Diets of syntopic black-knobbed sawbacks (Graptemys nigrinoda) and Alabama map turtles (Graptemys pulchra) in the Alabama River.
Freshwater turtles exhibit extensive variation in the morphology of the skull, jaws, jaw musculature, and neck that results as species adapt to a variety of feeding niches (Herrel et al., 2002). Diverse freshwater turtle assemblages occur in some parts of the world, where species occupy a variety of feeding niches. The map turtles and sawbacks (Emydidae: Deirochelyinae: Graptemys) are important contributors to the high diversity of freshwater turtle assemblages along the coast of the Gulf of Mexico in the southeastern United States (Buhlmann et al, 2009; Lindeman, 2013). They are distinguished by: (1) their high species diversity that is associated with drainage-specific endemism (nine of the 14 recognized species occur in single Gulf Coastal drainages); (2) exceptional dietary diversity that is associated with morphological variation both within and across species; and (3) their exceptional degree of sexual size dimorphism, with adult males having less than half the shell length and around one-tenth the body mass of adult females (Gibbons and Lovich, 1990; Lamb et al., 1994; Lindeman, 2000a, 2008, 2013; Stephens and Wiens, 2009). Female Graptemys segregate into micro-, meso-, and megacephalic groups (essentially narrow-headed, moderately broad-headed, and extremely broad-headed) that differ according to the degree to which they depend on bivalve and gastropod mollusks in the diet (reviewed in Lindeman, 2000a, 2013). In contrast most reports of diets for the much smaller male conspecifics indicate low consumption of mollusks, regardless of female diet.
Co- occurrence of species of Graptemys shows a strong pattern of geographic segregation according to the trophic morphology of adult females (Lindeman, 2000a). In particular the five species that have microcephalic females are each sympatric with species having mesoor megacephalic females: (1) G. sabinensis with the mesocephalic species G. pseudogeographica in the Sabine-Neches, Calcasieu, and Mermentau drainages; (2) G. ouachitensis with G. pseudogeographica and in some regions with a second mesocephalic species, G. geographica, in the Mississippi drainage; (3) G. oculifera with the megacephalic species G. pearlensis in the Pearl drainage; (4) G. flavimaculala with the megacephalic species G. gibbonsi in the Pascagoula drainage; and (5) G. nigrinoda with the megacephalic species G. pulchra in the Mobile Bay drainage. There is also some overlap of the mesocephalic species G. geographica with the megacephalic species G. pulchra, and to a much lesser extent with the microcephalic species G. nigrinoda, in some upper reaches of the Mobile Bay drainages (Lindeman, 2013). In addition recent reports place two megacephalic species, G. barbouri and G. emsti, in limited sympatry in part of the Choctawhatchee drainage (Godwin et al., 2014).
Dietary studies of sympatric species of Graptemys are limited to studies of female diets of two mesocephalic species and one microcephalic species in the Mississippi River in Wisconsin by Vogt (1981), who simply noted a qualitative similarity in the diets of males of the three species; studies of two of the same species (one meso- and one microcephalic) in a reservoir on the Tennessee River in western Kentucky (Lindeman, 1997, 2000b, 2013); and separate reports of the diets of syntopic microcephalic and megacephalic species that was limited with regard to the sample size of the latter (Seigel and Brauman, 1994; Selman and Lindeman, 2015). Prior to the present study, diets of sympatric species pairs of micro- and megacephalic species of Graptemys have not been compared with detailed attention to variation among size classes and between the sexes.
The primary objective of the present study was to conduct a comprehensive comparison of the diets of G. nigrinoda and G. pulchra of different age and sex classes for a site in the middle Alabama River where they are syntopic to determine the roles of body size, sex, and the trophic morphology of each species in determining diet. In addition diets of the two species are compared to those of congeners--particularly those of close relatives within the three-species sawback clade that includes G. nigrinoda and the five-species clade of species with megacephalic females that includes G. pulchra (Wiens et al, 2010)--to develop a more comprehensive view of dietary variation within and among species groups in the genus Graptemys.
Study area.--Turtles were sampled in a 2 km stretch of the Alabama River below Steele's Landing, a boat ramp off County Rd. 1, on the border of Autauga and Lowndes counties, Alabama (32.4305[degrees]N, 86.8330[degrees]W). The Alabama River is the mainstem river of the eastern half of the Mobile Bay drainage. It is a large and deep river that is highly regulated by three lock and dam structures. Water level in the study area rose by ca. 1 m in the early afternoon each day during typical flows, when regular releases were executed ca. 21 river km upstream at the Robert F. Henry Lock and Dam. The river substrate was mud, gravel, and sand. Large fixed woody debris was abundant in the river channel and provided ample basking opportunities for Graptemys.
