Ice nuclei in soil compromise cold hardiness of hatchling painted turtles, Chrysemys picta.

Hatchling painted turtles (Chrysemys picta) commonly overwinter within their natal nests and survive exposure to temperatures as low as -12 degrees C by supercooling. We report that the supercooling capacity of hatchling C. picta is reduced by direct contact with nest soil which, in samples from northwestern and north-central Nebraska, Indiana, and Ontario, contained potent ice nuclei active in the range of -3.5 degrees to -5 degrees C. These nuclei were sensitive to autoclaving and extractable in water. The supercooling capacity of C. picta hatched in native nest soil, or hatched in sterilized vermiculite (which lacks water-extractable nuclei), and subsequently exposed to nest soil, was reduced by ∼10 degrees C relative to control turtles that were hatched and reared in sterilized vermiculite. The effect of these nuclei was potentiated by the presence of environmental moisture, although even transient exposure to dry nest soil markedly reduced supercooling capacity in ∼ 50% of the turtles. Unlike turtle species that hibernate underwater (Sternotherus odoratus, Chelydra serpentina, Apalone spinifera), hatchlings of C. picta exhibited an extraordinary capacity for supercooling (temperature of crystallization, -16 degrees to -20 degrees C) when cooled in isolation from external ice nuclei. However, hatchlings of these four species were equally susceptible to inoculation by suspensions of the ice-nucleating bacterium, Pseudomonas syringae. Indirect evidence suggests that the soil nuclei are associated with such microbes. Nucleating activity was higher in soil collected within nests than in soil collected at the same depth, adjacent to these nests. Differences in the activities of ice nuclei in nesting soils may account for geographic and local variation in winter survival of hatchling C. picta. Our finding that similar agents occur in various other terrestrial habitats in central North America suggests that such nuclei may pose a formidable challenge to the overwintering survival of ectothermic animals that rely on supercooling to withstand frost exposure

Cold-hardiness and evaporative water loss in hatchling turtles.

North American turtles hatch in late summer and spend their first winter either on land or underwater. Adaptations for terrestrial overwintering of hatchlings in northern regions, where winter thermal and hydric regimes are harsh, have not been systematically investigated in many species. We measured intrinsic supercooling capacity, resistance to inoculative freezing, and desiccation resistance in hatchlings of terrestrial and aquatic turtles collected from northern (Terrapene ornata, Chrysemys picta bellii, Kinosternon flavescens, Chelydra serpentina) and southern (Chrysemys picta dorsalis, Trachemys scripta, Sternotherus odoratus, Sternotherus carinatus) locales. Supercooling capacity was estimated from the crystallization temperature of turtles cooled in the absence of external ice nuclei. Mean values ranged from −8.1° to −15.5°C and tended to be lower in terrestrial hibernators. Inoculation resistance was estimated from the crystallization temperature of turtles cooled in a matrix of frozen soil. These values (range of means: −0.8° to −13.6°C) also tended to be lower in the terrestrial hibernators, especially C. picta bellii. Mean rates of evaporative water loss varied markedly among the species (0.9–11.4 mg g−1 d−1) and were lowest in the terrestrial hibernators. Most species tolerated the loss of a modest amount of body water, although half of the sample of S. carinatus died from desiccation. In general, turtles did not regain lost body water from wet soil, and immersion in free water was required for rehydration. Therefore, desiccation resistance may be an important adaptation to terrestrial hibernation. Resistances to inoculative freezing and desiccation were directly correlated, perhaps because they are governed by the same morphological characteristics

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 oc- curs 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 evi- dence 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

