North American Freshwater Turtles Research Articles

Compensating for Small Body Size: The Reproductive Ecology of Southern Spotted Turtle (Clemmys guttata) Populations

Gradients in environmental conditions across a species' geographic distribution can drive variability in a variety of life history traits. In North American freshwater turtles, both body and clutch size have commonly been shown to vary latitudinally, and these two traits are often directly related, with larger individuals producing larger clutches. We studied the reproductive ecology in two Georgia populations of Spotted Turtles (Clemmys guttata) from 2016–2020 by attaching radio transmitters to female turtles during the breeding season. We x-rayed turtles to determine clutch sizes and used thread bobbins to locate nesting locations, allowing us to determine nest fates. Across all Spotted Turtle clutches (n = 41), mean clutch size was 2.1 (range: 1–4) eggs per clutch. Approximately 92% of individuals that we monitored produced at least one clutch during the breeding season, and we identified 16 instances of individuals producing more than one clutch in a single year, including six turtles triple clutching during 2018. We located 24 Spotted Turtle nests during the study, nine (37.5%) of which either hatched or partially hatched. The other nests were either depredated (41.7%), did not hatch due to infertility or environmental reasons (8.3%), or had an undetermined fate (12.5%). Our results indicate that annual reproductive output in southern Spotted Turtle populations can exceed that of northern populations where individuals produce a single larger clutch per reproductive season. Finally, opportunistic observations in Florida from 2014–2021 indicated that the reproductive season can begin over a month earlier than in southern Georgia, highlighting the variability in reproductive ecology even across a relatively short latitudinal distance.

Movement Ecology of the Imperiled Wood Turtle (Glyptemys insculpta) in a Lower Hudson River Watershed

Knowledge of the spatial ecology of many turtle species is lacking or limited by small sample sizes of study animals, short study periods, or incomplete representation of the species' geographic range, all of which can present barriers to science-based management and conservation. The wood turtle (Glyptemys insculpta) is a declining North American freshwater turtle that is now listed as threatened or endangered in several US states and Canadian provinces. Local-scale knowledge of wood turtle movement patterns and home range sizes is needed for more effective management and regulatory protection, yet the spatial ecology of this species remains undescribed in large portions of its range. We radiotracked 31 wood turtles for 1–5 yrs each in a stream system along the border of New York and Connecticut to describe their movement behavior and inform management efforts in this previously unstudied region. Annual and multiyear 95% minimum convex polygon home range sizes averaged 2.8 (± 3.79 SD) ha and 5.2 (± 7.36 SD) ha, respectively. Males had significantly larger annual and multiyear home ranges than did females, often by severalfold. Overlap of home ranges from one year to the next ranged from 10.5% to 99.7% and averaged 62.6% (± 22.86% SD). Home range centroids shifted 3.8–328.1 m (x̄ = 70.3 ± 80.31 m SD) from year to year and averaged 41.2 m (± 40.56 m SD) from the stream and 138.4 m (± 70.66 m SD) from the nearest road across all individuals. Most turtles' home ranges spanned one or both of the major roads in our study area, illuminating the threat of vehicle collision mortality to the viability of this population. Hibernaculum fidelity was low, with only 15% of turtles hibernating in the same location as in the previous year. Our results suggest that management efforts for wood turtles in western Connecticut and the adjacent region of New York should consider that males (the wider-ranging sex) use an average of 5.3 ha to meet their resource requirements over the course of one annual cycle, buffers of at least 116 m surrounding streams should be protected, habitats that are distant from roads should be prioritized for conservation, and measures that facilitate safe passage beneath roads should be implemented whenever roads are present near occupied wood turtle habitat.

