Reproductive strategies of sympatric freshwater emydid turtles in northern peninsular Florida

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Reproductive strategies of sympatric freshwater emydid turtles in northern peninsular Florida
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Reproductive strategies of sympatric freshwater emydid turtles in northern peninsular Florida
Jackson, Dale R.

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Biological Sciences
Volume 33 1988 Number 3


Dale R. Jackson


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Dale R. Jackson

Frontispiece. Alligator nest on Payne's Prairie, Alachua County, Florida, opened to expose
seven clutches of Pseudemys nelsoni eggs and one clutch of Trionyx ferox eggs (far lower right)
surrounding the central clutch of alligator eggs. Most of the alligator eggs had been destroyed
earlier by raccoons.


Dale R. Jackson*


Florida has the highest species diversity of emydid turtles in the New World. Four
relatively large, closely related species (Pseudemys floridana, P. nelsoni, Trachemys scripta, and
Deirochelys reticularia) occur sympatrically in lentic habitats in northern peninsular Florida,
although two (P. nelsoni and T. scripta) are essentially parapatric. Fossils of Pleistocene age or
older document a lengthy period of coexistence for these species in Florida.
The basic reproductive strategy of all four species involves four features: (1) multiple,
large clutches; (2) relatively small eggs; (3) delayed maturity; and (4) extended longevity. This
same basic strategy is found in most smaller, previously studied temperate turtles. In Florida,
however, the long growing season not only permits more clutches (four to six) per year but also
allows for larger body sizes and consequently larger clutches than are characteristic of most
temperate species. For each of the two largest species, (Pseudemys floridana and P. nelsoni)
clutch size is more highly correlated with body mass or volume than with plastral length.
Major temporal differences in reproduction exist among the species. Pseudemys nelsoni
and Trachemys scripta nest during spring and/or summer. In contrast, P. floridana and
Deirochelys reticularia begin nesting in September or October and continue through March (D.
reticularia) or June (P. floridana). The two patterns are contrasted as "summer" and "winter"-
nesting patterns. Field temperatures permit immediate and continuous development of eggs of
summer-nesting species following oviposition. Eggs of winter-nesting species, on the other hand,
become dormant below 20"C and initiate or resume development when soil temperatures exceed
this in the spring. Laboratory incubation experiments suggest that innate developmental
differences may exist between eggs representing each of the two nesting patterns. Hatchlings of
all four Florida species, unlike most northern species, apparently do not overwinter in the nests
but instead emerge during the summer rainy season.
Summer-nesting is viewed as the conservative retention of a reproductive pattern typical of
most north temperate reptiles. Large-bodied, fecund summer-nesting species may benefit from
predator satiation. Hypothetical advantages of winter-nesting include rapid hatchling growth,
reduced nest predation, and interspecific competitive advantage.

*Florida Natural Areas Inventory, The Nature Conservancy, 254 East Sixth Avenue, Tallahassee, FL 32303, USA, and Florida
State Museum, Gainesville, FL 32611, USA.

JACKSON, D.R. 1988. Reproductive Strategies of Sympatric Freshwater Emydid Turtles in
Northern Peninsular Florida. Bull. Florida State Mus., Biol. Sci. 33(3):113-158.



El estado de Florida demuestra la mayor diversidad especifica de tortugas emididas de las
Am6ricas. Coexisten cuatro species relativamente grandes y afines (Pseudemys floridana, P.
nelsoni, Trachemys scripta, Deirochelys reticularia) en ambientes dulceacuicolas del norte de la
peninsula, aunque dos (P. nelsoni y T. scripta) son practicamente parapAtricas. F6siles del
Pleistoceno o mis antiguos documentan un period largo de coexistencia para estas species en
La estrategia reproductive de las cuatro species es similar a la de la mayoria de las
tortugas menores, ya estudiadas de la zona templada: multiples nidadas grandes de huevos
relativamente pequefios, en combinaci6n con madurez tardia y gran longevidad. En Florida, en
contrast, la 6poca favorable larga permit mas nidadas (cuatro a seis) a la vez que mayor
tamafo de cuerpo y por ende mayores nidadas que en la mayoria de las species de climas
templadas. En las dos species mayores (Pseudemys floridana y P. nelsoni) el tamafio de la
nidada se relaciona mis con el peso o el volume del cuerpo que con el largo del plastr6n.
Hay diferencias significantes entire estas species respect a la 6poca de anidaci6n.
Pseudemys nelsoni y Trachemys scripta anidan durante la primavera o el verano, mientras que P.
floridana y Deirochelys reticularia comienzan a anidar en septiembre u octubre y contintan hasta
marzo (D. reticularia) o junio (P. floridana). Los dos patrons se distinguen como anidaci6n de
"verano" y de "invierno." Las temperatures del suelo permiten desarrollo inmediato y continue
de los huevos depositados durante el verano. En contrast, los huevos depositados durante el
invierno quedan inactivos debajo de 20 grades (C) e inician o reasumen el desarrollo cuando la
temperature del suelo supera este grado en la primavera. Incubaci6n experimental sugiere
diferencias innatas en el desarrollo entire los huevos de cada patr6n. En contrast con las
species nortefias, tortugas recien nacidas de las cuatro species no parecen pasar el invierno en
los nidos, sino que salen durante la 6poca lluviosa del verano.
Se consider la anidaci6n durante el verano como la retenci6n del patr6n reproductive
tipico de la mayoria de los reptiles de la zona templada. Las species fecundas de cuerpo grande
pueden beneficiary por saciar a los depredadores. Ventajas hipotdticas de anidar en el invierno
incluyen crecimiento rapido de los recidn nacidos, menor depredaci6n de los nidos, y ventajas en
la competici6n entreespecifica.


Introduction..................... ....................................................................................... 116
A cknowledgem ents.............. ....................................................................................................... 118
T he Species...................................... ............................................... ........................................ 118
Materials and Methods.............................. ...................... ............................... 120
Incubation and Development ........................................................... 121
R esults.......................................... ............................................................................... .............. 121
Reproductive Param eters ......................................................... ............................. 121
Reproductive Seasonality.......................................................... ............................... 126
Development and Hatchlings........................................................ .... 130
D iscussion........................................................................................................................... . 134
Seasonal Patterns of Reproduction.......................................... .................................... 140
Literature Cited............................... ............................................ ................................. ......... 152



As a group, turtles have remained as conservative in life history tactics as
they have in morphology. They are one of the few major extant orders of
ectothermic tetrapods never to have evolved viviparity (Packard et al. 1977;
Tinkle and Gibbons 1977; Shine 1985), nor is there any evidence of post-
nesting parental care. Further, and in contrast to all other vertebrates, the
evolutionary commitment to a rigid, protective exoskeleton prevents expansion
of the body cavity of females to accommodate proportionately large amounts
of reproductive matter. Selection therefore has been restricted primarily to the
trade-off between egg size and clutch size, clutch frequency, sex ratio, nesting
behavior, and, as I suggest in this paper, the temporal aspect of reproduction.
There is now an extensive literature describing reproductive cycles for
most temperate North American turtles, comprehensively reviewed by Moll
(1979) and Ewert (1979, 1985). Drawn mostly from work with relatively small
carnivorous and omnivorous turtles, these studies outlined a basic reproductive
strategy that includes the following features: correlations among female size,
clutch size, and egg size; occurrence of multiple annual clutches, extra-oviducal
migration of ova, follicular atrophy and corpora luteal regression; and the
division of the female reproductive cycle into a series of intergrading phases.
The purpose of this paper is to compare the reproductive patterns of four
closely related species of turtles known to have existed in sympatry since at
least the early Pleistocene, and to relate them to some of the biotic and
physical environmental parameters that may have acted as selective agents in
their evolution. The two species of Pseudemys studied are among the largest of
North American freshwater turtles and are obligate herbivores.
For most groups of reptiles, comparative studies of reproductive cycles
among closely related sympatric species are scarce. Such analyses have been
conducted more frequently with amphibians (e.g. Organ 1961; Tilley 1968;
Zweifel 1968; Heyer 1969; Caldwell 1973, 1987; Crump 1974; Wilbur 1977), a
group in which large assemblages of locally sympatric congeneric or
confamilial species often occur. Among reptiles this approach has been
restricted chiefly to lizards (e.g. see Huey et al. 1983; Stearns 1984; Pianka
1986; Tinkle and Dunham 1986; Vitt 1986; and references therein). However,
individuals in both of these groups generally have only short to moderate
lifespans. Comparative studies of long-lived reptiles, such as turtles and
crocodilians, are equally essential to the synthesis of life history tactics theory.
Nonetheless, detailed ecological studies of multispecies communities of turtles,
among the longest-lived of all vertebrates (Gibbons 1976, 1987), remain limited
(e.g. Mahmoud and Klicka 1972; Gibbons et al. 1982; Congdon et al. 1987).
Generally, these studies have revealed only minor seasonal reproductive
differences among sympatric species, though Goode and Russell (1968) and


Legler (1985) have noted important temporal differences among the
reproductive patterns of sympatric Australian pleurodires (family Chelidae).
Unfortunately, fossil records at the species level for all these groups are poorly
documented or nonexistent. Since their zoogeographic histories and durations
of sympatry are therefore subject to conjecture, hypotheses attempting to
account for differences in reproductive strategies among them must remain
guarded. Recent ecological and paleontological studies (Pregill and Olsen
1981; Ricklefs 1987) have drawn attention to the kinds of misconceptions (e.g.
interpretations of biogeography and community diversity) that may be
introduced into ecological theory from a lack of historical perspective. The
present study is among the first to compare life history strategies in a group of
closely related species that are known, from well documented fossil records, to
have evolved in sympatry.
In North America, turtles, and the family Emydidae (subfamily
Emydinae) in particular, reach their greatest species diversity and body size in
northern Florida. Four closely related emydines inhabit similar lentic
situations in northern peninsular Florida (see Gilbert 1978 for general habitat
descriptions). Two of the species, namely Pseudemys nelsoni and Trachemys
scripta, are nearly parapatric but may inhabit the same bodies of water where
their ranges meet; however, their geographic overlap was more extensive in the
Pleistocene (see below). The other five species-pairs are currently sympatric in
the study area. Though displaying minor microhabitat differences, three or
even all four species frequently coexist in the same waters. Interestingly, the
study area approximates the present northern limit of one species (Pseudemys
nelsoni), the present southern limit of a second (T. scripta), and the zone of
intergradation between two subspecies of each of the other two (P. floridana
and Deirochelys reticularia). All four species have histories in Florida
documented by fossils of Pleistocene age or older (see below). The relatively
equable Florida climate allows these species to remain active nearly year-round
and precludes the necessity of an extended period of brumation characteristic
of most north-temperate turtles. If interspecific competition among sympatric
turtles leads to the evolution of different nesting seasons as suggested by Moll
(1979), then one might expect evidence of this in peninsular Florida.
In this paper, I present empirical life history data for populations of the
above four species from northern peninsular Florida. Other workers (e.g. Carr
1940, 1952; Marchand 1942; Thomas 1972; Iverson 1977; Gibbons et al. 1982;
Congdon, Gibbons et al. 1983) previously have reported aspects of
reproduction in these species. However, insufficient data led them in some
instances to improper conclusions that concealed important adaptive seasonal
differences in reproductive cycles.
Reptilian eggs have received considerable scientific attention in the past
two decades. Ewert (1979, 1985) has reviewed much of our knowledge of the
development and physiological ecology of chelonian eggs. That two of the


species in the present study frequently nest during the coolest months of the
year prompted me to investigate the relationship between temperature and
embryonic development in these turtles. Of particular interest was whether
there might exist, among eggs of different species, developmental adaptations
to distinctly different temporal patterns of nesting.


