University of Central Florida STARS

Retrospective Theses and Dissertations

1984

The Reproductive Biology of STERNOTHERUS MINOR MINOR (Reptilia: Testudines: Kinosternidae) from the Southern Part of its Range in Central Florida

Cory R. Etchberger University of Central Florida

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STARS Citation Etchberger, Cory R., "The Reproductive Biology of STERNOTHERUS MINOR MINOR (Reptilia: Testudines: Kinosternidae) from the Southern Part of its Range in Central Florida" (1984). Retrospective Theses and Dissertations. 4719. https://stars.library.ucf.edu/rtd/4719 THE REPRODUCTIVE BIOLOGY OF STERNOTHERUS MINOR MINOR (REPTILIA: TESTUDINES: KINOSTERNIDAE) FROM THE SOUTHERN PART OF ITS RANGE IN CENTRAL FLORIDA

BY

CORY RANDAL ETCHBERGER B.A., Earlham College, 1981

THESIS Submitted in pa rti a 1 ful fi 11 ment of the requirements for the aster of Science degree in Biology in the Graduate Studies Program of the College of Arts and Sciences University· of Central Florida Orlando, Florida

Summer Term 1984 ABSTRACT Variation in chelonian reproducti"ve patterns is well documented. Previous studies of loggerhead musk turtles (Sternotherus minor) repro­ duction have not attempted to control for variation in 1a ti tu de, 1ocal population differences, and seasonal variation. The present study attempts to control for these variables by collecting turtles from one population for one reproductive season. The reproductive pattern of

~minor at the southern limit of its range (Central Florida) is com­ pared to those of i.:_ minor studied elsewhere. Both male and female musk turtles mature after five to six years and at approximately 60 mm plastron length. No sexual dimorphism in overall body size is evident. There is a significant relationship between testis mass and male body size. Spermatogenesis begins in June as testes begin to enlarge. A peak in the testicular cycle is observed in Au gust and September followed by testicular regression from October through January. A germinal quiescent phase is evident from February through April. Vitellogenesis in females begins in mid-September and the first clutch is laid in late October. Ovi positions continue until mid-June when fo 11 i cul a r regress ion begins. A brief but dis ti net ovarian quiescent period occurs in August. Mean clutch size is 3.0 (range= 1-5). Clutch size and clutch mass were significantly correlated with body size. Egg length is not significantly correlated with clutch size or plastron length. Four clutches per year are comnnn and some femal es probabl y produce five. Reproductive potential and individual reproductive effort are both correlated with body size. Testicular acti vi ty peaks si x rronths after a peak in the ovarian cycle. Similarities with other studies of Sternotherus minor include: timing of the reproductive cycles, mean female size, and size and age at maturi ty . Mean clutch size i n Central Florida is significantly larger than elsewhere. Thi s difference is explained by the fact that rrore females produce three and fo ur eggs. While similarities and differences in reproduct i ve characteristics do exist between Central Florida S. minor and nnre northern popul ations, it is clear that those similarities and differences must be interpreted with respect to the methods of data coll ection used. Annual reproductive poten­ tial is enhanced in the Central Fl or ida population. This is explained by greater resource availability whi ch is t ranslated into a greater repro due ti ve output. ACKNOWLEDGEMENTS

First and forerrost I would like to thank Dr. Llewellyn M.

Ehrhart, my major professor, for his excellent advice and support throughout this project. I would also like to thank the other committee members, Dr. I . Jack Stout, Dr. Haven Sweet, and Dr. Peter C.H. Pritchard, for their advice and for critically reviewing the thesis. I am indebted to the following people for their help in col­ lecting. specimens: Dr. Llewellyn Ehrhart, Karen Etchberger, Betty Lynne Bolt, Rebecca Bolt, Steve Myers, Rob Parsons, Dr. Peter C.H. Pritchard, Paul Rayrrond, Anders Rhodin, Susan Rhodin, Doug Scheidt, Rick Smith, Linnaeus, and Dr. Franklin F. Snelson. I would also like to thank Dr. Judy Edson for her help with the statistical analysis. Dr. Haven Sweet allowed me access to his

Apple computers for which I am roost grateful1• A special thanks is due to Dr. John B. Iverson for sparking my interest in turtles and for his review of the thesis. My wife, Karen, drew many of the figures and typed the manu­ script, but I thank her roost for her understanding and patience throughout this entire project.

iv TABLE OF CONT ENTS

LIST OF TABLES • • vi

LIST OF FIGURES • • vii

INTRO DUCT! ON . 1

STUDY AREA • ...... 5 MATERIALS AND METHODS 7

RES UL TS AND DISCUSSION • • • • . 9

Size and Age at Maturity • • • . 9

Sexual Dirrorphism . •. • 13

Ma 1e Reproductive Cyc 1e . . 13

Female Reproductive Cycle •• • ••••• . 19

Relationship of the Mal e and Femal e Cycles 24

Extrauterine Migration of Eggs • 24

Clutch Size • • • • . • • • . • • . 25 Frequency and Number of Cl utches . . . . • • • • 27 Eggs, Incubation and Hatchli ngs . • 32

Annual Reproductive Po t enti a 1 • 34

Reproducti ve Effort •• 38

CONCLUSIONS • • • •• ...... 40

APPENDIX 1 •• • • 42 LITERATURE CIT ED • • • 45

v LIST OF TABLES

1. Comparisons of reproductive characteristics from four

pop u1 a ti on s ...... 10 2. Monthly percentages of female reproductive characteristics .. 22 3. 1ean clutch size estimates ...... 26

4. Mean clutch size and clutch mass by size class .... 30 5. Mean egg sizes ...... 33

vi LI ST 0 F FI GIJRES

1. Size class distribution of adults ...... •...... 14 2. Relationship between log body weight and log pl astron

1 ength far adults . . • 15 3. Relationship between total testis mass and plastron length .. 17 4. tvbnthly variation in relative testis mass . . . • . • 18