Field methods.--Field work was conducted 27-31 May 2008, 14-22 May and 16-22 August 2009, 24 June-1 July 2010, 1-8 July 2011, 11-18 June 2012, and 21-25 June 2013. Most turtles were captured using unbaited fykenets (Vogt, 1980) and hoopnets modified as open-top basking traps (Lindeman, 2014), with greater reliance on the former in the first 3 y and greater reliance on the latter (with higher capture rates) in the last 3 y. Additional turtles were also captured using crawfish-wire basking traps (August 2009 only; Selman el al., 2012), a dipnet, and occasional hand capture.
Turtles were measured for plastron length (PL) to the nearest mm using a flexible plastic ruler pressed along the midline of the plastron. Body mass (BM) was measured using a series of Pesola spring scales, to the nearest 1 g for turtles <1000 g and to the nearest 10 g for larger turtles. Sex determination was made on the basis of the location of the cloaca relative to the rear rim of the carapace, with the cloaca distal in males and even with the rim in females (Vogt, 1980). Any individual larger than the minimum observed size of adult males but not exhibiting the cloaca distal to the carapacial rim was categorized as female, with females divided between mature and immature size classes based on the minimum sizes of females determined via palpation of eggs to be gravid (135 mm PL in G. nigrinoda, 185 mm in G. pulchra). Individuals smaller than the smallest mature male were categorized as unsexed juveniles, including hatchlings in their first full season of growth and 1 y olds exhibiting one post-hacthing scute annulus, which were analyzed together due to small sample size of 1 y olds. Before release each individual was marked with a unique (for each species) set of two or three notches filed into the marginal scutes (Cagle, 1939).
To sample feces turtles were confined 1-2 nights in plastic tubs in a few cm of water. Feces were collected using a sieve and stored in ethanol for later analysis. Although recaptures were common (15% of all captures in the last 3 y of the study, both species combined), no individual was sampled twice for feces, with the exception of female G. pulchra, which were resampled to further assess the mollusks on which they feed; the data from those recaptures were withheld from calculation of dietary metrics described below. Based on a consideration of the adequacy of sample sizes, sampling of G. nigrinoda for feces was discontinued after 2011 with the exception of one juvenile female captured in 2012 and sampling of juvenile and male G. pulchra for feces was discontinued after 2012.
Data analyses.--A body-size index (Gibbons and Lovich, 1990) was used to characterize interspecific size differences of males and females of the two species and sexual size dimorphism within each species, with regard to both PL and BM. As modified by Lovich and Gibbons (1992), the index gives the proportion by which the larger species or sex exceeds the smaller species or sex in average size; proportional differences are herein reported as percentages. Attempts to transform PL and BM data to normality were unsuccessful, therefore Wilcoxon rank-sum tests were used in interspecific comparisons of male and female size.
Fecal samples were examined under a stereo dissecting microscope at up to 30X magnification. Prey remains were sorted into taxonomic categories to the degree possible for partially digested, fragmented remains and volume for each category in a sample was determined to the nearest 0.1 mL via volumetric displacement in a graduated cylinder. Caddisfly larval cases were relatively intact and thus could be analyzed separately from other insect remains, which were generally too fragmented to identify. Prey categories in a sample that failed to displace at least 0.1 mL were estimated to be either 0.01 or 0.05 mL in volume. Samples displacing <0.1 mL in total volume were withheld from further analyses, except in the case of samples from unsexed juveniles, which were retained for analyses regardless of total volume.
For each prey category i within a class of turtles within a species, the percent frequency of occurrence (%[F.sub.i]) and mean percent of sample volume (%[V.sub.i]) were calculated and used to compute an Index of Relative Importance (IRI; Hyslop, 1980 as modified by Bjorndal el al., 1997) using the equation:
[IRI.sub.i] = (%[F.sub.i] x %[V.sub.i])/[SIGMA](%[F.sub.i] X %[V.sub.i]).
For a particular class of a species, values for IRI, sum to 100 across all prey categories, therefore IRI values are a useful means of distilling data on percent frequency and percent volume and making comparisons among dietary data sets (Lindeman, 2013).