I thank K. Ainslie, M. Conner, H. Converse, D. Deitz, J. C. Dickinson, Jr., S. Flamand, R.
Franz, D. Gicca, J. Iverson, H. Kochman, W. Link, P. Meylan, C. A. Ross, C. R. Smith, R. Vogt,
and M. Wygoda for their assistance in collecting turtles and eggs. I am especially grateful to
Justin Congdon, Mike Ewert, Whit Gibbons, and John Iverson for generously sharing
unpublished information and to Iverson in particular for bringing a number of pertinent
references to my attention. Ed Moll not only introduced me to my first turtle gonad but also
critically reviewed the manuscript and offered helpful comments, as did J. Steve Godley. Certain
aspects of this paper benefited from discussions with a number of ecologists at the University of
Florida and University of South Florida, most notably C. A. Lanciani, J. S. Godley, and D. T.
Gross. Reviews by Iverson, Congdon, and Lou Guillette were invaluable in improving the
manuscript. Katy NeSmith and William Boecklen provided statistical assistance. Finally, I
dedicate this paper to my parents, who unselfishly encouraged my boyhood enthusiasm for
turtles. Part of my field work was conducted under permits issued by the Florida Game and
Fresh Water Fish Commission and the Florida Department of Natural Resources. Laboratory
facilities were provided by the Florida State Museum and the University of Florida.


Pseudemys nelsoni, the Florida red-bellied turtle, is one of the largest
emydine turtles in North America (maximum female plastron length [PL] ca
310 mm; mass > 5.5 kg). Although restricted to southernmost Georgia and
the Florida peninsula today (Jackson 1978a; Vitt and Dunham 1980), fossils
from South Carolina reveal a formerly more extensive distribution in the
Southeastern Coastal Plain during the Pleistocene (Dobie and Jackson 1979).
The area of this study occurs near the northern limit of the present range of
the species (Jackson 1978a). The late Miocene P. caelata presumably was
immediately ancestral to P. nelsoni, which suggests this phyletic line was
present in northern peninsular Florida since at least that time (Jackson 1976).
Post-hatchling P. nelsoni are almost exclusively herbivorous (unpubl. data) and
occur in ponds, marshes, lakes and some low-gradient rivers.
Pseudemys floridana, which reaches sizes comparable to P. nelsoni (max
female PL ca 360 mm; mass > 6 kg), occurs throughout much of the
Southeastern Coastal Plain (Iverson 1986). Most specimens examined in this
study represent the Florida peninsular subspecies, P. f. peninsularis, the


peninsular cooter, although some individuals show signs of intergradation with
P. f. floridana. The habits and range of P. f. peninsularis coincide closely with
those of P. nelsoni, although the former is seemingly absent from the southern
Everglades. Of the four species, P. floridana is most poorly represented in the
fossil record; it is known only from Pleistocene deposits in Florida (unpubl.
The polytypic Trachemys scripta has the greatest distribution of the four
species studied and is the only one with a true northern component to its range
(Conant 1975). Additional populations currently assigned to T. scripta occur in
the tropics of Central and South America (Moll and Legler 1971). Trachemys
presumably is closely related to Pseudemys, of which it has been considered by
many workers to be a subgenus (see review by Seidel and Smith 1986). T. s.
scripta, the yellow-bellied turtle of the Southeastern Coastal Plain, is
intermediate in size (max female PL ca 265 mm) between Deirochelys
reticularia (below) and the two Pseudemys, although fossils from Florida
indicate a greater maximum size (PL ca 335 mm) in the Pleistocene (Jackson
1977). The study area lies at the present southern limit of distribution of T.
scripta in the eastern United States; however, Pleistocene fossils document the
species' former occurrence in southern peninsular Florida as well (Jackson
1977). Closely related forms, possibly ancestral to T. scripta, have lived in
Florida since at least late Miocene (Jackson in press). T. script is a
generalized omnivore (Marchand 1942; Hart 1979; unpubl. data) that may
inhabit almost any non-flowing body of freshwater within its range.
Deirochelys reticularia, the chicken turtle, is the smallest of the studied
species (max female PL ca 235 mm). A strict carnivore that feeds primarily on
arthropods (unpubl. data), this species is characteristic of shallow, non-flowing,
heavily vegetated bodies of freshwater in the Southeastern Coastal Plain. The
study area lies approximately in the zone of intergradation between the
subspecies D. r. reticularia and D. r. chrysea. Known from an extensive fossil
record in Florida, D. reticularia or its immediate ancestor, D. carr, has been
present in northern peninsular Florida since early to middle Miocene. The
genus probably arose from primitive Pseudemys stock in the Oligocene and is
therefore more closely related to that genus than to any other (Jackson 1978b).
Two other species of large turtles, which will be alluded to in this paper,
often occur sympatrically with these four. Pseudemys concinna is a large
herbivore (max female PL ca 370 mm; Allen 1938; Marchand 1942) most
closely related to P. floridana; it is restricted to lotic situations but does coexist
with the other species in some low-gradient rivers. Trionyx ferox, the largest
North American softshell turtle (max female PL ca 430 mm, CL 500 mm) and
a strict carnivore (Dalrymple 1977), often inhabits the same bodies of water as
all of the emydids studied. Fossils of both species document their existence in
Florida since at least late Pliocene (unpubl. data). Reproductive data for both
species will be reported elsewhere.


The fossil record from Florida suggests that all of the above species
formerly attained larger maxinmm sizes, a common trend among Recent
vertebrates but one rarely considered in relation to reproduction.


Reproductive data were collected kom 1973 to 1977 in northern peninsular Florida. Only
data collected within 70 km of Gainesalle, Alachua County (the majority within 15 km), are
included in the present analysis. Supplenentary data from beyond this area are introduced for
specific comparisons. Turtles were collected in baited hoop traps, basking traps, trammel nets
and dip nets, and by diving or by hand vhen they appeared on land or in aquatic vegetation too
dense to escape quickly. Turtles killed ly automobiles were used whenever possible to reduce
the number of individuals sacrificed.
Adult and juvenile turtles were weighed to the nearest 5 g and measured with calipers to
the nearest mm. Hatchlings were weighed to the nearest 0.01 g and measured to the nearest 0.1
mm with a dial caliper. Standard measurements, as described by Moll and Legler (1971),
included length of carapace (CL), width f carapace (CW), height of carapace (CH), and length
of plastron (PL); all measurements are staight-line, maximum, and reported in mm.
Maturity was determined in male by the presence of spermatozoa in the epididymides,
and in females by the presence of oviducl eggs, corpora lutea, or ovarian follicles greater than 14
mm diameter (in all species, follicles achieving this size prior to or during a nesting season are
almost always ovulated during that season rather than being retained or undergoing atresia).
Adults not dissected were sexed externlly by body size (females of all species grow to larger
maximum body sizes) and by secondary ex characters: enlarged preanal region of tail (housing
the penis) in males of all species, ani elongated foreclaws (utilized in courtship) in male
Pseudemys and Trachemys. Failure of pninsular Florida populations of these species to retain
growth annuli for more than a few months following ecdysis precluded the estimation of ages of
most individuals by this method (e.g. Ogle 1946). Moll and Legler (1971) likewise found the
method unsatisfactory for aging Panananian T. scripta. However, an estimate of maximum
percent post-maturational linear growth (PMGmax) for females of each species was obtained
from the following equation:
PMG = C-B x 100
ma C
where B and C are the sizes (PL) of tie smallest and largest mature females in a population,
Gonads and oviducts were removed from selected individuals and blotted and weighed
individually to the nearest 0.01 g. Shelled oviducal eggs were weighed separately and measured to
the nearest 0.1 mm with a dial caliper. ll egg measurements presented are from fully calcified
oviducal eggs, since eggs in nests are sub.ct to swelling by water absorption (Packard et al. 1977).
Ovarian follicles were grouped into appDximate size categories by diameter. Corpora lutea and
atretic follicles, both identified by gros morphology, were counted, measured, and likewise
grouped by size. Data were supplenmnted by dissection of a small number of preserved
specimens from the herpetological collection of the Florida State Museum.
Clutch size was determined fromdirect counts of eggs in nests, oviducal eggs, and fresh
corpora lutea. Difficulty in determiningproper groupings of follicles in these multiple-clutched
species can make them unreliable as indiators of future clutch sizes. Number of annual clutches
per female was estimated from corpora uteal size classes (after Moll and Legler 1971); corpora
lutea regress within a few weeks or monts of their formation (Cyrus et al. 1978; author's unpubl.
observ.). For each species, mean cluth mass and mean annual reproductive potential were
computed as the products of mean clutcl size times mean egg mass and mean annual number of
clutches, respectively.


Relative clutch mass (RCM; see review by Seigel and Fitch 1984) was determined as the
total mass of oviducal eggs in one clutch divided by female total mass, including the clutch.
Failure to evacuate the gut and bladder of specimens before weighing may cause my calculations
to underestimate actual values by one to three percent.
I followed Moll and Legler's (1971) stages of chelonian ovarian cyclicity: (1) follicular
enlargement; (2) ovulation and intrauterine period; (3) oviposition; and (4) a quiescent or latent
period. In multiple-clutched turtles, these phases are not mutually exclusive; i.e. while one set of
follicles is undergoing ovulation, other follicles representing subsequent clutches may be
undergoing enlargement. For detailed discussion of turtle reproductive cycles, see Moll (1979).
Nesting seasons were determined by direct field observations of nesting and terrestrially
wandering gravid females and by the presence of fresh corpora lutea or oviducal eggs.
All temperatures are given in degrees centigrade.