5. M:rnthly variation in the mean diameter of the largest

follicle ...... 21

6. Relationship between clutch size and plastron length • 28

7. Relationship between clutch mass and body mass • • • 29

8. Egg component analysis ..... • • 35

9. Relationship between reproductive potential and plastron

length ...... 37

10. Relationship between reproductive effort and clutch size . 39

vii INTRODUCTION

A major feature of any species' 1 ife history is the pattern of reproduction. Several characteristics must be considered when de­ scribing the reproductive biology of a species. The reproductive data that are rrost relevant to chelonians include: size and age at maturity, clutch size, frequency and timing of clutch production, and egg and hatchling characteristics. Reproductive data are available for all four North American freshwater turtle families, although they have not been studied to the same extent. Reproduction and growth were examined in the chelydrids Macroclemys temminki (Dobie, 1971) and Chelydra serpentina (White and M.Jrphy, 1973). The gonadal cycles of the two species are similar but~ serpentina produces larger clutches than~ temminki. The reproductive cycles of trionychids are similar, however the age and size at maturity and the number of clutches per year vary among species (Webb, 1962; PluTTITier, 1977; Robinson and Murphy, 1978). Much variation in reproductive characteristics exists among emydid turtles. One of the first investigators to quantify the ovarian cycle of an emydid was Powell (1967). He compared repro­ duction in Chrysemys picta and Clemmys insculpta from Nova Scotia. Chrysemys picta laid larger clutches in more northern latitudes, but this pattern was not observe~ in ~ insculpta. Clutch size and 2 body size are known to vary within a single geographic area (Gibbons and Tinkle, 1969; Ernst, 1971). Timing of the reprod~ctive cycles and number of clutches per year varies within a subspecies (Christiansen and Moll, 1973). Reproductive potential varies with body size in Graptemys pulchra and the average number of eggs laid per year is greater than in h barbouri (Shealy, 1976). The family Kinosternidae has been studied most extensively. Reproductive data for Sternotherus (Risely, 1933, 1938; Tinkle, 1958, 1961; Edgren, 1960; ·ahmoud, 1967; Gibbons , 1970; Mahmoud and Klicka, 1972; Iverson, 1977, 1978; Cox and Marion, 1978; McP herson and Marion, 198la, 198lb) and Kinosternon (Einem, 1956; Mahmoud, 1967; Mahmoud and Klicka, 1972; Christiansen and Dunham , 1972; Iverson, 1977, 1979a, 1979b; Hul se, 1982; and Gibbons, 1983) indicate certain similaities within the family. The male and female gonadal cycles 92nerally do not peak at the sarre time. The spermatogenic cycle usually peaks from two to six rmnths after a peak in the ovarian cycle. As in other turtle families, clutch size and timing of clutches vary within a species' range. Variation in reproductive activity for five species of turtles (Pseudemys floridana, .!:.:_ scripta, Deirochelys reticularia, Sternotherus odoratus and Kinosternon sub rubrum) from one geographic area has been documented (Gibbons, Green, and Patterson, 1982). Turtle reproduction is known to vary with latitude, season, or arrong populations from the same latitude in the same reproductive season. Geographic variation in chelonian reproductive patterns was 3 first reported in Sternotherus odoratus (Tinkle, 1961). Larger females and larger clutches occurred in rrore northern latitudes. Southern musk turtles matured at a smaller size than northern turtles. The same trend in latitudinal variation in body size and clutch size was observed in populations of Chrysemys picta (Moll, 1973). Mean clutch size in one population of Trionyx muticus from Kansas varied significantly from year to year (Plummer, 1977). Clutch size was not correlated with body size within three populations of~ picta from southern Mi chigan, but the population in whi ch mean female size was larger exhibited a greater mean clutch size (Gibbons and Tinkle, 1969). Previous investigators who have studied Sternotherus minor have not attempted to control for differences in latitude, season or population. Tinkle (1958) compared reproductive data in three species of Sternotherus. Specimens were collected throughout the species range over several years. He utilized fresh and museum specimens and found differences arrong the species in size and age at rraturity, clutch size, and reproductive potential. Reproductive characteristics of female ~minor from tvo populations (and from two sample periods) were studied in northwest Florida (Cox and Marion, 1978). Sternotherus minor was also studied in orth Florida by Iverson (1978). Turtles were actively collected from 1971-1974 and he supplimented his samples with museum specimens collected prior to 1971. Because there is much variation in ch el onian reproduction, these three studies (Tinkle, 1958; Cox and Marion, 1978; and Iverson, 1978) 4 may have introduced uncontrolled variables which could lead to erroneous conclusions. The purpose of this study was to provide reproductive information about male and female reproductive cycles of Sternotherus minor from the southern limit of its range in Central Florida. An attempt was made to control for thP. variables of latititude, local · population differences, and seasonal fluctu­ ations by collecting turtles from one population for one year.

These data are compared to the data of investigators who studied h minor reproduction but did not make an attempt to control for these variables (Tinkle, 1958; Cox and Marion, 1978; Iverson, 1978). A comparison of this population's reproductive strategy with that of other k i nos tern i ds i s a 1so i nc 1 ude d . STUDY AREA

The study area is located 4 km northeast of Oviedo, Florida in Seminole County (Sections 1, 3, and 35; the border of T 21S and T 20S;

R 31E). The surrounding area, known as the "Black Hamrrock", is primarily agricultural. Watercress is the primary crop but celery, lettuce, and citrus are also grown. Dirt roads parallel man-made drainage canals which run adjacent to the watercress fields. The watercress is grown in shallow, rectang~ar depressions and watered via wells. The runoff water flows from the fields into the drainage canals mentioned abowe and eventually north to Lake· Jessup, which is part of the St. Johns River drainage basin. Turtles were collected from two canals. One was 1 km long and fiowed in an east-west direction. It was 10 m wide at the top with steep banks, but only 3 mat water level. The primary vegetation on the south slope was saw palmetto (Serenoa repens) and live oak trees (Quercus virginiana). Turtles frequently took refuge anung the roots. The north slope had only short ground cover. A small amount of emergent aquatic vegetation (Lemna minor, and floating mats of water hyacinths) was present during summer rronths. The only subrrergent vegetation was algal mats that were nnst prominent in the shallows. The bottom of the canal was composed of hard sand in rrost places, but there were i ntennittent pockets of organic rruck.

