Northern map turtle / Tortue géographique

Species Account. Northern map turtle/Tortue géographique (Graptemys geographica)
Grégory Bulté
Department of Biology, Carleton University, Ottawa, ON Canada K1S 5B6
Email: gregbulte@gmail.com
Web: http://http-server.carleton.ca/~gbulte/

Map turtle carapace
Figure 1. Carapace of a juvenile female northern map turtles showing the characteristic yellow lines. Also note the serrated hind marginal scutes. Photo: G. Bulté. Click on thumb for larger version.

Taxonomy: Class: Reptilia, Order: Testudines, Familly: Emydidae, Genus: Graptemys, Species: Graptemys geographica. The northern map turtle was first described as the Lake Erie tortoise (Testudo geographica) by Charles LeSueur (LeSueur 1817). The latin name “geographica” and vernacular name “map” refers to the lines on the carapace which resemble the contour lines on a map (Figure 1). The northern map turtle was formerly referred to as the common map turtle. The common name was changed because of concerns that the adjective “common” would be interpreted as abundant while the species is listed as a species at risk in many states of the USA as well as in Canada (Crother et al. 2000). Here “common” was making reference to the wide geographic range of the species (Crother et al. 2000).

Description: The northern map turtle is a medium-sized freshwater turtle. The carapace of both sexes is brown to olive colour with reticulated yellow lines (Figures 1 and 2) but the patterns on the back tend to fade as the turtle ages. The plastron (the ventral part of the turtle) is mostly bright yellow. Head, tail and limbs are dark green with yellow lines (Figure 3). Both sexes also have a pair of yellow spots on the top of their head (Figure 3). The northern map turtle exhibits one of the most pronounced examples of sexual size dimorphism in turtles (Gibbons and Lovich 1990). In Lake Opinicon, adult females measure up to 265 mm long (plastron length) while males only measure up to 130 mm (Figure 4). Even with the size overlap, males and females can be distinguished by the relative length of the tail—males have longer tails and their cloacal opening lies past the margin of the carapace when the tail is extended; in females, the cloacal opening lies at the margin of the carapace when the tail is stretched. Immature females overlapping in size with males also have a more or less round carapace, while males have an oblong carapace, and female’s head is approximately 20% wider than the male’s (Figure 5).

Map turtle stripes
Figure 3. Male northern map turtle showing the characteristic yellow stripes on the head, neck and limbs, as well as the yellow triangle behind the eye. Also note the keeled vertebral scutes on the back of the turtle. Photo: G. Bulté. Click on thumbnail for larger version.

Sizes at sexual maturity.
Figure 4. Size distributions of male and female northern map turtles from Lake Opinicon, Ontario, Canada. Arrows indicate the estimated sizes at sexual maturity. From Bulté & Blouin-Demers 2009a.

Map turtle dimorphism.
Figure 5. Sexual dimorphism in head width in northern map turtles from Lake Opinicon, Ontarion, Canada, illustrated by the relationship between head width and plastron length. From Bulté et al. 2008b.

Map turtle range.
Figure 6. North American (A) and Canadian (B) distribution of the northern map turtle. Source: http://www.rom.on.ca/ontario/risk.php?doc_type=map&id=289

Distribution: The northern map turtle is broadly distributed in eastern and central North America (Figure 6a). In Canada, its range is limited to southwestern Québec and southeastern Ontario (Figure 6b).