Incubation and Development

Eggs were removed for incubation both from natural nests and the oviducts of gravid
females. Toward the latter part of the study, females determined by palpation to be gravid were
injected with oxytocin to induce oviposition (Ewert and Legler 1978) prior to release. Eggs were
incubated on petri plates placed within plastic storage boxes into which water was added to a
depth of ca 0.5 cm; these were kept in constant-temperature environmental chambers. Eggs were
candled periodically by passing a narrow beam of light through them to check for signs of
development. Hatchlings were weighed within two days of hatching, before resorption of the
yolk. Because of the varied shapes of eggs and hatchlings, mass is more useful than linear
measurements for interspecific comparisons (Ewert 1979).
During the early course of this study, only a very low percentage (10%) of Deirochelys eggs
was successfully incubated to hatching by using the same techniques (constant 280C-300C in a
humid chamber) that typically yielded much higher hatching successes (ca 70%) for other species.
Only one Deirochelys clutch, incubated at 250C, had a hatching success greater than 50% (five of
eight eggs); most failed even to initiate development. Upon determining that the nesting season
of this species was confined to the colder (and drier?) months of the year (see RESULTS), I
conducted a series of preliminary experiments to determine whether initial exposure of eggs to
low temperature, followed by subsequent exposure to higher temperatures, might not enhance
development, much in the manner that certain plant seeds require an initial cold period before
germination will occur (Bidwell 1974). Eggs incubated initially at 150C or 20C (later, 100C and
15C were found to be more appropriate, although 20C served adequately) were transferred
after an arbitrary number of days directly to a second chamber set at either 25C, 280C, or 300C.
Comparative experiments were conducted with eggs of P. nelsoni and P. floridana.
Data on nesting seasons and development were compared to local climatic and soil
temperature data extracted from Climatological Data, Florida (U.S. Dept. of Commerce 1973-
1977). Information on hatchling emergence, based on limited observations of hatchlings in the
field, was supplemented by the occurrence of hatchling turtles in the stomachs of alligators
captured (for other studies) from 1981 to 1983 in Alachua County. Hatchlings obtained in the
laboratory were either released or raised under semi-natural conditions.


Reproductive Parameters

Reproductive parameters for populations of all species in the study area
are summarized in Table 1. Ranges of values generally encompass the limited


data previously reported for these species in northern Florida (Marchand 1942;
Carr 1952; Iverson 1977). Except for curtailment of reproduction during a
severe drought in 1977, I detected no gross differences among data from
different years or habitats.
Size of females at maturity varies within a species; a few immature
females examined were as much as 40 mm longer than the minimum PL at
maturity given in Table 1. Linear growth of females following maturation is
limited to less than one-third of body size (PL) at maturation. Males of all
species studied are considerably smaller than conspecific females. All male
Deirochelys dissected were mature; Gibbons' (1969) estimate of 75-85 mm PL
at maturity for males from South Carolina is probably applicable to males from
Although absolute evidence of age at maturity was not obtained for any
species, the retention of at least two annuli by a small number of juvenile P.
floridana, P. nelsoni, and T. scripta allows the following minimum estimates for
these species: males, 3-4 years; females, 5-7 years. These values almost
certainly underestimate actual ages as they were extrapolated from the high
juvenile growth rates of a few individuals that clearly had grown very rapidly
during their first post-hatching yearss. Nonetheless, these estimates are
consistent with those obtained from an extensive mark-release-recapture
program conducted by Gibbons and his associates in South Carolina on
populations of P. floridana, T. scripta, and D. reticularia (Gibbons 1970, 1987;
Gibbons and Coker 1977; Gibbons and Greene 1978; J.W. Gibbons pers.
All mature females examined from the appropriate seasons exhibited
signs of reproductive activity. Ovarian examinations indicated that nearly all
adult females of each species produce three to six clutches annually. Difficulty
in determining precise numbers of clutches per year for most females,
however, precluded statistical tests of correlation between female size and
clutch numbers. Limited data suggest that small females may lay only one or
two clutches during what is presumably their first nesting season.
As is typical for turtles (Moll 1979), clutch size within a species is
positively correlated with female size. For the two largest species, P. nelsoni
and P. floridana, correlations are considerably higher for mass than length
(Table 2). Correlation of mean clutch size with mean body size also is positive
among species (r = 0.95 for both PL and mass), a common trend among
chelonians (Moll 1979).
For species that produce multiple clutches, differences in egg numbers
between successive clutches may be ecologically important (Ferguson et al.
1982). Although successive clutch sizes are relatively constant in some
populations of turtles (e.g. Chrysemys picta: Gibbons 1968b), progressive
reduction of clutch size throughout the season characterizes others, including
those of some emydids (Moll 1979). Limited data for the populations in this


study suggest that clutch size is independent of temporal position. In 29
females (6 P. nelsoni, 5 P. floridana, 4 T. scripta, 14 D. reticularia) for which
exact counts could be made of at least two sets of corpora lutea, the more
recent of two consecutive clutches was larger by two or more eggs in 14
instances, smaller in 11, and no different or within one egg in 11; this apparent
randomness (Wilcoxon's signed-rank tests, p > 0.05) occurred in all species.
For only 5 of 36 pairs of successive clutches was the difference greater than
three eggs.
In most turtles examined, the two ovaries were equally active in the
production of follicles. However, as for other species (Moll 1979), differential
and alternate activity of the ovaries in the production of successive clutches
occurred in a small number of individuals; in even fewer, one ovary
predominated consistently (Table 3). Post-ovulatory migration of ova to the
contralateral oviduct (Moll 1979) was common in all species and usually
resulted in an equalization of ova between the two oviducts. Unequal
distribution of oviducal eggs was rare (difference > 2 in only 4 of 26 gravid
females dissected), the most imbalanced ratio being 13:3 in a P. floridana (PL
278 mm; corresponding corpora luteal ratio 8:8).
Because of statistical limitations governing the treatment of ratios such as
RCM, clutch masses within and among the four species were compared by
one-way analysis of covariance with female body mass as the covariate.
Adjusted mean clutch masses of the two Pseudemys and Trachemys did
not differ significantly from each other (t-tests, p > 0.80), but all were
significantly lower than that of Deirochelys (t-tests, p < 0.01). Although there
appeared to be a slight trend toward decreasing RCM with increasing body
size within each species, this was not verified statistically (t-tests, p > 0.05).
For all species, egg size (mass) appeared independent of female size
(PL), but only for Deirochelys was a statistically adequate number of fresh
clutches from a relatively broad size-range of females available. Across the
female sizes represented (160-200 mm PL, n = 15), mean egg mass showed no
significant correlation with female PL (r = 0.22;p > 0.05).
Eggs of all three genera have thin (ca 0.3 mm) leathery shells
(parchment-shelled eggs of Packard et al. 1977) in contrast to the more
calcareous egg shells of kinosternids, trionychids, and some batagurine
emydids (e.g. Rhinoclemmys). The largest preovulatory follicles measured
were 20 mm in P. nelsoni and 22-23 mm (5.3-6.4 g) in P. floridana, T. scripta,
and D. reticularia. Fresh corpora lutea were ca 11 mm in diameter in each
Females of all four species deposit their eggs in subterranean nests ca 10-15 cm
deep. Nesting activity is typically, though not exclusively, diurnal and requires
approximately one hour. The nests of all are essentially the same with the
exception of the unusual side-holes constructed by P. floridana, as













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Table 2. Correlation coefficients (r) for relationships of clutch size to female plastron length
(PL) and body mass. Asterisks denote significance at 0.05 level.

Species PL Mass n

Pseudemysfloridana 0.57 0.95* 14
Pseudemys nelsoni 0.45 0.94* 15
Trachemys scripta 0.91* 0.95* 14
Deirochelys reticularia 0.87* 0.83* 23

described previously by Allen (1938), Marchand (1942), Carr (1952), and Franz
(1986). As with all studied turtles, there is no post-nesting parental care.

Reproductive Seasonality

Vitellogenesis and follicular growth occur throughout much of the year in
females of all four species, with only brief periods of quiescence after the
nesting season and perhaps during the coldest parts of winter (Fig. 1). Small
numbers of atretic follicles, rarely representing entire sets, were not
uncommon and occurred more frequently in females sampled near the ends of
their species' reproductive seasons. In two of four aestivating females (one
each of two P. nelsoni and two P. floridana) examined toward the end of an
extended drought (August 1977), entire sets of follicles were beginning to
atrophy; none of the four possessed preovulatory follicles, and it was evident
that reproduction by the two P. nelsoni had terminated after two clutches that
season. During the entire study I detected signs of potential senescence
(reduced number and size of clutches, high percentage of atretic follicles
during reproductive season) in only one turtle, a female D. reticularia (PL 177
mm, collected 26 January 1976) that had borne clutches of two and five eggs
and whose largest remaining follicles (9-11 mm) showed a high percentage of
atrophy (6 of 11). I found no evidence of biennial or triennial reproductive
cycles as reported by Gibbons (1969) for large Deirochelys in South Carolina,
Gibbons based his conclusion on the absence of preovulatory follicles from
four females but did not state when those turtles were examined nor whether
they bore corpora lutea. They may have represented reproductive females
examined at some time following their annual reproductive season.
Nonetheless, failure to reproduce during some years by mature female turtles


Table 3. Occurrence of unequal ovarian activity in Florida emydids. The first and third examples
illustrate dominance by one ovary, the second ovarian dominance followed by alternation, and
the remainder ovarian alternation between successive clutches. Sizes of two most recent clutches
determined from corpora lutea and of next potential clutch from preovulatory follicles; data
presented as left:right.

Second Most Most Recent Next Potential
Species Recent Clutch Clutch Clutch

Pseudemys floridana 4:6 8:9 2:11

Pseudemysfloridana 10:8 14:7 5:17

Pseudemys nelsoni 7:2 8:3 7:5

Tracremys scripta -1:9 9:6

Deirochelys reticularia 6:4 3:8

Deirochelys reticularia -1:4 4:2

Deirochelys reticularia 11:3 5:7

Deirochelys reticularia -9:5 3:10

has been reported elsewhere (see Congdon et al. 1987) and may occur, albeit
infrequently, in Florida emydids.
Important seasonal aspects of the female reproductive cycles, with notes
on natural nests, are summarized below by species.

Pseudemys nelsoni.-- Most nesting takes place from mid-June to mid-
July, although some occurs as early as the first week of May and as late as the
last week of August (Fig. 1). This species does not nest year-round as
conjectured by Carr (1952) and Iverson (1977). Lardie's (1973) report of a
female nesting in October in central Florida is unusual; two females I
examined from southern Florida (Collier Co.; 3 June 1956, 5 August 1974)
showed signs of a June-August reproductive season, and in the Everglades July
is known to be an important month for nesting (Kushlan and Kushlan 1980c).
Vitellogenesis occurs principally in the spring, although it may commence in
the fall so that at least some females bear enlarged follicles in March (Fig. 1).


o cOGoo








S *800

* y



0 oo00 0 0



I I I 1 2 I I i i I I I



* S




Figure 1. Maximum diameters of yolked follicles throughout the year in females of four
species of Florida emydids. A, Pseudemys nelsoni; B, Pseudemys floridana; C, Trachemys scripta;
D, Deirochelys reticularia. Solid circles = ovarian follicles; open circles = oviducal eggs (follicles
estimated at 23 mm).

Daytime temperatures of 18 P. nelsoni nests observed in mid-July 1976
ranged from 25.50C to 30C (from 50 below to 1* above ambient temperature),
the variation principally reflecting time of day and degree of shading. Eggs
removed from these nests and incubated at 280C hatched from the last week of
July through the first week of September. The alligator stomach sample
revealed that at least some hatchling P. nelsoni emerge by early autumn; 11
different alligators, collected from 10 September to 14 October (1981-1983),
contained 13 hatchling P. nelsoni (32-34 mm PL).


