Mexico to northeastern
Argentina. D. albiventris has a fragmented distribution in northern South
America, being generally found in premontane habitats but becoming the
numerically dominant species in the more xeric areas of Brazil, and finally the sole
species in southern Argentina to about 400 south latitude.
All three species have a similar morphology. They are the size of a
domestic cat, but are rat-like in body form. The tail is very sparsely haired and
prehensile. The ears are naked and show varying degrees of depigmentation. The
female possesses a well-developed pouch or marsupium. After approximately five
months of age, males are noticeably larger than females. Male weights in D.
virginiana can reach 4.6 kg while females rarely attain 3.0 kg. The underfur of
D. albiventris and D. virginiana can be well developed but D. marsupialis, with
its lowland, tropical distribution, usually lacks a well-developed underfur.
Basically all three species occupy similar ecological niches. The separation of D.
marsupialis from D. virginiana, based on morphology and cytogenetic evidence,
has been ably documented by Gardner (1973). Varejao and Valle (1982) present a
similar analysis for distinguishing D. albiventris from D. marsupialis.
D. virginiana is probably the most recently derived of the three species.
Subsequent research may indicate that "albiventris" is a composite of at least two
species. It may be fairly stated that the tropical, lowland, mesic habitat adapted
form, D. marsupialis, most nearly resembles the ancestor of all three recognized
species.


THE ENVIRONMENTAL SETTING


Our research was carried out at two primary localities: (1) The Katharine
Ordway Preserve-Carl S. Swisher Memorial Sanctuary, a 9,300 acre tract (37.6
km2) administered jointly by the Florida Museum of Natural History and the


114






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


School of Forest Resources and Conservation (University of Florida), is located in
northwestern Putnam County approximately 25 miles (40 km) east of Gainesville,
Florida. The preserve consists of a habitat mosaic including a dark-water riverine
system connecting with the St. Johns' River and sandhills containing depression
ponds and lakes. The sandhills are dominated by longleaf pine (Pinus palustris)
and turkey oak (Quercus laevis), while the dark-water system exhibits mesic
adapted trees and shrubs typical of north Florida (Quercus virginiana, Magnolia
grandiflora, Nyssa sylvatica, Carya glabra, and Vaccinium sp.). Descriptions of
these habitats are included in Laesle (1942), Humphrey et al. (1985), and Franz
and Hall (1990). Rainfall and correlated primary productivity are markedly
seasonal; however, there is considerable between-year variability in the timing and
extent of the rains. In an average year heavy rains should occur in December-
January and again from May to September. Mean annual rainfall is 135 cm
(National Oceanic and Atmospheric Administration 1960-1990), and about 60
percent of that falls between May and September. Temperature variation is
marked with cool months achieving freezing temperatures (<32F or 0C) on
some days from December to March.
(2) Hato Masaguaral, a working cattle ranch owned by Sr. Tomas Blohm
in the state of Guarico, Venezuela. This location is also a habitat mosaic located
at 8*34'N and 67*35'W. The protected area consists of approximately 3,000 ha
and includes tree islands (matas), low lying wet areas (esteros), and sandhills
(medanos). Open grasslands with scattered palms and low stature forests are the
dominant habitats. The vegetation and related drainage patterns have been
described by Troth (1979). The area is characterized by a strongly seasonal
climate divided generally into six dry months (Nov.-Apr.) and six wet months
(May-Oct.). Annual precipitation averages 1478 66 mm (August 1984) and
low lying areas are commonly flooded during the wet season. Temperature varies
only slightly during the year; the average monthly maximum and minimum
temperature is 35.2*C and 21.2C, respectively (Troth 1979). Although the
temperature variation is not as profound as that found in north Florida there is a
distinct seasonal variation in primary productivity. Rainfall is pronounced from
May to October but a drought occurs from December to April. As Robinson
(1986) has documented, rainfall synchronizes the primary productivity of this
tropical ecosystem. The original works on D. marsupialis in Venezuela are
summarized in O'Connell (1979) and August (1984).
In summary, we studied two species of didelphids in two strongly
seasonal environments. While one species, D. virginiana, is adapted to withstand
rather cool temperatures, both species have been able to adapt with respect to
pulsed primary productivity and to strongly seasonal environments.






