ABSTRACT
Freshwater turtle populations are declining globally as a result of anthropogenic activities. Threats to turtles in urban areas are exacerbated by road mortality and subsidized predators, which can lead to catastrophic shifts in population size and structure. Headstarting is used as a conservation tool to supplement turtle populations that may otherwise face extirpation. A headstarting program began in 2012 to recover a functionally extinct population of Blanding's Turtles (Emydoidea blandingii) 26in Rouge National Urban Park (RNUP), Ontario, Canada. The original population included five adults and one juvenile turtle. From 2014 to 2020, 270 headstarted turtles were released. The population has been monitored annually since 2014 using visual-encounter surveys, radio-telemetry, and live trapping (from 2018 onwards). We used mark-recapture and radio-telemetry data to quantify abundance, survival, and sex ratio of the headstarted turtle population. Using a Jolly-Seber model, we estimated abundance to be 183 turtles (20 turtles/ha) in 2020. Estimated survival of headstarted turtles approached 89%, except for turtles released in 2019 when survival was 43% as a result of a known mass mortality event at the study site. Pre- and post-release sex ratios were not significantly different (χ2 = 1.92; p = 0.16), but shifted from 1:1.5 to 1:1 male:female post-release. Given that the headstarted turtles have not yet reached sexual maturity, it is unclear whether headstarted turtles will reach adulthood and successfully reproduce to maintain a self-sustaining population. Thus, to evaluate the success of the headstarting program, long-term monitoring is required.
Subject(s)
Turtles , Animals , Female , Male , Population Density , Ontario , Fresh WaterABSTRACT
Advancements in the field of reintroduction biology are needed, but understanding of how to effectively conduct translocations, particularly with snakes, is lacking. We conducted a systematic review of snake translocation studies to identify potential tactics for reducing postrelease effects. We included studies on intentional, human-mediated, wild-wild, or captive-wild translocations to any location, regardless of motive or number of snakes translocated. Only studies that presented results for at least 1 of 4 outcomes (movement behavior, site fidelity, survival, or population establishment) were included. We systematically searched 4 databases for published studies and used 5 methods to search the gray literature. Our search and screening criteria yielded 121 data sources, representing 130 translocation cases. We quantified the association between 15 translocation tactics and short-term translocation outcomes by calculating odds ratios and used forest plots to display results. Snake translocations involved 47 species (from mainly 2 families), and most were motivated by research, were monitored for at least 6 months, occurred in North America, and took place from the 1990s onward. The odds of a positive snake translocation outcome were highest with release of captive reared or juvenile snakes, release of social groups together, delayed release, provision of environmental enrichment or social housing before release, or minimization of distance translocated. The odds of a positive outcome were lowest when snakes were released early in their active season. Our results do not demonstrate causation, but outcomes of snake translocation were associated with 8 tactics (4 of which were strongly correlated). In addition to targeted comparative studies, we recommend practitioners consider the possible influence of these tactics when planning snake translocations.
La biología de la reintroducción requiere de avances; sin embargo, hay muy poco conocimiento sobre cómo realizar efectivamente las reubicaciones, particularmente las de las serpientes. Revisamos sistemáticamente los estudios sobre reubicación de serpientes para identificar las potenciales maniobras de reducción del estrés postliberación. Incluimos estudios sobre las reubicaciones a cualquier localidad que hayan sido intencionales, mediadas por humanos, de ambiente silvestre a ambiente silvestre o de cautiverio a ambiente silvestre sin importar el motivo o el número de serpientes reubicadas. Sólo incluimos estudios que presentaran resultados para al menos 1 de los cuatro resultados posibles: conducta de movimiento, fidelidad al sitio, supervivencia o establecimiento poblacional. Buscamos sistemáticamente en cuatro bases de datos de estudios publicados y usamos cinco métodos para buscar en la literatura gris. Nuestros criterios de búsqueda y revisión resultaron en 121 fuentes de datos, las cuales representaron 130 casos de reubicación. Cuantificamos la asociación entre 15 maniobras de reubicación y los resultados a corto plazo de las reubicaciones mediante el cálculo de la razón de probabilidades y usamos diagramas de efecto para mostrar los resultados. La reubicación de serpientes incluyó a 47 especies (principalmente de dos familias) y la mayoría estuvo motivada por la investigación, fue monitoreada durante seis meses (al menos), se ubicó en América del Norte y ocurrieron a partir de la década de 1990. La probabilidad de que la reubicación de serpientes tuviera un resultado positivo fueron mayores con la liberación de serpientes criadas o juveniles, la liberación de grupos sociales en conjunto, la liberación retardada, el suministro de enriquecimiento ambiental o alojamiento previo a la liberación o la reducción de la distancia de reubicación. Esta misma probabilidad fue menor cuando las serpientes fueron liberadas tempranamente durante su temporada activa. Nuestros resultados no demuestran causalidad, pero los resultados de la reubicación de serpientes estuvieron asociados con ocho maniobras (cuatro de las cuales contaban con una correlación sólida). Además de los estudios comparativos focalizados, recomendamos que los practicantes consideren la posible influencia de estas maniobras cuando se planifiquen la reubicación de serpientes.