Pseudemys floridana.-- Females may nest in late fall (slight November
peak), winter, or early spring. The tendency of females to nest only on warmer
days during the winter produces periodic peaks of nesting synchrony in the
population; e.g. Allen (1938) reported finding more than 200 fresh nests on a
single day in January. Nesting activity declines in May and terminates by the
end of June (Iverson's [1977] report of a nesting female on 30 June is the latest
summer record). During the present study I observed gravid or nesting
females in all months except February, July, August, and September. Carr
(1940) and Goff and Goff (1932) documented nesting in February while
Netting (1929) anecdotally reported nesting in September. Although the latter
two reports are from north-central Florida, their conclusions probably apply to
the study area (though perhaps with lower frequencies). This leaves only a mid
summer (July-August) hiatus during which the species seemingly does not nest.
NoJe of the females I examined from these two months bore either fresh
corpora lutea or preovulatory follicles (Fig. 1). Conjecture that the species
nests year-round (Carr 1952; Iverson 1977) therefore seems unfounded. The
long nesting season results in the highest degree of female ovarian asynchrony
among the species studied. Additional data are needed to determine whether
some females nest primarily in the spring and others in the fall, as the ovaries
of some individuals seemed to suggest.
Goff and Goff (1932) recorded the temperature profile of a typical P.
floridana nest that was constructed in February and hatched in July. I have
observed recently hatched young (egg caruncle present, yolk scar not fully
closed) in the field in Hillsborough County, south-central Florida, in July,
August, and October immediately after their emergences from nests following
heavy seasonal rains. One alligator, collected 5 October 1981 in Alachua
County, contained a hatchling P. floridana. Recent hatchlings showing
detectable growth have been collected from September through December in
Orange County, central Florida (J. S. Godley pers. comm.).

Trachemys scripta.-- Preovulatory follicles are present from February
through mid-July. A few females begin nesting in early April, although most
commence in late April or early May. By the end of July nesting has
terminated, and preovulatory follicles are no longer present (Fig. 1). Iverson
(1977) recorded gravid females from 8 April to 27 July in this area during 1972
and 1973.
One clutch of eggs laid 30 May 1976 hatched on 26 August (88 days), but
the young did not emerge from the nest until 31 August, only after their yolk
sacs had been almost completely withdrawn; the soil had been saturated by
rain earlier in the week (J. B. Iverson pers. comm.).


Deirochelys reticularia.-- Nesting begins in mid-September, reaches a high
level in October, and continues as such until mid- to late February (no females
available from November). As with P. floridana, nesting may be forestalled
temporarily by cold weather, so that a high incidence of nesting often occurs on
the first warm day following an extended cold period (for instance, four gravid
females, the first seen wandering terrestrially in weeks, were observed along
one roadbed in less than 1 h on 12 February 1977, when ambient temperature
rose above 200C for the first time that month). Most reproduction ends by
early March. Although sample size is small for the summer months, it appears
that follicles do not reach preovulatory size again until early September (Fig.
1). Iverson's (1977) report of a gravid female on 31 May 1972 seems to
represent an individual not in synchrony with the main population. Speculation
that Deirochelys nests year-round (Carr 1952; Iverson 1977) appears incorrect.

Seasonal nesting profiles for populations of these species, based on the
several kinds of data discussed above, are depicted graphically in Figure 2.
Figure 3 presents seasonal climatic data for northern peninsular Florida,
including monthly soil temperatures at the approximate depth at which turtles
deposit their eggs. Soil temperatures presented in Figure 3 are in strong
accord with actual nest temperatures (Goff and Goff 1932; present study).
At least some sperm were present in the epididymides of all mature males
examined from throughout the year. Limited data suggest peak testicular
enlargement occurring in Pseudemys spp. and Trachemys from late July
through September, as in most temperate zone turtles (Moll 1979).

Development and Hatchlings

Females usually retain shelled eggs in the oviducts less than two weeks in
nature but may retain them 30-60 days in captivity. Candling of eggs
immediately following their departure from the oviducts revealed no signs of
advanced development regardless of length of time in the oviducts. A number
of studies indicate that turtle embryogenesis is suspended at the late gastrula
stage until laying occurs (Ewert 1979). An experimental observation obtained
during this study provides further support of this. An egg expelled from the
right oviduct of a captive P. nelsoni hatched 36 days later than eggs of the same
clutch that had been removed surgically from the left oviduct 37 days earlier
(all eggs incubated at 250C). Thus, unlike the case for many squamate reptiles
(Tinkle and Gibbons 1977), interspecific comparisons of incubation periods for
turtle eggs held at constant temperature and measured from the time of
oviposition appear to be valid.





W (57)



Figure 2. Approximate seasonal nesting patterns for populations of Trachemys script,
Pseudemys nelsoni, Pseudemys floridana, and Deirochelys reticularia in northern peninsular
Florida. Area beneath each curve represents one hundred percent of a population's annual egg
production; sample sizes, expressed as numbers of clutches, in parentheses.

Table 4 reports periods of incubation from oviposition (natural or induced) to
pipping as determined under constant laboratory conditions; only groups of
eggs from which at least one young hatched are included. For no species did
eggs incubate solely at 150C or 200C hatch. Hatching within a clutch is
approximately synchronous and rarely spans more than three days. Although
considerable variation in incubation period at constant temperature may exist
within a species (note periods for P. nelsoni at 24.7*C-250C), this does not
appear to be usual. Developmental rate is clearly temperature-dependent in
the manner reported previously for other species (e.g. Yntema 1978). Where
field data are available (e.g. Goff and Goff 1932), laboratory and field
incubation periods at equivalent temperatures are comparable. The
developmental rate of P. nelsoni is among the fastest known for turtles (see
Ewert 1979).


35- -25
30- -20

0 25- m \
oI >


C- ,, \ -I r"

1- 0



Figure 3. Climatic data for Gainesville, FL 2WSW: monthly mean minimum and maximum air
and soil temperatures for the years 1973-1977, and monthly mean precipitation for the years
1941-1970; soil temperatures taken at a depth of 10.2 cm in sandy soil under centipedegrass.

In contrast to the relatively high hatching success at 280C-300C observed for
eggs of some species (e.g. Pseudemys nelsoni, 81% of 98 eggs), only one egg
hatched from 11 whole or partial clutches of Deirochelys eggs (n = 60)
incubated at these temperatures (Iverson [1977] reported successful incubation
for 6 of 20 Deirochelys eggs under this regime). Most embryos failed to reach
1 cm; one that did reach full-term was grossly deformed. Likewise, only one-
third (5 of 15 from 2 clutches) of D. reticularia eggs held at 250C hatched (vs
81% hatch for 26 P. nelsoni eggs at 250C). The results of several temperature-
switching experiments contrast with this. Of 20 D. reticularia eggs (from four
different clutches) exposed to an early cold period (150C or 200C for 17-82
days) prior to their transfer to 280C or 300C, 13 (65%) either hatched or
contained large, viable embryos at the time they were opened for examination.
Gross examination by candling revealed no signs of development during the


Table 4. Incubation periods of Florida turtles from time of oviposition to pipping, determined at
constant temperature (+ 0.5C) in the laboratory.

Mean Days to Hatching
(Range; No. Hatched
Species Temp (C) /No. Incubated) Source

Pseudemys floridana

2 clutches
1 clutch
2 edltchesa

Pseudemys nelsoni





Trachemys scripta

> 1 clutch
> 1 clutch

Deirochelys reticularia

--- 29.0b

--- 29.0b

R-370 28.0
R-215 25.0

62.0 (all 62; 5/7)
65.0 (all 65; 3/8)
70.4 (70-71; 5/7)
68.0 (--; 18/--)
60.0 (--; 6/8)
70.0 (69-71; 10/15)
101.6 (-; 13/--)
118.5 (118-119; 2/2)
120.6 (120-122; 3/8)

45.0 (all 45; 5/6)
48.8 (48-50; 4/--)
80.25 (79-82; 4/5)
60.0 (all 60; 7/8)
54.4 (54-55; 9/9)
50.6 (50-51; 5/9)

69.0 (--; 1/6)
63.8 (-; 53/--)
66.0 + 1.5 (--; 2/5)
100.8 (--; 24/--)

78.0 (both 78; 2/8)

88.0 (87-89; 4/12)

81.0 (-; 1/4)
87.8 (87-89; 5/9)

present study
present study
present study
Ewert 1979
J. Iverson pers. comm.
present study
Ewert 1979
present study
present study

present study
Ewert 1979
present study
present study
present study
present study

present study
Ewert 1979
present study
Ewert 1979

Iverson 1977,
pers. comm.
Iverson 1977,
pers. comm.
present study
present study

a P.f. floridana (Leon County, Florida panhandle: M. Ewert pers. comm.)
temperatures not precisely controlled


cold periods. In contrast, although four eggs of P. nelsoni survived a short
period (19-20 days) of early cold exposure and proceeded to develop normally
following transfer to warmer temperature, eight held at 200C for more than 30
days died during embryogenesis after apparently failing to initiate diapause
(Ewert 1985) at this temperature. Hatching rates of P. floridana eggs were
equivalent (ca 50%) under both treatments (28 of 55 with and 13 of 27 without
an early cold period); when included, the initial cold period seemed merely to
delay development.
The sample of hatchlings from oviducal eggs of known mass is small but
suggests that hatchling mass is positively correlated with egg mass both within
(Deirochelys reticularia: r = 0.97, n= 7; Pseudemys floridana: r = 0.93, n = 23;
P. nelsoni: r = 0.87, n = 17; p < 0.01 for each) and between species (r = 0.97,
p < 0.01; Trachemys scripta excluded for insufficient data). This relationship
holds throughout the order Testudines (Ewert 1979).
Unlike hatchling marine turtles (Caretta: Milsom 1975), neonates of all
these species of freshwater emydids are negatively buoyant in water.


Wilbur (1975b) generalized that the greatest sources of mortality in
turtles are desiccation and predation of the eggs and predation of hatchlings.
Although levels of egg destruction were not quantified in the present study
(because of the difficulty of locating unpredated nests), qualitative observations
indicated that the loss of eggs and hatchlings to predation, desiccation, and
flooding are high in North Florida emydids, as they are in other turtles (e.g.
Wright and Funkhouser 1915; Allen 1938; Cagle 1950; Gibbons 1968a; Moll
and Legler 1971; Thomas 1972; Plummer 1976; Shealy 1976; Congdon, Tinkle
et al. 1983). Presumably these factors act as strong selective forces in the
evolution of their life history tactics. Preliminary data for the four North
Florida species (to be reported elsewhere) indicate that adult losses to
predation are normally low, whereas substantial adult mortality may occur
during infrequent but exceptionally harsh climatic conditions (e.g. drought).
The high reproductive potentials that result from the production of
multiple, large clutches of relatively small eggs by females of all four species
potentially can compensate for at least some of the heavy early mortality. Moll
(1979) described such a reproductive pattern as typical of most large aquatic
turtles, including marine turtles. Below I briefly examine four factors that
contribute most directly to the high reproductive potentials of Florida emydids:
body size, egg size, clutch size (both number of eggs and clutch mass), and
annual number of clutches.