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


EXPERIMENTAL DESIGN AND METHODS


Field work was initiated at both locations in 1982 and efforts in 1983
focused on marking as many pouch young as possible, thus ensuring that those
female opossums used in the experiment in 1984 were of known age as was their
reproductive status. In Florida, study animals were captured in Tomahawk live
traps set at approximately 0.4 km intervals along a major flow-through creek
system on the property. Both sides of the creek system were trapped and the total
number of trap sites was 50. In Venezuela, a total of 62 Tomahawk live traps was
set within an area measuring about four square kilometers; traps were set at
intervals of 0.25 km along six trap lines radiating from the ranch compound. At
both locations, trapping was conducted for five to seven consecutive days each
month. Most study animals were captured and recaptured during these routine
sessions, although for a few individuals it was sometimes necessary to set traps
just outside their den in order to recapture them; multiple traps were typically set
around dens at the time the young were to be weaned.
In order to study the reproductive strategies of D. marsupialis and D.
virginiana we developed the following experimental protocol (see also Austad and
Sunquist 1986). At each study site three groups of adult virgin females (10 each)
were trapped prior to the breeding season, weighed, measured, and fitted with a
radio collar. Radio telemetry enabled us to precisely locate females, retrap them,
and provision them at set intervals. An examination of the female's pouch at
monthly intervals enabled us to evaluate her reproductive condition, to age and
sex the young, and to toe clip and monitor the growth of pouch young. The three
groups of females were designated as follows: (1) Controls [C] were those that
were monitored only to gather data on the sex, growth, and survivorship of their
offspring and their physical condition; (2) Provisioned [p] were those from whom
the same data were collected but whose diet was supplemented with 125 gms of
catfood and fish at 2-day intervals. Provisioning was initiated from at least three
to four weeks prior to conception (based on the seasonality previously established)
and continued until the end of the breeding season; Delayed Reproductives [DR]
were those whose embryonic young were removed repeatedly from the pouch.
Females reenter estrus within two to eight days following loss of young (Gardner
1982). Adding the gestation period of 13 days to the time of return to estrus
indicates a female could potentially have a new litter every two to three weeks.
By trapping monthly we were able to remove the next set of pouch young when
they were less than two weeks old. The delayed reproductive treatment was
included to yield information on the potential reproductive cost to females who
conceived, but lactated for only a brief interval.






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


Definitions and Criteria


Date of birth.-- The ontogeny of pouch young has been well documented
in D. virginiana and the timing of developmental stages appears to be reasonably
fixed so that from the appearance of certain morphological characteristics young
can be aged to within three days for their first month in the pouch (Reynolds
1952; Gardner 1982). The date of birth was then set by backdating from the
estimated age of the young. This method was also used to age young of D.
marsupialis. In addition, the birth date of many litters was known to have
occurred within a 1- to 3-day period based on repeated examination of individual
females at short intervals.
Length of lactation.-- The length of lactation was measured as the
number of days from the birth date of a litter until lactation had ceased. The latter
was judged to have occurred when milk could no longer be expressed from the
teat. A reduction in mammary development (teat and tissue) usually preceded the
cessation of milk production. Repeated captures of females at the estimated time
of weaning facilitated regular examinations. Weaning of young was thought to
occur just prior to the end of lactation.
Longevity.-- Longevity was measured as the number of days from birth
to death only for those individuals whose birth and death dates were reliably
known.
Survivorship.-- Annual survivorship was measured as the proportion of
females who were known to have survived into their second year of reproduction.
This method essentially represents the minimum number known alive as those few
individuals who disappeared or whose fate was not known were excluded from the
analysis.
Home range.-- Home range sizes of females were computed using the
minimum convex polygon method (Mohr 1947). Range sizes were calculated for
individuals who were monitored for three months or longer. Animals were
occasionally located at night, but most locations represent daytime rest sites, thus
range sizes are likely to underrepresent actual area used. Provisioned females were
located at two-day intervals for at least eight months per year, or two to three
times more often than females in the Control and Delayed Reproductive groups.
Growth rate.-- Growth rates of pouch young were determined from
animals who were removed from females in the Delayed Reproductive treatment,
and from young who became temporarily detached from the teat during marking
or examination of the female. The weight (mass) of young in the pouch was
reliably predicted from tail length for opossums in Venezuela and Florida.
Lifetime reproductive output.-- Lifetime reproductive output of females
was measured as the total number of litters an individual was known to have had
and that she subsequently reared to at least 70 days of age. The 70 days represents
the youngest age at which an opossum was found to have survived on its own,
although most young of this age would probably not survive. Control and






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


Provisioned females were lumped since there was no significant differences in
their longevity or reproductive parameters.
Recapture rate of young.-- Recapture rate of offspring was determined
only for young who were marked in the pouch and subsequently captured when
independent. The age of independence was set at 100-110 days, which also
coincides with the length of lactation.


