Coluber Research Articles

Contrasting the depths of divergence between gene-tree and coalescent estimates in the North American racers (Colubridae: Coluber constrictor)

Abstract The North American racers (Coluber constrictor) are widely distributed across the Nearctic and numerous studies have demonstrated extensive variation in morphology, ecology, and population genetic structure. Here we take an integrative approach to understand lineage diversification within this taxon by combining genomic sequence capture data, mtDNA sequence data, morphometrics, and ecological niche models. Both the genomic data and mtDNA phylogeographic analyses support five lineages distributed across the range of this species. However, demographic model selection based on these two datasets strongly conflict in both the model of divergence and estimates of timing of lineage divergence. While mtDNA and concatenated genomic data suggest a Miocene origin of these distinct groups, coalescent-based demographic models with the sequence capture data suggest lineage diversification occurred at ~33 kya in allopatry without gene flow. Using linear morphological measurements of head shape we demonstrate that lineages distributed largely east and west of the Mississippi River are distinguishable. Furthermore, ecological niche models demonstrate that lineages distributed in subtropical habitats have environmental niche space that is significantly differentiated from lineages distributed across the continent. Taken together, these results suggest that ecology is an important axis of lineage divergence within this group and that more fine-scale analyses may find even greater differentiation between the populations identified here. This abstract translated to Spanish is avaliable in the Supporting Infromation section (Este resumen traducido al español está disponible en la sección, Supporting Infromation).

A species-specific digital PCR assay for the endangered blue racer (Coluber constrictor foxii) in Canada.

The only population of the endangered blue racer (Coluber constrictor foxii) in Canada occurs on Pelee Island, Ontario. The species is threatened by multiple factors, including habitat degradation and loss, road mortality, persecution, and potentially predation. We designed and evaluated the performance of an environmental DNA droplet digital PCR assay that can be used for multiple facets of conservation of this species. We tested the assay in silico and in vitro using DNA of blue racers and co-occurring snake species and estimated the LOD and LOQ using synthetic DNA. As wild turkey predation has been suggested to negatively affect racers, we tested the assay on eight wild turkey faecal samples. Our assay is specific, can detect the target species at very low levels of concentration (0.002 copies/µL), and can accurately quantify copy numbers ≥ 0.26 copies/µL. We detected no racer DNA in any wild turkey faecal sample. More faecal samples collected at strategic locations during snake peak activity on Pelee Island would enable a more thorough assessment of the possibility of turkey predation. Our assay should be effective for other environmental samples and can be used for investigating other factors negatively affecting blue racers, for example, helping to quantify blue racer habitat suitability and site occupancy.

Prevalence of Ophidiomycosis (Snake Fungal Disease) at a High Disturbance Remediated Landfill and at a Low-Impacted Forest Research Site in East Tennessee, USA

Ophidiomycosis (snake fungal disease; SFD) is a disease of conservation concern caused by the fungus Ophidiomyces ophidiicola that threatens the health of snake populations worldwide. Gaps exist in our knowledge about the prevalence of this disease across landscapes. In our study, we compared the prevalence of ophidiomycosis between a low-impacted forest site (n = 93) and a highly disturbed remediated landfill (n = 53) in Anderson County, Tennessee, USA. Free-ranging snakes were examined for the presence of skin lesions that are consistent with ophidiomycosis and were swabbed to detect O. ophidiicola DNA using quantitative PCR (qPCR). Apparent ophidiomycosis (qPCR-positive and skin lesions present) was diagnosed at both sites, but there was no significant difference in prevalence between the two sites (24.7% at the forest site; 22.6% at the landfill site). Apparent ophidiomycosis was most prevalent in Racers (38%; Coluber constrictor) and Ring-Necked Snakes (26%; Diadophis punctatus). There was no difference in ophidiomycosis status between sites for the most-sampled species: Racers, Black Rat Snakes (Pantherophis obsoletus), and Ring-necked Snakes (Diadophis punctatus). Our study represents the first report of ophidiomycosis at focal sites in Tennessee. The findings suggest that O. ophidiicola may be ubiquitous across the landscape and point to the need for further study of diverse habitat types for the prevalence of O. ophidiicola.