Ecology: Diet composition. As many other species in the genus Graptemys, the northern map turtle can be considered a specialist predator. Its diet is almost exclusively composed of mollusks and insects larvae, although crayfish and other aquatic invertebrates have also been reported (Vogt 1981, Lindeman 2006). In Missouri, northern map turtles were found to feed exclusively on one species of snails (White and Moll 1992). In Lake Opinicon, Ontario, the diet is almost exclusively composed of mystery banded snails (Viviparus georgianus), zebra mussels (Dreissena polymorpha), and caddisfly larvea (Nectopsyche sp) (Figure 7) (Bulté et al. 2008a). Males and females northern map turtles often differ in diet composition (Vogt 1981, Lindeman 2006). Females generally consume more mollusks while the diet of males is more variable and typically includes more insects larvae. In Lake Opinicon, the diet composition of males and females is similar, although males tend to consume more caddisfly larvae and fewer zebra mussels than females (Figure 7). In addition, females can ingest much larger snails and mussels than males (Bulté et al. 2008a). Differences in diet between the sexes are concordant with sexual dimorphism in the size and shape of the feeding structures of each sex (see section on trophic morphology below).

Figure 7. Diet composition of northern map turtles from lake Opinicon, Ontario. From Bulté et al. 2008a.

Sexual dimorphism in trophic morphology. A fascinating feature of many species of the genus Graptemys is the sexual dimorphism in feeding structures or trophic morphology (See Lindeman 2000). In many Graptemys species including G. geographica, females have wider head (Figure 5) and wider alveolar surface (crushing surface of the jaws) than males (Lindeman 2000). In Lake Opinicon, at equal body size female’s head are on average 20% wider than the male’s (Bulté et al. 2008b). Interestingly, within the genus Graptemys, sexual dimorphism in trophic morphology has evolved to be more pronounced in molluscivorous species such as the northern map turtle (Lindeman and Sharkey 2001). This type of dimorphism seems to be analogous to the sexual dimorphism in the mouthparts of mosquitoes. In mosquitoes, only females have mouthparts designed to suck blood. This type of dimorphism in mouthparts and diet is a way for females to meet the energetic demand of egg production (i.e. females could not fuel egg production on the same diet as males). Similarly, because females northern map turtles are able to crush larger mollusks than males, they have access to a greater quantity and diversity of mollusks, allowing them to gather the energy they require to produce eggs. This is evidenced by the fact that females with wider head for their body size have a higher body condition index (a measure of energy reserves) and produce heavier hatchlings (Bulté et al. 2008b).

The northern map turtle and dreissenids mussels. Zebra mussels and Quagga mussels (Dreissena bugensis) belong to the family Dreissenidae.  These non-native mussels are now widespread in North America where they are highly invasive. Consequently, dressenid mussels are now part of the diet of many mollusk-eating animals, including the northern map turtle (Lindeman 2006, Bulté and Blouin-Demers 2008). In Lake Opinicon, zebra mussels makes up on average 31% of the diet of adult females but only 6% of the diet of males (Bulté et al. 2008a). Whether northern map turtles selectively eat zebra mussels or eat them only because their native prey were extirpated by dreissenids is currently unknown. However, data from Lake Opinicon indicates that northern map turtles prefer trap-door snails over zebra mussels. Indeed, the diet of adult females is composed on average of 59 % snails and 31% zebra mussels, despite mussels being 74 times more abundant than snails (Bulté et al. 2008a).

It has been suggested that zebra mussel consumption by map turtles could increase the trophic transfer of contaminants such as mercury from the turtle’s food to the turtles (Serrouya et al. 1995, COSEWIC 2002). Zebra mussels were found to be an important pathway for the trophic transfer of contaminants in aquatic foodwebs (Bruner et al. 1994, Mazak et al. 1997, Cope et al. 1999, Custer and Custer 2000). In Lake Opinicon, however, there is no clear evidence that zebra mussel consumption has increased the trophic transfer of mercury to map turtles (Bulté, unpublished data).

Distance moved
Figure 8. Mean distance moved per day (m/day, ± standard error) by Northern Map Turtles followed by radio-telemetry in Lake Opinicon and in the St. Lawrence River, Ontario, Canada. From Carrière et al. 2009. Click on thumb for larger version.