Some Natural History Data for Didelphis


The natural history of Didelphis has received several recent reviews
(Hunsaker 1977; Gardner 1982; Seidensticker et al. 1987). The young of
Didelphis are born after a 13- to 14-day gestation period, and upon emerging from
the birth canal climb unassisted to the pouch whereupon they attach to a teat.
During their development we can distinguish two phases prior to weaning. A
phase of obligate teat attachment where the young remain with the nipple
constantly in the mouth until approximately 60 days of age. Then follows the so-
called nest phase where the young are left in a nest while the female often forages
alone and returns each day to suckle the young. The nest phase begins to
terminate with weaning when the young commence to forage either by
accompanying the mother or as a single individual. Weaning occurs at
approximately 100 days of age. Since there is an obligate teat attachment phase
the maximum number of young is fixed at 13 in Didelphis, since this is the
average teat number. Shortly after obtaining independence the young gradually
disperse. The dispersal phase may be brief or extended, whereupon they establish
a more or less permanent home range. Wright (1989) noted that surviving female
offspring may remain within their mother's home range for months while male
siblings begin to expand their range within a month or so of independence (see
also Gillette 1980). Although some workers report Didelphis to be nomadic, in
our experience the study populations in Florida and Venezuela showed rather
stable home ranges as adults unless there was some environmental change (e.g.,
drought) that forced them to switch their foraging localities (Sunquist et al. 1987).
Upon attaining sexual maturity in the year after their birth the males
range widely during the breeding season, apparently seeking out females with
which to mate (Ryser 1992). A male will guard and copulate with a female during
her estrous period. Males are known to fight severely among themselves
contesting over a female. The female requires a secluded denning site for rearing
her young, and a suitable foraging area. Once a female becomes established she
tends to remain, utilizing the same home range and denning sites throughout her
entire period of reproduction. In both species, females tend to produce on the
average two litters in the year following their birth. Rarely, does a female attempt
reproduction in the third year. There is reason to believe that the females, even
under optimal conditions, become reproductively senescent when past 28 months






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


of age (see Jurgelski 1974). If a female should lose her litter before weaning she
will come into estrus within 2 to 8 days, and upon conception attempt another
reproductive effort. Normally it takes a female slightly over 100 days to raise a
litter, and thus only two litters are possible in a seasonal environment during the
year following her attainment of sexual maturity. It is possible then to distinguish
two age classes of young animals which we term "first-litter animals" and
"second-litter animals." Given the two birth peaks (Fig. 1), it will be noted that
the litters from the two birth pulses may have different survival advantages. It
will be appreciated that those young deriving from the second litter will attain
sexual maturity in the following year at a smaller body size than their half-siblings
who were born following the first conception of a reproductive year. This is an
important consideration in the analysis of our data. In the following presentation
we explore several issues. Since a female has 13 teats, we ask the question, why
does the mean litter size average around seven young? We wondered what effect
provisioning their mother would have on the development of young.
Furthermore, we investigated the consequences of preventing a female from
undertaking a long lactation. Would such a female attempt to increase her litter
size on subsequent reproductive attempts? Would such a female have an increased
lifespan? Finally, we tried to assess what effect maternal condition had on litter
size and the weaned weight of young.
Our research on the Florida species was more difficult than was the case
in Venezuela. This derives from several factors. First, the population in Florida
existed at a lower density, and trapability of entire litters at the time of dispersal
was more difficult than in Venezuela. A drought in the spring of 1985 caused
most of our Florida females to shift to areas of permanent water. In some cases,
females were inaccessible to us in swamps. This disrupted the feeding program
and did not allow us to replicate the 1984 manipulations. Thus, in the
presentation of results sometimes we refer only to Venezuela where all of the
experimental procedures were replicated in the second year.


RESULTS


For both study areas the maximum longevity of females was about 1,000
days but mean longevity was less than two years. The earliest recorded age at first
reproduction for females was about 245 days in Florida and 172 days in
Venezuela. The seasonal onset of reproduction in Florida is much sharper than in
Venezuela (see Figure 1).
The study site in Venezuela has a pulsed productivity, but during the
rainy season has a higher productivity compared to the sandhills of north-central
Florida. As a result, densities of Didelphis were consistently higher in Venezuela
and home ranges smaller than was the case in Florida (O'Connell 1979, August
1984, Sunquist et al. 1987, Ryser 1992).








BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)






REPRODUCTIVE SEASONALITY--FLORIDA
(1983-1988, N 304)

NUMBER OF LITTERS BORN


WEEKS OF THE YEAR


REPRODUCTIVE SEASONALITY--VENEZUELA
(1983-1986, N 238)

NUMBER OF LITTERS BORN
70

60-

50

40

30

20

10-

0-
1 5 9 13 17 21 25 29 33 37 41 45 49
WEEKS OF THE YEAR


Figure 1. Reproductive seasonality of opossums in Florida and Venezuela.