An index of dietary overlap ([O.sub.jk]) was calculated for pairwise categories within and between species, using the equation of Lawlor (1980):
[O.sub.jk] = [SUMMATION]([p.sub.ij][P.sub.ik])/[[[SIGMA]([p.sub.ij.sup.2]) x [SUMMATION] ([P.sub.ik.sup.2])].sup.0.5]
where [p.sub.ij] and [p.sub.ik] are the mean proportions by volume of the prey taxon i for the turtle classes j and k being compared. Dietary overlap values were then converted to pairwise distance values ([D.sub.jk]) using the equation
[D.sub.jk] = -ln([O.sub.jk])
and [D.sub.jk] values were used to construct a diagram using unweighted pairwise group mean averaging (UPGMA; Sneath and Sokal, 1973) to depict dietary similarity among the eight size and sex classes (four per species). For comparison a UPGMA diagram was also constructed to show dietary similarity among the four size and sex classes of each species of the only other case of a syntopic species pair of Graptemys for which diet has been quantified, Graptemys ouachitensis and Graplemys pseudogeographica in a western Kentucky reservoir (Lindeman, 1997, 2000, 2013).
I captured 156 G. nigrinoda and 58 G. pulchra between 2008 and 2013. A total of 92 G. nigrinoda were sampled for feces: 19 adult females, 43 adult males, seven juvenile females, and 23 unsexed juveniles (all of the last group being hatchlings in their first full year of growth). A total of 54 G. pulchra were sampled for feces: 19 adult females, 20 adult males, 11 juvenile females, and four unsexed juveniles (three of the last group were hatchlings in their first full year of growth and one was a 1 y old). Samples from eight G. nigrinoda (seven males, one juvenile female) were withheld from analyses because they displaced <0.1 mL in total volume, while all samples from G. pulchra displaced at least 0.1 mL in total volume and were included in analyses.
Morphometric data for size and age classes (including individuals not sampled for feces) are given in Table 1. On average adult female G. pulchra were 23% longer in PL than adult female G. nigrinoda and 125% heavier in BM, with both differences being significant (PL: Z = 5.78, P < 0.0001; BM: Z = 5.98, P < 0.0001). Adult males exhibited less of an interspecific size difference, with G. pulchra males being 10% longer and 36% heavier, although both differences were again significant (PL: Z = 4.92, P < 0.0001; BM: Z = 5.21, P < 0.0001). Sexual size dimorphism was markedly greater in G. pulchra than in G. nigrinoda, as adult females were 121% longer and 1071% heavier than adult males in G. pulchra vs. only 97% longer and 607% heavier in G. nigrinoda.
The most important prey taxon of male G. nigrinoda was freshwater sponges (IRI = 69), with caddisfly larvae (IRI = 19), other insects (IRI = 4), and filamentous algae (IRI = 7) also achieving relatively high importance (Table 2). Freshwater sponges were less important in the diets of females, although sponges were also their most important prey (IRI = 58 for juvenile females, 48 for adult females); other important taxa were filamentous algae (IRI = 39 for adult females but absent from samples from juvenile females), insects (IRI = 13 for juvenile females and 7 for adult females), and caddisfly larvae (IRI = 22 and 4, respectively). Unsexed juveniles had the strongest reliance on sponges (IRI = 89). Sponges were most prevalent in both percent frequency of occurrence and mean percent volume in the diet of unsexed juveniles, followed by males and juvenile females, and then adult females. Small wood fragments were present in 16 of 23 (70%) fecal samples from juveniles, 17 of 43 (40%) samples from males, 3 of 7 (43%) samples from juvenile females, and 8 of 19 (42%) samples from females. Samples that contained sponge remains were significantly more likely to contain wood fragments (39 of 71, 55%) than samples that lacked sponge remains (5 of 21, 24%; [[chi square].sub.1] = 6.29, P = 0.012).
The major prey of male G. pulchra were invasive Asian clams (Corbicula spp.; IRI = 64), followed by insects (IRI = 23) and native unionid mussels (IRI = 11; Table 3). The major prey of female G. pulchra were Asian clams (IRI = 60 for juvenile females and 77 for adult females) and native unionids (IRI = 37 and 22, respectively). For the four sampled unsexed juveniles, three hatchlings (PL 35-45 mm) passed only insect fragments (IRI = 90 for all four samples), while a 1-yr-old (PL 60 mm) passed primarily Asian clams (IRI = 9 for all four samples).
Pairwise overlap indices were high for all intraspecific comparisons of sex and age classes and low for all interspecific comparisons, which was reflected in a deep separation of the age and sex classes between the two species in UPGMA clustering (Fig. 1). Clustering of sex and age classes within each species proceeded in stepwise fashion according to relative body size, albeit in reversed patterns for the two species: in G. nigrinoda, the two smallest-bodied classes, unsexed juveniles and adult males, clustered first and were then joined in sequence by juvenile females and adult females, while in G. pulchra, the two largest-bodied classes, juvenile and adult females, clustered first and were then joined in sequence by adult males and unsexed juveniles.