Range-wide phylogeography of Blanding’s Turtle [Emys (= Emydoidea) blandingii

Documentation of intraspecific genetic lineages and their evolutionary history can provide insight for current and future conservation and management actions. The Blanding’s Turtle, Emys (= Emydoidea) blandingii, is a long-lived species with a relatively narrow latitudinal distribution centered around the Great Lakes, but extending from Nebraska to Nova Scotia. It is listed as endangered or threatened throughout most of its range mainly due to habitat loss. Microsatellite loci have been predominantly used to test and generate hypotheses concerning the number of evolutionarily significant units and the history of lineage diversification in this species. Here we describe haplotypes from two mitochondrial and three nuclear loci generated from 32 localities across the species’ range to provide an additional perspective on existing patterns. Haplotype and nucleotide diversity were low in both sets of loci, with mitochondrial polymorphism comparable to the lowest found in any North American freshwater turtle. Spatial analyses of population differentiation supported the presence of two groups with a boundary in eastern Ontario that is roughly associated with the Appalachian Mountains as proposed by Mockford et al. (Conserv Gen 8:209–219, 2007). We suggest that the low diversity in these loci is likely related to periodic range contractions and expansions associated with glacial cycles and that the two groups recovered result from a deeper history of diversification. Our results are broadly consistent with previously identified range-wide structure and help to reconcile population structure found at smaller spatial scales, outcomes that will better inform conservation decision making for the species.

Altered spring phenology of North American freshwater turtles and the importance of representative populations.

Globally, populations of diverse taxa have altered phenology in response to climate change. However, most research has focused on a single population of a given taxon, which may be unrepresentative for comparative analyses, and few long‐term studies of phenology in ectothermic amniotes have been published. We test for climate‐altered phenology using long‐term studies (10–36 years) of nesting behavior in 14 populations representing six genera of freshwater turtles (Chelydra, Chrysemys, Kinosternon, Malaclemys, Sternotherus, and Trachemys). Nesting season initiation occurs earlier in more recent years, with 11 of the populations advancing phenology. The onset of nesting for nearly all populations correlated well with temperatures during the month preceding nesting. Still, certain populations of some species have not advanced phenology as might be expected from global patterns of climate change. This collection of findings suggests a proximate link between local climate and reproduction that is potentially caused by variation in spring emergence from hibernation, ability to process food, and thermoregulatory opportunities prior to nesting. However, even though all species had populations with at least some evidence of phenological advancement, geographic variation in phenology within and among turtle species underscores the critical importance of representative data for accurate comprehensive assessments of the biotic impacts of climate change.

A new polystomatid (Monogenea, Polystomatidae) from the mouth of the North American freshwater turtle Pseudemys nelsoni.

Based on material collected from Pseudemys nelsoni (Reptilia: Chelonia: Emydidae) during a parasite survey of the herpetofauna around Gainesville, Florida, USA, Polystomoides nelsoni sp. n. is described as a new polystome species. This parasite was found in the oral and pharyngeal region of the host. In a sample of nine Pseudemys nelsoni, three specimens were found to release polystome eggs. One turtle was euthanized and dissected and found to be infected in the oral region with 19 specimens belonging to an as-yet-unknown Polystomoides. This is only the fifth Polystomoides recorded from the Nearctic realm. This species is distinguished from known species by a combination of characteristics including marginal hooklet morphology, body length and haptor dimensions.

Damselflies (Zygoptera) as paratenic hosts for Serpinema trispinosum and its report from turtle hosts from Oklahoma, USA.

Third-stage larvae of the nematode Serpinema trispinosum (Leidy, 1852) were collected from the midgut of four of five species of adult damselflies (Zygoptera) from a non-irrigated restored semipermanent wetland located in Stillwater, Oklahoma, USA. Of the four infected damselfly species, prevalence and mean abundance was highest for the southern spreadwing, Lestes disjunctus australis Walker (10%, 0.2 ± 0.8) and lowest for the familiar bluet, Enallagma civile (Hagen) (2.5%, 0.04 ± 0.3); whereas mean intensities were lowest for the citrine forktail, Ischnura hastata (Say) (1.5 ± 0.5) and the eastern forktail, Ischnura verticalis (Say) (1.0 ± 0). This is the first record of larvae of S. trispinosum from damselflies. Serpinema trispinosum adults have been reported from 18 species of North and Central American freshwater turtles, whereas microcrustaceans such as copepods serve as intermediate hosts and snails, fish and amphibians serve as paratenic hosts in this nematode's life cycle. However, dietary studies of the 18 species of freshwater turtles reported as definitive hosts for S. trispinosum indicate that aquatic insects including damselflies are more commonly reported in turtle diets than are fish or amphibians. Additionally, unlike snails and amphibians, larval damselflies predominantly feed on microcrustaceans, and our observation of S. trispinosum infecting damselflies may reflect the importance of these insects as paratenic hosts. In the present study, we provide new host information and measurements for third-stage larvae of S. trispinosum from damselfly hosts along with measurements for adult male and female S. trispinosum from turtle hosts from Oklahoma, USA.