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


Mortality sources differed between Venezuela and Florida. In Florida,
adult females were killed by bobcats (Felis rufus, n=4); great homed owls (Bubo
virginianus, n=3); alligators (Alligator mississippiensis, n=2); foxes (Urocyon
cinereoargenteus, n=2); and humans (n=3). In Venezuela confirmed predation
included the ocelot (Felis pardalis); boa (Constrictor constrictor); caiman
(Caiman crocodylus), but above all the screw worm (Callitroga sp.) inflicted an
unrelenting morality in the llanos (Wright 1989, Sunquist unpubl.).
First, let us place the reproductive performance of the two species in
perspective. Here we include additional data from Venezuela and Florida, since
we had several parallel studies going on over the years and accumulated a great
deal of data for non-manipulated females. In Florida, most females produced only
two litters and the mean litter size was seven (Table 1). At the onset of the first
reproductive period, 96.8% of adult females had young in the pouch (n= 185). Of
those females that did not produce, four were very old and did not attempt
reproduction in their third year. At least 91.1% of the females in the population
gave birth to a second litter (n= 156). Of the 14 that did not reproduce, 8 were old
individuals. Some females attempted a third litter (7.4%; n=68). Only one
female successfully reared three litters in a given calendar year. In Florida, none
of the females attempted to have young in the same year as their birth. The age of
first reproduction by a female in Florida varied from 245 to 345 days depending
on whether she was a first- or second- litter female.
In Venezuela, at the onset of the first reproductive period, 93 % of the
females (n=200 of 215) had pouch young. Of the 15 without young in the pouch,
nine were females weighing less than 1 kg (very young) and four were judged to
be old. In the second attempt at reproduction, 97% of the females had young in
the pouch (n=59). The two females without young were judged to be old. As in
Florida, 7.4% of the females in Venezuela attempted to raise a third litter
(n=136). Furthermore, in Venezuela, 7% of the females (n=84) had young in
the same year as their birth. Age at first reproduction in Venezuela varied from
172 to 345 days. As in Florida, only one female in Venezuela successfully reared
three litters in a single calendar year. The proportion of females in the population
which were breeding are the minimum estimates since some females may have had
a litter but were not recaptured to confirm.
In both habitats, reproduction is highly seasonal. Figure 1 summarizes
the time of birth for the first and second litters in Florida and Venezuela. In
Florida, the birth peaks occur in the second week of February and the last week of
May. In Venezuela, the birth peaks are about three weeks later than in Florida.
The figure indicates also that a minority of females will attempt to rear a third
litter.
Our two treatment groups did not differ in home range size from the
controls; this result held for both Florida and Venezuela (Table 2). The extent of
the home range does not, however, reflect activity, and we did not monitor
movements on an hourly basis during the night. Hence, the control groups may
well have ranged more within their home range than the treatment groups. It






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


Table 1. Litter size ( SE) of non-manipulated female Didelphis.


Location 1st Litter 2nd Litter t-test


FLORIDA (1983-88) 6.68 0.10 6.57 0.20 p = 0.607
(n = 145)a (n = 120)a

VENEZUELA (1983-86) 7.38 0.16 7.95 0.46 p =0.252
(n =87) (n = 40)


hncludS data collected by D. Wrigh in 1987-88.


Table 2. Home range size analysis of female Didelphis.


Treatments


Location C p DR Test


Home range size
(ha SE)

VENEZUELA 34.0 5.1 29.3 4.9 38.1 5.5 ANOVA
(n = 14) (n = 15) (n =12) p > 0.05

FLORIDA 58.7 9.6 84.7 9.9 73.1 6.7 t-test, C vs. p
(n = 18) (n = 17) (n = 6) p = 0.056

Months monitored

VENEZUELA 9.0 8.5 12.1
(range 6-18) (5-16) (5-18)

FLORIDA 9.2 9.6 11.8
(3-18) (3-23) (8-16)






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


should be noted that the Venezuela population showed consistently smaller home
ranges, reflecting the higher productivity of the Venezuelan habitat when
compared with the sandhills of Florida.
The temporal patterning of reproduction is summarized in Table 3. The
interval between the birth of the first and second litters was of similar duration for
provisional and control females. The difference in interbirth interval was not
significant for Venezuela but approaches it for Florida. The duration of lactation
for the first and second litters were approximately the same for the provisioned
and the control females at both locations. However, the length of lactation for the
second litter was 1-2 weeks longer. A comparison of the duration of lactation for
the first litter and the interval between the birth of first and second litters indicates
that females were lactating and pregnant at the same time.
There was a significant difference in the weight of a female at first
breeding, depending on whether she was born in the first or second litter of the
previous year. This difference was most pronounced in the Venezuelan
population. First-litter females weighed on average 1.63 kg at first conception,
while second- litter females weighed 1.17 kg (see Table 4). In Venezuela second-
litter females lactated for a longer period of time during the rearing of their first
litter than did the older cohort (see Table 5). When we examined the effort of
provisioning it was clear that the smaller second-litter females could rear a litter
more quickly than comparable aged controls. Thus, provisioning had a positive
effect (see Table 6).
During the teat-attachment phase there was an occasional loss of young.
The number of young lost from a litter varied from one to four (mode= 1) and
there was no apparent differential by sex. All losses occurred when the young
were from 17 to 50 days of age. There were twice as many reductions in
provisioned versus control litters in both Venezuela and Florida but the
differences were not significant (Table 7).
The mean litter size for both Florida and Venezuela did not differ
significantly between the first and second litters born (Table 1), nor was there any
effect of treatment on litter size when provisioned animals were compared with
controls (see Table 8). When, for individual females, we examined successive
litters, that is change in litter size from first to second as a function of treatment,
those females that were provisioned tended to increase their litter size slightly in
both Venezuela and Florida (Table 9). There was also a suggestion in the
Venezuelan population that the experimental females that were not allowed to
reproduce (DR's) attempted larger litter sizes on successive conceptions until the
end of the reproductive season when litter size declined.
Figures 2 and 3 summarize the growth data for pouch young during the teat-
attachment phase. There appears to be no differential investment in male or
female offspring during the first 60 days of lactation. Regression analysis
indicated no significant difference between males and females in slope (Venezuela:
t=0.963, 1 d.f., p=0.3359; Florida: t=-0.985, 1 d.f., p=0.3260). It will be
appreciated that tail length is a very good predictor of body weight for young in







BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


Table 3. Temporal pattern of reproduction.