[FIGURE 1 OMITTED]
Two syntopic species of Graplemys differed strongly in diet across all age and sex categories, with each species showing a body-size gradient in reliance upon its predominant prey. Sponges had high importance scores in the microcephalic species G. nigrinoda, particularly in the smaller-bodied classes, while bivalve mollusks had high importance scores in the megacephalic species G. pulchra, particularly in the larger-bodied classes.
In a large-bodied population of G. nigrinoda from the delta of the Mobile Bay drainages, as in the present study, sponges were the most important prey and were more important in male diets than in female diets (Lahanas, 1982; see further quantification in Lindeman, 2013). Sponges are presumably taken via grazing on submerged deadwood, a behavior that has been described in G. nigrinoda (Lahanas, 1982; Waters, 1974) as well as for G. flavimaculala, G. sabinensis, and male G. ernsti (Shively and Jackson, 1985; Seigel and Brauman, 1994; Selman and Qualls, 2008; J. Godwin, pers. comm.). Ingestion of small wood fragments by G. nigrinoda probably occurred incidental to feeding on sponges. Wood fragments were more than twice as prevalent in samples that contained sponges as in samples that did not, supporting the link between sponge feeding and incidental ingestion of wood fragments.
The dependence upon freshwater sponges by all classes of Graplemys nigrinoda is remarkable, because relatively few vertebrates feed heavily on sponges, presumably due to the protective nature of sponge spicules and defensive chemicals (Hill et al, 2005). In marine environments the hawksbill turtle (Eretmochelys imbricala) is a selective sponge specialist and several coral reef fish species from diverse taxa also specialize on sponges (Meylan, 1988; Leon and Bjorndal, 2002; Andrea el al., 2007). In freshwater environments apparently minor sponge feeding typifies the Australian chelid Rheodytes leukops and traces of sponges occur in the diet of the Texas river cooter, Pseudemys lexana (Legler and Cann, 1980; Tucker et al., 2001; Lindeman, 2007). However, the only reports of sponges predominating in freshwater turtle diets concern Graplemys. Besides G. nigrinoda, strong reliance on sponges also typifies the microcephalic species G. flavimaculala (Seigel and Brauman, 1994; W. Selman and P. Lindeman, unpubl. data). In addition Kofron (1991) reported high incidence of wood fragments in the stomachs of the microcephalic species G. oculifera; although he did not report sponges in the diet of the species, it is possible he simply did not recognize partially digested sponge remains in the museum specimens he dissected. If sponges are confirmed to also be an important prey of G. oculifera, it would mean that all three species of the "sawback" clade (sensu Wiens et al., 2010) are similar in this regard. Much lower importance of sponges in the diet has also been found for the microcephalic species G. ouachilensis and G. sabinensis, the mesocephalic species G. pseudogeographica and G. versa, and males of the megacephalic species G. gibbonsi (Lindeman, 1997, 2000b, 2006a; Selman and Lindeman, 2015; P. Lindeman, pers. observ.).
Native unionid bivalves have previously been reported in the diet of adult female G. pulchra from creeks in the Tallapoosa subdrainage of the Mobile Bay basin (Shealy, 1976). Megacephalic females of two closely related species (G. emsti and G. gibbonsi) feed almost exclusively on invasive Asian clams, however, as do the mesocephalic females of G. caglei and G. versa, therefore the mix of native and nonnative bivalves reported herein for G. pulchra is a unique finding for the genus Graptemys (Shealy, 1976; Porter, 1990; Lindeman, 2006a; Ennen el al, 2007; Selman and Lindeman, 2015). In the kinosternid turtle Slemolherus carinatus in Oklahoma, local abundance of Corbicula was inversely related to prevalence of native mollusks (snails and unionid mussels) in the diet (Atkinson, 2013). Similarly, the diet of the kinosternid Slemolherus odoraluswas more dominated by Corbicula in an urban creek in Arkansas that had abundant populations of the invader (Wilhelm and Plummer, 2012) than it was in a Missouri reservoir, where Corbicula and native unionid and sphaeriid mussels were all taken at similar moderate frequencies (Ford and Moll, 2004). It is possible Corbicula is a less dominant exotic invader in the mussel fauna of the middle Alabama River than in the other areas where the diets of mega- and mesocephalic Graptemys species have been studied, which would explain the contrast in the results of the present study.