Habitat and spatial ecology. The northern map turtle is often refer to as a river turtle as it inhabits only large rivers and lakes. In Eastern Ontario, they are found in rivers such as the St. Lawrence, the Ottawa, and the Gananoque, and lakes including the Rideau lakes. Although, the northern map turtle is an excellent swimmer capable of living in fast-moving waters, it actively seeks shallower microhabitats with slow moving water and important aquatic plant cover (Carrière 2010). In addition, Carrière (2007) showed that northern map turtles in the St. Lawrence River select undeveloped shorelines, and avoid heavily developed shorelines.

In rivers, adult females tend to use deep and fast moving water more than males and small females (Pluto and Bellis 1986, Carrière 2010). In contrast in Lake Opinicon, a lentic habitat, males and females do not differ in habitat use (Bulté et al. 2008a). Adult females are larger than males, and thus capable of swimming faster (Pluto and Bellis 1986). Thus, in rivers with fast moving water, females are likely less limited in their movement and habitat use than males. Seasonal movement patterns and home range size also contrast between lotic (i.e. rivers) and lentic (e.g. lakes) habitats. Using radio-telemetry, Carrière et al. (2009) found that adult females in the St. Lawrence River moved longer distances (Figure 8) and had larger home ranges (Figure 9) than adult females from Lake Opinicon. Males and juvenile females, however, had similar home range size (Figure 8) and movement patterns at each sites (Figure 9). Movement patterns of adult females vary as a function of season in the St-Lawrence River but not in Lake Opinicon (Carrière et al. 2009). In the St. Lawrence River, females moved longer distances (up to 5 km) during the nesting season than during the rest of the active season. Lower nest site availability in the StLawrence River is potentially explaining why adult females from this site are moving longer distances during the nesting season (Carrière et al. 2009).

Figure 9. Home range area (ha; mean± standard error) for each reproductive class of Northern Map Turtles followed by radio-telemetry in Lake Opinicon and the St. Lawrence River, Ontario, Canada. From Carriète et al. 2009. Click on thumb for larger version.

Seasonal activity pattern and hibernation. In Eastern Ontario, northern map turtles emerge from their hibernation sites around mid- to late April. In Lake Opinicon, they are often seen basking and mating around their communal hibernation sites a few days after ice-off. At emergence in the spring, turtles will stay around their hibernation site for a few days up to approximately three weeks, after which they disperse to their summer home ranges. Summer home ranges can be located several kilometers away from hibernation sites (Carrière et al. 2009). Northern map turtles are faithful to their home range and individuals will often use not only the same bay but also the same basking sites several years in a row (Bulté pers. obs.). Around mid- to late August, turtles start to migrate toward their hibernation sites and by mid- to late September large numbers of turtles can be observed basking near communal hibernation sites. Exactly when turtles go into hibernation is unknown. However, map turtles were observed mating in the spring in water as cold as 8°C, suggesting that they can potentially be active quite late in the fall as well. Map turtles in Lake Opinicon were observed to be active as late as late October.

Map turtles hibernate communally (Graham et al. 2000) and several hundred individuals can be found hibernating together (G. Bulté pers. obs.). The physical and chemical characteristics of map turtle hibernation sites are not well documented. In the Lamoille River in Vermont, map turtles hibernate at a depth of 6 to 7 meters at  water temperatures ranging between 0.1 and 1.2°C. In Lake Opinicon, they tend to hibernate in shallower water (>2 m; Bulté unpublished data). Relative to other local species, such as the painted turtles (Chrysemys picta) and the common snapping turtles (Chelydra serpentina), the northern map turtle is intolerant of anoxia during hibernation (Reese et al. 2001) and must have access to dissolved oxygen throughout the winter. Thus northern map turtles seek well-oxygenated water for hibernation and do not burrow in the mud like painted and snapping turtles (Graham and Graham 1992, Graham et al. 2000). This intolerance to anoxia likely limits the distribution of map turtles (Reese et al. 2001). During hibernation northern map turtles rely entirely on extra-pulmonary routes for oxygen uptake (Crocker et al. 1999, Reese et al. 2001), including bucco-pharyngeal and cloacal respiration (Crocker et al. 1999). Extra-pulmonary oxygen uptake during hibernation is also enhanced by an increase in the affinity of blood for oxygen at low temperatures (Maginniss et al. 2004).