Subject(s)
Conservation of Natural Resources , Snakes , Animals , Conservation of Natural Resources/methods , North America , Snakes/geneticsABSTRACT
Adult mortality is often the most sensitive vital rate affecting at-risk wildlife populations. Therefore, road ecology studies often focus on adult mortality despite the possibility for roads to be hazardous to juvenile individuals during natal dispersal. Failure to quantify concurrent variation in mortality risk and population sensitivity across demographic states can mislead the efforts to understand and mitigate the effects of population threats. To compare relative population impacts from road mortality among demographic classes, we weighted mortality observations by applying reproductive value analysis to quantify expected stage-specific contributions to population growth. We demonstrate this approach for snapping turtles (Chelydra serpentina) observed on roads at two focal sites in Ontario, Canada, where we collected data for both live and dead individuals observed on roads. We estimated reproductive values using stage-classified matrix models to compare relative population-level impacts of adult and juvenile mortality. Reproductive value analysis is a tractable approach to assessing demographically variable effects for applications covering large spatial scales, nondiscrete populations, or where abundance data are lacking. For one site with long-term life-history data, we compared demographic frequency on roads to expected general population frequencies predicted by the matrix model. Our application of reproductive value is sex specific but, as juvenile snapping turtles lack external secondary sex characters, we estimated the sex ratio of road-crossing juveniles after dissecting and sexing carcasses collected on roads at five sites across central Ontario, Canada. Juveniles were more abundant on roads than expected, suggesting a substantial dispersal contribution, and the road-killed juvenile sex ratio approached 1:1. A higher proportion of juveniles were also found dead compared with adults, and cumulative juvenile mortality had similar population-level importance as adult mortality. This suggests that the impact of roads needs to be considered across all life stages, even in wildlife species with slow life histories, such as snapping turtles, that are particularly sensitive to adult mortality.
Subject(s)
Turtles , Humans , Animals , Male , Female , Reptiles , Ontario , Animals, WildABSTRACT
AbstractSpecies with environmental sex determination (ESD) have persisted through deep time, despite massive environmental perturbation in the geological record. Understanding how species with temperature-dependent sex determination (TSD), a type of ESD, persist through climate change is particularly timely given the current climate crisis, as highly biased sex ratios and extinction are predicted. Since 1982, we have studied primary sex ratios of a reptile with TSD (Chelydra serpentina). Primary sex ratios remained unchanged over time, despite warming in the environment. Resilience of the primary sex ratio occurred via a portfolio effect, realized through remarkable intra-annual variation in nest-level sex ratios, leading to a relatively consistent mean annual sex ratio. Intra-annual variation in nest-level sex ratios was related to variation in egg burial depth coupled with large clutch sizes, creating thermal gradients in the nest and promoting mixed-sex clutches. Furthermore, both locally and globally, sustained increases in nighttime air temperature contribute more to warming than increases in daily maximum temperature, but development rate was affected more strongly by maximum daily air temperature, conferring additional resilience to overall warming. Our study suggests that some TSD species may be resilient to warming and provides an example of how ESD may persist under environmental change.
