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Latitudinal variation in egg and clutch size in turtles JOHNB. IVERSON,CHRISTINE P. BALGOOYEN,KATHY K. BYRD,AND KELLYK. LYDDAN Department of Biology, Earlham College, Richmond, IN 473 74, U.S. A. Received February 23, 1993 Accepted September 16, 1993 IVERSON,J.B., BALGOOYEN,C.P., BYRD,K.K., and LYDDAN,K.K. 1993. Latitudinal variation in egg and clutch size in turtles. Can. J. Zool. 71: 2448-2461. Reproductive and body size data from 169 populations of 146 species (56% of those recognized), 65 genera (75%), and 11 families (92%)of turtles were tabulated to test for latitudinal variation in egg and clutch size. Body-size-adjusted correla- tion analysis of all populations (as well as within most families) revealed (i) a significant negative relationship (r2 = 0.26) between latitude and egg size, (ii) a significant positive relationship (r2 = 0.2 1) between latitude and clutch size, and (iii) no relationship between latitude and clutch mass. Phylogenetic contrast analyses corroborated these patterns. Clutch size was also negatively correlated with egg size across all populations as well as within most families. We evaluate the applicability to turtles of hypotheses postulated to explain such latitudinal patterns for other vertebrate groups. The observed pattern may be the result of latitudinal variation in selection on egg size and (or) clutch size, as well as on the optimal trade-off between these two traits. IVERSON,J.B., BALGOOYEN,C.P., BYRD,K.K., et LYDDAN,K.K. 1993. Latitudinal variation in egg and clutch size in turtles. Can. J. Zool. 71 : 2448-2461. Les donnCes relatives h la reproduction et h la taille ont CtC enregistrkes chez 169 populations de 146 espkces (56% des espkces actuelles), 65 genres (75 %) et 11 familles (92%) de tomes; ces donnCes ont CtC organiskes en tableau afin d'Ctudier la variation latitudinale de la taille des oeufs et du nombre d'oeufs par couvCe. Un analyse des corrClations ajustCes en fonction de la taille du corps chez toutes les populations (de mkme que chez la plupart des familles) a rCvClC (i) une corrClation nkgative significative (r2 = 0,26) entre la latitude et la taille des oeufs, (ii) une corrklation significative positive (r2 = 0,21) entre la latitude et le nombre d'oeufs par couvCe et (iii) l'absence de corrklation entre la latitude et la masse des couvCes. Des analyses phylogCnCtiques par contrasts ont corroborC ces rCsultats. Le nombre d'oeufs par couvCe Ctait Cgalement en corrCla- tion nCgative avec la taille des oeufs chez toutes les populations et chez presque toutes les familles. Nous Cvaluons la possibi- lit6 d'application aux tortues des hypothkses invoquCes pour expliquer les patterns de variation latitudinale chez d'autres groupes de vertCbrCs. Les rdsultats observCs peuvent ktre attribuables h la variation latitudinale de la sClection qui agit sur la taille des oeufs et (ou) la taille des couvCes, de meme qu'h un Cquilibre entre ces deux facteurs. [Traduit par la rCdaction] Introduction ence in clutch or egg size between tropical and temperate turtles. Considerable research (both empirical and theoretical) has However, neither study specified the criterion by which turtles been directed at latitudinal variation in clutch or litter size in were classified as tropical or temperate, and that criterion was vertebrates. Most of the attention has focussed on birds (e.g., inconsistently applied in both studies. For example, Elgar and Lack 1948; Cody 1966; Klomp 1970; Ricklefs 1980; Godfray Heaphy (1989) consider Kinosternon integrum temperate, with et al. 1991), but some work has also targeted fishes (e.g., Leg- a range from 16 to 29" N latitude, but consider K. sonoriense get and Carscadden 1978; Healey and Heard 1984; Fleming tropical with a range from 29 to 35"N latitude, due north of and Gross 1990), amphibians (e.g., Moore 1949; Cummins that of K. integrum. 