The long growing season of peninsular Florida facilitates rapid growth to
large body sizes among many reptilian inhabitants. Pseudemys nelsoni, P.
floridana, and P. concinna mature at larger body sizes than all other North
American emydids and perhaps because of this depend upon herbivory (Pough
1973; Wilson and Lee 1974). Trachemys scripta and Deirochelys reticularia
from Florida grow substantially larger than conspecifics from more northerly
localities. Wilbur (1975a) suggested that intense selection for rapid growth
plus an increase in fecundity with body size may account for the evolution of
delayed maturity (and pronounced sexual size dimorphism) in northern
Chrysemys picta. These factors appear equally operative for southeastern
emydids, although other parameters also may select for delayed maturity
(Stearns 1977). The increase in net reproductive rate with delayed maturity
must be sufficient to offset the loss of early reproduction. Increased
reproductive life expectancy associated with delayed maturity should further
increase fitness (Cole 1954; Tinkle et al. 1970). Additional selective pressure
for rapid growth to a large body size prior to maturity is exerted on these
emydid turtles because they must coexist with the chelonivorous Alligator
mississippiensis. The large size at maturity and exceptionally low post-
maturational growth of female P. nelsoni (Table 1), coupled with other aspects
of shell morphology and microhabitat use (author's unpubl. data), suggest that
alligator predation may act as an especially strong selective agent for this
Eggs of Florida emydids are small (sensu Moll 1979) and relatively
independent of female size. Selection has proceeded in the direction of high
fecundity and low energy per progeny rather than towards morphological and
behavioral attributes that might increase survivorship of individual eggs and
hatchlings. This contrasts with the strategy (Moll's Pattern II) evolved by some
truly tropical emydids (e.g. Rhinoclemmys) in which egg size, hatchling size,
and egg shell thickness are presumably increased at a cost of lower fecundity.
The lower limit of approximately 10 g for egg size of Florida emydids perhaps
represents the minimal energetic investment necessary for normal
development and production of a hatchling with effective survival potential.
Positive correlation of clutch size with female size, both within and
between species, is a common trend in most groups of vertebrates and implies
that females are producing nearly maximal clutches for their body (and egg)
sizes. I suggest that for the four freshwater species studied, as for marine
turtles (Bustard 1979), morphology rather than energetic limits maximum
clutch volume of a female. Two lines of evidence imply that volume of the
body cavity, rather than some linear measurement such as oviduct length,
imposes a design constraint (Stearns 1977) upon clutch volume in aquatic
emydids. One is the occasional unequal distribution of oviducal eggs (e.g.
13:3). The other is the considerably higher intraspecific correlation of clutch


size with body mass, in contrast to length, in the two larger but not in the two
smaller species (Table 2).
The importance of egg capacity as a function of body cavity volume
cannot be overemphasized. Nearly all previous researchers have accepted
length (PL or CL) as an adequate measure of turtle body size against which to
compare ecological parameters. That correlations with length often have been
high is a consequence not so much of the paramount importance of length but
rather of the small absolute change in volume that accompanies a given linear
change at the relatively small sizes (< 250 mm CL) of most previously studied
species. For larger turtles, a comparable linear change produces a far greater
absolute change in body volume. Thus, although linear dimensions may be
acceptable approximations of ecological size for small turtles, they may not be
so for large turtles. Because this became clear only after the present analysis
had been completed, and to facilitate direct comparisons with pre-existing
literature, I retained the use of PL for computation of some parameters in this
That an increase in clutch size rather than egg size is responsible for the
association between clutch mass and body size in female Trachemys scripta was
reported previously for a population from South Carolina (Congdon and
Gibbons 1983). However, that this relationship holds also for Deirochelys in
Florida contrasts markedly with the findings of Congdon, Gibbons et al. (1983),
who reported that egg size, rather than clutch size, shows a strong positive
relationship to body size of D. reticularia in South Carolina. Simultaneous
examination of our two data sets (Fig. 4) sheds some light on, though cannot
resolve, this seeming paradox. Overlap of the ranges of body sizes between our
two samples is low (less than 50%). If, as suggested by Congdon, Gibbons et
al. (1983), some aspect of morphology (e.g. width of the pelvic canal) limits
mean egg size of the relatively smaller females in the South Carolina
population, then perhaps this constraint is relaxed in Florida in which females
typically reproduce at larger body sizes.
The absence of post-nesting parental care frees turtles to reproduce
repeatedly in one season if sufficient energy reserves are available. The actual
numbers of clutches laid yearly per female (Table 1) exceed all previous
estimates for the species under study and rank among the highest known for
emydid turtles. Although depositing several temporally spaced clutches may.
reduce the impact of nest predation on a female's total annual reproductive
output (Moll 1973; Christiansen and Moll 1973), it may also be the only
functional means for a turtle to achieve a high annual reproductive potential
given the constraints on maximum clutch size. Tinkle and Gibbons' (1977:45)
suggestion that the production of multiple clutches by turtles is possible as a
result of the "generally omnivorous diets of most species" is clearly irrelevant.
In northern peninsular Florida, herbivores, carnivores, and omnivores all
produce multiple clutches. That the maximum number of clutches a female can


01 ,---^ ........
L0 I -- "N-

0 J
LU/ 0

1y) 10- / --
0 ) / o o o
m/ '4 o or
S / *-------cL^---
/ /

Z / o /
S8- // 0 /

6- o
140 160 180 200

Figure 4. Relationship of parental body size to mean wet mass of eggs of Deirochelys
reticularia. Open circles = South Carolina sample, extracted from Congdon et al. (1983); solid
circles = Florida sample, present study; polygons added for visual clarity.

lay per season may be energetically limited is suggested by several previous
studies of the effects of food availability on reptilian reproduction (e.g. Fitch
1970, 1985; Barbault 1976; Gibbons et al. 1983). Further, the marked post-
maturational decrease in linear growth rates from the high growth rates
characteristic of juvenile emydid turtles suggests finite limits on the amount of
energy that can be assimilated by mature female emydids.
Geographic variations in clutch size and annual reproductive potential have
been reported for many reptiles and are most often correlated with geographic
(especially latitudinal) differences in body size and potential length of the
growing season (Fitch 1985). Reproductive data for most non-Florida
populations of the species under investigation are inadequate to make
definitive geographic comparisons; however, data assembled by Gibbons and
his colleagues in South Carolina permit limited analyses. Compared with
conspecifics from Florida, the annual reproductive potential of Deirochelys
reticularia in South Carolina is lower as a result of smaller body size (t = 4.65,
p < 0.001), smaller clutches (t = 2.38, p < 0.05), and perhaps fewer clutches
per season (Table 5; Gibbons 1969; Congdon, Gibbons et al. 1983). Similar
reductions of annual reproductive potential may characterize more northerly
populations of Pseudemys floridana (Thomas 1972; Gibbons and Coker 1977)


Table 5. Plastral lengths and clutch sizes of mature female Deirochelys reticularia and Trachemys
scripta in Florida (FL) and South Carolina (SC). All South Carolina data are from Congdon and
Gibbons (pers. comm.). Values are mean 1 standard deviation.

Population n PL (mm) Clutch Size

Deiroclelys reticularia
FL 27 176 12.8 9.5 3.6
SC 49 161 13.8 7.6 2.9
Trachemys script
FL 22 211 10.8 10.6 2.7
SC (small) 69 203 27.1 6.9 2.6
SC (large) 30 258 7.8 11.2 2.7

and Trachemys scripta (Cagle 1950; Webb 1961; Congdon and Gibbons 1983;
Table 5), although locally aberrant environmental conditions may obscure this
trend. In South Carolina, female T. scripta in some habitats (thermally altered
sites and coastal barrier islands) mature at unusually large body sizes but
produce clutches comparable in size to those produced by much smaller
Florida conspecifics (Table 5; Gibbons and Sharitz 1974; Parmenter 1980;
Congdon and Gibbons 1983). Nonetheless, small-bodied T. scripta from South
Carolina, though only slightly smaller than their Florida counterparts (t = 1.99,
p = 0.05), lay considerably smaller clutches (t = 5.62, p < 0.001). Thus,
although most of the species of turtles examined by Fitch (1985) showed a
northward increase in clutch size, the trend is weaker than he thought. Among
the present group of species, the only non-Florida populations that apparently
exceed the reproductive potentials of Florida conspecifics under natural
conditions are the tropical forms currently assigned to T. scripta, whose greater
body sizes permit not only larger clutches but also larger eggs (Medem 1962;
Moll and Legler 1971). By analogy, the greater maximum sizes of Pleistocene
conspecifics of these species presumably allowed for larger clutches and higher
reproductive potentials, although other factors (e.g. predation or climate) may
have been equally or more important in selecting for large body size.
Despite criticism of the use of relative clutch mass (RCM) as a measure
of reproductive effort (see Cuellar 1984 for a review), the relationship may be
valid for turtles. In contrast to snakes and lizards, whose bodies expand in
proportion to increases in RCM, changes in clutch mass have virtually no effect
on the external morphology of a gravid female turtle, whose body is encased in


a rigid, bony shell. Whereas foraging tactics and escape from predators may be
critical determinants of RCM for squamate reptiles (Vitt and Price 1982;
Seigel and Fitch 1984), these factors are likely to be far less important in the
evolution of chelonian RCM's. Additionally, for females of the aquatic
emydids studied, all of which continue to feed while gravid, the energetic costs
of courtship and territorial maintenance, mechanical support of the egg load
(buoyed by the water column), and post-nesting reproductive behavior are all
minimal. Furthermore, from an extensive survey of the relationship between
turtle egg and hatchling masses, Ewert (1979) concluded that clutch mass is
directly proportional to caloric input in interspecific comparisons.
The RCM of Deirochelys, the smallest of the species studied, is nearly
twice that of the two Pseudemys and Trachemys (Table 1). This is consistent
with the findings of Congdon and Gibbons (1985), who demonstrated that
RCM decreased with increasing body size among 12 taxonomically diverse
species of North American turtles. A higher RCM probably implies a greater
relative investment of energy per clutch. Proportionately larger clutches in
Deirochelys may be energetically permissible because of the assimilation
efficiency associated with a carnivorous diet. Concomitantly, specializations in
Deirochelys for carnivory of invertebrate prey may place energetic limits on its
maximum body size (Pough 1973; Wilson and Lee 1974) that in turn would be
expected to limit clutch size. The morphological constraints on RCM in
Deirochelys may be relaxed by having a relatively larger body cavity space
available to hold eggs, a consequence not only of the structure of the shell itself
(high sides, thin bones) but also of the smaller proportion of the body cavity
occupied by a digestive tract adapted to carnivory.
The RCM's of all four species are small compared to values for squamate
reptiles (estimated from the literature to fall between 0.15 and 0.45 for most
species; see Iverson 1979a; Vitt and Price 1982; Seigel and Fitch 1984; Fitch
1985; Seigel et al. 1986), although they are comparable to values obtained from
a broad size and taxonomic range of turtles (e.g. Kinostemon baurii, 0.08:
Iverson 1979b; Chelonia mydas, 0.034: Hirth 1971). The production of
multiple clutches is less common among temperate squamates and, if RCM's
are additive, may allow turtles with low RCM's to put forth comparable annual
reproductive efforts despite morphological constraints. Nonetheless, of the
several criteria indicative of high reproductive effort in lizards (Tinkle 1969;
Tinkle and Hadley 1975), Florida emydids display only one, namely multiple
clutches, and it is probable that the low RCM's are representative of low
reproductive efforts. Such low efforts are expected for populations in which
survivorship of adults from one breeding season to the next is relatively high
(Williams 1966a, b; Tinkle and Hadley 1975).
Giesel (1976) predicted that populations experiencing high pre-
reproductive mortality relative to reproductive age mortality should increase
fitness by delayed reproduction, extended iteroparity, and a flattening out of


the m distribution. Reproductive uncertainty is thereby countered by
spreading reproduction over a number of nearly equally weighted ages of
reproduction. Giesel supported his predictions with data from lizards, birds,
insects, and plants. Data from the present study and much of recent chelonian
literature suggest that the reproductive strategies of many freshwater emydine
turtles also accord with these predictions.