Subject(s)
Sex Ratio , Turtles , Animals , Climate Change , Reptiles , Sex Determination Processes , TemperatureABSTRACT
Emerging infectious diseases (EIDs) are typically characterized by novelty (recent detection) and by increasing incidence, distribution, and/or pathogenicity. Ophidiomycosis, also called snake fungal disease, is caused by the fungus Ophidiomyces ophidiicola (formerly "ophiodiicola"). Ophidiomycosis has been characterized as an EID and as a potential threat to populations of Nearctic snakes, sparking over a decade of targeted research. However, the severity of this threat is unclear. We reviewed the available literature to quantify incidence and effects of ophidiomycosis in Nearctic snakes, and to evaluate whether the evidence supports the ongoing characterization of ophidiomycosis as an EID. Data from Canada remain scarce, so we supplemented the literature review with surveys for O. ophidiicola in the Canadian Great Lakes region. Peer-reviewed reports of clinical signs consistent with ophidiomycosis in free-ranging, Nearctic snakes date back to at least 1998, and retrospective molecular testing of samples extend the earliest confirmed record to 1986. Diagnostic criteria varied among publications (n = 33), confounding quantitative comparisons. Ophidiomycosis was diagnosed or suspected in 36/121 captive snakes and was fatal in over half of cases (66.7%). This result may implicate captivity-related stress as a risk factor for mortality from ophidiomycosis, but could also reflect reporting bias (i.e., infections are more likely to be detected in captive snakes, and severe cases are more likely to be reported). In contrast, ophidiomycosis was diagnosed or suspected in 441/2,384 free-ranging snakes, with mortality observed in 43 (9.8 %). Ophidiomycosis was only speculatively linked to population declines, and we found no evidence that the prevalence of the pathogen or disease increased over the past decade of targeted research. Supplemental surveys and molecular (qPCR) testing in Ontario, Canada detected O. ophidiicola on 76 of 657 free-ranging snakes sampled across ~136,000 km2. The pathogen was detected at most sites despite limited and haphazard sampling. No large-scale mortality was observed. Current evidence supports previous suggestions that the pathogen is a widespread, previously unrecognized endemic, rather than a novel pathogen. Ophidiomycosis may not pose an imminent threat to Nearctic snakes, but further research should investigate potential sublethal effects of ophidiomycosis such as altered reproductive success that could impact population growth, and explore whether shifting environmental conditions may alter host susceptibility.
ABSTRACT
Roads 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.
ABSTRACT
One of the main threats to freshwater turtle populations is habitat destruction, which occurs as a result of human activities such as infrastructure development, forestry, aggregate extraction, and agriculture. However, the impacts of these activities on thermoregulatory opportunities for turtles are not well understood. We examined the impacts of forestry and aggregate extraction on thermal characteristics of wood turtle (Glyptemys insculpta) habitat in the Sudbury District, Ontario, by measuring the differences in absolute temperature, thermal landscape structure, and habitat thermal quality among relatively undisturbed sites (Nâ¯=â¯2), harvested forestry sites (Nâ¯=â¯2), and aggregate pits (Nâ¯=â¯2) in 2015. We also tested the potential use of the thermal landscape concept as a predictor of habitat thermal quality. Undisturbed habitats were of higher thermal quality than impacted sites in terms of temperatures experienced in situ by wild wood turtles in their natural home ranges, and never reached temperatures that would be injurious to turtles (i.e., below CTMIN or above CTMAX). The undisturbed sites were of lower quality in terms of optimal temperatures (i.e., Tset), and were generally cooler and their temperatures less variable than those in impacted habitats. The thermal landscape concept provided a useful predictor of habitat thermal quality when the influence of time of day was factored into the predictive model. Our data are important to the conservation and management of wood turtles because they provide a preliminary quantification of the thermal impacts of natural resource extraction on the habitat of an endangered species, and can guide the development of mitigation and rehabilitation plans by providing measures of, and targets for, thermal habitat quality.