Thermoregulation and basking behaviour. Like all reptiles, the northern map turtle is an ectotherm, meaning that it relies predominantly on environmental sources of heat (as opposed to metabolic heat) to regulate its body temperature. Because important physiological processes such as digestion, excretion, metabolic rate, and embryogenesis depend on the body temperature of ectotherms, precise thermoregulation is important for their growth and reproduction. This is especially true for species living in a cold climate. Bulté and Blouin-Demers (2010) estimated that the optimal body temperature of a northern map turtle for energy assimilation is between 28 and 32°C. This temperature would be almost impossible to reach by staying submerged in the water even in July. Thus, like most freshwater turtles, the northern map turtle bask sat the surface of the water or out of the water to expose its body to solar radiation (Boyer 1965).

Temperature profiles
Figure 10. Hourly average body temperature (solid line) of northern map turtles during their active season (May-September) in Lake Opinicon compared to the maximum surface temperature of the lake (dash line). Click on thumb for larger image.

Bulté and Blouin-Demers (unpublished) measured that juvenile females northern map turtle in Lake Opinicon bask 36 to 67 % of the time during their daily activity period. Basking behaviour allows them to elevate their body temperature substantially above the surface temperature of the water (Figure 10). For instance in May, their body temperature in Lake Opinicon reaches, on average on a daily basis, a maximum of 18°C above the surface temperature of the water (Bulté and Blouin-Demers 2010). Basking is essential for northern map turtles to reach their optimal temperature for energy assimilation (Bulté and Blouin-Demers 2009b). Bulté and Blouin-Demers (unpublished) estimated the basking behaviour allows northern map turtles from Lake Opinicon to increase their metabolized energy intake by 17.1 to 30.2 %. Thus basking behaviour is important for their energy budget and thus for the growth and reproduction. However, it should also be noted that basking may serve other purposes than maximizing energy assimilation, such as enhancing vitamin metabolism (Ferguson et al. 2003), desiccating leeches (Ernst 1971), and creating fever to fight infection (Monagas and Gatten 1983).

Reproduction: The extreme sexual size dimorphism in northern map turtles is accompanied by an important difference in age at sexual maturity (Figure 11). In Lake Opinicon, males were estimated to take 4 to 5.5 years to reach sexual maturity whereas estimate for females ranges from 10.5 to 13 years (Bulté and Blouin-Demers 2009). Males display a markedly elongated tail (a secondary sexual characteristic) at about 75 mm in plastron length. Of 130 gravid females observed in Lake Opinicon, the smallest had a plastron length of 193 mm, which is likely close to the minimum size at sexual maturity for females in the Rideau area (Bulté and Blouin-Demers 2009). Ryan and Lindeman (2007) reported 169 mm as the minimum plastron length for a gravid female in Pennsylvania. Despite females requiring more time to reach sexual maturity, they maintain higher absolute growth rate than males (Bulté and Blouin-Demers 2009).

Size at maturity.
Figure 11. Size as a function of age for male and female northern map turtles from Lake Opinicon, Ontario. Dots indicate estimated size at maturity. From Bulté & Blouin-Demers 2009a.

Very little information is available regarding the gametic cycles of northern map turtles but it likely resembles other that of temperate turtles. Most temperate zone turtles studied to date appear to have similar gametic cycles (Kuchling 1999). In males, spermatogenesis likely peaks in late summer and as in other emydids, such as the painted turtle and the red-eared slider, males are likely capable of storing viable sperm in their epididymis throughout the year (Gist et al. 2002). Courtship and mating typically occurs in the fall and early spring when map turtles are near their hibernation sites. The courtship behaviour of map turtles is not well documented but it appears less ritualized than in other member of the same family (emydidae) like painted turtles and red-eared sliders. Courtship involves head-bobbing while facing the female but the significance of this behaviour is unknown.
In Lake Erie (Pennsylvania) clutch size was reported to range between 3 and 21 eggs (average: 12 eggs) (Ryan and Lindeman 2007) whereas in Lake Opinicon clutch size varied between 2 and 18 eggs (average: 8.4 eggs) (Bulté et al. 2010). As in many freshwater turtles, clutch mass increases with female body size in northern map turtles (Ryan and Lindeman 2007, Bulté et al. 2008b). Ryan and Lindeman (2007) also found that clutch size increases with body size but such a relationship was not found in Lake Opinicon (Bulté et al. 2008b).