5 6

Turtles were also collected from a canal 0.5 km long that flowed in a north-south direction. This canal was 2 m wide at the top and the banks sloped gradually down to a width of 1 mat water level. Oa k trees (Quercus virginiana) lined both sides of the northern third of the canal, and watercress fields paralleled the canal along the rest of its length. Submerged vegetation included Hydr illa sp. and algal mats. The bottom of the canal was hard sand. Water fiowed from this canal into the previously described canal. Water in both canals was usually clear and the flow was 0.5 m/sec. Water depth ranged from less than 5 cm in the shall ows to 2 min the pools. The water level remained fairly constant throughout the year except imrTEdiately fo lowing heavy rains when the water level rose and the water became turbid. Surface water temperature ranged from 14° C (January) to 28.5° C (August). MATERIALS AND METHODS

Sixty-five female and 23 male Sternotherus minor were collected from June 1983 to May 1984. Specimens were collected either by hand or by seining. Most specimens were examined with in 48 hours after capture. External rrorphological measurements included: carapace length (CL), plastron length (PL), mass, and the number of abdominal scute annuli. Age estimates were made by counting the abdominal scute annuli (growth rings) . Each annulus on the abdo minal scute rep­ resents the end of the previous year's growth, while the area between the annuli indicates growth (Sexton , 1959). Annul i tended to become snnoth and difficult to count with age especially when there were rrore than seven or eight annuli present. A sample of females found by palpation to have oviducal eggs were held for two weeks prior to dissection to allow for complete shell for­ mation. Oviducal eggs and ovaries were excised and measured. All ovarian follicles >4 mm in diame:ter and all corpora lutea were counted and measured. The length, width, and mass of each egg were recorded. Immediately after weighing, 49 of the eggs were examined for egg com­ ponent analysis. The shell was cut in half and the yolk and albumen were expelled onto a paper towel. The shell was blotted dry with a Kim-Wipe and the wet shell mass was recorded. The excised yolk was also blotted dry of albumen and the largest diameter and mass were recorded. The albumen mass was then calculated by subtracting the sum

7 8 of the wet yolk mass and wet shell mass from total egg mass. Twenty­ two fully she l led oviducal eggs were incubated in sand at 25° C. Imme­ diat ely foll owin g hatching neonates were me asu red (PL and CL) and we i ghed . After excision, ma xi mum length, mi ni mum l ength, and mass were measured for eac h test is. All l i near rrea surements were taken wi t h a vernier caliper to the nearest rrm . Body ma ss was measured on a tripl e beam balance, accurate to the nearest gm. Mea su remen t s of excised reproductive organs were determined to the nearest 0.01 gm or mm with a Torbal Model ET-1 balance and vernier caliper. Specimens were tagged, fixed in 10% formal in, and later transfered to 40% isopropanol and depo sited i n the USF ve rtebrate collection. Slopes of least squ ares reg ression l ines were considered signifi­ cantly different by comparin g the standa rd errors of the regression coefficients (Sokal and Rohl f, 1981). Me ans were compared by Student's t-test calculated on an Appl e II pl us co mputer . Significance levels are shown when the data are presented. RES UL TS AND DISCUSSION

Size and Age at Matu rity Maturity in ma1es was determined by the presence of sperm in the epididymis. The smallest mature male was 57.0 mm p1astron length (PL) and had six abdominal scute annuli; whereas the largest i ITTTiature ma 1e was 63. 2 mm PL and had seven annuli. These data indicate that males typically mature at approximately 60 mm PL and at five to six years of age. Females were considered mature if oviducal eggs, corpora lutea, or ovarian follicles >Anm in diameter were present. By these criteria the smallest mature female measured 60.1 ITTn PL and had six annuli. No juvenile female turtles were collected in the study area but an immature Sternotherus minor (61.2 mm PL) was collected 10 km south of the study area. The smallest female with oviducal eggs measured 65.0 rrrn PL and had six annuli. Female h_f:llinor apparently mature after five or six yea rs and at approximately 60 mm PL. A comparison of reproductive characteristics from previous studies with those observed here is in Table 1. Male and female S. minor mature at the same size in Central Florida. These data support the suggestion by previous investigators that 60 mm PL is required for sexual maturity (Table 1). Onset of maturity in nnst chelonians is correlated with size rather than with age ("1:>11, 1979). Maleh odoratus, however, mature at the same age

9 Table 1. Comparisons of reproductive characteristics of Sternotherus minor from Central Florida with those of four other populations. Values are means . *indicates that the mean was significantly different at the 0.05 level. + indicates the mean was different due to a different measuring technique. ND indicates that no data are available for that character.

Reproductive Tinkle Cox & Marion Iverson Etchberger Character ( 1958) (1978) "(1978) (1984)

Maturit~ (~) ..,_. Size 60 mm PL ND ND 60 mm PL ...:::> Age 4-7 years ND ND 5-6 yea rs

Maturi t~ (~) Size 60 mn PL 60 mm PL 60 ITT1l PL 60 mn PL Age 5-6 years ND 5-6 years 5-6 years - x Size ND ND 77.2 mm PL 78 .4 mm PL

51- Reproductive cy__cl e ovarian cycle begin ND early Sept. early Sept. mid-Sept.

end ND early July eatl y July 1ate June Table 1. - - Continued

Reproductive Tinkle Cox & Marion Iverson Etchberger Character (1958) ( 1978) (1958) (1984)

yo 1 k di a meter ND 15 . 9 rrm + 16.5 mm+ 19 . 2 mm

maxi mum foll icl e ND 17.3 mm 17.0 mm 17 . 2 mm diame t er clutch size ~ ~ roodal number ND ND 2 3

preovul atorv follicles 2.7 2. 5* 2. 3* 3 . 0

oviducal eggs ND 2.4* 2.6* 3.0

co ·rpora 1 utea ND 2 .4* 2.4* ·.2. 9

egg size

width ND 17.1* 17.2 17.5

length ND 28.5* 28.5 27.9

mass ND 4.57* ND 5.27 Table 1. -- Continued

Reproductive Tinkle Cox & a rion Iverson Etchberger Character (1958) ( 1978) (1978) ( 1984)

