Egg Components and Utilization during Development ...

COPEIA, 1983, NO. 1

264

cosa, does not possess an anti-bacterial action. Perhaps most of these secretions act as lubricating but not as anti-bacterial agents. The embryological derivation of Duvernoy's gland in extant colubrids differs from that of either labial gland (Kochva, 1978). The present study indicates that the secretion of Duvernoy's gland may function differentially as well, at least in terms of anti-bacterial activity. Further work upon the functions of the secretions of Duvernoy's gland of other colubrid species and the venom of elapid and viperid snakes is needed to assess more clearly the importance and scope of the anti-bacterial activity. However, the results here clearly demonstrate that the secretion of Duvernoy's gland, at least in an extant colubrid species, is effective in inhibiting growth of bacteria cultured from the mouth of the snake. Thus the secretion may function in the upkeep of dental surfaces through a cleaning action. Acknowledgments.-I would like to thank the following people for their generous assistance. Darwin Vest and Becky Vest obtained the secretions necessary for this study. Herbert Nakata and Ronald Barry of the Bacteriology Department were instrumental in the culturing and identification of bacterial colonies and gave valuable and appreciated suggestions in experimental technique. Charles Petersen and David Schaub added valuable comments on the hypothesis of the study and its statistical analysis. Jon Mallatt, Carl Gans and Herbert Nakata reviewed the manuscript and gave very helpful criticism. As always, my wife Lori gave her encouragement. Last but foremost, I would like to thank Kenneth Kardong for his enthusiasm, patience, and aid in my work. LITERATURECITED 1896. Remarkson the dentition of snakes and on the evolution of the poison-fangs.

BOULENGER,G. A.

AND S. FINEGOLD. 1979. Bacteriology of rattlesnake venom and implications for therapy. J. Inf. Dis. 140:818-821. 1980. Evolutionary patterns in KARDONG, K. V. advanced snakes. Amer. Zool. 20:269-282. KOCHVA,E. 1965. The development of the venom gland in the Opisthoglyph snake Telescopusfallax with remarks on Thamnophis sirtalis (Colubridae, Reptilia). Copeia 1965:147-154. . 1978. Oral glands of the Reptilia, p. 43161. In: Biology of the Reptilia. 8B. Physiology. C. Gans and K. A. Gans (eds.). Academic Press, New York. ANDC. GANS. 1970. Salivary glands of snakes. ~, Clin. Toxic. 3:363-387. POPE, C. H. 1958. Fatal bite of captive African rearfanged snake (Dispholidus). Copeia 1958:280-282. SARKER,S. C. 1923. A comparative study of the buccal glands and teeth of the Opisthoglypha, and a discussion on the evolution of the order from Aglypha. Proc. Zool. Soc. Lond. 1923:295-322. SAVITZSKY, A. H. 1980. The role of venom delivery strategies in snake evolution. Evolution 34:11941204. SMITH, M., AND A. BELLAIRS. 1947. The head glands of snakes, with remarks on the evolution of the parotid gland and teeth of the Opisthoglypha. J. Linn. Soc., Zool. 41:351-368. STEEL, R. G. D., AND J. H. TORRIE. 1980. Principles and procedures of statistics. A biometrical approach. McGraw-Hill Book Co., New York. TAUB,A. M. 1967. Comparative histological studies on Duvernoy's gland of colubrid snakes. Bull. Amer. Mus. Nat. Hist. 138:1-50. THOMAS, R. G., AND F. H. POUGH. 1979. The effect of rattlesnake venom on digestion of prey. Toxicon 17:221-228. VEST, D. 1981. The toxic secretion of the wandering garter snake Thamnophiselegans vagrans. Toxicon 19:831-839. E. A. 1948. Enzymes of snake venoms and ZELLER, their biological significance, p. 459-495. In: Advances in enzymology. F. F. Ford (ed.). Interscience Publ., New York.

W. JANSEN. Departmentof Zoology, Washington State University, Pullman, Washington 99164. Accepted 14 Jan. 1982.

DAVID

Proc. Zool. Soc. Lond. 1896:614-616. A. 1978. Antibacterialactivityin the skin

QEVIKBAS,

secretion of the frog Rana ridibunda. Toxicon 16: 195-197. FITZSIMONS, D., AND H. M. SMITH. 1958. Another rear-fanged South African snake lethal to humans. Herpetologica 14:198-202. GANS,C. 1978. Reptilian venoms: some evolutionary considerations, p. 1-42. In: Biology of the Reptilia. 8B. Physiology. C. Gans and K. A. Gans (eds.). Academic Press, New York.

AND UTILIZATION EGG COMPONENTS DEVELOPMENT IN AQUATIC DURING care of hatchlings is not TURTLES.-Parental

GOLDSTEIN, E., D. CITRON, H. GONZALEZ,F. RUSSELL

known among turtles. Therefore, other than

Copeia, 1983(1), pp. 264-268

? 1983 by the American Society of Ichthyologists and Herpetologists

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HERPETOLOGICAL NOTES TABLE

1.

265

LEAN DRY MASS, LIPID MASS AND LIPID FRACTION IN TURTLE EGGS OF EIGHT POPULATIONS OF SEVEN

SPECIES. HLG and LLG =

High and low lipid groups, respectively.

Egg lean dry weight (g)

H L

G

L L

Lipid (g)

Lipid (%)

C. picta1 N = 51/11 C. picta2 N = 17/2

1.107 ? 0.027 0.767-1.507 1.445 ? 0.069 1.053-2.105

0.324 ? 0.009 0.199-0.490 0.420 +_0.013 0.331-0.558

22.68 ? 0.33 18.40-28.90 22.75 ? 0.59 16.97-29.05

P. scripta3 N = 11/2 G. ouachitensis2 N = 53/5

2.285 ? 0.064 2.001-2.566 1.940 ? 0.038 1.364-2.540

0.960 ? 0.040 0.804-1.218 0.622 ? 0.013 0.446-0.830

29.52 ? 0.54 27.39-33.44 24.36 ? 0.42 15.97-34.00

G. geographica1 N = 4/1 C. serpentina1 N = 30/5 E. blandingit N = 13/3

2.110 ? 0.087 2.003-2.371 2.592 ? 0.068 2.045-3.400 3.004 ? 0.087 2.640-3.498

0.399 ? 0.022 0.358-0.459 0.446 ? 0.018 0.297-0.634 0.550 ? 0.016 0.450-0.629

15.90 ? 0.39 14.96-16.80 14.63 ? 0.33 10.40-17.90 15.56 ? 0.54 12.47-18.58

S. odoratust

1.712

N = 2/1

-

1.567-1.858

0.230

-

0.211-0.249

11.85

11.85-11.86

N = eggs/clutches. Mean + SE.

(min-max).

1 = Michigan; 2 = Wisconsin; 3 = South Carolina.

the cost of nesting, the eggs of turtles represent nearly the total reproductive investment in offspring by females. The material and energy in a turtle egg is first utilized for embryonic development within the egg and secondarily for hatchling maintenance and possibly growth. Because some hatchlings of some species emerge from the nest a short time after hatching while others delay emergence for months (Gibbons and Nelson, 1978), the amount of stored material and energy required by hatchlings may vary considerably. The varying requirements for hatchling survival may be reflected in the lipid and lean fractions of the egg and in the amounts of these fractions utilized for embryonic development versus initial needs of the hatchlings. Few data are available on the components of turtle eggs (Ricklefs and Burger, 1977; Ewert, 1979). Although some data on conversion of dry weight or energy of eggs to hatchlings are available for lizards (Ballinger and Clark, 1973; Licht and Moberly, 1965; Ricklefs and Cullen, 1973; Tinkle and Hadley, 1973; Vitt, 1974), there are no data for changes in lean and lipid masses during development of any reptile. We report on both lipid and nonlipid components of fresh eggs of eight populations of

seven species of North American turtles (Chrysemyspicta, Pseudemysscripta, Graptemysouachitensis, Graptemysgeographica, Chelydra serpentina, Emydoidea blandingi and Sternotherus odoratus), and also on changes in lean dry and lipid weights during development in three species of syntopic turtles in Michigan (C. serpentina,E. blandingi and C. picta). These latter species emerge from brumation in late March through early April and lay their eggs from late May through early July in loose soils adjacent to aquatic habitats. The eggs incubate in the nest through Sept. The hatchlings of C. serpentinaand E. blandingi then emerge from their nests and move to the swamps and marshes while the hatchlings of C. picta remain in the nest until the following April or early May when they emerge (Tinkle et al., 1981). Methods.-Eggs were taken from turtles collected for determination of reproductive state and body lipids or from recently constructed nests of C. serpentina and E. blandingi. Turtles and eggs were collected during 1977-1979 from areas near the E. S. George Reserve of the University of Michigan, Livingston County, Michigan. Eggs of C. picta and G. ouachitensis from

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266

COPEIA, 1983, NO. 1 +0. I

-0.0

PS

HLG Y =-1.260+1.270X

- 0.2 ~-0.3

r2= 0.92

n = 19

-0.4 -0 4*GO

-

0 -0.6 -0.7

-

EL S-o.e - 0.8 - .2 - .3

-0.?

/

CPM

r=

*

0.79

LLG Y=-2.039 r2. 0.79

0.0

+0.2

0.4

0.6

0.8

LEAN MASS (g) EGG LEAN Ln EGG Ln MASS (g)

1.0

+1.290X

1.2

Fig. 1. The relationshipof egg lipid mass to lean dry mass in eight populationsof seven species of aquatic

turtles. (CPM = Chrysemys picta, Michigan; CPW = Chrysemys picta, Wisconsin; GO = Graptemysouachitensis,Wisconsin; PS = Pseudemysscripta, South Carolina; SO = Sternotherousodoratus, Michigan; GG = Graptemysgeographica, Michigan; CS = Chelydraserpentina, Michigan; EB = Emydoideablandingi, Michigan). Triangle signifies

group mean.

Wisconsin, and P. scripta from South Carolina were supplied by other investigators. Each clutch of C. serpentina,E. blandingi and C. picta from Michigan was separated into two groups. One group was frozen for lipid extraction and the other was incubated at room temperature (_29 C). Because restricted water availability has been shown to reduce size at hatching in some turtles (Packard et al., 1981), all eggs were incubated on a water-saturated sand substrate and the inside of the incubation chamber was periodically misted with water. After the hatchlings freed themselves from their eggs, they were immediately frozen and total lipids were extracted following the procedures described below for eggs. Whole eggs of all species were freeze-dried to constant weight and ground with a mortar and pestle. Eggs were soaked in chloroform (10: 1 solvent to solute ratio) at room temperature for a minimum of 2 days. The solvent and dissolved lipids were vacuum filtered, the solvent distilled, and the remaining lipids weighed to 0.1 mg. Statistical significance levels are 0.05 unless otherwise noted. Results.-Among the seven species, mean dry mass of eggs ranged from 1.4 g to 3.6 g, with dry mass, lean mass and lipid mass of egg generally increasing with body size of the species (Table 1). Nested ANOVA revealed that al-

though the majority of the variance (82.3%) in egg mass was due to species effects (F = 22.5; P < .05; df = 6, 22), a significant portion of the remaining variance (12.3%) was due to individuals within species (F = 14.5; P < .05; df = 22, 151). Linear regression of log normal (In) transformed lipid mass on In lean dry mass for eggs of all species yielded a model (In Y = -1.115 + 0.624x) which accounted for 42% of the variation in egg lipid mass. However, this analysis also indicated that within the sample there may be two distinct groups of eggs, a group with high proportional egg lipids (HLG) and a group with low proportional egg lipids (LLG). One way analysis of covariance showed no significant differences in the slopes of the relationship of the mean dry masses of egg lipid with lean among species (F = 2.28; P = 0.319; df = 6,22). Analysis of covariance of lipid mass using lean mass of eggs as a covariate revealed that the adjusted mean lipid level differed significantly between the two groups (HLG t = 0.65 g, +0.042 2 SE, N = 19; LLG x = 0.30 g, 0.082 2 Linear SE, N = 10; F = 142.8; P