Also unique in the present results is the high incidence of bivalve mollusks in diets of male G. pulchra. In most reports strongly insectivorous males typify the other species of Graptemys that have meso- or megacephalic females (Lindeman, 2000b, 2006a, b; Sanderson, 1974; Shealy, 1976; Selman and Lindeman, 2015). Previous exceptions involving high rates of molluscivory in male Graptemys have concerned small gastropod prey rather than bivalve prey (White and Moll, 1992; Bulte et al., 2008; Richards-Dimitrie et al., 2013).
Bivalve mollusks were nearly absent from the diet of G. nigrinoda in the present study (IRI values [less than or equal to] 1). In the Mobile Bay delta, G. nigrinoda of both sexes reached larger sizes than specimens from the Alabama River (to 102 mm PL in males and 202 mm PL in females) and had moderate IRI values (7 for males, 16 for females) for a small native bivalve, Mytilopsis leucophaeata (Lahanas, 1982; Lindeman, 2013). In the delta region, G. pulchra is rare enough to be effectively absent ecologically, raising the possibility that the large body size and moderate molluscivory of G. nigrinoda in the delta results from ecological release (Lindeman, 2013), as has also been postulated for G. flavimaculala in the near absence of G. gibbonsi in the lower Pascagoula River (Selman, 2012). However, Mytilopsis leucophaeata is a small, thin-shelled, brackish-water species that does not occur in upstream reaches such as the middle Alabama River (Marelli and Gray, 1983). Therefore, the degree of molluscivory in these two populations is not directly comparable to the extent that it may be influenced by differences in factors such as size and shell hardness of the resident bivalve species.
The present study is the first published comprehensive report of dietary overlap among all age and sex classes of two syntopic species of Graptemys, as previous dietary studies of the genus have been carried out primarily on single species (reviewed in Lindeman, 2013). Descriptions of dietary differentiation in the genus Graptemys have tended to emphasize differences among the large adult females, for which trophic morphological differences are most well developed (Vogt, 1981; Lindeman, 2000a, 2013), yet all age and sex classes were strongly differentiated between species in the present study (Fig. 1).
The diets of syntopic G. ouachilensis (microcephalic females) and G. pseudogeographica (mesocephalic females) in western Kentucky were reported for combined age and sex classes in Lindeman (2000b), but further breakdown by class is given in other sources (Lindeman, 1997, 2013), allowing a UPGMA diagram to be constructed for comparison to Figure 1. The result (Fig. 2) shows a pattern very different from the pattern in Figure 1, with close clustering of unsexed juveniles of the two species and close clustering of adult males of the two species but separation of female classes of the two species, with G. pseudogeographica females being more molluscivorous and G. ouachilensis females being more insectivorous. The pattern in Figure 2 is similar to what Vogt (1981) reported for syntopic G. ouachitensis, G. pseudogeographica, and G. geographica in Wisconsin, although his lack of quantification for male diets, which he simply stated were very similar, does not allow construction of a UPGMA diagram. Also apparently similar to the Kentucky and Wisconsin results is the case of sympatric G. flavimaculala (microcephalic, primarily spongivorous females) and G. gibbonsi (megacephalic, primarily molluscivorous females) in the Leaf River of Mississippi (Seigel and Brauman, 1994; Selman and Lindeman, 2015), which have less differentiation of diets in males. Further dietary studies of species in syntopy, with quantification of diets from all classes, will be necessary to determine the prevalence of the two patterns reported to date, i.e., interspecific dietary differentiation that is strongly evident only for female classes (Vogt, 1981; Seigel and Brauman, 1994; Lindeman, 1997, 2000; Selman and Lindeman, 2015) vs. dietary differentiation that typifies all size and sex classes (present study).
[FIGURE 2 OMITTED]
Acknowledgments.--I thank W. Selman for assistance with sampling in 2009, F. Armagost for assistance with sampling in 2013 and P. Johnson for assistance with unionid identifications. For several helpful comments on the manuscript, I thank C. Atkinson and J. Godwin. Partial funding for this study was received through a Faculty Senate Grant from Edinboro University of Pennsylvania and a Faculty Professional Development Committee Grant from the Pennsylvania State System of Higher Education.
Andrea, B. R., D. Batista, C. L. S. Sampaio, and G. Muricy. 2007. Spongivory by juvenile angelfish (Pomacanthidae) in Salvador, Bahia State, Brazil, p. 131-137. In: M. R. Custodio, G. Lobo-Hajdu, E. Hajdu and G. Muricy (eds.). Porifera research: biodiversity, innovation and sustainability. Serie Livros 28, Museu Nacional, Rio de Janeiro, Brazil.
Atkinson, C. L. 2013. Razor-backed musk turtle (Stemotherus carinatus) diet across a gradient of invasion. Herpetol. Consent. Biol., 8:561-570.