% transuteri ne migration ND 45 .2 % 45 % 67.6 % (19/42) (9/20) (23/34) es ti mated number of 2 4 3 4 annual I-' clutches N estimated reproductive 6.3 9.6 7.3 12.0 potenti a 1 13 but at different sizes (Tinkle, 1961). Sexual Ditmrphism The frequency distribution of male and female plastron lengths is in Figure 1. There was a significant correlation between log weight and log PL in all adult turtles (Figure 2). However, the slopes of the least squares lines for log weight and log PL were not significant1 y different between ma 1es and fema 1es (ma 1es : logWT= -2.93 + 2.73(logPL) ~ 0.12 S.E.; females: logWT= -2.62 + 2.55(logPL) +- 0.18 S.E.). There was no significant difference between mean plastron lengths of the two sexes (Appendix 1). No sexual diroorphism in overall body size is evident. Male Reproductive Cycle Mature males had elliptical testes that were flacid and white. Testis width ranged from 3.9 mm to 14.9 mm and lengths varied · between 4.9 mm and 17.5 mn. No histological examination of the testes was performed, but a descriptive account of spermatogenesis in relation to gross morphology of the testis is presented here. Spermatogenesis is divided into 5 phases (tvnll, 1979): 1) germinal quiescence- a regressed size of semeniferous tubules and testis is associated with this period between gametogenic cycles; 2) gonial proliferation- proliferation of spermatogonia via mitosis; 3) spermatocytogenesis- appearance of spermatids and primary 20

in w 15 OMALES ..J }- ~ FEMALES 0: => ~ LL. 10 0 a:: w co ~ ::::> z 5

60-64 70-74 75-79 Bo-84 85-89 90-94 95 .. 99 100-104

PLASTRON LENGTH (mm) Figure 1. Size class· distribution of adult male and female Sternotherus minor from Central Florida. 15

... 0 2.4 A MALES 0 .A 0 FEMALES 8_.. •• 2.3 0 ... 2 t- ... :r: 0 (.!) ... • 0 -w 2.2 ;:: Ct 0 2. I 00 o · .& 2.0 0

I. 9 1.7 5 . 1.8 0 1.85 · 1.9 0 L95 2.0 0 log PL

Figure 2. Relationship between log body weight and log plastron length for male and female Sternotherus minor from Central F]orida (.r= 0.905; p <0.01; n= 87). ~ least squares regression line for the entire sample (sexes combined) is shown. 16 and secondary spermatocytes via meiosis; 4) spermiogenesis- maturation of spermatids from spermatozoa and an increased size of the testis; and 5) spermiation- spermatozoa in Sertoli cells are released and rrove into the epididymis; reduction in testis size. Because there was a positive relationship between body mass and testis mass (Figure 3), the data were standardized by dividing testis mass into body mass for each male. The eight specimens that derron­ strated this relationship best are represented as squares in Figure 3. These turtles were collected during the peak of testicular activity in July, August, September, and October. The seasonal changes in the testicular cycle are shown in Figure 4. The testes began to enlarge in spermatocytogenesis by July and attained their maximum size in spermiogenesis in August and September. Testes began to regress in October as spermiogenesis declined. Testi s size continued to decrease from November to January as mature spermatozoa were passed into the epididymis. The testes were smallest during the germinal quiescent phase from Fe ruary to April when adult turtle testes were as small as immature turtle testes. No previous studies have dealt with the male reproductive cycle of Sternotherus minor. However there are similarities in the testi­ cular cycle between .?_:_minor in Central Florida and S. odoratus from Central Alabama (McPherson and Marion, 198la). Maxirrum testis size in h odoratus was attained from August through mid-September. In Central Florida S. minor testis mass also peaked in August and 17

0 •• 60 70 80 90

PLASTRON LENGTH (mm}

Figure 3. Relationship between t est is ma ss and body size in Sternotherus minor from Central Florida (r= 0.591 ; p <0.01; n= 21). The least squa~es regression l i ne for al l data is shown. Squares represent turtles co 11 ected during Jul y, Au gust, September, and October. Circles represent turtles collected f rom the rest of the year. See text for details . 18

• 60 • •

(/) en 50 30 t- •

J A s 0 N D J F M A M J MONTH

Figure 4. Monthl5 variation in relative testis mass ( testis mass X 10,00 I body mass) in Sternotherus minor from Centra 1 Florida. 19

September. Testis mass did not begin to decline until November in both h odoratus and Central Florida i.:_ minor. The germinal qui es cent period occurred in February and March in h odoratus and from February to April in S. minor. June was the transitional rronth when testes began to enlarge in both h mi nor and~ odoratus. The same phases are seen in the two species and the timing of the cycles appears to coincide. Histological examination of~ minor testes is needed to determine the exact periodicity of the phases. Contrary to the data reported here, Mahrrou d and Klicka (1972) found no relationship between testis size and body size in h odoratus, h carinatus, Kinosternon fl avescens or h subrubrum. Mc Pherson and Mari on (198 la) reported a 11 tendency 11 for 1 arger turtles to have larger testes but presented no data. However, testis size was correlated with body size in some populations of Chrysemys picta (Gibbons, 1968). Female Re·produc ti ve Cycle The female reproductive cycle can be divided into 4 overlapping phases (tvb 11 , 1979) : 1) follicular enlargement- vitellogenesis begins as yolk is accumu- lated in the ovarian follicles and a preovulatory follicular size is attained ( >14 mm diameter in Sternotherus minor); enlargement of follicles occurs in groups in turtles that lay more than one clutch annually; 2) ovulation and intrauterine phase- the ova are shelled in the oviducts; 20