Southeastern US Snake Species are Vulnerable to Egg Predation by Red Imported Fire Ants (Solenopsis invicta)

Invasion and spread of Red Imported Fire Ants (RIFA; Solenopsis invicta) is cited as a possible cause for enigmatic reptile declines in the southeastern United States. Reptiles are negatively affected by RIFA through predation of eggs, hatchlings, and adults. We used short-term (12-h) field trials early in incubation to evaluate whether RIFA could successfully depredate intact eggs from six species of native terrestrial oviparous snakes: North American Racer (Coluber constrictor), Speckled Kingsnake (Lampropeltis holbrooki), Prairie Kingsnake (L. calligaster), Rough Greensnake (Opheodrys aestivus), Black Ratsnake (Pantherophis obsoletus) and Great Plains Ratsnake (P. emoryi). Then we used an artificial nest field experiment at the end of incubation to test whether RIFA predation differed between a species that has apparently declined in areas of its range where RIFA has invaded (L. holbrooki) and a species that has apparently not declined (C. constrictor). We measured pip–hatch and incubation time for each species in the laboratory to determine whether differences in time between pipping and hatching (pip–hatch time) could account for interspecific differences in RIFA predation on eggs. Overall, RIFA predation rates on snake eggs were high for all species (25–67% during early trials, 50–100% at end of incubation), although P. obsoletus was only depredated after hatching in the field. Coluber constrictor had significantly shorter pip–hatch times than other species, but probability of predation by RIFA did not differ for C. constrictor and L. holbrooki. Our study provides novel observations of RIFA predation and suggests that time spent in nest, eggshell characteristics, and nest microhabitat may be more important than pip–hatch time in mediating vulnerability of snake eggs to RIFA predation.

Spatiotemporal Patterns of Snake Captures and Activity in Upland Pine Forests

Patterns of species' occurrences across space and time are fundamental components to understanding their ecology, as this variation often reflects responses to local environmental gradients. We built species-specific models to understand the spatial and temporal factors predicting captures and activity of five snake species in upland pine forests: copperhead (Agkistrodon contortrix), racer (Coluber constrictor), coachwhip (Masticophis flagellum), western ratsnake (Pantherophis obsoletus), and western ribbonsnake (Thamnophis proximus). From mid-May to mid-July across 3 y (2018, 2019, 2020), we monitored boxtraps in two upland pine forests experiencing different management regimes: (1) subjected to frequent thinning and prescribed burning, and (2) subjected to infrequent thinning and prescribed burning. Significantly more copperheads and western ribbonsnakes were captured at the infrequently thinned and burned forest, whereas significantly more racers were captured at forest subjected to frequent thinning and burning. As the summer progressed, captures decreased each subsequent month for both racers and western ratsnakes, with the fewest captures in July. Western ratsnakes were the only species to exhibit a response to the weather in that activity decreased with increasing rainfall. No variables were significant predictors of coachwhip captures. The variation in captures across space may be attributed to the physiological tolerances of each species based on their habitat preferences or differences in prey availability at each forest. Interactions between the physiological tolerances, foraging behaviors, or their reproductive phenology may be underlying the temporal variation in activity patterns.

Observations of Snakes and Game Birds in a Managed Pine Barren in Massachusetts

Pinus rigida (Pitch Pine)–Quercus ilicifolia (Scrub Oak) barrens require active management to maintain, but the effects of forest management on snakes and game birds is poorly understood. We conducted vegetation surveys and examined incidental encounter data of a variety of snake and game bird species on a managed pine barren in Montague, MA, from 2008 to 2018. We recorded 73 observations, including 44 Coluber constrictor constrictor (Northern Black Racer) and 7 Meleagris gallopavo (Wild Turkey) nests. All of our observations were in managed habitats (Scrub Oak, treated Pitch Pine, and powerline corridors) which had low (<30%) tree canopy cover. Observed densities of Northern Black Racers did not significantly vary among these open-canopy habitats, or with time since treatment between 2 to 8 years since initial harvest in treated Pitch Pine. We did not conduct extensive surveys in unmanaged, closed-canopy Pitch Pine forests; thus, we were unable to determine the relative use by racers and game birds of unmanaged versus managed habitats. Nevertheless, snakes and game birds were using and nesting in the managed habitats at least to some extent. Our findings on racers and game birds from this study are preliminary, but combined with results from other studies, they suggest that ecosystem management in pine barrens can benefit snakes and game birds, along with a wide variety of other taxa.