Environmental remodelling of GABAergic and glutamatergic neurotransmission: Rise of the anoxia-tolerant turtle brain

Climate cooling over the past one hundred thousand years has resulted in seasonal ice cover at northern and southern latitudes that has selected for hypoxia and anoxia tolerance in some species, such as freshwater turtles. At the northern reaches of their range, North American freshwater turtles spend 4 months or more buried in the mud bottom of ice covered lakes and ponds. From a comparative perspective this gives us the opportunity to understand how an extremely oxygen-sensitive organ, such as the vertebrate brain, can function without oxygen for long periods. Brain function is based on complex excitatory (on) and inhibitory (off) circuits involving the major neurotransmitters glutamate and, γ-aminobutyric acid (GABA) respectively. When a mammalian brain becomes anoxic, glutamate levels rise within minutes resulting in excitotoxic cell death which does not occur in anoxic turtle brain. The response in turtle brain has been remodelled – GABA levels rise rapidly resulting in large inhibitory GABA receptor currents and inhibition of glutamate receptor function that together depress neuronal activity.

The North American Freshwater Turtle Research Group (NAFTRG)


 
 
 
 Researchers today understand the importance of incorporating undergraduate research experiences (URE) and citizen-science methods into data collection and long-term research projects. The North American Freshwater Turtle Research Group (NAFTRG) is an example of a project in which both methods are implemented. The NAFTRG conducts long-term studies on turtle populations in seven state park springs in Florida and the largest freshwater spring in Texas. Although the study began as an undergraduate biology class, it has expanded throughout the years into a study that many parks and researchers rely upon for important data on turtle populations and for information that helps manage the stability of ecosystems. Through the use of UREs, the research investigators are enabling undergraduates to gain valuable research experiences while maintaining a volunteer base that has a vested interest in the study itself. Students from Pennsylvania State University, University of North Florida, Peninsula College, Freed-Hardeman University, and Western Washington University have chosen to participate in the study. Many of these students have volunteered additional time and efforts during subsequent research trips. A project of this nature enables students to see the importance of ecosystem awareness. Through the use of citizen science, investigators can form a large volunteer base while incorporating sophisticated ecological methodologies and furthering coonservation efforts. Many participating citizen scientists have jobs unrelated to the sciences; they volunteer their time because they understand the importance of the group’s objectives and are willing to support them with their time and energy. Our current volunteer base receives further support from local zoos, aquariums, amusement parks, and the public. Based on standardized values for volunteer work, citizen scientists and donations from governmental and non-governmental organizations have contributed approximately one million dollars to this project. Citizen science is helping to bridge the gap between the general public and the scientific community by allowing the two to work together in monitoring, managing, maintaining, and understanding the ecological issues around us.
 
 
 
 

Two new polystomes (Monogenea: Polystomatidae) from the eyes of North American freshwater turtles

Two new polystomes (Monogenea: Polystomatidae) from the eyes of North American freshwater turtles

Two new polystomes (Monogenea: Polystomatidae) from the eyes of North American freshwater turtles

Neopolystoma moleri n. sp. and Neopolystoma grossi n. sp. are described as new polystome species on the eyes of Apaloneferox and Pseudemys concinna floridana, respectively from Florida, USA. Eleven other polystome species are currently knownfrom chelonian hosts in the USA, but only Neopolystoma elizabethae and Neopolystoma fentoni were described from the eye.Ocular polystomes are characterized as having spindle-shaped eggs; an exceptionally firm grip on the host; as well as the abilityto stretch, which gives them the advantage of being stationary while extending to feed, reducing the risk of being dislodged.The two new species can be distinguished from known Neopolystoma species by a combination of characteristics including marginal hooklet morphology.