Conservation: Listing. The following listing information were obtained from the National Heritage Information Centre. (http://nhic.mnr.gov.on.ca/MNR/nhic).

GRANK (global rank across the entire range): G5 = globally secure demonstrably secure under present conditions (21 Nov. 1996)
SRANK (provincial or sub-national level): S3 = Vulnerable in the nation or state/province due to a restricted range, relatively few populations (often 80 or fewer), recent and widespread declines, or other factors making it vulnerable to extirpation.
Ontario General Status: SECURE Ontario General Status (01-Nov-99)
Committee on the Status of Endangered Wildlife in Canada (COSEWIC): Special concern (2002) = may become a threatened or an endangered species because of a combination of biological characteristics and identified threats.
Ontario Ministry of Natural Resources status: Special concern (01-Nov. 1999) = sensitive to human activities or natural events
Listing for the United States can be found on www.graptemys.com

Threats.  The Canadian range of the northern map turtle is limited to the most populated area in Canada (Figure 6a). Moreover, the northern map turtle exclusively uses large lakes and rivers also favoured by humans for recreational and commercial purposes. Thus most Canadian populations of northern map turtles are faced with high levels of human activities.

As a group, turtles are also extremely vulnerable to artificial increases in adult mortality. The life histories of turtles are characterized by high adult survivorship and long reproductive lifespans that compensate for the low survivorship of eggs and young (Congdon et al. 1993, 1994). Consequently slight increases in adult mortality can lead to important population declines (Congdon et al. 1993, 1994). Many human activities artificially decrease the survivorship of adult turtles and may thus lead to important population declines.

Anthropogenic sources of mortality affecting adult northern map turtles include roads, fisheries bycatch, and mortality caused by collision with powerboats.

Adult female turtles often use the gravely or sandy shoulder of roads to lay their eggs. Thus adult females are especially vulnerable to road mortality during the nesting season (Steen et al. 2006). The impact of road mortality on Canadian populations of northern map turtles is not well documented. However, it was shown that even slight road mortality can lead to dramatic population declines of turtles (Gibbs and Shriver 2002).

Bycatch by commercial fisheries can be a major source of mortality in turtles (Dorcas et al. 2007). Although, there is no current estimate of the population level impact of this practice in Canada, Carrière (2005) found this practice to be a potentially serious menace to northern map turtle. Commercial fisheries as a threat to northern map turtles and other freshwater species greatly requires investigation because bycatch can greatly affect turtle populations (Dorcas et al. 2007).

Collision with powerboats is a serious source of mortality for some populations of northern map turtles. Bulté et al. (2010) examined 1317 northern map turtles from the St-Lawrence Island National Park (SLINP) and Lake Opinicon for propeller injuries. They found that 8.3% of the turtles from SLINP had unambiguous propeller scars (Fig. 12) compared to 3.8% in Lake Opinicon. However, at both sites, adult females had more scars than males and juvenile females. At the SLINP, nearly 15% of the adult females had scars compared to 7% in Lake Opinicon. The difference in the frequency of propeller injuries appears to be caused by behavioural and survivorship differences between the sexes. Bulté et al. (2010) estimated the risk of extinction of both population using population viability analysis. Given their observed frequency of turtles surviving a collision (i.e. turtles with scars), they found that both population will become extinct if more than 10% of the turtles that get hit by a boat die.