Bjorndal, K. A., A. B. Bolten, C. J. Lagueux, and D. R. Jackson. 1997. Dietary overlap in three sympatric congeneric freshwater turtles (Pseudemys) in Florida. Chelan. Consent. Biol., 2:430-433.
Buhlmann, K. A.,T. S. B. Akre, J. B. Iverson, D. Karapatakis, R. A. Mittermeier, A. Georges, A. G. J. Rhodin, P. P. van Dijk, and J. W. Gibbons. A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelon. Consent. Biol., 8:116-149.
Bulte, G., M.-A. Gravel, and G. Blouin-Demers. 2008. Intersexual niche divergence in northern map turtles (Graptemys geographica): the roles of diet and habitat. Can. J. Zool., 86:1235-1243.
Cagle, F. R. 1939. A system of marking turtles for future identification. Copeia, 1939:170-173.
Ennen, J. R., W. Selman, and B. R. Kreiser. 2007. Graptemysgibbonsi (Pascagoula map turtle). Diet. Herpetol. Rev., 38:200.
Ford, D. K. and D. Moll. 2004. Sexual and seasonal variation in foraging patterns in the stinkpot, Stemotherus odoratus, in southwestern Missouri. J Herpetol., 38:296-301.
Gibbons, J. W. and J. E. Lovich. 1990. Sexual dimorphism in turtles with emphasis on the. slider turtle (Trachemys scripta). Herpetol. Monogr., 4:1-29.
Godwin, J. C, J. E. Lovich, J. R. Ennen, B. R. Kreiser, B. Folt, and C. Lechowicz. 2014. Hybridization of two megacephalic map turtles (Testudines: Emydidae: Graptemys) in the Choctawhatchee River drainage of Alabama and Florida. Copeia, 2014:725-742.
Herrel, A., J. C. O'Reilly, and A. M. Richmond. 2002. Evolution of bite performance in turtles./. Evol. Biol., 15:1083-1094.
Hill, M. S., N. A. Lopez, and K. A. Young. 2005. Anti-predator defenses in western North Atlantic sponges with evidence of enhanced defense through interactions between spicules and chemicals. Mar. Ecol. Prog. Ser., 291:93-102.
Hyslop, E. J. 1980. Stomach contents analysis--a review of methods and their application. J Fish Biol., 17:411-429.
Kofron, C. P. 1991. Aspects of the ecology of the threatened ringed sawback turtle, Graptemys oculifera. Amphibia-Reptilia, 12:161-168.
Lahanas, P. N. 1982. Aspects of the life histoiy of the southern black-knobbed sawback, Graptemys nigrinoda delticola Folkerts and Mount. Unpublished M.S. Thesis, Auburn University, Auburn, AL. 275 p.
Lamb, T., C. Lydeard, R. B. Walker, and J. W. Gibbons. 1994. Molecular systematics of map turtles (Graptemys)'. a comparison of mitochondrial restriction site versus sequence data. Syst. Biol., 43:543-559.
Lawlor, L. R. 1980. Overlap, similarity, and competition coefficients. Ecology, 61:245-251.
Legler, J. M. and J. Cann. 1980. A new genus and species of chelid turtle from Queensland, Australia. Contrib. Sci. Nat. Hist. Mus. Los Angeles Co., 324:1-18.
Leon, Y. M. and K. A. Bjorndal. 2002. Selective feeding in the hawksbill turtle, an important predator in coral reef ecosystems. Mar. Ecol. Prog. Ser., 245:249-258.
Lindeman, P. V. 1997. Effects of competition, phylogeny, ontogeny, and morphology on structuring the resource use of freshwater turtles. Unpublished Ph.D. dissertation, University of Louisville, Louisville, KY. 233. p.
--. 2000a. The evolution of relative width of the head and alveolar surfaces in map turtles (Testudines: Emydidae: Graptemys). Biol. J. Linn. Soc., 69:549-576.
--. 2000b. Resource use of five sympatric turtle species: effects of competition, phylogeny, and morphology. Can. J. Zooi, 78:992-1008.
--. 2006a. Diet of the Texas map turtle (Graptemys versa): relationship to sexually-dimorphic trophic morphology and changes over five decades as influenced by an invasive mollusk. Chelon. Consent. Biol, 5:25-31.
--. 2006b. Zebra and quagga mussels (Dreissena spp.) and other prey of a Lake Erie population of common map turtles (Emydidae: Graptemys geographica). Copeia, 2006:268-273.