Seasonal Patterns of Reproduction

Overlying the above components of reproductive effort is the strategy of
optimal reproductive timing. Field and laboratory observations of hatchling
turtles have shown that individuals that sustain the highest rates of growth
during their first year of life enjoy higher rates of survival as well as possible
competitive advantages over small conspecifics (Legler 1960; Gibbons 1968a;
Froese and Burghardt 1974; Wilbur 1975a; Swingland and Coe 1979).
Selection for rapid early growth is therefore intense. Time of emergence of
hatchlings, and therefore nesting seasons of adults, must play a major role in
determining the quality of extrinsic factors (e.g. food availability, length of
growing season, competition) that influence the extent to which hatchlings
achieve intrinsic growth potentials. As a vivid illustration of this, the mean
linear pre-winter growth (8 mm) of a pair of July/August Pseudemys floridana
hatchlings, which I raised outdoors under semi-natural conditions, was 27 times
that (0.3 mm) of a pair of early October hatchlings raised under otherwise
identical conditions. Nest season timing must be a highly adaptive response to
both physical and biotic selective pressures.
The degree to which nesting season can be altered by natural selection is
directly dependent on climatic equability and predictability. Although by
definition (Tinkle et al. 1970) the environment of northern peninsular Florida
is temperate (i.e. seasonal), winters are far less harsh than those in much of
North America, and, in fact, the peninsula sometimes is considered subtropical
(e.g. McNab 1974). Additionally, the coexistence of several closely related
species often is accompanied by the partitioning of resources, including
temporal partitioning of reproductive activity. Coupling Florida's relatively
moderate climate with its high chelonian diversity, it might be predicted that
the greatest range of nesting seasonality among North American turtles would
occur in peninsular Florida. Indeed, that is precisely what does occur.
Figure 2 reveals two distinct patterns of reproduction among the species
studied: (1) a restricted nesting season of 3 to 4 months maximum duration
centered around a late spring or early summer peak (Trachemys scripta and
Pseudemys nelsoni), and (2) an extended nesting season (6 to 10 months)
beginning in the fall and continuing through winter and into the following


spring, with no real single peak, followed by cessation of nesting activity during
the warmest months of the year (P. floridana and Deirochelys reticularia). For
convenience, I shall refer to the first seasonal pattern as "summer-nesting" and
the second as "winter-nesting." The shorter duration of the former pattern
results in a generally higher level of reproductive synchrony among conspecific
females. The marked success of two very different seasonal strategies of
nesting within a group of sympatric, closely related species that occur in similar
environments and which are subject to similar selective pressures has not been
noted previously among north temperate turtles. The ability to store sperm
suggests that for turtles ultimate factors are more important than proximate
factors in determining female reproductive cycles (Moll 1979). A
consideration of ultimate factors that may have been responsible for
determining the nesting seasons of these Florida emydids is therefore in order.

'Summer-nesting pattern.-- A restricted late spring or summer nesting
season characterizes most north temperate turtles previously studied (Moll
1979), including some non-Florida populations of Pseudemys floridana
(Thomas 1972) and perhaps Deirochelys reticularia (Anderson 1965; David
1975). Climatic factors, particularly temperature, probably dictate this
seasonality. In most of the north temperate region, turtles are relatively
inactive throughout the winter. Even if no physiological barriers to activity
existed, environmental barriers, such as the freezing of pond surfaces and the
upper layers of soil, would prevent nesting. Therefore, nesting can proceed
only following resumption of activity in the spring and only after passage of
sufficient time to complete sequestration of energy reserves for reproduction.
The 60 to 90 days of appropriate temperatures necessary for incubation of
most turtle eggs (Ewert 1979) are generally available throughout the north
temperate latitudes to any egg laid by mid-summer. Whether young turtles
emerge shortly following hatching or remain in the nest until the following
spring is largely climate-dependent. If only a short period of time suitable for
feeding and growth follows hatching, as is the case for most north temperate
turtles, then the risks of predation and physical exposure, followed by the need
to find a protective winter retreat, may outweigh the benefits of the limited
growth that can be accomplished before cold weather arrives. Hence, it is
commonplace for many North American summer-nesting species of turtles to
practice "delayed emergence" (Gibbons and Nelson 1978).
The occurrence of a late spring to mid-summer nesting season in
Trachemys scripta and Pseudemys nelsoni (as well as P. concinna and Trionyx
ferox) in northern peninsular Florida may be explained most simply as the
conservative maintenance of a north temperate reproductive pattern.
Although P. nelsoni no longer occurs north of southernmost Georgia, its sister
species, P. rubriventris, exists in disjunct populations in the Atlantic Coastal
Plain as far north as Massachusetts. Like P. nelsoni, P. rubriventris nests from


mid-May to August (Smith 1904; Conant and Bailey 1936; Babcock 1938;
Richmond and Goin 1938; Graham 1971). Limited data (Pritchard 1978;
McCoy and Vogt 1979; U.S. Fish and Wildlife Service 1986) suggest a
comparable nesting period for the third member of the P. rubriventris species
group, P. alabamensis, which is endemic to the Mobile Bay drainages of
Alabama. Likewise, more northern populations of T. scripta (Alabama,
Illinois, Kentucky, Louisiana, North Carolina, South Carolina, Tennessee)
maintain approximately the same nesting season (late April to mid-July) as
Florida conspecifics (Brimley 1909; Cagle 1950; Carr 1952; Gibbons 1970;
Mount 1975). Even in the tropics, T. scripta maintains a short seasonal nesting
cycle, but timing there is determined by precipitation rather than temperature
(Panama: Moll and Legler 1971; Colombia: Medem 1962).
Whereas northern relatives of Pseudemys nelsoni and Trachemys scripta
generally practice delayed emergence (Gibbons and Nelson 1978), several
months suitable for foraging and growth typically follow hatching in Florida,
and emergence usually occurs in late summer or early fall. The shorter
incubation period of P. nelsoni relative to T. scripta perhaps compensates for
its slightly later nesting season. Emergence of hatchlings from nests may be
facilitated by precipitation (Carr 1952; pers. observe) which in this region is
heaviest from June through September (53% of the year's rainfall occurs
during these 4 months; Fig. 3). The importance of rainfall as a cue for
emergence was demonstrated by Moll and Legler (1971) for tropical T. scripta,
although Gibbons and Nelson (1978) were unable to show such a correlation
for temperate (South Carolina) turtles.
In sufficiently dense populations, a restricted seasonal nesting pattern, in
which most reproductive activity is confined to the relatively short span of 10 to
15 weeks, can result in a tremendous concentration of a single resource (turtle
eggs) available to opportunistic predators. Additionally, inter-clutch time per
female is necessarily short (2 to 3 weeks), and many females are likely to use
the most favorable nesting sites repeatedly. Generalized, switching predators
may form a search image and specialize on such a temporarily abundant
resource (Curio 1976). Temporary specialization on seasonally available
reptile eggs or hatchlings is practiced by many vertebrate predators (e.g. Blair
1960; Neill 1976). Wilbur (1975a) suggested that raccoons may undergo such a
density-dependent feeding response to Chrysemys picta eggs, while sixty years
earlier Harper (in Wright and Funkhouser 1915), observing the spring carnage
of turtle eggs (mostly Trachemys and Pseudemys) in the Okefenokee Swamp,
Georgia, remarked that "the edges of the canal were literally torn up in the
middle of May, 1912, by bears, coons, etc., which search for cooter eggs."
Raccoons are known to be important predators of both turtle and alligator
eggs in northern peninsular Florida (Deitz and Hines 1980; Franz 1986).
Turtles conceivably may counter such exploitation by predator swamping
or satiation. In species that benefit from predator satiation, predation exerts


intense stabilizing selective pressure against individuals that reproduce out of
phase with the remainder of the population (Janzen 1971); nonetheless, perfect
synchrony is neither required nor expected (Stearns 1976). Among reptiles the
phenomenon has been ascribed commonly to sea turtles (Carr 1967; Richards
and Hughes 1972; Bustard 1979). It should be a viable strategy for freshwater
turtles that meet the following criteria: they must be large enough to produce
large clutches (hence, selection for delayed maturity), be capable of producing
several clutches in a limited time, and occur in high densities. Pseudemys
nelsoni often fulfills these criteria in northern peninsular Florida. A
quantitative measure of the ability of P. nelsoni to use this strategy was
determined on Payne's Prairie, an extensive marsh in Alachua County with
restricted nesting sites, limited numbers of mammalian predators, and a high
density of turtles. P. nelsoni frequently lays its eggs in alligator nests (Goodwin
and Marion 1977; Deitz and Jackson 1979; Kushlan and Kushlan 1980c), which
are constructed at the beginning of the turtle's nesting season (Deitz and Hines
1980). Most alligator nests on Payne's Prairie contain P. nelsoni eggs (Deitz
and Jackson 1979). On 14 July 1976, David Deitz and I examined an alligator
nest (ca 1.5 m x 1 m) that recently had been attacked by raccoons. Several
alligator eggs had been eaten and others exposed; no turtle eggs were exposed.
Excavation of the nest revealed seven clutches of P. nelsoni eggs (judged by
their states of development to be from seven different females) and a single
clutch of Trionyxferox eggs (total of 112 eggs) surrounding the central clutch of
alligator eggs (Frontispiece). Predators earlier had destroyed four clutches of
P. nelsoni eggs at this nest prior to oviposition of the alligator eggs. We re-
examined the nest on 22 July and found four new clutches of P. nelsoni eggs
(52 eggs). More than 200 turtle eggs had been deposited in a two-week period
in the nest by this date, after which the nest became inaccessible to us because
of flooding. The approximate coincidence of nesting seasons of P. nelsoni, T.
ferox, and Alligator mississippiensis may increase the potential for predator
satiation at the community level (Janzen 1971).
Aside from the preceding, major benefits achieved by turtles that use
alligator nests as oviposition sites in northern Florida are the suitability of the
medium for digging and subsequent incubation, and perhaps a concomitant
increase in protection from flooding. Although turtle eggs may receive some
protection against predators from nest attendance by adult alligators (Kushlan
and Kushlan 1980a, c), this benefit seems reduced in northern Florida today.
Active defense of nests by female alligators is rare (at least against man) on
Payne's Prairie (Deitz and Hines 1980); furthermore, clutches of turtle eggs
laid prior to the alligator's often are inadvertently destroyed by restructuring
activities of the alligator (D. Deitz pers. comm.). Additionally, three of us (A.
Carr, D. Deitz, and myself) independently have observed aggressive adult
alligators attack and drive off P. nelsoni that were attempting to nest in
alligator nests.