Geographic Variation in Sexual Size Dimorphism in Painted Turtles (Chrysemys picta)

Geographic variation in body size may reflect adaptations to local environments, and sexual size dimorphism (SSD) arises from ultimate and proximate factors acting differently on males and females in those environments. The Painted Turtle (Chrysemys picta) is a wide-ranging North American freshwater turtle species with known female-biased SSD. We hypothesized that, in more seasonal environments, the disparity between adult female and male body size would be more pronounced (i.e., the sexual dimorphism index (SDI, female body size/male body size) would be higher) than in more moderate environments because selective pressures on females to maximize reproductive output would result in relatively larger body sizes (fecundity advantage hypothesis) in extreme environments. We predicted that the SDI would be higher in populations at northern latitudes and middle longitudes than in southern and coastal populations. We conducted linear and nonlinear regression analyses using data from the literature and museum records, extrapolated data, and unpublished data on adult male and female carapace and plastron lengths from 65 locations. In contrast to our prediction, SDI decreased with increasing latitude. With respect to longitude, the trend supported our prediction in that the SDI was slightly higher for interior populations and lower for coastal populations; however, the relationship was not significant. Future research should examine sex differences in carapace height and body volume which may more directly reflect selective pressures on female fecundity than straight-line shell lengths. Geographic variation in body size may reflect adaptations to local environments, and sexual size dimorphism (SSD) arises from ultimate and proximate factors acting differently on males and females in those environments. Sexual size dimorphism can result from sexual selection, selection for increased female fecundity, and ecological niche divergence (Hendrick and Temeles, 1989; Shine, 1989; Andersson, 1994). Sexual selection occurs through male-male competition or through female mate choice, both potentially resulting in large male body size relative to females (Weckerly, 1998; Cox et al., 2003). Relatively large female body size may evolve if maximization of body cavity volume maximizes the capacity for ovarian development (Darwin, 1871; Fairbairn and Shine, 1993; Honek, 1993). Ecological niche divergence refers to environmental pressures such as sex-specific food requirements and differences in trophic struc- tures that result in body size differences (Selander, 1966; Nudds and Kaminski, 1984; Shine, 1989; Temeles et al., 2000). In addition, proximate factors such as conspecific variation in growth rates (Shine, 1990; Rutherford, 2004), age and size at maturity (Gibbons and Lovich, 1990; Shine, 1990; Lovich et al., 1998; Zuffi et al., 2006), and sex-specific patterns of mortality (Stewart, 1985; Shine, 1990; Haenel and John-Alder, 2002) have been shown to affect SSD in reptile populations. Among freshwater turtle species, conspecific pat- terns of SSD have been attributed to habitat type combined with male mating strategy (Berry and Shine, 1980), sex-specific mobility (Bonnet et al., 2001; Kaddour et al., 2008), sex-specific feeding ecology (Tucker et al., 1995; Lindeman and Sharkey, 2001; Lindeman, 2006), and female-biased SSD has been linked to fecundity advantage (Berry and Shine, 1980; Gibbons and Lovich, 1990; Brophy, 2006; Munoz

Conservation genetics of Blanding’s turtle and its application in the identification of evolutionarily significant units

Blanding’s turtle is a North American freshwater turtle whose main range occurs south of the Great Lakes; disjunct populations occur east of the Appalachian Mountains from New York to Nova Scotia. The species is listed as threatened or endangered in most of its range. We employed five variable microsatellites to examine samples of 300 individuals in 12 populations. Estimates of F ST based on pairwise comparisons of populations ranged from 0.000 to 0.465. Phylogenetic analysis of these F ST values reveals that the Appalachian Mountains and the Hudson River appear to present major barriers to gene flow in Blanding’s turtle. The extent of fine-scale genetic structure previously reported in the Nova Scotian populations was not found in other parts of the species’ range. We recommend that populations separated by the Appalachian Mountains as well as the highly disjunct Nova Scotian populations of Blanding’s turtle be recognized as evolutionarily significant units.

Comparative shell buffering properties correlate with anoxia tolerance in freshwater turtles

Freshwater turtles as a group are more resistant to anoxia than other vertebrates, but some species, such as painted turtles, for reasons not fully understood, can remain anoxic at winter temperatures far longer than others. Because buffering of lactic acid by the shell of the painted turtle is crucial to its long-term anoxic survival, we have tested the hypothesis that previously described differences in anoxia tolerance of five species of North American freshwater turtles may be explained at least in part by differences in their shell composition and buffering capacity. All species tested have large mineralized shells. Shell comparisons included 1) total shell CO2 concentration, 2) volume of titrated acid required to hold incubating shell powder at pH 7.0 for 3 h (an indication of buffer release from shell), and 3) lactate concentration of shell samples incubated to equilibrium in a standard lactate solution. For each measurement, the more anoxia-tolerant species (painted turtle, Chrysemys picta; snapping turtle, Chelydra serpentina) had higher values than the less anoxia-tolerant species (musk turtle, Sternotherus odoratus; map turtle, Graptemys geographica; red-eared slider, Trachemys scripta). We suggest that greater concentrations of accessible CO2 (as carbonate or bicarbonate) in the more tolerant species enable these species, when acidotic, to release more buffer into the extracellular fluid and to take up more lactic acid into their shells. We conclude that the interspecific differences in shell composition and buffering can contribute to, but cannot explain fully, the variations observed in anoxia tolerance among freshwater turtles.

LACTATE LIMITS LIFE

![Figure][1] Most North American freshwater turtle neonates typically hatch in late summer or early fall and move from their subterranean nests to nearby lakes and ponds, avoiding winter's subzero temperatures in the water's depths. However, painted turtle ( Chrysemys picta ) hatchlings

Anoxia tolerant brains.

While medical science has struggled to find ways to counteract anoxic brain damage with limited success, evolution has repeatedly solved this problem. The best-studied examples of anoxia-tolerant vertebrates are the crucian carp and some North American Freshwater turtles. These can survive anoxia for days to months, depending of temperature. Both animals successfully fight any major fall in brain ATP levels, but the strategies they use to accomplish this are quite divergent. The anoxic turtle suppresses brain activity to such a degree that it becomes virtually comatose. The underlying mechanisms involve closing down ion conductances and releasing GABA and adenosine. By contrast, the crucian carp remains active in anoxia, although it suppresses selected brain functions, and avoids lactate self-poisoning by producing an exotic anaerobic end-product. These animals provide unique models for studying anoxic survival mechanisms both on a molecular and physiological level.

Helminth parasites of the western painted turtle, Chrysemys picta belli (Gray), including Neopolystoma elizabethae n. sp. (Monogenea: Polystomatidae), a parasite of the conjunctival sac.

Neopolystoma elizabethae n. sp. is described from the conjunctival sac of the western painted turtle Chrysemys picta belli (Gray), from the Upper Peninsula of Michigan. This is the first species found in this location from chelonians in North America. The new species differs from all other species of Neopolystoma in possessing a circle of 8 genital spines that are recurved and possess a crescent-shaped base. Eight additional species of helminths were found in the 5 turtles examined in this study. All are common parasites of North American freshwater turtles. An additional species of Monogenea (Polystomoidespauli) was found in the oral cavity. Four species of Digenea (Eustomos chelydrae, Allassostomoides chelydrae, Spirorchis kirki, and Spirorchis parvus) and 3 species of Nematoda (Spiroxys contorta, Serpinema trispinosus, and Amphibiocapillaria serpentina) were also found. The following are reported from Michigan for the first time: P. pauli, S. kirki, and A. serpentina.