Subject(s)
Conservation of Natural Resources , Ecosystem , Temperature , Turtles , Animals , Forestry , Natural ResourcesABSTRACT
Global climate is warming rapidly, threatening vertebrates with temperature-dependent sex determination (TSD) by disrupting sex ratios and other traits. Less understood are the effects of increased thermal fluctuations predicted to accompany climate change. Greater fluctuations could accelerate feminization of species that produce females under warmer conditions (further endangering TSD animals), or counter it (reducing extinction risk). Here we use novel experiments exposing eggs of Painted Turtles (Chrysemys picta) to replicated profiles recorded in field nests plus mathematically-modified profiles of similar shape but wider oscillations, and develop a new mathematical model for analysis. We show that broadening fluctuations around naturally male-producing (cooler) profiles feminizes developing embryos, whereas embryos from warmer profiles remain female or die. This occurs presumably because wider oscillations around cooler profiles expose embryos to very low temperatures that inhibit development, and to feminizing temperatures where most embryogenesis accrues. Likewise, embryos incubated under broader fluctuations around warmer profiles experience mostly feminizing temperatures, some dangerously high (which increase mortality), and fewer colder values that are insufficient to induce male development. Therefore, as thermal fluctuations escalate with global warming, the feminization of TSD turtle populations could accelerate, facilitating extinction by demographic collapse. Aggressive global CO2 mitigation scenarios (RCP2.6) could prevent these risks, while intermediate actions (RCP4.5 and RCP6.0 scenarios) yield moderate feminization, highlighting the peril that insufficient reductions of greenhouse gas emissions pose for TSD taxa. If our findings are generalizable, TSD squamates, tuatara, and crocodilians that produce males at warmer temperatures could suffer accelerated masculinization, underscoring the broad taxonomic threats of climate change.
Subject(s)
Embryonic Development/physiology , Global Warming , Hot Temperature/adverse effects , Reptiles/growth & development , Sex Determination Processes/physiology , Animals , Embryo, Nonmammalian/embryology , Female , Male , Population Dynamics/statistics & numerical data , Population Dynamics/trends , Sex RatioABSTRACT
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.
ABSTRACT
Life histories evolve in response to constraints on the time available for growth and development. Nesting date and its plasticity in response to spring temperature may therefore be important components of fitness in oviparous ectotherms near their northern range limit, as reproducing early provides more time for embryos to complete development before winter. We used data collected over several decades to compare air temperature and nest date plasticity in populations of painted turtles and snapping turtles from a relatively warm environment (southeastern Michigan) near the southern extent of the last glacial maximum to a relatively cool environment (central Ontario) near the northern extent of post-glacial recolonization. For painted turtles, population-level differences in reaction norm elevation for two phenological traits were consistent with adaptation to time constraints, but no differences in reaction norm slopes were observed. For snapping turtle populations, the difference in reaction norm elevation for a single phenological trait was in the opposite direction of what was expected under adaptation to time constraints, and no difference in reaction norm slope was observed. Finally, among-individual variation in individual plasticity for nesting date was detected only in the northern population of snapping turtles, suggesting that reaction norms are less canalized in this northern population. Overall, we observed evidence of phenological adaptation, and possibly maladaptation, to time constraints in long-lived reptiles. Where present, (mal)adaptation occurred by virtue of differences in reaction norm elevation, not reaction norm slope. Glacial history, generation time, and genetic constraint may all play an important role in the evolution of phenological timing and its plasticity in long-lived reptiles.