3) nesting- oviposition of the clutch in a nest dug by the female; and 4) latent (quiescent) phase- little or no reproductive activity and minimal size of the ovaries. Follicles began to enlarge in early September (Figure 5). Since no preovulatory follicles were present during the quiescent phase, all enlarged follicles pr~seet during the nesting season were assumed ovulated and laid. Turtles ovulated their first clutch of the season between mid-October and late November. A peak in reproductive activity occurred from December through May when rrost females possessed enlarged follicles, oviducal eggs or corpora lutea (Table 2 and Figure 5). A female collected on 3 June had two oviducal eggs, but no preovulatory follicles, indicating this wa s her last clutch of the season. The latent phase was characterized by a decrease in ovarian activity beginning in June. June, July, and August were the only rronths when mean follicle di'ameters were not greater than pre­ ovul atory size (14 rrm) (Figure 5). The percentage of turtles with oviducal eggs was lowest in July, August, and September and there was no indication of any follicular or ovulatory activity in the rro nth o f Aug us t (Tab 1 e 2 ) . The female reproductive cycle of Central Florida S. minor is very similar to that found in North Florida populations. Vitello­ genesis in North Florida begins in early September, reproduction peaks from December to May and the last clutch is ovulated in late June or early July (Table 1). The brief quiescent period (August) 21

20

8 4 7 7 9 -E -E 3 ~ 15 3 3 w ..... 3 $ w ~ II

5 JASON DJ FMAMJ MONTH Figure 5. f>'bnthly variation in mean diameter of the largest ovarian follicle observed in Sternotherus mi nor females from Cent ra 1 Florida. Hori zonta 1 lines represent means, vertic~l lines represent ranges, rectangles represent - 1 standard error on each side of the mean. Table 2. Monthly frequency of preovul atory follicles ( >14 mm), one set of corpora lutea, two sets of corpora lutea, and oviducal eggs in Sternotherus minor from Central Florida.

1 set of 2 sets of Enlarged corpora corpora Oviducal Sample follicles 1 utea lutea eggs Month size n % n % n % n %

July 1983 3 1 33 0 0 0 0 0 0

August 11 0 0 0 0 0 0 0 0 N N Se ptember 3 3 100 0 0 0 0 0 0

October 7 6 86 1 14 0 0 1 14

November 3 2 67 3 100 0 0 3 100

December 7 5 71 7 100 2 28 6 86

January 1984 8 8 100 8 100 1 13 7 87

February 4 4 100 4 100 3 75 3 75 March 7 4 57 7 100 6 86 6 86 April 9 7 78 9 100 6 67 5 55 May

June 3 2 67 3 100 1 33 2 67 23

in the present study coincides closely with that found in North Florida populations (Table 1).

The largest ovarian follicle was 17.2 mn; follicles were ovulated with a diameter near 17 mm. This value agrees closely with the largest follicle diameter measured in North Florida populations (Ta~le 1). Corpora lutea decreased in size after ovulation but they were macroscopically visible even after oviposition of a second clutch. Two size classes of corpora lutea were often present, distinguished by t heir relative states of regression. The largest set of corpora lutea represent s the most recent clutch and any other smaller corpora lutea present indicate a previous clutch. No females with oviducal eggs had the corresponding corpora 1utea in any state of regression

(maxi mum diameter 5-6 mm). The same phenomenon has been reported in orth Florida h m_inor (Cox and Marion, 1978; Iverson, 1978) and

Kinosternon baurii (Iverson, 1979b). Nineteen females had 2 distinct sets of corpora lutea (Table 2). The first turtle with 2 sets appeared on 16 December and subsequently turtles with 2 sets were collected on 28 December (1 turtle),

18 January (1), 27 February (3), 21 March (3), 27 March (3), 9 April

(2), 16 April (4), and 1 June (1). The second clutch was smaller than the first clutch in eight turtles; equal in six turtles; and larger than the first clutch in five. 24

Relationship of the Male and Female Cycles The spermatogenic cycle peaked 6 nnnths after a peak in the ovarian cycle (Figures 3 and 4). Sperm are only available for fertilization after they are passed into the epididymis, therefore during this period, testis mass was smallest. Testes were in a state of regression from November to April (when the ovarian cycle was rrost active). The disparity in the timing of the male and female cycles requires that both sexes be able to store mature sperm. Mature sperm were found in the epi di dymi s throughout the year in male S. minor. This has been observed in nurrerous other turtle species (Robinson and M.Jrphy, 1978; White and M.Jrphy, 1973;

~Pherson and Marion, 1981a). Females are known to lay viable clutches years after they have been isolated from males of the same species (Barney, 1922; Ewing, 1943). Fall mating has previously been suggested in h odoratus (Risely, 1933; McPherson and Marion, 198la). No mating was observed in the present study, but since the t esticular cycle is sif"lil ar to S. odoratus (M:Pherson and Marion, 1981a) from Central Alabama, I suspect that most mating in S. minor occurs in the fall. Extrauterine Migration of Eggs Ova released from one ovary do not necessarily rrove into the corresponding oviduct. Instead, ova may migrate across the body cavity and enter the opposite oviduct. Extrauterine (transuterine) migration was determined to have occurred when unequal numbers of oviducal eggs and corpora lutea were observed on either side of the 25 reproductive tract. Extrauterine migration was observed in 67.6 % (23/34) of the turtles with oviducal eggs. Five of these

23 turtles showed evidence of at least t\t~o eggs migrating. Migration of ova was seen more frequently in the present study than in other studies of h minor (Tabl e 1). The number of fresh corpora lutea equaled the number of oviducal eggs in all turtles except for one fema 1 e where two ovi ducal eggs were present but three corpora lutea were counted; the third broken ovum was free in the body cavity. The first evidence of transuterine migr ation was reP,orted in Terrapene ornata and h carolina (Legler, 1958) and in Sterno­ therus odoratus (Tinkle, 1959). Legler (1958) and Iverson (1978, 1979b)suggested that migration might serve to equalize the repro­ ductive tract volumes, while Tinkle (1959) and Moll and Legler (1971) suggested that this phenomenon is du e to chance. Net migration of eggs was away from the tract with the larger ovary in only 10 of the 23 cases. These data support the suggestion that transuterine migration is due to chance (Tinkle, 1959; MJll , and Legler, 1971). Clutch Size

Average c 1 u tch size was not s i gni fi cantl y different whether calculated by counts of enlarged follicles, oviducal eggs, or corpora lutea (Table 3). Clutch size ranged from 1 to 5 and the rmde was 3. Mean clutch size in Central Florida Sternotherus minor was significantly larger than reported for the two North 26

Table 3. Clutch size in Sternotherus mjnor from Central Florida as indicated by preovulatory follicles ( >14 nm), oviducal eggs, and corpora lutea. Shown are means, ! 1 standard deviation, ranges (in parentheses), and sample sizes.