In addition to direct sources of mortality, northern map turtle populations are faced with habitat loss and degradation. Carrière (2007) demonstrated that northern map turtles in the St-Lawrence River actively avoid developed shorelines are select more pristine shorelines indicating that altered shorelines are sub-optimum habitat for the species. Moore and Seigle (2006) found that disturbance from boating activities can greatly affect the normal nesting and basking behaviours of the yellow-blotched map turtles (Graptemys flavimaculata) in Mississippi.

Research need:

Sexual size dimorphism. The northern map turtle exhibits one of the most extreme sexual size dimorphism in tetrapods. The advantage of large body size in females is relatively well understood. However, the benefits of being small in males remain mostly unknown in most animals. Studies designed to elucidate these benefits would contribute significantly to a general understanding of the evolution and maintenance of sexual size dimorphism. These may include studies using microsatlellite loci to link paternity to body size and controlled mate choice experiments.

Hibernation. The physiology of hibernating is fairly well documented in the northern map turtle. It is considered anoxia intolerant during hibernation. Thus hibernation sites providing the appropriate levels of dissolved oxygen might be limiting. Studies on habitat selection would be particularly useful to identify suitable hibernation sites and may help us to understand why this species hibernates communally. In addition, all physiological studies on hibernation have so far been done with adult females. Being 10 times smaller (in mass) than females, males likely have very different oxygen requirements during hibernation and may thus be less restricted than females in their choice of hibernation sites.

Conservation. Mortality caused by roads and commercial fisheries bycatch can be substantial but the impacts of these potential threats remain largely unknown. Studies designed to understand the population level impact of these threats are greatly needed. In addition, disturbance of basking behaviours by boats can potentially affect the energy budget of northern map turtles. Studies designed to quantify the importance of disturbance and its energetic implications would be very valuable. Finally, powerboats were shown to be a serious threat to some populations of northern map turtles. This threat could potentially be reduced by restricting boat traffic or speed with navigation buoys. The efficacy of such conservation measures on the behaviour of northern map turtles as well as other aquatic wildlife needs to be assessed.