The Female Reproductive Cycle of the Florida Softshell Turtle (Apalone ferox)

This study of the female reproductive cycle of Apalone ferox in south Florida was based on 220 reproductive tracts salvaged from females butchered for meat. Some females mature at sizes as small as 24 cm plastron length (PL; ca. 31 cm carapace length), but some may not mature until 30 cm PL. When compared to data from other parts of the species range, body size and size at maturity show no evidence of geographic variation. Follicles first reach ovulatory size in late February, and females first bear oviducal eggs in early March. Nesting season apparently lasts from late March to early August, during which each female may produce as many as five or six clutches of 9-38 eggs (mean = 20.6). This annual fecundity is higher than any other North American freshwater turtle species. However, 9% of mature females (i.e, >30 cm PL) had inactive ovaries (i.e, maximum follicle diameters <6 mm and no corpora lutea) during the reproductive season, suggesting that some females may not reproduce every year. Clutch size increases with female body size, but egg size does not (mean, 28.2 mm x 27.5 mm, 12.3 g). The lack of egg size variability across body size, clutch size, season, and geography suggests selection for optimal egg size. Clutch mass averages 4.1% (3.0-5.2%) of spent body mass and does not vary seasonally. Apalone ferox reaches a larger size, has larger eggs, and produces as many as twice the number of clutches per year as its North American congeners; however, it is quite similar reproductively to several Old World trionychid species, including its closest outgroups.

Plasma ion balance of North American freshwater turtles during prolonged submergence in normoxic water

1. 1. Plasma ion (Na +, K +, Cl −, HCO − 3, lactate, Ca, and Mg) concentrations were measured during apneic submergence in aerated water at 10°C of 4 species of freshwater turtles: Chelydra serpentina serpentina (Chelydridae), Chrysemys picta bellii (Emydidae), Sternotherus odoratus (Kinosternidae), and Trionyx spiniferus asperus (Trionychidae). Measurements were made at intervals up to 21, 13, 100, and 100 days, respectively. In addition, final wet and dry masses were measured in Sternotherus and Trionyx and compared to control values to assess changes in body water and dry mass. 2. 2. In Chelydra and Chrysemys, which have a relatively poor aquatic O 2 uptake capacity, plasma ions changed as previously reported in animals submerged in anoxic water; [Na +] was unchanged, [K +], [Ca], and [Mg] were evaluated, and [Cl −1] and [HCO − 3] were depressed. This overall pattern is probably a regulated response and respresents a compensation for the severe acidosis exhibited by these animals. 3. 3. In Sternotherus and Trionyx, which have effective aquatic respiration and could remain submerged much longer, plasma ion concentrations, except [K +] and [lactate], fell due (largely in Sternolherus, less so in Trionyx to dilution by water uptake. Both species were slightly alkalotic after prolonged normoxic submergence, and we suggest that changes in ion concentrations can be considered as compensatory to this alkalosis. 4. 4. We conclude that these turtles fall into two distinct physiologic response types. In Chelydra and Chrysemys, normoxic submergence at 10°C is limited principally by acidosis, and observed plasma ionic changes act to counteract this effect; in Sternotherus, and to a much lesser degree, Trionyx, the limitation is largely osmoregulatory, due to a failure to exclude ambient water and to maintain ionic homeostatasis.