Treatments


Location C p t-test


Interval (days SD) between
birth of 1st and 2nd litter
VENEZUELA 97.7 8.4 95.0 4.7 p > 0.20
(n = 28) (n = 14)
FLORIDA 97.3 5.0 94.2 7.1 p > 0.05 < 0.10
(n = 64)a (n = 12)
Length of lactation
(days SD) for 1st litter
VENEZUELA 93.2 5.5 93.1 2.8 p > 0.90
(n = 18) (n = 14)
FLORIDA 94.1 5.0 92.0 4.1 p > 0.70
(n = 15) (n = 6)
Length of lactation
(days SD) for 2nd litter
VENEZUELA 105.2 6.5 107.3 6.5 p > 0.50
(n = 9) (n =7)
FLORIDA 102.5 9.8 99.3 7.8 p > 0.40
(n = 17)a (n =7)

l"nchale data molcted by D. Wright in 1987-88.






Table 4. Weight (kg SD) of control females at first breeding as a function of age.


Location 1st Litter 2nd Litter t-test


VENEZUELA 1.63 0.16 1.17 + 0.18 p < 0.005
(n =23) (n = 17)
FLORIDA 1.87 0.17 1.26 0.46 p < 0.05
(n = 18) (n = 16)


124







SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS 125


Table 5. Length of lactation (days SD) by 1st and 2nd litter control females for Ist litter of year.


Location 1st Litter Females 2nd Litter Females t-test


VENEZUELA 92.5 5.6 97.3 5.0 p > 0.05 < 0.1
(n= 11) (n = 4)







Table 6. Length of lactation (days SD) by 2nd litter females for 1st litter of year.


Treatments


Location C p 1-test


VENEZUELA 97.3 5.0 93.7 1.4 p > 0.05 < 0.1
(n=4) (n=6)







Table 7. Number of litters in which a size reduction occurred as a function of treatment.


Treatments


Location C p Fisher's exact test


VENEZUELA 5/30 10/30 p = 0.116

FLORIDA 1/15 3/13 p = 0.356






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


Table 8. Litter size and sex ratio analysis.


VENEZUELA FLORIDA
Treatment Treatment


C p C p


Litter size ( SD) 7.50 2.02 7.75 2.01 6.80 1.53 7.31 1.81
at start of lactation (n = 36) (n = 36) (n = 26) (n = 29)

Litter size at 7.14 2.15 7.14 1.70 6.56 1.81 7.17 2.16
weaning (n = 22) (n = 21) (n = 9) (n = 6)

Sex ratio (M:F) 132:138 158:121a 81:70 103:81a
at start (n = 36) (n = 36) (n = 23) (n = 25)

Sex ratio at 75:82 85:65b 28:31 25:18
weaning (n = 22) (n = 21) (n = 9) (n = 6)

Number of male 18/31 20/32 13/23 12/19
biased litters

Number of litters 5 4 0 6
with equal sex ratios


ap < 0.05, binomil test
bp > 0.05 < 0.1




the pouch. On the other hand, during the nest phase the young males begin to
increase in size relative to their sibling females, and at weaning young males
average about 3 to 10 gm heavier than females. When we examined the control
versus experimental litters for both Venezuela and Florida, the weight at weaning
of young from provisioned females was significantly higher (see Table 10).
As reported by Austad and Sunquist (1986), one effect of provisioning is to
bias a female's litter towards a larger percentage of males (Table 8). This is in
part a function of the condition of the female not only at the time of conception
but also at the end of lactation, which would affect the second litter. Thus it is
not unlikely that females producing their first litter will on average be in better
condition than when they produce the second litter so we would expect a higher
percentage of first litters to be male biased. In general, there were more litters
that were male biased for provisioned females compared to controls. For
example, in Florida in 1984, 11 of 13 litters were male biased (p < 0.05),
whereas in 1985, the year of the drought, only one of six litters was male biased






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


Table 9. Successive litter size.


Treatments


Location C p DR


VENEZUELA (n = 13) (n = 14) (n = 14)
Litter size increased
from 1st to 2nd 5/13 11/14 11/14
Decreased 6/13 2/14 0/14
No change 2/13 1/14 3/14
FLORIDA (n = 9) (n = 10) (n = 7)
Litter size increased
from 1st to 2nd 2/9 5/10 4/7
Decreased 2/9 4/10 2/7
No change 5/9 1/10 1/7


Fisher's exact lt, comparing the aociation of litter size chang by tatnrUnt.
Venezula: Cverm p, p = 0.055; Florida: Cversus p, p = 0.657.








Table 10. Weight (g SD) of young Didelphis at weaning.