Winter-nesting pattern.-- Although "winter" (i.e. dry season)
reproduction is wide-spread among tropical reptiles (e.g. Inger and Greenberg
1966; Moll and Legler 1971; Quay 1974), restriction of nesting to the cooler
months of the year is all but unheard of for reptiles of the north temperate
zone. Thus, even though Carr (1952) had observed Deirochelys reticularia
nesting only from September to January in Florida, it was natural for him to
suppose that nesting occurred year-round in the species. The tendency of
other biologists (e.g. Ernst and Barbour 1972; Mount 1975; Iverson 1977; Moll
1979) to iterate Carr's supposition, despite the lack of substantial confirmatory
data, has led to general acceptance of Deirochelys as one of the few
nonseasonal nesters among temperate reptiles. Iverson (1977), in fact, even
erected a separate category, "continuous nesters," to include Deirochelys and
two species of Pseudemys (P. floridana and P. nelsoni) whose patterns of
reproduction likewise have been misinterpreted.
Despite the passage of more than a half century since it first was reported
to the scientific community, winter reproduction by Florida emydids has
received surprisingly little attention. Noting the production of eggs by a captive
female Pseudemys floridana collected in January 1927, Netting (1929) asked,
"Can any reader suggest an explanation for this case of unseasonal egg-laying?"
After a lapse of 60 years, my studies address Netting's query.
A nesting option available to turtles in peninsular Florida, but not to their
northern kin, is fall and winter oviposition. Soil temperatures at nest depths
(10-15 cm) never approach freezing and during the five years of study never
dropped below 90C (Fig. 3). Air (Fig. 3) and water temperatures permit turtle
activity on most days throughout the winter. Brumation or prolonged inactivity
is unnecessary, and some food (plant and animal) is available year-round.
Peninsular Florida populations of two species of emydids, D. reticularia and P.
floridana, have taken advantage of these conditions by nesting during the
winter. A small number of other turtles, notably Kinosteron baurii and
Stemotherus minor (Iverson 1978, 1979b; Cox and Marion 1978) independently
have adopted a similar strategy. The rarity of an extended winter (fall to
spring) nesting season among temperate reptilian life histories warrants
speculation as to its adaptive nature and evolutionary origin.
I have already alluded to the vulnerability of the hatchling stage and the
urgency for rapid growth. In peninsular Florida, rapid growth is achieved most
effectively by hatchlings that can take maximum advantage of the long growing
season. Eggs laid in fall, winter, and early spring can begin development as
soon as temperature permits; they should hatch as early as the weather and
intrinsic factors regulating development allow. Coordination of emergence
with the summer rainy season, rather than remaining in the nest until the
following spring, is clearly adaptive in terms of the time (3 to 6 months) that is
available for growth. Since essentially no development takes place during


winter months when soil temperatures remain below 20"C, all eggs of a species
laid from late fall to early spring develop in approximate synchrony; field
evidence of this was presented by Goff and Goff (1932) for P. floridana.
Therefore, with the possible exception of P. floridana eggs laid late in the
season (May-June), there should be among eggs (and hatchlings) little selective
differential associated with date of oviposition within the extended "winter"
For this strategy to be successful there must be an appropriate food
resource readily available to hatchlings by late spring. Although Packard et al.
(1977) suggested that more effective exploitation of a seasonally abundant food
source by early emerging young is one possible selective force for viviparity, the
strategy holds equally for oviparous reptiles (Cott 1961; Chapman and
Chapman 1964; Inger and Greenberg 1966; Wiewandt 1977). During their first
year, young Pseudemys as well as Deirochelys practice at least partial carnivory,
the dietary properties of animal food presumably being more favorable to
rapid growth and hardening of the shell than the plant material consumed by
older individuals (Marchand 1942; Gibbons 1967; Clark and Gibbons 1969; D.
Moll 1976). Several years of aquatic sampling in ponds and marshes in the
study area have left me with the subjective impression of a very high
abundance of small aquatic invertebrates (insects, crustaceans, annelids, etc.)
and vertebrates (fish, amphibian larvae) during late spring and early summer.
Such potential prey may be especially concentrated before summer rains
permit dispersal (Dickinson 1948; Kushlan 1974, 1976, 1979; Kushlan and
Kushlan 1980b). Additionally, new vegetative growth is available throughout
the spring and summer.
Nesting in the winter may accrue an additional anti-predatory benefit.
Because most predation of turtle eggs occurs within a few days of oviposition
(Christens and Bider 1987; pers. observe) the probability of predation is
relatively independent of the length of time that an egg is in the nest.
Therefore, the increased time that eggs laid in fall or winter require before
hatching should not increase their availability to predators. Rather, dispersal
of eggs throughout a period of 6 to 10 months, with no single nesting peak,
should reduce their reliability as a food source to potential o6phages. Most
predators of turtle eggs are generalists that specialize seasonally on turtle eggs.
The unreliability of eggs of winter-nesting turtles may preclude seasonal
specialization on eggs and the associated formation of search images. This
should be especially beneficial to smaller, carnivorous turtles that occur in low
densities (e.g. Deirochelys reticularia) and which therefore are incapable of
satiating predators.
The basis of a third potential selective advantage of winter-nesting to
Pseudemys floridana--reduction of interspecific competition--requires a brief
examination of the biology of the species in other parts of its range. Of the
four species studied in northern peninsular Florida, P. floridana has the most


poorly defined nesting season, nesting occurring throughout a ten-month
period with a short respite during the two hottest months of the year (July and
August). Whether this pattern is better referred to as extended "winter-
nesting" or interrupted continuous nesting is debatable. A comparison of this
pattern with the nesting season of P. floridana elsewhere is instructive.
Whereas reports of nesting from just north and south of the study area
(Okefenokee Swamp, southern Georgia: Wright and Funkhouser 1915; central
peninsular Florida: Netting 1929, Goff and Goff 1932) are in general accord
with those from northern peninsular Florida, data from more northerly
localities are not. Thomas (1972) reported restriction of the nesting season in
the lower coastal plain of Alabama, Georgia, and the Florida panhandle to the
summer months of June through August (perhaps beginning in early May) with
a June peak, followed by a period of reproductive quiescence during October
and November. Gibbons and Coker (1977) noted nesting activity from mid-
May to late June in South Carolina. Wright and Funkhouser (1915) likewise
described a June peak in the Okefenokee, so nesting there may coincide more
closely with that of populations to the north and west than with that of
conspecifics to the south. Furthermore, hatchlings from Alabama and South
Carolina presumably overwinter in the nest (Thomas 1972; Gibbons and Coker
1977). It thus appears that north of peninsular Florida P. floridana displays the
typical north temperate pattern of a late spring-early summer nesting season,
with overwintering in the nest, whereas in peninsular Florida the species has
for physical and/or biotic reasons adopted a greatly extended nesting season
that excludes mid-summer. I have yet to find any factor--thermal tolerances of
eggs or embryos, critical thermal maxima of adults (Hutchinson et al. 1966),
resource availability, etc.--that physically would preclude P. floridana from
nesting in the peninsula at the time it nests elsewhere. I suggest, in addition to
the general selective advantages developed above, a specific biotic factor
favoring the adoption of winter-nesting by P. floridana in the Florida peninsula.
Only in peninsular Florida does Pseudemys floridana co-occur with an
emydid turtle of similar size and habits (P. nelsoni). As shown above, P.
nelsoni exhibits a restricted summer nesting season (June-August), during
which dense populations may produce enormous numbers of eggs. By laying
cold-tolerant eggs during fall and winter, P. floridana assures its hatchlings the
opportunity to exploit resources and initiate growth before P. nelsoni
hatchlings begin to emerge. The time gained by earlier nesting more than
offsets the relatively small difference in mean developmental periods. Coupled
with a slightly larger mean size at hatching, the additional time for early growth
by young P. floridana may reduce competition between the two species during
their early omnivorous periods.
Competition with young Deirochelys reticularia is assumed to be negligible
as a consequence of the specialized trophic apparatus of that species (Jackson
1978b). Unfortunately, the dearth of ecological information on hatchling


turtles precludes estimation of the extent of competition among them.
Nonetheless, the importance of seasonal reproductive and/or juvenile size
differences in reducing competition among young of ecologically similar
species has been noted for a number of amphibians and lizards (e.g. Anderson
1968; Worthington 1968; Telford 1971; Crump 1974; Walters 1975; Barbault
1976; Orr and Maple 1978). Additionally, although differences in nest sites
may exist between female P. nelsoni and P. floridana, analogous to those noted
elsewhere between P. floridana and Trachemys scripta (Thomas 1972),
potential competition for nest sites is eliminated by non-overlapping
reproductive seasons. (Moll [1979] drew the same conclusion for Costa Rican
sea turtles that share the same nesting beach.) Similar benefits may accrue in
some riverine habitats, where P. floridana may coexist with a different summer-
nesting species, P. concinna (Marchand 1942; author's unpubl. data). In
contrast, P. floridana is conspicuously absent from two other situations in
Florida: (1) rivers characterized by dark waters, seasonally low temperatures,
and frequent flooding (Crenshaw 1955); and (2) shallow marshes subject to
seasonal drought (e.g. Payne's Prairie, Alachua Co.; most of Florida
Everglades). P. concinna, which is morphologically adapted for riverine
existence, monopolizes the former habitat, as does P. nelsoni the latter; food
levels are highly seasonal in both.
Based on these data, I propose the following hypothesis: in peninsular
Florida habitats in which food is abundant and available year-round, P.
floridana can coexist with a potentially superior but reproductively restricted
competitor (P. nelsoni or P. concinna) by virtue of a high level of temporal
reproductive plasticity that allows the former to nest during that portion of the
year that is unavailable to the latter; in habitats where food levels are highly
seasonal, this expression of reproductive plasticity is not possible, and P.
floridana is excluded. By analogy, the late Pleistocene disappearance of T.
scripta from most of peninsular Florida (Jackson 1977), the current domain of
the summer-nesting P. nelsoni, may reflect competitive failure as a result of
inability to modify its nesting strategy.
Comparison of the reproductive season of a more northern population of
Deirochelys with that of Florida conspecifics is likewise instructive. Female D.
reticularia in South Carolina presumably begin nesting in late August and
September, then cease until the following February or March when nesting
activity is completed. In some years, a small percentage of females produce
their last clutch as late as April or early May (Gibbons 1969; Gibbons and
Greene 1978; Congdon et al. 1983). It is probable that such an "interrupted"
nesting season is derived from a more continuous, winter-nesting season as
occurs today in Florida, where the lineage is known to have existed for at least
10 million years. As the population expanded northward, climatic factors
probably dictated a mid-winter interruption of the nesting season. Based on
studies conducted in an artificially warm environment, Gibbons and Sharitz


(1974) suggested that the present temperature regime in South Carolina is
similarly responsible for the abbreviation of potentially prolonged breeding
seasons of several species of frogs and fishes. Thus, it is probably unwise to
view the bimodall reproductive season" of Deirochelys in South Carolina as a
unique reproductive cycle (contra Congdon, Gibbons et al. 1983). Similar
comparisons of the nesting seasons of temperate vs tropical populations of two
species of marine turtles, Chelonia mydas and C. depressa, further implicate
temperature as a major proximate factor in the determination of chelonian
nesting seasons (Moll 1979).
There remains a number of unexplored factors that potentially might
determine nesting seasons. Physiological and behavioral (e.g. basking)
differences among the species might preclude summer-nesting species from
nesting in the winter, but a restriction in the opposite direction is less likely.
Interspecific differences in the capabilities of females to store sperm have been
linked to seasonal differences in the reproductive cycles of other vertebrates
(McNab 1974) and cannot be dismissed automatically here. That seasonal
availability of the dietary resources of adults might regulate nesting seasons of
these species, independently of competition, seems at first glance unlikely.
Winter-nesting species include both a strict herbivore (Pseudemys floridana)
and a strict carnivore (Deirochelys reticularia); summer-nesting species include
one herbivore (P. nelsoni) and one omnivore (Trachemys scripta).
Nevertheless, the importance of lipid accumulation to reproductive cycles is
well known for squamate reptiles and likewise may prove highly significant to
turtles (Brenner 1970).

From the Standpoint of the Egg (Developmental Ecology).-- A
subsurface nest at any time of year offers a more thermally stable environment
than one exposed to the atmosphere; diel soil temperatures in northern Florida
rarely fluctuate more than 3 degrees, even though ambient temperatures may
vary 10 degrees or more (Fig. 3). Despite this, eggs of summer- and winter-
nesting turtles are exposed to completely different environmental regimes
following oviposition. Eggs of summer-nesters almost immediately encounter
temperatures nearly optimal for rapid development (determined in the
laboratory as ca 27*C-29*C; compare Table 4). Development is initiated
quickly and proceeds fairly rapidly without interruption; most hatching is
complete by late August or early September. Eggs of winter-nesters, on the
other hand, usually encounter soil temperatures of about 14C-16C, rarely
lower than 100C or higher than 200C, for a few weeks to several months
following oviposition. Results of developmental experiments described earlier,
as well as field data of Goff and Goff (1932), indicate that little or no
development occurs in this temperature range for these species. The eggs
remain dormant though viable, in a state of arrested development (embryonic
diapause: Ewert 1985), until spring soil temperatures exceeding ca 20*C permit


embryogenesis to resume. Goff and Goff (1932) reported natural incubation
periods of 150 days and 120 days, respectively, for eggs laid on 8 February and
8 March 1931 (Lake Co., FL); eggs laid in autumn would require more than
200 days before hatching.
Results of preliminary developmental experiments are not conclusive but
do support several testable hypotheses:
(1) Exposure of eggs to a period of low temperature (20C) prior
to the onset of development does not hinder and in fact may
increase hatching success of winter-nesting turtles. Such
facilitation does not occur for summer-nesters, the eggs of
which instead show increased mortality in response to
prolonged periods (more than one month?) of low
(2) Inhibition of early embryogenesis at moderately low
S temperatures (ca 20*C) is greater for winter-nesting species
than for summer-nesting species (biochemical or physiological
differences?), with a consequently higher mortality rate for
embryos of the latter group if low temperatures persist.
(3) Inhibition of or a pronounced decrease in the rate of
development at low temperatures can be tolerated at any time
during embryogenesis by winter-nesters (although in nature it
usually would occur during relatively early stages).
(4) Levels of mortality induced by prolonged periods of low
temperatures are dependent upon developmental stage in
turtles, early embryonic stages being more cold-resistant than
later ones (Yntema 1960 provided limited evidence of this).
Confirmation of these hypotheses would suggest that winter-nesting species
evolved specific mechanisms that adapted (or pre-adapted) them for nesting at
a time of relatively low temperature that is followed predictably by a period of
rising and higher temperatures, the latter period subject to unpredictable but
brief returns to cooler conditions (spring cold fronts). Such mechanisms not
only may be absent from summer-nesting species but also may vary
geographically. Although not investigated here, embryonic tolerances to
substrate moisture levels also may differ between winter- and summer-nesting
species. Clearly, additional laboratory experiments coupled with temperature
and moisture data from natural nests would prove rewarding. Biologists
investigating properties of turtle eggs and embryos should use caution in
extending any data obtained from eggs of a single species in one geographic
area (Tinkle and Gibbons 1977; Ewert 1979).
Physiologically, reptilian embryos behave like typical ectothermic
organisms in their responses to temperature (Packard et al. 1977; Ewert 1985).
That is, within a range tolerable to the embryo, metabolism and rate of
development increase with temperature. An optimum temperature for


maximum rate of embryogenesis seems to exist for each species; deviations
may increase mortality or produce anomalies whose severity is proportional to
the amount of deviation from the optimum. However, reductions of
temperature far below optimum, rather than leading to gross anomalies or
even death, may simply retard development and delay hatching. Such arrested
development, or diapause, is distinct from overwintering or delayed emergence
of hatchlings (Gibbons and Nelson 1978), although its ecological consequences
may be similar. As the present study suggests, the delay in hatching time,
rather than being an ill effect (Packard et al. 1977), actually may be an integral
part of the life history tactics of some organisms. At least for P. floridana,
diapause seems to be facultative rather than obligate; determination of
whether Deirochelys might represent an obligate diapauser will require further
experimentation. The timing of the cold period that induces diapause may be
critical. Yntema (1978) has shown that for Chelydra serpentina incubated at
200C, not only is developmental retardation more marked in earlier than in
later stages, but in fact during the last two weeks of embryogenesis the rate of
development approaches temperature-independence. For diapausing reptiles
that oviposit in the fall, soil temperatures during late fall and winter must be
sufficiently low to arrest development yet not so low that they cause eggs to
freeze or preclude nesting or other reproductive activity. Thus, the temperate
winter-nesting strategy as defined herein is likely confined to a single
circumtemperate band in each hemisphere, the widths and precise latitudes of
which depend upon local climatic conditions. This paper documents use of this
strategy by two species of turtles at 29*40'N latitude and that of Goode and
Russell (1968) by a third (Chelodina expansa) at 35*56'S latitude. Data
summarized by Wilson (1968) suggest that the tortoise Geochelone pardalis
also adopts such a strategy in South Africa (ca 33S latitude) while following a
more "typical" developmental pattern at lower latitudes.
Although untested in the present study, the effects of incubational
temperature on sexual differentiation in turtles (see Ewert 1985) may be
relevant to the evolution of nesting seasons. Temperature-dependent sex
determination is known to be operant in southeastern Trachemys scripta (Bull
et al. 1982) and Deirochelys reticularia and is probable in Pseudemys floridana
(M. Ewert pers. comm.); P. nelsoni has not been tested. If the mechanism that
characterizes most emydines examined thus far (i.e. production of females only
when soil temperatures are above ca 28*C at least half of the time) applied to a
species in northern Florida, then selection might have favored a summer-
nesting pattern (a winter-nester with a 280C critical temperature would
produce few females). However, if females also differentiated at some cooler
temperatures, as in Chrysemys picta (Schwarzkopf and Brooks 1987), or if
either the critical temperature were relatively low or the critical developmental
period were not reached prior to rapid spring warming, then winter-nesting
might be possible. With their diversity of nesting seasons, the emydines of


northern Florida should be especially interesting subjects for detailed studies
of environmental sex determination.

Concluding Thoughts.-- Whatever the nature of differences that actually
exist between winter- and summer-nesting turtles--whether morphological,
behavioral, physiological, or ecological--it is clear that in peninsular Florida,
populations of two species of emydids (Pseudemys nelsoni and Trachemys
scripta) have remained rigidly attached to ancestral reproductive patterns
whereas those of two others (P. floridana and Deirochelys reticularia) have
escaped these restrictions and adopted a successful new pattern. I assume a
genetic basis for these differences, although experiments such as those
suggested by Connell (1980, 1983) are needed to confirm this. No other
detailed comparative study of North American turtle reproductive strategies
has revealed such pronounced seasonal differences. Four closely related
species of kinosternid turtles (three of which are sympatric in Arkansas)
examined by Mahmoud and Klicka (1972) exhibited a summer-nesting pattern.
Likewise, nearly all members of multispecies turtle communities studied by
Congdon in Michigan (summarized by Congdon et al. 1987) and Gibbons in
South Carolina (several aforementioned papers) nest during late spring and
summer, except for Deirochelys as noted above. In these cases, restrictions of
highly seasonal climates likely have subordinated selective pressures that
otherwise might have favored the expression of any existing plasticity. In
contrast, examination of the literature on the reproductive biology of Florida
kinosternids (Carr 1952; Iverson 1977, 1978, 1979b; Cox and Marion 1978;
Etchberger and Ehrhart 1987) reveals temporal differences that may prove
comparable to those of Florida emydids.
In the southern hemisphere at least two assemblages of freshwater side-
necked turtles (suborder Pleurodira) present excellent opportunities for
detailed comparative studies of reproductive ecology. Analyses by Goode and
Russell (1968) and Legler (1985) of the reproductive patterns of sympatric
Australian chelids have revealed temporal differences remarkably parallel to
those of Florida emydids. Eggs of Emydura macquarii and Chelodina
longicollis are laid in spring and hatch within a few months, whereas those of C
expansa are laid in autumn and overwinter as very early embryos, not resuming
development until the following spring. Vanzolini (1977) pointed out the need
for a thorough examination of the reproductive biologies of turtles of the genus
Podocnemis (Pelomedusidae), at least six species of which occupy the rivers of
tropical South America. His preliminary data suggested not only interspecific
temporal reproductive differences geared to regimes of rivers and hence to
rainfall patterns, but also intraspecific differences among populations living in
different rivers.
It is tempting, and perhaps easier, to explain the occurrence of autumn-
or winter-nesting by a temperate reptile as the retention of a characteristic that


was adaptive when the species maintained a different geographic distribution
(e.g. more tropical). At least in this study, however, I believe that the winter-
nesting strategy coupled with the impressive fossil record of Deirochelys
precludes this line of reasoning. Furthermore, if the thermal requirements of
eggs are adjusted to existing thermal conditions and are an important
determinant of a species' distribution, as proposed by Licht and Moberly
(1965) for oviparous lizards, then species utilizing a winter-nesting strategy are
at least as well adapted to their present environment as are sympatric species
that practice the more usual summer-nesting pattern. The reproductive
patterns of Florida emydids stand in marked contrast to those of long-term
tropical residents (see e.g. Moll and Legler 1971).
Likewise, temporal differences in reproductive cycles among sympatric
species have been used as one line of evidence for the relative recency of
sympatry, the differences having evolved under distinct climatic regimes (e.g.
Asplund and Lowe 1964; Lin 1980; Edmunds 1982; Legler 1985). The present
study suggests that temporal reproductive differences alone do not justify this
conclusion, so that supplementary lines of evidence must be provided.


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