Subject(s)
Phenotype , Seasons , Turtles/physiology , Animals , Michigan , OntarioABSTRACT
Roadways pose serious threats to animal populations. The installation of roadway mitigation measures is becoming increasingly common, yet studies that rigorously evaluate the effectiveness of these conservation tools remain rare. A highway expansion project in Ontario, Canada included exclusion fencing and ecopassages as mitigation measures designed to offset detrimental effects to one of the most imperial groups of vertebrates, reptiles. Taking a multispecies approach, we used a Before-After-Control-Impact study design to compare reptile abundance on the highway before and after mitigation at an Impact site and a Control site from 1 May to 31 August in 2012 and 2013. During this time, radio telemetry, wildlife cameras, and an automated PIT-tag reading system were used to monitor reptile movements and use of ecopassages. Additionally, a willingness to utilize experiment was conducted to quantify turtle behavioral responses to ecopassages. We found no difference in abundance of turtles on the road between the un-mitigated and mitigated highways, and an increase in the percentage of both snakes and turtles detected dead on the road post-mitigation, suggesting that the fencing was not effective. Although ecopassages were used by reptiles, the number of crossings through ecopassages was lower than road-surface crossings. Furthermore, turtle willingness to use ecopassages was lower than that reported in previous arena studies, suggesting that effectiveness of ecopassages may be compromised when alternative crossing options are available (e.g., through holes in exclusion structures). Our rigorous evaluation of reptile roadway mitigation demonstrated that when exclusion structures fail, the effectiveness of population connectivity structures is compromised. Our project emphasizes the need to design mitigation measures with the biology and behavior of the target species in mind, to implement mitigation designs in a rigorous fashion, and quantitatively evaluate road mitigation to ensure allow for adaptive management and optimization of these increasingly important conservation tools.
Subject(s)
Movement/physiology , Snakes/physiology , Turtles/physiology , Animals , Conservation of Natural Resources/methods , Ecosystem , Ontario , Population DynamicsABSTRACT
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. Autumn-emerging 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.
Subject(s)
Hibernation/physiology , Nesting Behavior , Turtles/physiology , Animals , Body Size , Ecosystem , Female , Ontario , Oviposition , Predatory Behavior , Sarcophagidae , Seasons , WaterABSTRACT
Conservation biology integrates multiple disciplines to expand the ability to identify threats to populations and develop mitigation for these threats. Road ecology is a branch of conservation biology that examines interactions between wildlife and roadways. Although the direct threats of road mortality and habitat fragmentation posed by roads have received much attention, a clear understanding of the indirect physiological effects of roads on wildlife is lacking. Chronic physiological stress can lower immune function, affect reproductive rates and reduce life expectancy; thus, it has the potential to induce long-lasting effects on populations. Reptiles are globally in decline, and roads are known to have negative effects on reptile populations; however, it is unknown whether individual responses to roads and traffic result in chronic stress that creates an additional threat to population viability. We successfully extracted reliable measures of corticosterone (CORT), a known, commonly used biomarker for physiological stress, from claw trimmings from painted turtles (Chrysemys picta) captured at three study sites (road-impacted site, control site and validation site). Corticosterone levels in claws were evaluated as a measure of chronic stress in turtles because CORT is deposited during growth of the claw and could provide an opportunity to examine past long-term stress levels. While male turtles had higher CORT levels on average than females, there was no difference in the level of CORT between the road-impacted and control site, nor was there a relationship between CORT and turtle body condition. In validating a novel approach for non-invasive measurement of long-term CORT levels in a keratinized tissue in wild reptiles, our study provides a new avenue for research in the field of stress physiology.
ABSTRACT
Bergmann's rule states that, among conspecific populations, individuals are larger in cooler than in warmer environments as a consequence of selection related to heat conservation. Many of the most comprehensive assessments of Bergmann's rule to date have examined clinal patterns in body size among species assemblages. Our study is a more direct test of Bergmann's rule because we examine the pattern within a single, widely distributed species. We examined geographic variation in body and cell size in the spotted turtle ( Clemmys guttata). Our analysis of 818 turtles collected from the entire range (45-28 degrees N), indicated that body size increased with latitude; however, the relationship was driven by a population of large turtles at the northern extreme of the species' range. When the northern population was removed from the analyses, Bergmann's rule was not supported, and the smallest turtles occurred near the central part of the species' distribution. Recent literature has suggested that latitudinal clines in body size may simply be a physiological byproduct of the effects of temperature on cell division, resulting in larger cells, and hence larger organisms, from cooler temperatures. Measurements of the diameter of skin cells did not support the hypothesis that cell size increases with latitude and decreases with temperature in the spotted turtle, nor was there a significant relationship between body size and cell size. Our study suggests that neither Bergmann's rule nor cell size variation sufficiently explain the body size cline observed in the spotted turtle. We hypothesize that patterns in body size are related to variation in female size at maturity and reproductive cycles.