Preovul atory 2.96 +- 1.22 follicles (1-5) n= 31 Ovi duca 1 3.00 ± 0.71 eggs (2-4) n= 33 Corpora 2.89 +- 0.87 1 utea (2-5) n= 27 Overall 2.95 +- 0.96 (1-5) n= 91 27

Florida populations (Table 1). Because there is no significant difference in mean female size between Central Florida S. minor and North Florida females, (Tabre 1) the difference in clutch size is not due to body size. Average clutch size in the present study was 3.0 but no other population studied exhibited a mean clutch size greater than 2.7 (Table 1). The maxirrum number of eggs was similar in all populations but Central Florida S. minor had a higher roodal number (Table 1). Therefore Central Florida S. minor does not increase clutch size by increasing body size or rraxi.llllm clutch size. Instead, there were nnre turtles laying three and four eggs in Central Florida. Clutch size was posi­ tively correlated with plastron length (Figure 6) and clutch mass was correlated with female body mass (Figure 7). Mean clutch size and mean clutch mass by female size class are presented in Table 4. The trend is for larger turtles to lay larger and heavier clutches. This is true for North Florida populations

as well (Cox and Marion, 1978; Iverson, 1978). Frequen£y and Number of Clutches The period between oviposition of clutches appears to be approximately 60 days. The first turtle with preovulatory follicles after the quiescent phase was collected on 19 September. The first turtle with incompletely shelled oviducal eggs was collected on 30 October. The period for development of preovulatory follicles to a partially shelled egg is approximately 45 days. (The period during which the ova are in the oviduct prior to shelling is probably very w N 3 w x u 2 .. • • ••• • r ~ co~ ~ u

65 70 75 00 85 90 95

PLASTRON LENGTH (mm) Figure 6. Relationship between clutch size and body size in Sternotherus minor from Central Florida(r= 0.635; p <0.01; n= 43). · The least squares regression line is shown. Clutch size is based on oviducal eggs. 25 •

-E .PJ 20 en en ...... J u 10

5'---"------.J------+------+------t------+------t------t 100 120 140 160 180 200 220 240 BODY MA SS (qm)

Figure 7. Relationship between clutch mass and body mass in Sternotherus minor from Central Florida (r= 0.713; p <0.01; n= 32). The least squares regression line is shown. Clutch mass was subtracted from body mass. Table 4. Mean clutch size and mean clutch mass by size class (plastron length) in Sternotherus minor from Central Florida. Clutch size is based on numbers of oviducal eggs.

Size class n Clutch Clutch (mm) size mass

65-69 3 2.0 8.7 70-74 7 2.6 13.5 75-79 12 3.2 16.9 80-84 8 3.3 17 .8 85-89 3 3.7 20.3 31 short because I did not observe any unshelled ova and previous investigators have seen very few; Iverson, pers. corrm.). The period during which the eggs remain in the oviducts before oviposition is probably less than three weeks (Cox and Marion, 1978; Iverson, 1978; present study). Other turtles exhibiting the first preovulatory fol­ licles of the season were collected on 17 October. Three turtles dis­ sected on 28 Novenber had completely shelled eggs and preovulatory follicles. These data indicate that some follicles are ovulated in mid-October, while other turtles do not ovulate their first clutch of the season until mid-November. This delay in ovulation allows egg 1 ayi.ng to occur every month between October and June. Cox and Marion (1978) noticed the sarre pattern of staggered ovulation in North

Florida~ minor. Two months is the internesting period reported for North Florida h minor (Cox and Marion, 1978; Iverson, 1978) and in Kinosternon baurii (Iverson, 1979b). The sum of the number of sets of corpora 1 utea and preovul atory follicles in a turtle is an estimate of the number of clutches laid in one season. Twenty-six females possessed one set of corpora lutea which suggests that at least two clutches per year are corrmon. Four­ teen other turtles had two sets of corpora lutea and preovulatory follicles indicating that three clutches are also very comrron. A11 females co 11 ected between 28 November and 3 June showed evidence of laying rrultiple clutches. The nesting season, defined here as the period during which females possessed oviducal eggs was from 30 October to 3 June. The internesting period of 60 days suggests that 32 five clutches are possible in some females. Tinkle (1958) found littl e evi de nce for ITTJltiple clutches but he speculated that~ minor mi ght lay more than a single clutch. Three and four clutches: were suggested by I ve rson (197 8) and Cox and Marion (1978) respectively. My data indi cate that l aying four clutches annually is comnnn at the southern limit of S. minor' s ran ge. Eggs, Incubation and Hatchl i ngs

A summary of st at i stics for eg g characteristics is pre~ented in Table 5. All egg characteristics were significantly different from those reported by Cox and Mar i on ( 1978), but not significantly dif­ ferent from other North Florida h mi nor eggs (Table 1). The signifi­ cantly larger yolk diameter i n the present study is explained by a different measuring technique. I measured yolks while they rested on a flat surface . Previous investigators measured them while the yolk was suspended in liquid (Iverson , per. co mm .). Therefore, the mean in the present study i s l arger due to a different measuring technique and not necessarily bec au se of inherent differences. Mean egg length was not significantly correlated with either female plastron length (r= 0. 236; p < 0.05; n= 30) or clutch size (r= 0.236; p < 0.05; n:;: 30). The sarre wa s true for North Florida S. minor (Iverson, 1978) and for othe r kinosternids (Iverson, 1979a, 1979b). Egg compo nent anal ysis was performe d on 49 eggs. Eggs were classified i nto on e of thr ee categories according to the extent of shell forma­ t ion: opaque (very so f t shell; yolk can easily be seen in egg; very fragile); soft (shell somewhat calcified, but still pliable); hard Table 5.+ Mean egg sizes in Sternotherus minor from Central Florida. Means are followed by - 1 standard deviation. Ranges appear in parentheses; sample sizes are also shown. All measurerrents a re in nm.

Egg Length Egg Width Egg Mass Yolk Di a meter Yolk Mass w w

+ 27.9 +- 1.9 17. 5 + - 1.1 5.2. 7 +- 0.78 2.31 +- 0.38 19. 2 - 1.0 (21.2-32.6) (12.7-19.5) (1.97-6.70) (1.55-2.92) (17.0-20.9) n= 93 n= 93 n= 97 n= 39 n= 44 34

(fully shelled; porcelain-like and brittle). The mean percentage for yolk, shell, and albumen in each category is presented in Figure 8. The relative amount of shell increased as the egg became rmre calcified. Yolk and albumen percentages decreased as the shelling process progressed. Few data are available for egg component percentages. The 18% shell mass in fully shelled eggs is higher than the 13.2% re- ported for .h minor (rtoll, 1979). . + Average plastron length of four hatchlings was 18.2 - 0.21 mn (range= 18.0- 18.5); carapace length of four averaged 23.5 +- 0.37 (range= 23.1- 24.0). Unfortunately the small sample size in the present study prohibits any meaningful corrparisons. Annual Reproductive Potential The reproductive potential is the sum of all eggs deposited in one year. SuTTlTling the number of corpora lutea and preovulatory fol 1 icl es present at one time is one method of estimating the mini rrum number of eggs deposited by a fema 1 e in a single year (Shealy, 1976). A mean reproductive potential of 5.9 eggs per female was calculated by this method. Reproductive potential can also be calculated by multiplying the mean clutch size by the nurrber of clutches laid per year (Iverson, 1979b). The number of clutches ranged from two to five, therefore the annua 1 repro­ ductive potential could range from 6.0 (3.0 X 2) to 15.0 (3.0 X 5). The reproductive potential for 2 clutches (6.0) is close to the minirrum estimated reproductive potential of 5.9. E G G C 0 M PO N ENT S EGG COMPONENTS EGG COMPONENTS FOR FOR FOR OPAQUE EGGS SOFT EGGS HARD EGGS n= 3 n= 24 n= 22

0 0 a

c w U1

c c

a:% albumen a: °lo albumen o: % albumen b: % shell b: %shell b:% shell c: % yolk c: % yolk c: % yolk

Figure 8. Egg component analysis for eggs from Central Florida Sternotherus minor. See text for details. 36

The annual reproductive potential reported here (12.0, based on 4 clutches) is higher than that found in other h minor studies (Table 1), and for various sternotherine turtles (h carinatus; 10.3, Tinkle, 1958; h odoratus; 10.3, Tinkle, 1961; h odoratus; 9.6, Iverson, 1977). The larger clutch size and the ability of Central Florida h minor to produce at least 4 clutches increases the annual reproductive potential. Figure 9 illustrates the relationship between reproductive potential and female body size. Larger turtles tended to lay more eggs in a season. There are two components to reproductive potential: nuni>er of clutches and clutch size. Turtles ranging in size from 65.0 to 89.2 nm PL showed evidence of laying nultiple clutches, therefore body size was not a factor in determining the number of clutches in a season. Because clutch size was correlated with body size, clutch size is probably a more important compon­ ent of annual reproductive potential than the nurrber of clutches. Larger clutch size and an extended nesting season both contributed to a higher reproductive potential in larger Graptemys pulchra (Shealy, 1976). However, I found no evidence that larger S. minor tended to have an extended nesting season. This also suggests that larger clutch size (larger body size) is primarily responsible for increased reproductive poteetial. ..J I~ •••• -..... 0 • :::> 5 • • 0 0 • a:: • • • • a. • • w 0: 0 • 60 10 BO 90 100

P L AST R 0 N LE N GT H (mm~

Figure 9. Relationship between reproductive potential and body size in Sternotherus minor from Central Florida (r= 0.536; p <0.01; n= 48. The least squares regression line is shown. Reproductive potential is the sum of preovulatory follicles and corpora lutea. 38

Reproductive Effort Ind i vi dual reprpducti ve effort (clutch mass X 100/ body mass) varied from 4.1% to 14.4%. Individual reproductive effort was correlated with clutch size (Figure 10) but not with body mass (r= 0.038; n= 32; p < 0.05). This suggests that female S. minor invest rrore effort (energy) in larger clutches. Unfortunately no other data are available for individual reproductive effort. The mean reproductive effort per clutch was calculated by the ratio of mean clutch mass (mean clutch size X mean egg-mass)/ mean female mass (Iverson, 1979b). The average reproductive effort in Central Florida h minor was 9.23% ((2.9 X 5.27 gm X 100)/ 165.5 gm). Mean reproductive effort for Kinosternon baurii was 8.23% (Iverson, 1979b); h minor apparently invests more energy in each clutch than K. baurii 15 •

l- a:: • 0 u... • u_ WIO w > 1- (.) :::> 0 • 0 0:: a.. • w • 0:: 5 •

2 3 4 'CLUTCH . SlZE

Figure ,10. Relationship between reproductive effort (clutch mass X 100/body mass) and clutch size in Sternotherus minor from Central Florida (r= 0.521; p <0.01; n= 32). The least squares regression line is shown. CONCLUSIONS

Variation in chelonian reproductive patterns is well documented.

Reproductive characteristics vary with latitude, time, and annng local populations. Previous investigators have pooled reproductive data from several years, and across geographic areas. These investigators may have introduced uncontrolled variables tnat could lead to erro­ neous conclusions about the reproductive characteristics of a species.

The data in the present study were co 11 ected from one population of

Sternotherus minor for one full year in an attempt to control for the variables of latitude, local population differences, and seasonal fluctuations.

\~hile similarities in reproductive characteristics do exist between Central Florida h minor and nnre northern populations, it is clear that those similarities must be interpreted with respect to the methods of data collection used. Furthermore, comparisons with other studies show that significant differences do exist, especially in annual reproductive potential. The larger mean clutch size seen in the present study is not explained by body size or by a larger maxirrum clutch size. Rather, the larger clutch size is attributed to a higher modal number, i.e., to the fact that more females are capable of laying three eggs.