Road avoidance and its energetic consequences for reptiles

CITATION: Paterson, J. E., et al. 2019. Road avoidance and its energetic consequences for reptiles. Ecology and Evolution, 9(17):9794-9803, doi:10.1002/ece3.5515.The original publication is available at https://onlinelibrary.wiley.comRoads are one of the most widespread human-caused habitat modifications that can increase wildlife mortality rates and alter behavior. Roads can act as barriers with variable permeability to movement and can increase distances wildlife travel to access habitats. Movement is energetically costly, and avoidance of roads could therefore impact an animal's energy budget. We tested whether reptiles avoid roads or road crossings and explored whether the energetic consequences of road avoidance decreased individual fitness. Using telemetry data from Blanding's turtles (Emydoidea blandingii; 11,658 locations of 286 turtles from 15 sites) and eastern massasaugas (Sistrurus catenatus; 1,868 locations of 49 snakes from 3 sites), we compared frequency of observed road crossings and use of road-adjacent habitat by reptiles to expected frequencies based on simulated correlated random walks. Turtles and snakes did not avoid habitats near roads, but both species avoided road crossings. Compared with simulations, turtles made fewer crossings of paved roads with low speed limits and more crossings of paved roads with high speed limits. Snakes made fewer crossings of all road types than expected based on simulated paths. Turtles traveled longer daily distances when their home range contained roads, but the predicted energetic cost was negligible: substantially less than the cost of producing one egg. Snakes with roads in their home range did not travel further per day than snakes without roads in their home range. We found that turtles and snakes avoided crossing roads, but road avoidance is unlikely to impact fitness through energetic expenditures. Therefore, mortality from vehicle strikes remains the most significant impact of roads on reptile populations.https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.5515Publisher's versio

Cues used by predators to detect freshwater turtle nests may persist late into incubation

Previous studies have found that turtle nest depredation is concentrated immediately post-oviposition, likely because cues alerting predators to nest presence are most obvious during this time. In Algonquin Provincial Park, Ontario, we examined the frequency of nest depredation during the incubation period for Snapping Turtles (Chelydra serpentina [Linnaeus, 1758]) and Midland Painted Turtles (Chrysemys picta marginata [Agassiz, 1857]). Contrary to most past findings, nest depredation occurred throughout the incubation period for both species. In fact, 83% and 86% of depredation interactions with Snapping and Painted Turtle nests, respectively, occurred more than a week after oviposition at our study site. Peaks in nest depredation (weeks with ≥10% nest depredation) occurred late in incubation and may have coincided with hatching. Trail cameras deployed at four nesting sites revealed six predator species interacting with nests. The presence of predators at nest sites increased late in the incubation period indicating a persistence or renewal (from hatching) of cues; additional research is necessary to determine the nature of these cues. These findings have implications for both research and turtle conservation. Further research should examine the relationship between temporal changes in predator species’ density and patterns of nest depredation. Additionally, in areas where protective nest caging is used as a species recovery action, it may be important to ensure that cages remain in place throughout the incubation period until emergence of hatchlings

Sex-biased seasonal capture rates in Painted Turtle (Chrysemys picta)

We examined captures of Painted Turtle (Chrysemys picta) in Algonquin Provincial Park, Ontario, Canada, during the understudied summer–autumn transition period (August–September). The proportion of captured male turtles increased relative to the proportion of females during the late summer and early autumn sampling period, leading to male-biased capture rates in a population with a strongly female-biased sex ratio. We consider explanations for the capture bias in relation to sex-specific activity patterns and briefly discuss the implications of sampling period on the outcome of population structure studies

Desiccation of herpetofauna on roadway exclusion fencing

Significant advances have been made to minimize the detrimental effects of roads on wildlife, but little is known about unintended negative consequences of mitigation strategies. Here, we present observations of adverse effects on herpetofauna of exclusion fencing at Presqu’ile Provincial Park, Ontario. A total of 15 individuals (one salamander, nine anurans, and five snakes) were found dead on unburied fencing, apparent victims of desiccation and/or heat exposure. Air temperatures did not differ between days when dead herpetofauna were and were not found on the fence; however, the fence surface was significantly warmer than the air. Our study shows that fence temperature and design may hinder animals escaping from the road to cooler refugia, and we discuss possible solutions

Anti-predator defenses of Brown Bullheads (Ameiurus nebulosus) and interactions with Snapping Turtles (Chelydra serpentina)