ECOLOGY AND PHYSIOLOGY OF HIBERNATION AND OVERWINTERING AMONG FRESHWATER FISHES, TURTLES, AND SNAKES

Summary1. Freshwater fishes are the most northerly of freshwater ectotherms, followed by frogs. North American freshwater snakes, turtles, and salamanders do not range farther north than southernmost Canada.2. Freezing and desiccation are the main challenges during terrestrial hibernation of ectotherms. Oxygen depletion, water balance, and ionic balance are the major problems for air breathing ectotherms that hibernate underwater.3. The importance of accumulation of energy stores for overwintering among fishes depends upon the length and severity of the winters, whether or not there is springtime reproduction, body size, latitude, and the availability and use of food during overwintering.4. Fishes can decrease energy demands during the winter by reductions in activity, metabolic depression, and entrance in semi‐torpidity.5. Adaptations for coping with hypoxia and anoxia among overwintering freshwater fishes may include metabolic depression, a decrease in blood O2affinity, microhabitat selection, air breathing, short‐distance migration, biochemical modifications aimed at adjusting glycolytic rates, and alcoholic fermentation.6. Freshwater turtles have a worldwide northern limit of approximately 50° N, which means that some species spend about half of their lives hibernating.7. Aquatic turtles normally hibernate underwater, although occasionally they hibernate on land. In water they usually hibernate in a hypoxic or anoxic (mud) environment and in relatively shallow water. Wintertime movements of unknown frequency occur in some species.8. The hatchlings of many turtle species can overwinter in the nest. Among northern species this behaviour is most common among painted turtles, whose hatchlings can withstand freezing.9. Mortality among adult turtles is probably highest during the hibernation cycle.10. Temperature appears to the most important cue for entry and exit from hibernation among freshwater turtles.11. Little is known of the energetics of overwintering turtles. Energy stores for overwintering may be more important at lower latitudes than at higher ones, due to the higher metabolic rates of overwintering, but non‐feeding, southern turtles.12. The ability of turtles to tolerate submergence is a function of temperature, degree of water oxygenation, latitude of origin, efficacy of extrapulmonary respiratory pathways, and metabolic rate.13. For turtles that hibernate in an anoxic hibernaculum, and for those without sufficient extrapulmonary uptake of O2to allow metabolism to be completely aerobic, the most important physiological perturbation is an acidosis developed from a continuing production of lactate. If sufficient O2can be obtained, the most likely factors limiting hibernation time are water balance and ion balance.14. Mechanisms of turtles for coping with acidosis include metabolic depression, integumental CO2loss, bicarbonate buffering, and changes in ion concentrations that minimize the decrease in SID (strong ion difference). The most important among the latter are a decrease in plasma [Cl‐] and large increases in plasma calcium and magnesium.15. Turtles are unique among reptiles in their ability to maintain both cardiovascular and nervous system function during prolonged anoxia.16. Turtles gain weight from water uptake during submerged hibernation, but apparently maintain some kidney function; however, osmoregulation is one of the least known areas of the physiology of hibernation.17. Recovery of turtles upon emergence commences with a rapid hyperventilatory compensation of pH, followed by a slower adjustment of ion levels. Basking speeds recovery greatly.18. While hibernation of turtles in the northern parts of their ranges is most likely very stressful physiologically, northern range limits are more likely to be determined by reproductive restraints than by the rigors of extended hibernation.19. The superior ability of turtles to tolerate anoxia may be more the result of an annual hibernation than of their diving habits during active periods of the year.20. Freshwater snakes usually hibernate on land. However, they appear to be capable of aquatic hibernation and may not do so because of the risk of death from anoxia.21. Some species of terrestrial snakes are known to hibernate underwater, and are able to do so in the laboratory for months. In the field, this behaviour is considered opportunistic, as there is no evidence to suggest that any snakes can tolerate extended anoxia.

Responses to Anoxia during Simulated Hibernation in Northern and Southern Painted Turtles

The painted turtles, Chrysemys picta, with four subspecies, have the largest range and most northern distribution of any North American freshwater turtle. C. p. bellii in Canada may hibernate for as much as 6 mo, while C. p. dorsalis on the Gulf Coast may not hibernate at all. We subjected both subspecies to simulated hibernation conditions by submerging them in anoxic water at 3°C without access to air to compare physiological responses. Initial acid—base and ionic statuses of animals acclimated to 3° were the same in both subspecies. As anoxia continued, both subspecies showed similar changes in all measured parameters, but the rates of change were greater in dorsalis than in bellii. By day 46, the plasma pH of dorsalis had fallen to 6.96, a change that required °180 d in bellii. By day 38, the acidosis was entirely due to lactate formation in both groups, and it had induced compensatory changes in ionic concentrations, particularly large increases in total Ca and total Mg in the blood. We conclude that the only adaptation required of bellii to enable it to endure longer winters than dorsalis is an ability to limit lactate accumulation, by having either a lower metabolic rate and/or a great ability to eliminate lactate. It is known that hibernation in a normoxic environment would be less stressful physiologically than in an anoxic one, but turtles apparently choose the latter. We suggest that the physiological stress of prolonged anoxia and the requirements of subsequent recovery in the spring are outweighed by considerations of predator avoidance during the winter. Tolerance of the physiological perturbations resulting from prolonged anoxia may limit the northern distribution of freshwater turtles.