Evidence of Intraguild Predation in a Snake Assemblage: Bigger Seems Better

Intraguild predation can play a significant role in structuring species composition with intraguild prey under both competitive and predatory pressure from intraguild predators. How intraguild prey are able to persist at sites with their predators is a complex issue with empirical evidence not always supporting theoretical models, indicating a need for more in situ research. A prominent grassland predator in the south central region of Pennsylvania, Coluber constrictor constrictor (Northern Black Racer), co-occurs with potential prey snakes including Lampropeltis triangulum (Eastern Milksnake) and Thamnophis sirtalis sirtalis (Eastern Gartersnake). Starting in 2008, this 7-year study examined how intraguild predation may differentially influence the body size and demographic traits of prey species in south-central Pennsylvania at sites with and without Northern Black Racers. The body size of adult Eastern Milksnakes was unaffected by the presence of racers. Eastern Milksnakes were more abundant, but with fewer juveniles, at racer-present sites. Adult female Eastern Gartersnakes were larger in body size, and adult males were less frequently encountered, in racer-present sites. These results indicate that intraguild predation in a snake community may affect the body size and demographic traits of prey species differentially, likely through predatory exclusion. However, the exact mechanisms behind our findings, and the resulting dynamics of snake diversity, are unclear and require further analyses.

THE NATURAL HISTORY OF THE NORTHERN BLACK RACER (COLUBER CONSTRICTOR CONSTRICTOR) IN SOUTH-CENTRAL PENNSYLVANIA

Long-term species surveys are effective tools for identifying changes in population demography which is of particular importance for those in threatened habitats such as grasslands. Due to their cryptic nature, snakes can benefit greatly from these types of surveys but multiyear surveys for snakes are rare in Pennsylvania and the surrounding region. We conducted coverboard surveys of the grassland specialist Northern Black Racer (Coluber constrictor constrictor) over eight years separated into two sampling periods (2008-2012 and 2015-2017) across a habitat-mosaic in south-central Pennsylvania. We recorded information on their body size, demography, and monthly activity. We compared these traits between the sampling periods to determine how they vary over time. A total of 70 Northern Black Racers were captured during this project. As expected, grasslands were heavily exploited by Northern Black Racers highlighting their importance to this species. There was a shift from relatively larger-bodied, older individuals towards relatively smaller-bodied, younger individuals between the sampling periods, but the sex ratio remained unchanged. Monthly activity of adults was unimodal in both sampling periods, but the month of peak activity varied and there was a possible effect of precipitation on this difference. The change in age structure between the sampling periods suggested that a widespread mortality event, possibly from exceedingly cold overwintering conditions, may have culled older individuals resulting in a younger cohort to fill the void. As Northern Black Racers are an important grassland predator, our data show the benefits of long-term surveys through detecting changes in demographics that could potentially influence long-term survival of a population.

Bachman's Sparrow survival and nest predation response to a hardwood canopy reduction experiment

AbstractWhere historical fire regimes have been disrupted, reduction in woody vegetation is often used to maintain or restore habitat for grassland and early successional birds. In pine savanna ecosystems of the southeastern USA, mechanical hardwood canopy reduction can restore pine savanna communities and is often employed on privately owned lands to improve habitat for the Northern Bobwhite (Colinus virginianus), although scant empirical evidence exists of its effects on target or non‐target species. We measured the response of a pine savanna specialist, the Bachman's Sparrow (Peucaea aestivalis), to large‐scale hardwood reduction in a before–after–control–impact design on two properties where two‐year fire‐return intervals were established and the Bachman's Sparrow population was stable. We investigated the effects of mechanical hardwood reduction on Bachman's Sparrow daily nest survival, cause‐specific nest mortality and adult male annual survival. During the four‐year study, we monitored 107 Bachman's Sparrow nests, recorded 49 nest predation events, and banded 113 adult male Bachman's Sparrows. We found Bachman's Sparrow nest and adult survival were resilient to changes in the hardwood canopy and did not differ significantly between treatment and control sites. Average annual adult male survival was 0.41 (0.32–0.52) and daily survival rate of nests with surveillance declined annually from 0.94 (0.92–0.96) to 0.88 (0.83–0.92). The identity of predators at nests was dominated by two snake species, black racer (Coluber constrictor) and corn snake (Pantherophis guttata). We found evidence for opposing treatment effects on the frequency of nest depredations by the dominant species; racers responded positively and corn snakes responded negatively. Our results suggest a moderate midstory canopy does not limit Bachman's Sparrow vital rates when management includes frequent prescribed fire. Our results also suggest hardwood reduction to mitigate nest predation may be complicated with a diverse predator suite.

Snakes on a lane: Road type and edge habitat predict hotspots of snake road mortality

Roads constitute just 1% of the total land in the US, but their impacts on wildlife are significant and far-reaching. Snakes are particularly susceptible to road mortality because many species do not avoid crossing roads, may use the road’s surface to thermoregulate, or freeze when approached by a vehicle. We conducted opportunistic surveys to collect road mortality points for snakes in southeastern Ohio over 15 years (2003–2018). We used logistic regression to predict roadkill hotspots and evaluate variables that influence road mortality. The species most frequently found dead on roads were Black Ratsnakes (Pantherophis spiloides), Northern Black Racers (Coluber constrictor), Eastern Gartersnakes (Thamnophis sirtalis), and Rough Greensnakes (Opheodrys aestivus). Across the 14 snake species we recorded dead on roads, percent pasture within a 100 m buffer of the roadkill point, township route, county route, and state route were all negative predictors of road mortality. All surveys started in Athens, Ohio, and distance to roadkill locations was a positive predictor for road mortality. These results indicate that high-traffic roads pose a risk to snake populations, but that mortality also occurs on low-traffic roads as well. Our top model showed that low levels of pasture embedded in other land cover types was an important predictor of roadkill, suggesting that edge habitat contributes to snake road mortality. Because road mortality does not seem to be localized, road mortality mitigation structures such as underpasses and fences may have limited benefits for snake populations in our study area. The creation of edge habitat away from roads could provide snakes with necessary habitat without increasing their risk of mortality.

Predator responses to fire: A global systematic review and meta-analysis.

Knowledge of how disturbances such as fire shape habitat structure and composition, and affect animal interactions, is fundamental to ecology and ecosystem management. Predators also exert strong effects on ecological communities, through top-down regulation of prey and competitors, which can result in trophic cascades. Despite their ubiquity, ecological importance and potential to interact with fire, our general understanding of how predators respond to fire remains poor, hampering ecosystem management. To address this important knowledge gap, we conducted a systematic review and meta-analysis of the effects of fire on terrestrial, vertebrate predators world-wide. We found 160 studies spanning 1978-2018. There were 36 studies with sufficient information for meta-analysis, from which we extracted 96 effect sizes (Hedges' g) for 67 predator species relating to changes in abundance indices, occupancy or resource selection in burned and unburned areas, or before and after fire. Studies spanned geographic locations, taxonomic families and study designs, but most were located in North America and Oceania (59% and 24%, respectively), and largely focussed on felids (24%) and canids (25%). Half (50%) of the studies reported responses to wildfire, and nearly one third concerned prescribed (management) fires. There were no clear, general responses of predators to fire, nor relationships with geographic area, biome or life-history traits (e.g. body mass, hunting strategy and diet). Responses varied considerably between species. Analysis of species for which at least three effect sizes had been reported in the literature revealed that red foxes Vulpes vulpes mostly responded positively to fire (e.g. higher abundance in burned compared to unburned areas) and eastern racers Coluber constrictor negatively, with variances overlapping zero only slightly for both species. Our systematic review and meta-analysis revealed strong variation in predator responses to fire, and major geographic and taxonomic knowledge gaps. Varied responses of predator species to fire likely depend on ecosystem context. Consistent reporting of ongoing monitoring and management experiments is required to improve understanding of the mechanisms driving predator responses to fire, and any broader effects (e.g. trophic interactions). The divergent responses of species in our study suggest that adaptive, context-specific management of predator-fire relationships is required.

Red-shouldered Hawk (Buteo lineatus) predation on North American Racer (Coluber constrictor) in the Arkansas Ozarks

Red-shouldered Hawk (Buteo lineatus) predation on North American Racer (Coluber constrictor) in the Arkansas Ozarks

Helminths of the Northern Black Racer, Coluber constrictor constrictor Linnaeus (Squamata: Colubridae), from North Carolina, U.S.A.

Twenty-three salvaged specimens of Coluber constrictor constrictor Linnaeus (Northern Black Racer) from North Carolina, U.S.A., were examined for gastrointestinal helminths. Eighteen species of helminths (4 trematodes, 2 cestodes, 10 nematodes, and 2 acanthocephalans) are reported, representing 6 new host records and 6 new geographic distribution records. At 52% prevalence, immature physalopterids were the most prevalent helminth, followed by another nematode, Abbreviata terrapenis, at 43%. Specimens of the cestode Oochoristica sp. were the most prevalent (48%) platyhelminth, and macracanthorhynchid cystacanths were the most prevalent (17%) acanthocephalan.

HOST FACTORS AND TESTING MODALITY AGREEMENT ASSOCIATED WITH OPHIDIOMYCES INFECTION IN A FREE-RANGING SNAKE POPULATION IN SOUTHEAST OHIO, USA.

Snake fungal disease (SFD) is an emerging mycotic disease caused by Ophidiomyces ophiodiicola, and has been demonstrated to impact snake populations of conservation concern in the United States negatively. Although Ophidiomyces has been shown to affect diverse taxa and to have a broad distribution, host factors associated with infected individuals and optimal testing protocols are not yet well characterized. The purpose of this study was to evaluate host factors and agreement across testing modalities associated with Ophidiomyces infection in a free-ranging snake population in southeast Ohio. Wild-caught snakes were swabbed and biopsied to test for Ophidiomyces via quantitative polymerase chain reaction (qPCR), culture, and histopathology. The host parameters assessed were species, sex, snout-vent length, body weight, month captured, and presence of gross skin lesions. A total of 8/30 individuals across three species-Black Racers (Coluber constrictor), Grey Ratsnakes (Pantherophis spiloides), and Eastern Gartersnakes (Thamnophis sirtalis sirtalis)-tested positive via at least one testing modality for Ophidiomyces infection. There were no associations between sex, snout-vent length, or weight and Ophidiomyces infection status. A higher proportion of individuals with gross lesions tested positive for Ophidiomyces than those without gross lesions, and most individuals that tested positive were caught in April or May. A low level of agreement was observed across testing modalities. Swab qPCR identified the most Ophidiomyces-positive individuals, and fungal culture identified the fewest at 0 individuals. Although there are limitations associated with a sample size of 30, these findings support the potential of this pathogen to infect individuals broadly across species and size, highlighting the relevance of this disease for snake conservation efforts. They also suggest that although little agreement was observed across test modalities, the concurrent use of multiple modalities is a more sensitive method for characterizing prevalence and distribution of Ophidiomyces.

North American Racer (Coluber constrictor) on Grand Bahama, The Bahamas

North American Racer (Coluber constrictor) on Grand Bahama, The Bahamas

The herpetofauna of Wallops Island, Accomack County, Virginia: A case study of a vulnerable community

abstractBarrier islands are valuable models for evolutionary and conservation biology studies. Since 2010, we have investigated the herpetofauna of Wallops Island, Virginia, 25 years after a seminal study. We used combinations of taxon-specific field techniques to maximize accuracy. A total of four species of amphibians and seven species of reptiles were identified. The most abundant amphibian and reptile were Fowler&amp;#x92;s toad (Anaxyrus fowleri) and the North American racer (Coluber constrictor), respectively. We report three previously undetected amphibians and the likely prior misidentification of another. We also identified a new snake species. The diamond-backed terrapin (Malaclemys terrapin) is only seasonally abundant on the island, in contrast to the year-round well-established Eastern mud turtle (Kinosternon subrubrum), while only a few juveniles of the common snapping turtle (Chelydra serpentina) were detected. No lizards were found in the island. These limited yet interesting herpetofauna face momentous environmental challenges derived from global climate change and rising sea level.

Snake mortality and cover board effectiveness along exclusion fencing in British Columbia, Canada

We report on snake mortalities along exclusion fencing in southern British Columbia, showing Western Yellow-bellied Racer (Coluber constrictor mormon) deaths were disproportionately higher than our encounter rates with the species within the snake community. This suggests racers were susceptible to fence mortality more so than Northern Pacific Rattlesnakes (Crotalus o. oreganus) or Great Basin Gophersnakes (Pituouphis catenifer deserticola). Datalogger recordings revealed temperatures under cover boards were well above the tolerable temperatures of the three snake species, although the boards appeared to temper ambient heat more efficiently than natural vegetation. We caution that the effects of fencing and cover boards may vary across ecosystems and snake species.

A new coccidian parasite (Apicomplexa: Eimeriidae: Eimeria) from the southern black racer, Coluber constrictor priapus (Reptilia: Ophidia: Colubridae) from Arkansas, USA.

Between April 2012 and October 2017, 18 southern black racers, Coluber constrictor priapus, were collected from nine counties of Arkansas (n = 13) and McCurtain County, Oklahoma (n = 5) and their faeces examined for coccidian parasites. One of 18 (6%) C. c. priapus harboured an eimerian that we describe here as new. Oocysts of Eimeria dunni sp. nov. were subspheroidal with a lightly pitted bi-layered wall measuring L × W 24.0 × 21.1 and L/W ratio of 1.2. A micropyle was absent but an oocyst residuum and polar granule were present. Sporocysts were ovoidal and measured 11.9 × 8.1 with L/W of 1.5. A Stieda body was present but substieda and parastieda bodies were absent. The sporocyst residuum was composed of medium-sized granules aligned along perimeter of sporocyst or in a dispersed mass. This represents the first valid eimerian reported from the southern black racer.

Response of reptile and amphibian communities to the reintroduction of fire in an oak/hickory forest

Fire can have diverse effects on ecosystems, including direct effects through injury and mortality and indirect effects through changes to available resources within the environment. Changes in vegetation structure such as a decrease in canopy cover or an increase in herbaceous cover from prescribed fire can increase availability of preferred microhabitats for some species while simultaneously reducing preferred conditions for others. We examined the responses of herpetofaunal communities to prescribed fires in an oak/hickory forest in western Kentucky. Prescribed fires were applied twice to a 1000-ha area one and four years prior to sampling, causing changes in vegetation structure. Herpetofaunal communities were sampled using drift fences, and vegetation attributes were sampled via transects in four burned and four unburned plots. Differences in reptile community structure correlated with variation in vegetation structure largely created by fires. Amphibian community structure differed on a yearly basis, indicating that sampled communities were likely influenced by environmental factors other than the burning. We found taxa-specific differences in abundances for Coluber constrictor, Diadophis punctatus, Sceloporus undulatus, Lithobates clamitans and snakes as a group, being more abundant in burned areas while Anaxyrus sp., Notophthalmus viridescens and Plethodon glutinosus were more abundant in unburned areas. Differences in amphibian taxa abundances may have been influenced by availability of aquatic breeding habitat and yearly weather variation. Our results suggest that the vegetation structure changes caused by prescribed fire can have indirect impacts on reptile abundances and community structure, while not significantly impacting amphibian communities.

Auguste Ghiesbreght’s natural history explorations in Oaxaca and other parts of Mexico until 1854

Los autores revisan las colecciones de historia natural hechas por Auguste Ghiesbreght de “Oaxaca” y otras áreas entre 1838 y 1854. Especímenes de relevancia taxonómica son por ejemplo el holotipo de la ‘corredora’ Coryphodon oaxaca Jan (Coluber constrictor L.), una entre varias especies de anfibios y reptiles (col. Ghiesbreght) no registradas en el Estado de Oaxaca, o bien algunas aves de México meridional atribuidas implícitamente a Ghiesbreght pero en realidad recolectadas por otros naturalistas. Material zoológico y una multitud de plantas de “Oaxaca” (col. 1841–1854) incluyendo muchos especímenes tipo provienen de otras partes y particularmente de las regiones interiores del Golfo de México desde Hidalgo hasta el área del Pico de Orizaba. Estos resultados tienen consecuencias respecto a localidades tipo, distribución y posiblemente la sistemática en diferentes grupos de animales y campos de la botánica.