--. 2007. Diet, growth, body size, and reproductive potential of the Texas river cooter (Pseudemys texana). Southw. Nat., 52:586-594.
--. 2008. Evolution of body size in the map turtles and sawbacks (Emydidae: Deirochelyinae: Graptemys). Herpetologica, 64:32-46.
--. 2013. The map turtle and sawback atlas: ecology, evolution, distribution, and conservation. Univ. Oklahoma Press, Norman. 460 p.
--. 2014. New wine in old bottles: using modified hoopnets to catch bait-averse basking turtles. Herpetol. Rev., 45:597-600.
Lovich, J. E. .and J. W. Gibbons. 1992. A review of techniques for quantifying sexual size dimorphism. Growth Deuel. Aging., 56:269-281.
Marelli, D. C. and S. Gray. 1983. Conchological redescriptions of Mytilopsis sallei and Mytilopsis leucophaeta of the brackish western Atlantic. The Veliger, 25:185-193.
Meylan, A. 1988. Spongivory in hawksbill turtles: a diet of glass. Science, 239:393-395.
Porter, D. A. 1990. Feeding ecology of Graptemys caglei Haynes and McKown in the Guadalupe River, Dewitt County, Texas. Unpublished M.S. thesis, West Texas State University, Canyon, TX. 41 p.
Richards-Dimitrie, T., S. E. Gresens, S. A. Smith, and R. A. Seigel. 2013. Diet of northern map turtles (Graptemys geographica): relationship to sexual dimorphism and potential impacts of an altered river system. Copeia, 2013:477-484.
Sanderson, R. A. 1974. Sexual dimorphism in the Barbour's map turtle, Malaclemys barbouri (Carr and Marchand). Unpublished M.A. thesis, University of South Florida, Tampa, FL. p. 94
Seigel, R. A. and R. J. Brauman. 1994. Food habits of the yellow-blotched map turtle (Graptemys flavimaculata). Mississippi Mus. Nat. Sci. Mus. Tech. Rep., 28:1-18.
Selman, W. and C. Qualls. 2008. Graptemys flavimaculata (yellow-blotched map turtle). Foraging behavior. Herpetol. Rev., 39:215.
--, J. M. Jawor, and C. P. Qualls. 2012. Seasonal variation of corticosterone levels in Graptemys flavimaculata, an imperiled freshwater turtle. Copeia, 2012:698-705.
--, and P. V. Lindeman. 2015. Life history and ecology of the Pascagoula map turtle (Graptemys gibbonsi). Herpetol. Conserv. Biol., 10:781-800.
Shealy, R. M. 1976. The natural history of the Alabama map turtle, Graptemys pulchra Baur, in Alabama. Bull. Florida St. Mus. Biol. Sci., 21:47-111.
Shively, S. H. andJ. F. Jackson. 1985. Factors limiting the upstream distribution of the Sabine map turtle. Am. Midi. Nat., 114:292-303.
Sneath, P. H. A. and R. R. Sokal. 1973. Numerical taxonomy. W.H. Freeman and Co, San Francisco, CA. 573. p.
Stephens, P. R. and J. J. Wiens. 2009. Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch's rule, and sympatric divergence. Evolution, 63:910-925.
Tucker, A. D., C. J. Limpus, T. E. Priest, J. Cay, C. Glen, and E. Guarino. 2001. Home ranges of Fitzroy River turtles (Rheodytes leukops) overlap riffle zones: potential concerns related to river regulation. Biol. Conserv., 102:171-181.
Vogt, R. C. 1980. Natural history of the map turtles Graptemys pseudogeographica and G. ouachitensis. in Wisconsin. Tulane Stud. Zool. Bot., 22:17-48.
--. 1981. Food partitioning in three sympatric species of map turde, genus Graptemys (Testudinata, Emydidae). Am. Midi. Nat., 105:102-111.
Waters, J. C. 1974. The biological significance of the basking habit in the black-knobbed sawback, Graptemys nigrinoda Cagle. Unpublished M.S. thesis, Auburn University, Auburn, AL. p. 81
White, D., Jr. .and D. Moll. 1992. Restricted diet of the common map turtle Graptemys geographica in a Missouri stream. Southw. Nat., 37:317-318.
Wiens, J. J., C. A. Kuczynski, and P. R. Stephens. 2010. Discordant mitochondrial and nuclear gene phylogenies in emydid turtles: implications for speciation and conservation. Biol. J. Linn. Soc., 99:445-461.
Wilhelm, C. E. and M. V. Plummer. 2012. Diet of radiotracked musk turtles, Stemotherus odoratus, in a small urban stream. Herpetol. Conserv. Biol, 7:258-264.