Ictalurid catfishes have sharp spines on their dorsal and pectoral fins that can be hazardous to predators. The pectoral spines may lock in an abducted position, effectively increasing body size and preventing ingestion by gape-limited predators. Further, sharp spines may injure predators or increase prey handling time, affording catfish opportunities for escape. As part of a long-term mark–recapture study of turtle ecology in Algonquin Provincial Park, Ontario, Canada, we documented the presence of Brown Bullheads, Ameiurus nebulosus, in the diet of Snapping Turtles, Chelydra serpentina. Here, we report on injuries inflicted by the pectoral spines of bullheads on Snapping Turtles during predator–prey interactions and provide a brief literature review of the functional significance and potential dangers of catfish pectoral spines to predators

Incubation temperature in the wild influences hatchling phenotype of two freshwater turtle species

Background: The nest environment influences phenotypic traits of hatchling turtles. Female turtles select nest sites that promote hatchling survival, and alter nesting behaviour in response to changing environments. Differences in phenotype generated by incubation environment could provide variation in traits that natural selection can act upon. The relationship between incubation temperature in the laboratory and post-hatching phenotype is well documented, but whether incubation in nature generates biologically meaningful levels of phenotypic variation is less well studied. Questions: (1) What are the effects of canopy cover, laying date, and nest depth on incubation temperature? (2) What are the relationships between incubation temperature, egg mass, and hatchling phenotype? (3) What are the sex-specific effects of incubation temperature on phenotypic variation in two turtles with temperature-dependent sex determination? Organisms: Painted turtle (Chrysemys picta) and snapping turtle (Chelydra serpentina) nests and hatchlings from Algonquin Park, Ontario, Canada. Methods: In 2010 and 2011, we measured canopy cover at nests and hourly temperatures within nests throughout incubation. Post-parturition, we measured egg mass of each clutch. After emergence, we measured hatchling righting response (time taken to flip from carapace to plastron), carapace length, and mass. Conclusions: Canopy cover and oviposition date did not affect nest temperature, but nest depth influenced daily temperature variance in snapping turtle nests. However, limited variation in environmental characteristics suggests that a female's ability to select microhabitats that adaptively affect offspring survivorship or phenotype is limited. Female painted turtles with heavier eggs selected nest sites that were warmer. Nest incubation temperature was related to multiple hatchling characteristics. Painted turtle hatchling carapace length was positively related to mean incubation temperature, but snapping turtle hatchling size was not related to incubation temperature. Painted turtle hatchling righting response was not related to incubation temperature, but snapping turtle hatchlings from warmer nests righted themselves more quickly and hatchlings from nests with greater temperature variance righted more slowly. Our predicted nest sex ratios suggested that warmer nests with heavier eggs would produce female hatchlings. Also, in both species, carapace length was greater for hatchlings from nests predicted to produce females than from nests predicted to produce males. These findings from a natural setting help to inform future research on the adaptive significance of temperature-dependent sex determination.20 page(s

Potential sources of intra-population variation in the overwintering strategy of painted turtle (Chrysemys picta) hatchlings

Many temperate animals spend half their lives in a non-active, overwintering state, and multiple adaptations have evolved to enable winter survival. One notable vertebrate model is Chrysemys picta, whose hatchlings display dichotomous overwintering strategies: some hatchlings spend their first winter aquatically after nest emergence in the autumn, whereas others overwinter terrestrially within their natal nest with subsequent emergence in the spring. The occurrence of these strategies varies among populations and temporally within populations; however, factors that determine the strategy employed by a nest in nature are unknown. We examined potential factors that influence intra-population variation in the overwintering strategy of C. picta hatchlings over two winters in Algonquin Park, Ontario. We found that environmental factors may be a trigger for the hatchling overwintering strategy: Autumn-emerging nests were sloped towards the water and were surrounded by a relatively higher percentage of bare ground compared with spring-emerging nests. Autumnemerging hatchlings were also relatively smaller. Overwintering strategy was not associated with clutch oviposition sequence, or mammalian or avian predation attempts. Instead, autumn emergence from the nest was associated with the direct mortality threat of predation by sarcophagid fly larvae. Body condition and righting response, measured as proxies of hatchling fitness, did not differ between overwintering strategies. Costs and benefits of overwintering aquatically versus terrestrially in hatchling C. picta are largely unknown, and have the potential to affect population dynamics. Understanding winter survival has great implications for turtle ecology, thus we emphasize areas for future research on dichotomous overwintering strategies in temperate hatchling turtles.10 page(s