40 41

The two rmst important reproductive characteristics- clutch size and the number of annual clutches- appear to be enhanced at the south­ ern 1 imit of~ minor's range. The increased reproductive potential is interesting in light of the fact that reproductive potential might be expected to decrease at the limit of a species' range. The artifi­ cial environment created to grow watercress seems to have had a positive impact on at least one turtle species. The large volume of underground water pumped into the canals .creates a habitat that may well simulate the karst spring runs that constitute optimal habitats for the species throughout most of its range. It seems reasonable to assume that the nutrient rich underground water and the extremel y abundant food supply (e.g. snails and bivalves) are aspects of increased resource availablity whi ch, in turn, are translated into greater reproductive output. Future research into the biology of this population could include a mark and recapture procedure to detennine growth rates, and a quantified resource availability study to determine biomass of food present. These studies would help to determine whether increased food availability is the fundamental reason for the elevated reproductive potential of S. minor. APPENDIX 1

t1lrph ological characteristics for adult Sternotherus minor from Centra 1 Florida. * i ndi ca tes that the specimen was collected 10 km so ut h of t he study area.

Fema 1es Da te Field Carapace Plastron Examined lumb er Length (mm) . Length (mm) Mass (gm)

3 June 1983 003 92. 2 74.4 138 3 June 006 10 2.5 81.5 181 3 June 008 11 1. 8 90.1 233 *5 July 014 84.0 61.2 29 July 017 108 .8 86.2 198 29 Jul 018 10 3.2 81. 3 172 29 July 020 95. 3 74.2 143 11 Aug 025 95.1 77 .5 142 11 Aug 026 86 .2 71.6 119 12 Aug 027 106 .7 82.0 198 12 Aug 028 115 .0 87.4 223 12 Aug 030 106.0 83.5 188 1 Aug 031 89 .1 69.2 114 19 Aug 032 110. 0 86.2 249 19 Aug 034 85. 0 66.0 109 21 Aug 035 96.1 76.4 111 21 Aug 036 106 .1 80.2 176 21 Aug 037 97 :o 76.7 139 19 Sept 039 100 .1 72.1 166 19 Sept 040 97 .8 72.2 132 19 Sept 042 95 .0 71. 3 126 17 Oct 050 96.7 73.1 151 17 Oct 05 1 102.3 79.1 177 30 Oct 056 80.0 60.1 82 30 Oct 057 97.f) 76.0 144 30 Oc t 058 90.0 67.0 116 3() Oct 059 99.2 75.2 131 30 Oct 060 110.3 82.0 220 28 Nov 061 87.8 79.3 126 28 Nov 065 90.0 70.0 131 28 Nov 066 98.0 76.0 149 16 Dec 068 104.0 81.0 172 16 Dec 069 105.6 78.2 231 16 Dec 070 94.1 73.8 164

42 43

Appendix 1.--Continued.

Fema 1 es Date Field Carapace Pl as tron Examined Number Length (mm) 1 ength (mm) ~-1as s (gm)

27 Dec 1983 072 110. 0 82.0 219 28 Dec 073 96.7 79.1 175 28 Dec 074 92.2 74.2 129 28 Dec 075 101 .8 75.4 180 18 Jan 1984 076 86.4 66.1 117 18 Jan 077 123.0 100.6 285 18 Jan 078 108.9 84.0 215 19 Jan 079 104 .0 84 .1 203 19 Jan 080 98.1 75.3 178 21 Jan 81 92.3 72.2 112 21 Jan 082 94.0 72 .6 140 24 Jan 083 97 .5 78.1 147 21 Feb 086 114 .8 85.3 237 27 Fe 087 104.5 81.5 181 27 Feb 088 115.0 89.2 259 27 Feb 089 97.1 76.2 171 21 arch 093 110.5 84 .3 219 21 arch 094 94 .0 70.8 132 27 arch 095 102.6 80.2 157 2 arch 100 98.2 79.2 161 27 March 096 93.0 75.() 155 27 March 097 99.0 74 .4 154 27 March 098 110.0 80.0 198 9 Apri 1 101 99.0 76.6 159 9 April 102 112.8 88.8 235 16 Apri 1 103 97.5 72.8 143 16 April 104 102.0 83.9 191 16 Apri 1 105 86.0 66.2 120 16 Apri 1 106 85 .5 65.0 97 16 Apri 1 107 92.3 73.7 116 25 Apri 1 108 86.0 65.0 103 25 Apri 1 109 114.6 92.0 222 Mean: 99.6 77 .4 165 S. D. : 9.0 7.3 44.5 n: 65 65 64 Range: 80.0-123.0 60.1-100.6 82-285 44

Appendix 1.--Continued.

Mal es Date Field Carapace Pl as tron Examined Number Length (mm) Length (mm) Mass (gm)

1 June 1983 004 111.8 87 .0 217 1 June 005 100.0 78 .0 153 3 June 007 104.8 77 .2 168 29 July 019 88 .1 64 .o 92 12 Aug 029 102.0 . 78. 9 193 19 Aug 033 106.0 83.0 207 21 Sept 041 93.6 68.8 122 21 Sept 043 116. 3 86.6 232 21 Sept 044 112.0 87.0 266 28 Oct 053 85.0 63.2 93 28 Oct 054 119 .0 85.1 237 28 Oct 055 110.8 85.6 241 28 Nov 062 106.0 80.1 176 28 Nov 063 108.0 78.5 186 28 Nov 064 96.0 69.0 116 28 Nov 067 96.5 72.9 146 27 Dec 071 85.0 66.2 103 19 Jan 1984 084 108. l 79.9 169 21 Feb 085 81.9 58.3 83 14 March 090 80.0 57. 7 85 14 March 091 97.0 72.5 136 14 March 092 85.6 62.2 106 9 April 099 112.0 80.5 198 Mean: 100.2 74.6 162 S. D. : 11. 7 9.7 55.9 n: 23 23 23 Range: 80 .0-119 .0 57.7-87 .0 83-266 LITERATURE CITED

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45 46

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