Submitted 1 May 2015
Accepted 18 December 2015
(1) Corresponding author: Telephone: (814) 732-2447; e-mail: firstname.lastname@example.org
PETER V. LINDEMAN (1)
Department of Biology and Health Sciences, Edinboro University of Pennsylvania, 230 Scotland Road, Edinboro 16444
TABLE 1.--Body sizes (midline plastron length, PL, in mm and body mass, BM, in g) for two species of Graptemys in the Alabama River Graptemys nigrinoda Unsexed Adult Juvenile Adult juveniles males females females N 27 65 ii 53 Mean PL 45.3 81.0 97.2 159.3 SE 1.43 0.66 5.60 1.39 Range 34-68 67-94 77-130 135-180 Mean BM 25.1 99.3 176.3 701.7 SE 2.61 2.49 30.82 15.62 Range 11-55 59-158 93-395 417-954 Graptemys pulchra Unsexed Adult Juvenile Adult juveniles males females females N 4 23 ii 19 Mean PL 47.2 89.0 155.3 196.6 SE 4.68 1.43 8.36 1.32 Range 35-60 73-102 111-181 185-207 Mean BM 25.4 134.6 794.7 1575.8 SE 7.09 6.35 111.85 42.95 Range 10-48 84-208 248-1160 1170-1940 TABLE 2.--Diet of the black-knobbed sawback (Graptemys nigrinoda), with index of relative importance (IRI) calculated from mean percent volume (%V) and percent frequency of occurrence (%F). Juvenile females were <135 mm midline plastron length, the size of the smallest gravid female Unsexed juveniles Adult males (N = 23) (N = 43) Taxon %V %F IRI %V %F IRI Sponges 74 91 89 54 77 69 Insect fragments 11 43 7 9 26 4 Caddisfly larvae 7 35 3 19 60 19 Spiders Water mites 0.03 2 0.00 Bryozoan colonies 3 9 0.3 2 5 0.2 Asian clams 0.9 9 0.1 1 7 0.1 Native bivalves 0.9 9 0.1 Moss 0.09 2 0.00 Leaf fragments 0.09 2 0.00 Fruits 1 2 0.06 Stalked algae 0.05 2 0.00 Filamentous algae 4 22 1 12 35 7 Fungal fruiting bodies Juvenile females Adult females (N = 7) (N = 19) Taxon %V %F IRI %V %F IRI Sponges 54 71 66 35 63 45 Insect fragments 13 43 9 9 37 7 Caddisfly larvae 17 71 21 5 37 4 Spiders 0.3 5 0.03 Water mites Bryozoan colonies Asian clams 2 29 0.9 3 26 1 Native bivalves 4 16 1 Moss 0.1 5 0.02 Leaf fragments 0.4 14 0.09 1 16 0.4 Fruits 8 11 2 Stalked algae Filamentous algae 33 53 39 Fungal fruiting bodies 14 14 3 3 5 0.3 TABLE 3.--Diet of the Alabama map turtle (Graptemys pulchra) with index of relative importance (IRI) calculated from mean percent volume (%V) and percent frequency of occurrence. Juvenile females were <185 mm midline plastron length, the size of the smallest gravid female Unsexed juveniles Adult males (N = 4) (N = 20) Taxon %V %F IRI %V %F IRI Asian clams 21 25 9 52 85 64 Native bivalves 14 55 11 Sphaeriid clams 1 10 0.2 Snails Insect fragments 75 75 90 24 65 23 Caddisfly larvae 4 25 1 1 15 0.3 Water mites 0.2 5 0.01 Sponges Leaf fragments 3 10 0.4 Filamentous algae 4 20 1 Juvenile females Adult females (N = 11) (N = 19) Taxon %V %F IRI %V %F IRI Asian clams 51 91 60 63 95 77 Native bivalves 39 73 37 30 58 22 Sphaeriid clams Snails 2 36 1 0.6 16 0.1 Insect fragments 8 18 2 0.9 21 0.2 Caddisfly larvae Water mites 0.01 5 0.0008 Sponges 0.2 9 0.03 5 5 0.3 Leaf fragments 0.3 27 0.09 0.05 16 0.01 Filamentous algae 0.2 5 0.01
|Printer friendly Cite/link Email Feedback|
|Author:||Lindeman, Peter V.|
|Publication:||The American Midland Naturalist|
|Date:||Apr 1, 2016|
|Previous Article:||Acute artificial light diminishes central Texas anuran calling behavior.|
|Next Article:||Assessing predation risks for small fish in a large river ecosystem between contrasting habitats and turbidity conditions.|