Literature cited

  1. Bruner, K. A., S. W. Fisher, and P. F. Landrum. 1994. The role of the zebra mussel, Dreissena polymorpha, in contaminant cycling: 1. The effect of body size and lipid content on the bioconcentration of PCBs and PAHs. Journal of Great Lakes Research 20:725-734.
  2. Bulté, G., and G. Blouin-Demers. 2008. Northern map turtles (Graptemys geographica) derive energy from the pelagic pathway through predation on zebra mussels (Dreissena polymorpha). Freshwater Biology 53:497-508.
  3. Bulté, G., and G. Blouin-Demers. 2009. Does sexual bimaturation affect the cost of growth and the operational sex ratio in an extremely size dimorphic reptile? Écoscience 16:175-182.
  4. Bulté, G., and G. Blouin-Demers. 2010. Implications for thermoregulation of extreme sexual size dimorphism in northern map turtles (Graptemys geographica). Oecologia in press.
  5. Bulté, G., M. A. Carrière, and G. Blouin-Demers. 2010. The impacts of recreational powerboating on northern map turtles (Graptemys geographica). Aquatic Conservation: Marine and Freshwater Ecosystems in press.
  6. Bulté, G., M. A. Gravel, and G. Blouin-Demers. 2008a. Intersexual niche divergence in northern map turtles (Graptemys geographica): the roles of diet and habitat. Canadian Journal of Zoology 86:1235-1243.
  7. Bulté, G., D. J. Irschick, and G. Blouin-Demers. 2008b. The reproductive role hypothesis explains trophic morphology dimorphism in the northern map turtle. Functional Ecology 22:824-830.
  8. Carrière, M. A. 2005. Effects of commercial fishing traps on a map turtles population in Thompson’s bay, St-Lawrence River. in C. a. a. r. c. network, editor. Annual meeting of the Canadian amphibian and reptile conservation network, Ottawa, ON.
  9. Carrière, M.A. and Blouin-Demers G. 2010. Habitat selection at multiple spatial scales in northern map turtles (Graptemys geographica).Canadian Journal of Zoology. 88:846-854.
  10. Carrière, M. A., G. Bulté, and G. Blouin-Demers. 2009. Spatial ecology of Northern Map Turtles (Graptemys geographica) in lotic and lentic habitats. Journal of Herpetology,. Journal of Herpetology 43:597-604.
  11. Congdon, J. D., A. E. Dunham, and R. C. V. Sels. 1993. Delayed sexual maturity and demographics of Blanding turtles (Emydoidea blandingii) – Implications for conservation and management of long-lived organisms. Conservation Biology 7:826-833.
  12. Congdon, J. D., A. E. Dunham, and R. C. V. Sels. 1994. Demographics of common snapping turtles (Chelydra serpentina) – Implications for conservation and management of long-lived organisms. American Zoologist 34:397-408.
  13. Cope, W. G., M. R. Bartsch, R. G. Rada, S. J. Balogh, J. E. Rupprecht, R. D. Young, and D. K. Johnson. 1999. Bioassessment of mercury, cadmium, polychlorinated biphenyls, and pesticides in the upper Mississippi river with zebra mussels (Dreissena polymorpha). Environmental Science & Technology 33:4385-4390.
  14. COSEWIC. 2002. Assessment and status report on the northern map turtle, Graptemys geographica, in Canada. Committee on the status of endangered wildlife in Canada (COSEWIC).
  15. Crocker, C. E., G. R. Ultsch, and D. C. Jackson. 1999. The physiology of diving in a north-temperate and three tropical turtle species. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 169:249-255.
  16. Crother, B. I., J. A. Boundy, J. A. Campbell, K. de Queiroz, D. R. Frost, R. Highton, J. B. Iverson, P. A. Meylan, T. W. Reeder, M. E. Seidel, J. Sites, J. W. , T. W. Taggart, S. G. Tilley, and D. B. Wake. 2000. SSAR (Society for the Study of Amphibians and Reptiles) Scientific and Standard English Names of Amphibians and Reptiles of North America North of Mexico, with comments regarding confidence in our understanding. Herpetological Circular 29:1-82.
  17. Custer, C. M., and T. W. Custer. 2000. Organochlorine and trace element contamination, in wintering and migrating diving ducks in the southern Great Lakes, USA, since the zebra mussel invasion. Environmental Toxicology and Chemistry 19:2821-2829.
  18. Dorcas, M. E., J. D. Wilson, and J. W. Gibbons. 2007. Crab trapping causes population decline and demographic changes in diamondback terrapins over two decades. Biological Conservation:334-340.
  19. Ernst, C. H. 1971. Seasonal incidence of leech infestation on painted turtle, Chrysemys picta. Journal of Parasitology 57:32-&.