1986), reptiles (e.g., Moll 1979; Fitch 1980, 1985), and mam- Because latitudinal variation in egg and clutch size has been mals (e.g., Lord 1960; May and Rubenstein 1985). The usual demonstrated in other vertebrate groups as well as within (but not universal) pattern is for clutch or litter size to increase several species of turtles (Table I), and because earlier studies with latitude. On the other hand, relatively little empirical work had suggested that clutch size and egg size did vary latitudinally has been done on latitudinal variation in egg size in vertebrates across turtle species (e.g., Moll 1979, and references above), (but see Fleming and Gross 1990 for a fish, Cummins 1986 for we reexamined these latitudinal patterns in turtles based on a a frog, Ewert 1985 for a turtle family, and Murphy 1978 for larger data set than was available to previous authors. Specifi- a bird), but research suggests that egg size generally decreases cally, after removing the effects of body size, we expected with latitude. (i) larger clutches of smaller eggs in species at high latitudes Several early reviews of reptilian reproductive strategies (after Moll 1979 and Fitch 1980, among others), (ii) heavier discussed interspecific latitudinal variation in clutch size and clutches at high latitudes (after Elgar and Heaphy 1989; and egg size in turtles (Moll 1979; Ewert 1979; Fitch 1980, 1985; Iverson 1992b), and (iii) a negative correlation between egg Gibbons 1983; Legler 1985). Based on that literature a pattern size and clutch size (after Rohwer 1988; Elgar and Heaphy of increasing clutch size and decreasing egg size with latitude 1989; and Read and Harvey 1989). would seem to be well established. ow ever, two recent global analyses of reproductive strategies in turtles (Wilbur and Morin Methods 1988; Elgar and Heaphy 1989) attempted to investigate latitu- Average values for adult female nonspent body mass (BM), clutch dinal Patterns in both egg and clutch size (both standardized size, egg wet mass, and latitude were compiled or estimated from the for body size) by comparing "tropical" and "temperate" turtle literature or unpublished data (Appendix) for 169 populations of 146 species. Neither study could demonstrate a significant differ- species of turtles (ca. 56% of those recognized), representing 65 genera Pr~ntedin Canada 1 Imprime au Canada IVERSON ET AL. 2449 TABLE1. Turtle species for which clutch size or egg size has been reported or is indicated to vary with latitude CS vs. ES vs. Species LAT LAT Source(s) Chelydra serpentina Brooks et al. 1986; Congdon et al. 1987; J.B. Iverson, unpublished data Caretta caretta (west Atlantic coast) Marquez 1990 Apalone mutica Webb 1962 Apalone spinifera Webb 1962 Lissemys punctata Das 199 1 Kinosternon flavescens Iverson 1989b, 199 1 Kinosternon odoratum Tinkle 196 1 ; Mitchell 1985b Kinosternon subrubrum Gibbons 1983 Chrysemys picta Iverson and Smith 1993 Christiansen and Moll 1973; Moll 1973 Deirochelys reticularia Jackson 1988 Malaclemys terrapin Seigel 1980 Trachemys scripta (temperate) Cagle 1950 Jackson 1988 Trachemys scripta (tropical) Vogt 1990 NOTE: CS, clutch size; ES, egg size; LAT, latitude. Note that only those relationships marked with an asterisk represent correlations for which the effects of body size were removed. A zero indicates that no relationship was identified; a question mark indicates that a relationship was not analyzed statistically. TABLE2. Correlation analysis comparing latitude, egg mass, clutch size, and clutch mass LAT vs. EM LAT vs. CS LAT vs. CM EM vs. CS LAT vs. BM Family n r r r r r All families 169 -0.49*** -0.09 -0.20* +0.27*** -0.12 Chelidae 21 -0.62** +0.52* +O. 19 -0.38 +O. 10 Trionychidae 10 -0.53 +0.02 -0.15 +0.37 -0.18 Kinosternidae 24 -0.85*** +0.66*** +O.Ol -0.50* -0.36 Emydidae 36 -0.57*** +0.03 -0.36* +0.39* -0.34* "Bataguridae' ' 27 -0.62*** +0.08 -0.23 +0.47* -0.22 Testudinidae 25 -0.54** -0.20 -0.40* +0.57** -0.40* NOTE: LAT, latitude; EM, egg mass; CS, clutch size; CM, clutch mass. All data are untransformed *P < 0.05. **P < 0.01. ***P < 0.001. (75%)and 11 families (92%).Although some species were represented see Sessions and Larson 1987; after Felsenstein 1985 and Harvey and by more than one population, the overall sample sizes were large Pagel 199 1) for individual turtle families (with 2 10 populations) enough and the analyses (see below) robust enough that their inclusion using latitude versus the residuals of the natural logs of clutch size, did not bias the results. Average clutch mass was calculated as the egg mass, and clutch mass against log, BM. The phylogenetic product of clutch size and egg mass unless explicitly listed in the hypotheses on which this analysis was based are reviewed in Iverson reference source. Herein, "egg size" refers only to egg mass. (1992~)and Carr (1 99 I), except that the testudinid clade was removed Reproductive traits were first correlated with latitude by least-squares from the supposedly paraphyletic "batagurid" clade, and the "stauro- regression of untransformed values (Table 2). However, because body typid" clade was separated from the kinosternid clade for the analyses. size may be correlated with life history traits in turtles (Congdon and It should be obvious that the validity of phylogenetic contrast analysis Gibbons 1985; Elgar and Heaphy 1989; Iverson 1992b), the effects is predicated on the assumptions that the current phylogenetic hypothesis of body size on reproductive traits were removed by regression analysis. is correct and that the life history data accurately reflect average popu- Specifically, we used the residuals of the natural log of each trait lation values. All analyses were performed with StatviewTMsoftware regressed on the natural log of BM as our "size-adjusted" data for on a MacintoshTMcomputer.
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  • Flattened Musk Turtle US Fish & Wildlife Service Recommended Sampling Protocol

    Flattened Musk Turtle US Fish & Wildlife Service Recommended Sampling Protocol

    Flattened Musk Turtle US Fish & Wildlife Service Recommended Sampling Protocol The flattened musk turtle (FMT) is a secretive cryptic species that is restricted to the Black Warrior River system, presently believed to occur upstream of the Bankhead Dam in portions of Blount, Cullman, Etowah, Fayette, Jefferson, Lawrence, Marshall, Tuscaloosa, Walker, and Winston Counties. It is seldom observed at the water surface because of its ability to augment its respiration subcutaneously, although it basks occasionally. It generally inhabits streams with drainage areas greater than 8 square miles, relatively clean substrates, and low turbidity, but may be found in suboptimal habitats. FMT may also be found in the lower reaches of smaller streams that flow into larger streams known to harbor FMT, and headwaters and margins of impounded lakes. Its primary food sources are macroinvertebrates, particularly snails, mussels, and insects. A general sampling protocol for this species should include the following considerations: 1. Determine if the aquatic habitat is suitable for this species. Optimal habitat is permanent oligotrophic streams from one to five feet deep containing abundant rocky ledges, slabs, logs, debris, and pools. Generally, aquatic habitats that lack flowing water, relatively clean substrates, benthic macroinvertebrates, and low turbidity are unsuitable. Adequate quantitative and photographic documentation of unsuitable habitat must be presented to the Daphne Field Office if a field survey that includes trapping is thought to be unnecessary by the consultant. 2. Visual searches in lieu of trapping are not acceptable unless a FMT is found and the consultant wishes to report that the FMT is present at a site. In this case, trapping would not be required unless the FMT must be held during construction activities.