Treatments


Location C p r-test


First litter
VENEZUELA 91.7 17.9 151.3 33.0 p < 0.0005
(n = 29) (n = 15)
FLORIDA 102.9 1.8 153.0 12.4 p < 0.0004
(n =5) (n = 5)
Second litter
VENEZUELA 81.8 21.3 128.2 33.7 p < 0.0005
(n = 14) (n = 24)







BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


OPOSSUM GROWTH DATA
FEMALES (VENEZUELA)


LOG TAIL LENGTH (mm)


OPOSSUM GROWTH DATA
MALES (VENEZUELA)


2 2.4 2.8 3.2 3.6 4 4.4 4.8 5.2
LOG TAIL LENGTH (mm)





Figure 2. Body weight (mass) of female and male opossum young in the pouch as predicted by tail length
(Venezuela).









SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS 129





OPOSSUM GROWTH DATA
FEMALES (FLORIDA)
5

logY = 1.4817 IogX 2.4648

4 r= .9935

N = 86


3 -


2 I I













1.6 2 2.4 2.8 3.2 3.6 4 4.4 4.8

LOG TAIL LENGTH (mm)





OPOSSUM GROWTH DATA
MALES (FLORIDA)
5

4.5 logY 1.4615 logX -2.3815 ++

r2= .9918
4-
N = 71
3.5 -

3-
0 +


1 -

0 1.5-

1 +



0

-0.5 I
1.6 2 2.4 2.8 3.2 3.6 4 4.4 4.8

LOG TAIL LENGTH (mm)





Figure 3. Body weight (mass) of female and male opossum young in the pouch as predicted by tail length

(Florida).






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


(see Table 8). The same trend was evident for provisioned females in Venezuela
where 20 of 32 litters were male biased (p > 0.07 < 0.08). Females, whether
provisioned or not, that are in good condition throughout lactation produce male-
biased litters. We can look at these data by comparing control and provision
females and looking at females in both groups that gained weight over the interval
of lactation. Some control females, of course, gained weight even though they
were not provisioned. An inspection of Table 11 indicates that regardless of the
treatment, those females that showed weight gains over the course of lactation
tended to bias their litters towards males. Of course, the provisioned females
were more predictable in terms of biasing the litter to males, by producing not
only a greater mass of young at weaning, but also increasing their weight
throughout the lactation period. The data for Florida are suggestive of the same
trends for Venezuela but we had a smaller sample size.
In Table 8 we examined the litter size and sex ratio for Venezuela and
Florida. While there was no difference between control and provisioned females
with respect to litter size, the sex ratio was definitely biased toward males at the
start of lactation and at the end of lactation for the provisioned females. If we
perform a similar analysis comparing first litter with second litter, again we find
in the second litter that provisioned females biased their litters toward males (see
Table 12).
The sex ratio of litters of older, that is second-year females, in Venezuela
was biased toward females (69:95, n=22, p < 0.04). Similarly, the proportion
of litters that were female biased (14 of 19) was significantly different (p=0.0318)
from that expected by chance. In Florida, however, there was no sex ratio bias in
litters of second-year females (37:35, n= 10, p > 0.4) or in the number of biased
litters (7 of 10, p=0.172).
The survivorship of young as a function of treatment is examined in
Table 13. For the Venezuelan data, male offspring of provisioned females were
recaptured post-weaning significantly more often than males from control litters.
The comparison was not significant for the Florida data. We may examine the
effect of our treatment on the survivorship of reproducing females. In Table 14
we present data for the three treatment groups suggesting that females who were
denied the stress of lactation (DR) tended to survive longer. The differences in
survivorship approaches significance for Venezuela. In Table 15 we present
"longevity" data based on days from birth until the animal died, thus do not
represent calendar ages. These data indicate that in Venezuela, at least, those
females that were experiencing delayed reproduction through successive loss of
litters tended to live longer than the control females, although the differences are
not significant.
Lifetime reproductive effort by females of both species is portrayed in Table
16. The results for Florida and Venezuela are comparable. Most females bear
from one to two litters in their lifetime (75% Florida; 89% Venezuela). It






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


Table 11. Effect of female condition on sex ratio of litters by treatment.


Number of litters with
biased sex ratios


Weight gain or loss between initiation Fisher's
of lactation for 1st and 2nd litters Male Female exact test


VENEZUELA
Controls Weight increased 11 3 p < 0.004
Weight decreased 0 5
Provisioned Weight increased 10 3 p < 0.04
Weight decreased 1 4
FLORIDA
Controls Weight increased 5 1 p > 0.20
Weight decreased 1 2
Provisioned Weight increased 4 2 p < 0.08
Weight decreased 0 4







Table 12. Litter size and sex ratio analysis by year and 1st and 2nd litters.


Location Litter size Sex ratio (M:F) n


VENEZUELA
Controls 1984 1st litter 7.2 40:52 10
1984 2nd litter 6.7 32:28 9
1985 1st litter 8.4 40:52 11
1985 2nd litter 7.7 20:26 6
Provisioned 1984 1st litter 6.1 32:29 10
1984 2nd litter 9.0 45:36 9
1985- Ist litter 7.8 49:29 10
1985 2nd litter 8.4 32:27 7
FLORIDA
Controls 1984 1st litter 7.2 19:24 6
1984 2nd litter 7.0 8:6 4
1985- 1st litter 6.1 35:26 10
1985 2nd litter 7.6 19:14 5
Provisioned 1984 1st litter 7.6 45:31 11
1984 2nd litter 6.7 26:14 6
1985 1st litter 7.7 22:24 6
1985 2nd litter 7.3 7:8 6







BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


Table 13. Recapture rate of independent young.


Treatments

2-sample
Location C p binomial test


VENEZUELA
Males 16/71 30/85 p < 0.05
Females 20/82 23/70 p > 0.10
FLORIDA
Males 13/29 11/33 p > 0.10
Females 18/36 19/34 p > 0.30



Table 14. Annual survivorship of female Didelphis.


Treatments


Location C p DR Chi-square test


VENEZUELA p > 0.05 < 0.1
Alive 3 1 6
Dead 15 9 6
% Alive 17 10 50
FLORIDA p > 0.9
Alive 6 5 4
Dead 17 16 9
% Alive 26 24 31



Table 15. Longevity (days SD) of female Didelphis.


Treatments


Location C p DR Test


VENEZUELA 554.4 135.4 506.0 80.8 579.3 100.0 ANOVA
(n= 16) (n = 11) (n= 12) p > 0.25
FLORIDA 559.2 187.3 483.2 76.6 404.7 137.5 t-test, C vs. DR
(n = 12) (n = 14) (n = 9) p = 0.062







SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


Table 16. Lifetime reproductive output of female Didelphis.


Number of females


Number of litters reared VENEZUELA FLORIDA
to 70 days of age (n = 37) (n = 39)


1 16 12
2 17 17
3 4 6
4 0 3
5 0 1








Table 17. Litter size of delayed reproductive.


Litter size


Location 1st litter 2nd litter 3rd litter


VENEZUELA 6.286 8.214 8.643
(n = 14) (n = 14) (n = 14)

FLORIDA 6.143 6.143 5.714
(n = 7) (n = 7) (n = 7)


Scheffe's ist significant differnc between Ist vs. 2nd litter size in Venzuela (p < 0.05); 2nd not diffrnt from 3rd.
No significant diffeence in Florida.






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


would appear that these two species are geared to perform a maximum
reproductive effort in the year following their birth.
Females subjected to a reduced lactation time exhibit a tendency on
subsequent pregnancies to increase their litter size and then decline in litter size,
perhaps due to ovarian senescence. This was evident only in the Venezuelan
population (Table 17).


DISCUSSION


We have presented the study of two didelphid species in two rather
different environments, although both study sites exhibit seasonal pulses in
primary productivity. Both habitats have experienced dramatic changes in
vegetative cover during the last 5,000 years deriving from global climatic
changes, and to some extent the opossums can be viewed as "pioneers."
The ultimate puzzle is how the female regulates her litter size and the sex
ratio. Male opossums appear to have a straightforward reproductive strategy--
mate with as many females as possible (Ryser 1992). Females have a different set
of priorities--mate with a strong, dominant male; seek and maintain a secure den
site in an area which will sustain her through the rearing of her two litters. We
have by means of some simple field experiments attempted to clarify some of the
issues.
It would appear that in at least two species of Didelphis the female has
some control over her litter size and the sex ratio of each litter. The exact
mechanisms whereby she exercises such control are poorly understood.
A female who has an enhanced food supply will bias her litter towards
males. The young of provisioned females achieve higher weaning weights when
compared with controls and perhaps a better survivorship potential. Females
denied a prolonged lactation will conceive periodically after the loss of the young
and often will increase their litter size until age and physiological senescence take
their toll. The foregoing conclusion suggest a trade-off between aging and
nutritional plane. This is further suggested by an examination of weaning weights
of first- and second-litter young (Table 10). Lactation was one to two weeks
longer for the second litter, but young were significantly lighter at weaning than
the first litter. One should remember that the female Didelphis in the year
following her birth in seasonal environments has only about 400 days in which to
successfully reproduce. Recall that in such seasonal environments a female must
invest about 228 days in reproducing two litters. The time frame is tight and
pregnancy commences before lactation ceases, a phenomenon also discussed by
Kiltie (1988) for other vertebrates.
Reproducing a surplus of males when she is in good physical condition
can enhance the spread of 50% of the female's genetic material. The males are
polygynous and, although requiring extra energy for their growth, are certain to







SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


inseminate many females should they survive to adulthood (Austad and Sunquist
1986).
These experiments suggest fruitful avenues for future research. Didelphis
is an excellent model. Females are easily trapped and have a finite and limited
opportunity to reproduce.
Didelphis albiventris has not been studied in the same detail as have D.
marsupialis and D. virginiana. What information we do have indicates that it is a
habitat generalist with feeding habits quite similar to other species in the genus.
In Uruguay, females have an average litter size of 9.4, while farther to the north
in Argentina the mean number of young per litter was recorded at 7.1 (Barlow
1965). In seasonal environments, reproduction tends to be highly pulsed and an
average of two litters are produced per female in their breeding year. Once again,
the seasonality of rainfall and primary productivity appears to regulate the timing
of reproduction (Barlow 1965; Crespo 1982; Cerqueira 1984). In captive studies,
Cerqueira (1984) found that litter size was maximal in heavier females. Litter size
for Didelphis virginiana and D. marsupialis appears to vary somewhat with
latitude. For both species larger litters are born in populations that occur at
higher latitudes than populations occurring nearer the equator (O'Connell 1979).
In this study provisioned females had slightly larger litters than controls.
A female in excellent physical condition tends to wean young at a higher
body weight than females in poorer condition. Weight at weaning may be
enhanced by provisioning the lactating female. Provisioned females tend to have
litters biased toward males, but control females that maintain excellent body
condition also produce litters biased toward the male sex. While there is no
apparent difference in the growth rate of pouch young when the sexes are
compared during the teat attachment phase, young males are weaned at a slightly
heavier weight than their sister siblings. The mechanism whereby a female
regulates the size of her litter and the sex bias in the litter is not known. We do
know, however, that for Didelphis virginiana the number of ova shed exceeds the
number of young born and usually the female gives birth to more young than she
can possibly rear. The maximum number of young born that has been recorded is
25 and the maximum young that reached the pouch, 21; but the largest permissible
litter size is just 13 given the obligate teat attachment phase and the mean number
of 13 teats per female (Reynolds 1952; Hartman 1952).
Our field data indicate that on the average a female of either species is
able to rear just two litters a year. Less seasonal environments may permit the
rearing of a third litter by a larger percentage of females than we found in the
Venezuela and Florida study areas. In accordance with laboratory data, females
appear to go through one year of reproduction, usually in the year following their
birth (Jurgelski 1974). Although some of our females which were delayed in
reproduction attempted to produce litters throughout the reproductive season, they
were, of course, denied the opportunity to rear a litter. Upon losing her litter a
female will usually come into estrus within eight days. Thus a female has the
capacity to conceive over a period of about 12 months. But the long lactation time






BULLETIN FLORIDA MUSEUM NATURAL HISTORY VOL. 36(4)


usually allows the female to only raise two litters in seasonal environments. In
northern Venezuela, Cordero (1985) reported that mean maximum longevity for
D. marsupialis was about 21.8 months. Data from captives are in accord with the
results from the field (Jurgelski 1974). Some of our delayed reproductive females
lived longer than control or experimental females that reproduced. However,
although there is obviously some physiological stress to reproduction the life span
of a female is not markedly changed by not reproducing and her reproductive
potential is in no way extended. Indeed it appears that the species are geared to
produce two litters in the year following their birth whereupon physiological
senescence reduces the probability of further reproduction in the following year.
Thus the average reproductive output for females of these species in the two
habitats is about 14 young. Provisioning or an excellent nutritional intake can
bias the sex ratio of the litter toward males and slightly increase the mean litter
size, but does not extend the female's reproductive period beyond the single year
of maximum reproductive effort. In a way, the females of Didelphis behave as if
they were "annuals" geared to a single extended season of reproduction.
The bias toward males by healthy females appears to increase the
probability that the female will disseminate at least half of her genotype in the
next generation. While males do not appear to be more expensive to raise based
on the growth data during the teat attachment phase, clearly they are taking more
nutrition just prior to weaning given the increase in growth over that displayed by
their sister siblings. Post-weaning, the growth of males is appreciably greater
than that of females. A large male has the potential to mate many females in the
following year, thus it would appear that if a female can afford to produce large,
healthy males at weaning she will avail herself of this opportunity. For a further
discussion of the phenomenon see Austad and Sunquist (1986).
Didelphis reproduction patterns should not be considered typical for the
New World marsupials. Data concerning the life history of the genus Caluromys
presented by Charles-Dominique (1983) and Charles-Dominique et al. (1981)
convince us that within the subfamily Caluromyinae different selective forces may
have been at work in shaping life history strategies (Atramentowicz 1982, Perret
and Atramentowicz 1989, Eisenberg 1989, Julien-Laferribre and Atramentowicz
1990). The same caution may well be applied to an analysis of the life history of
the last extant species of the Microbiotheriidae Dromiciops australis (Mann 1958;
Marshall 1978). On the other hand, the analysis of reproductive data for some
species of Marmosa suggests a convergence in life history strategy towards
Didelphis (O'Connell 1983; Eisenberg 1988). It should be noted that Pine et al.
(1985) have established significant evidence that Monodelphis dimidiata in the
pampas of Argentina may be a near semelparous mammal and approximate in its
reproductive strategy the syndrome described for Antechinus stuartii (Lee and
Cockburn 1985).






SUNQUIST & EISENBERG: REPRODUCTION IN FEMALE DIDELPHIS


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