  20. Ferguson, G. W., W. H. Gehrmann, K. B. Karsten, S. H. Hammack, M. McRae, T. C. Chen, N. P. Lung, and M. F. Holick. 2003. Do panther chameleons bask to regulate endogenous vitamin D-3 production? Physiological and Biochemical Zoology 76:52-59.
  21. Gibbons, J. W., and J. E. Lovich. 1990. Sexual dimorphism in turtles with emphasis on the slider turtle (Trachemys scripta). Herpetological monographs 4:1-29.
  22. Gibbs, J. P., and W. G. Shriver. 2002. Estimating the effects of road mortality on turtle populations. Conservation Biology 16:1647-1652.
  23. Gist, D. H., S. M. Dawes, T. W. Turner, S. Sheldon, and J. D. Congdon. 2002. Sperm storage in turtles: A male perspective. Journal of Experimental Zoology 292:180-186.
  24. Graham, T. E., and A. A. Graham. 1992. Metabolism and behavior of wintering common map turtles, Graptemys geographica, in Vermont. Canadian Field-Naturalist 106:517-519.
  25. Graham, T. E., C. B. Graham, C. E. Crocker, and G. R. Ultsch. 2000. Dispersal from and fidelity to a hibernaculum in a northern Vermont population of Common Map Turtles, Graptemys geographica. Canadian Field-Naturalist 114:405-408.
  26. Kuchling, G. 1999. The reproductive biology of the Chelonia. Springer-Verlag, Berlin.
  27. Lindeman, P. V. 2000. Evolution of the relative width of the head and alveolar surfaces in map turtles (Testudines : Emydidae : Graptemys). Biological Journal of the Linnean Society 69:549-576.
  28. Lindeman, P. V. 2006. 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.
  29. Lindeman, P. V., and M. J. Sharkey. 2001. Comparative analyses of functional relationships in the evolution of trophic morphology in the map turtles (Emydidae : Graptemys). Herpetologica 57:313-318.
  30. Maginniss, L. A., S. A. Ekelund, and G. R. Ultsch. 2004. Blood oxygen transport in common map turtles during simulated hibernation. Physiological and Biochemical Zoology 77:232-241.
  31. Mazak, E. J., H. J. MacIsaac, M. R. Servos, and R. Hesslein. 1997. Influence of feeding habits on organochlorine contaminant accumulation in waterfowl on the Great Lakes. Ecological Applications 7:1133-1143.
  32. Monagas, W. R., and R. E. Gatten. 1983. Behavioral fever in the turtles Terrapene carolina and Chrysemys picta. Journal of Thermal Biology 8:285-288.
  33. Moore, M. J. C., and R. A. Seigel. 2006. No place to nest or bask: Effects of human disturbance on the nesting and basking habits of yellow-blotched map turtles (Graptemys flavimaculata). Biological Conservation 130:386-393.
  34. Pluto, T. G., and E. D. Bellis. 1986. Habitat utilization by the turtle, Graptemys geographica, along a river. Journal of Herpetology 20:22-31.
  35. Reese, S. A., C. E. Crocker, M. E. Carwile, D. C. Jackson, and G. R. Ultsch. 2001. The physiology of hibernation in common map turtles (Graptemys geographica). Comparative Biochemistry and Physiology a-Molecular and Integrative Physiology 130:331-340.
  36. Ryan, K. M., and P. V. Lindeman. 2007. Reproductive allometry in the common map turtle, Graptemys geographica. American Midland Naturalist 158:49-59.
  37. Serrouya, R., A. Ricciardi, and F. G. Whoriskey. 1995. Predation on zebra mussels (Dreissena polymorpha) by captive reared map turtles (Graptemys geographica). Canadian Journal of Zoology 73:2238-2243.
  38. Steen, D. A., M. J. Aresco, S. G. Beilke, B. W. Compton, E. P. Condon, C. K. Dodd, H. Forrester, J. W. Gibbons, J. L. Greene, G. Johnson, T. A. Langen, M. J. Oldham, D. N. Oxier, R. A. Saumure, F. W. Schueler, J. M. Sleeman, L. L. Smith, J. K. Tucker, and J. P. Gibbs. 2006. Relative vulnerability of female turtles to road mortality. Animal Conservation 9:269-273.
    Vogt, R. C. 1981. Food partitioning in 3 sympatric species of map turtle, genus Graptemys (Testudinata, Emydidae). American Midland Naturalist 105:102-111.
  39. White, D., and D. Moll. 1992. Restricted diet of the common map turtle Graptemys geographica in a Missouri stream. Southwestern Naturalist 37:317-318.

Reviewers: Pamela Rutherford (Univ. Brandon) and Robert Montgomerie (Queen’s Univ.)

Advertisements

2 thoughts on “Northern map turtle / Tortue géographique”

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out / Change )

Twitter picture

You are commenting using your Twitter account. Log Out / Change )

Facebook photo

You are commenting using your Facebook account. Log Out / Change )

Google+ photo

You are commenting using your Google+ account. Log Out / Change )

Connecting to %s

%d bloggers like this: