RESUMEN
Snake fungal disease (SFD; ophidiomycosis), caused by the pathogen Ophidiomyces ophiodiicola (Oo), has been documented in wild snakes in North America and Eurasia, and is considered an emerging disease in the eastern United States of America. However, a lack of historical disease data has made it challenging to determine whether Oo is a recent arrival to the USA or whether SFD emergence is due to other factors. Here, we examined the genomes of 82 Oo strains to determine the pathogen's history in the eastern USA. Oo strains from the USA formed a clade (Clade II) distinct from European strains (Clade I), and molecular dating indicated that these clades diverged too recently (approximately 2,000 years ago) for transcontinental dispersal of Oo to have occurred via natural snake movements across Beringia. A lack of nonrecombinant intermediates between clonal lineages in Clade II indicates that Oo has actually been introduced multiple times to North America from an unsampled source population, and molecular dating indicates that several of these introductions occurred within the last few hundred years. Molecular dating also indicated that the most common Clade II clonal lineages have expanded recently in the USA, with time of most recent common ancestor mean estimates ranging from 1985 to 2007 CE. The presence of Clade II in captive snakes worldwide demonstrates a potential mechanism of introduction and highlights that additional incursions are likely unless action is taken to reduce the risk of pathogen translocation and spillover into wild snake populations.
Asunto(s)
Dermatomicosis , Onygenales , Animales , Dermatomicosis/epidemiología , Dermatomicosis/microbiología , Genética de Población , Serpientes/genética , Estados UnidosRESUMEN
Emerging fungal pathogens are a direct threat to vertebrate biodiversity. Elucidating the mechanisms by which mycoses impact host fitness is an important step towards effective prediction and management of disease outcomes in populations. The vertebrate acute stress response is an adaptive mechanism that allows individuals to meet challenges to homeostasis and survival in dynamic environments. Disease may cause stress, and coping with fungal infections may require shifts in resource allocation that alter the ability of hosts to mount an acute response to other external stressors. We examined the glucocorticoid and glycemic response to acute capture stress in a population of free-living pygmy rattlesnakes, Sistrurus miliarius, afflicted with an emerging mycosis (ophidiomycosis) across seasons. In all combinations of disease status and season, acute capture stress resulted in a significant glucocorticoid and glycemic response. While disease was not associated with elevated baseline or stress-induced corticosterone (CORT), disease was associated with an increased glucocorticoid stress response (post-stress minus baseline) across seasons. Both baseline and stress-induced glucose were lower in snakes with ophidiomycosis compared to uninfected snakes. The relationship between glucose and pre- and post-stress CORT depended on infection status, and positive correlations were only observed in uninfected snakes. The variables which explained CORT and glucose levels were different. The pattern of CORT was highly seasonal (winter high - summer low) and negatively related to body condition. Glucose, on the other hand, did not vary seasonally or with body condition and was strongly related to sex (male high - female low). Our results highlight the fact that circulating CORT and glucose are sensitive to different intrinsic and extrinsic predictor variables and support the hypothesis that disease alters the acute physiological stress response. Whether the effects of ophidiomycosis on the acute stress response result in sublethal effects on fitness should be investigated in future studies.
Asunto(s)
Corticosterona , Glucocorticoides , Humanos , Animales , Masculino , Femenino , Serpientes , Estrés FisiológicoRESUMEN
Mounting an immune response may be energetically costly and require the diversion of resources away from other physiological processes. Yet, both the metabolic cost of immune responses and the factors that impact investment priorities remain poorly described in many vertebrate groups. For example, although viviparity has evolved many times in vertebrates, the relationship between immune function and pregnancy has been disproportionately studied in placental mammals. To examine the energetic costs of immune activation and the modulation of immune function during pregnancy in a non-mammalian vertebrate, we elicited an immune response in pregnant and non-pregnant pygmy rattlesnakes, Sistrurus miliarius, using lipopolysaccharide (LPS). Resting metabolic rate (RMR) was measured using flow-through respirometry. Immune function was examined using bactericidal assays and leukocyte counts. The RMR of pygmy rattlesnakes increased significantly in response to LPS injection. There was no statistically significant difference in the metabolic response of non-reproductive and pregnant snakes to LPS. Mean metabolic increments for pregnant females, non-reproductive females, and males were 13%, 18% and 26%, respectively. The ratio of heterophils to lymphocytes was elevated in response to LPS across reproductive categories; however, LPS did not impact plasma bactericidal ability in non-reproductive snakes. Although pregnant females had significantly higher plasma bactericidal ability compared with non-reproductive snakes prior to manipulation, their bactericidal ability declined in response to LPS. LPS administration also significantly reduced several litter characteristics, particularly when administrated relatively early in pregnancy. Our results indicate that immune performance is energetically costly and is altered during pregnancy, and that immune activation during pregnancy may result in tradeoffs that affect offspring in a viviparous reptile.
Asunto(s)
Crotalinae , Placenta , Animales , Metabolismo Basal , Femenino , Masculino , Embarazo , Reptiles , SerpientesRESUMEN
Venom is a complex molecular phenotype that shows high levels of variation in expressed proteins between individuals within and between populations. However, the functional significance of this variation in terms of toxicity towards prey is largely unknown. Here, we assessed the relative toxicity of venom from individual pygmy rattlesnakes ( Sistrurus miliarius) on brown anoles ( Anolis sagrei) using a novel assay involving tests of fixed doses of venom from individual snakes on individual lizards. We found high levels of functional variation between individual venoms within populations with individual differences (nested within population) explaining 3.6 times more variation in toxicity than population differences. Our results suggest a previously unappreciated adaptive significance to within-population variation in venom. They argue that selective mechanisms that maintain variation within populations may be of equal or greater importance to divergent selection leading to local adaption between populations as evolutionary explanations of venom variation within species.
Asunto(s)
Venenos de Crotálidos , Crotalus , Lagartos , Animales , Fenotipo , ProteínasRESUMEN
Seasonal constraints on the timing and intensity of reproductive events shape observed variation in life history strategies across latitudes. Selection acts on the endocrine mechanisms that underlie reproductive investment. It is therefore important to examine the seasonal relationship between hormones and reproduction in geographically and phylogenetically diverse taxa. Snakes have proven to be a valuable model in investigations of seasonal hormone production and behavior in field-active vertebrates, but most research has focused on temperate populations from highly seasonal environments. To reduce this bias, we provide a description of the seasonal relationships among testosterone, corticosterone, body condition, and reproductive behavior in a subtropical population of Pygmy Rattlesnakes, Sistrurus miliarius. In central Florida, Sistrurus miliarius exhibits a prolonged breeding season (September-January) compared to most temperate zone snakes. Despite the extended breeding season, the pattern of testosterone in the population was highly seasonal and very similar to temperate pitvipers with a shorter mating season. Testosterone declined steadily through the mating season, but males sampled while engaging in mating behaviors had higher testosterone compared to solitary males throughout the mating season. Testosterone was negatively related to corticosterone throughout the breeding season and during times of year when the gonads were presumed to be quiescent and no mating behavior was observed. Testosterone was positively related to individual body condition both within and outside of the breeding season. A review of the literature reveals no consistent pattern regarding the relationship between corticosterone and testosterone in snakes, but suggests that the condition-dependence of steroid production may be consistent across snake taxa.
Asunto(s)
Corticosterona/metabolismo , Testosterona/metabolismo , Animales , Cruzamiento , Reproducción , Reptiles , Estaciones del AñoRESUMEN
Theory predicts that predator-prey interactions can generate reciprocal selection pressures on species pairs, which can result in local adaptation, yet the presence and pattern of local adaptation is poorly studied in vertebrate predator-prey systems. Here, we used a reciprocal common garden (laboratory) experimental design involving comparisons between local and foreign populations to determine if local adaptation was present between a generalist predator-the pigmy rattlesnake (Sistrurus miliarius)-and a co-occurring prey-the squirrel treefrog (Hyla squirella). We conducted toxicity trials using snake venom from two populations separated by 340 km tested on prey from sympatric and allopatric populations, resulting in data from four venom origin-frog origin combinations. We assessed venom effectiveness using two measures (frog mortality at 24 h and time to frog death) and then used regression analyses to look for a signal of local adaptation with either measure. We found evidence for local adaptation for one measure (time to death), but not the other (frog mortality). We argue that in this system, the time to death of a prey item is a more ecologically relevant measure of venom effectiveness than is frog mortality at 24 h. Our results document an example of local adaptation between two interacting vertebrates using a whole-organism assay and a local versus foreign criteria and provide evidence that population-level variation in snake venom is adaptive.
Asunto(s)
Adaptación Fisiológica , Anuros , Venenos de Crotálidos , Aclimatación , Animales , FenotipoRESUMEN
Species of Pterygodermatites are spirurid nematodes that have expanded their geographic distribution worldwide. They infect a variety of mammalian definitive hosts with few reports of potential paratenic infections in amphibian and reptile hosts. In this study, we report Pterygodermatites sp. larvae identified in free-ranging, invasive Cuban treefrogs (Osteopilus septentrionalis), from central Florida, United States. Encysted larvae were recovered from the skeletal muscle and/or the coelomic cavity of three frogs; molecular characterization of the small subunit (18S) ribosomal RNA and cytochrome oxidase I genes of the parasites matched reported sequences of Pterygodermatites (Mesopectines) whartoni (Tubangui, 1931). This is a parasite native to Southeastern Asia and to the best of the authors' knowledge, it is the first report of the species in the New World. The recovery of invasive Pterygodermatites from invasive Cuban treefrogs in North America highlights the growing concern regarding the potential impact non-native parasites and invasive species may have on native wildlife populations.
RESUMEN
Raillietiella orientalis is established in Florida and rapidly spreading both geographically and in known host species. A banded water snake (Nerodia fasciata), purchased in Michigan at a regional reptile show, expectorated a pentastome whose morphology and DNA sequence indicated that it was R. orientalis. This event indicates that, through the pet trade, R. orientalis has been spread 1,500 km from its previously known distribution limit. Fecal sample analyses indicated that the snake was shedding large numbers of embryonated eggs for at least several months. The diversity of reptile species that are both known hosts of R. orientalis in Florida and are commonly sold in the pet trade indicates that this invasive pentastome may become a widespread health concern for pet owners and veterinarians.
Asunto(s)
Colubridae , Pentastomida , Animales , Florida , MichiganRESUMEN
In this study we sequenced and annotated the complete mitochondrial genome of the invasive reptile parasite Raillietiella orientalis using Illumina DNA sequencing. The length of the mitogenome was 15,320 bp and had a GC content of 33.1%. The mitogenome contained 13 protein-coding genes, two ribosomal RNA genes, and 22 tRNA genes, the order of which was diagnostic of Pancrustacean mitogenomes. A phylogenetic tree constructed from the 13 protein-coding genes of R. orientalis and 26 other Pancrustacean mitogenomes supported the placement of R. orientalis as part of the monophyletic subclass Pentastomida within the Maxillopoda and sister to the subclass Branchiura.
RESUMEN
Cuban treefrogs, Osteopilus septentrionalis, were grossly examined for parasites and parasite species confirmed by PCR. Angiostrongylus cantonensis larvae were recovered from the hind leg muscle of O. septentrionalis. This is the first report of the zoonotic rat lungworm in the Cuban treefrog and new geographic location (Volusia County) in Florida, US.
Asunto(s)
Angiostrongylus cantonensis , Enfermedades de los Roedores , Infecciones por Strongylida , Angiostrongylus cantonensis/genética , Animales , Anuros , Florida/epidemiología , Reacción en Cadena de la Polimerasa/veterinaria , Ratas , Enfermedades de los Roedores/parasitología , Infecciones por Strongylida/epidemiología , Infecciones por Strongylida/parasitología , Infecciones por Strongylida/veterinariaRESUMEN
Snake fungal disease (ophidiomycosis) is an emerging infection of snakes caused by Ophidiomyces ophiodiicola. Little is known about mechanisms of this pathogen's transmission and its implications for conservation of wild snake populations. We report four cases with evidence of vertical transmission of O. ophiodiicola from dam to offspring.
Asunto(s)
Dermatomicosis/veterinaria , Transmisión Vertical de Enfermedad Infecciosa/veterinaria , Onygenales/aislamiento & purificación , Serpientes/microbiología , Animales , Animales Salvajes , Dermatomicosis/microbiología , Dermatomicosis/transmisión , OvoviviparidadRESUMEN
Snake fungal disease (SFD) is caused by the fungus Ophidiomyces ophiodiicola and its documentation in wild snake populations has risen sharply in the past decade. Little is known regarding the fate of individual, free-ranging snakes afflicted with SFD. We monitored an afflicted population of pygmy rattlesnakes ( Sistrurus miliarius) at Lake Woodruff National Wildlife Refuge in Central Florida, US for 2 yr. The severity of SFD in individual snakes was unrelated to the probability of their recapture later in the study, and half of the snakes diagnosed as severely infected at the onset of the study were recaptured later with no clinical signs of SFD. The clinical progress of 12 serially recaptured individuals also showed that individuals cleared the infection and fluctuated between no or low and severe clinical signs over the 2-yr study.
Asunto(s)
Crotalinae/microbiología , Micosis/veterinaria , Animales , Ascomicetos , Florida/epidemiología , Micosis/epidemiología , Micosis/microbiología , Micosis/patologíaRESUMEN
Venom toxicity assessments are often based upon non-native surrogate prey species that are not consumed in the wild by the venomous predator. This raises questions about the relevance of toxicity results on these "model" prey in addressing ecological or evolutionary questions about venom effects on native prey. We explore this issue by comparing the toxicity of venom from pygmy rattlesnakes (Sistrurus miliarius) on taxonomically-diverse sets of model (non-native) and native prey. Specifically, we compared rattlesnake venom toxicity for nine species from three broad taxonomic groups of prey (reptiles, mammals, and amphibians) to determine whether estimates of venom toxicity for the non-native model species of each group was representative of species which were native prey. In all three groups, model species (Anolis sagrei, Mus musculus, and Lithobates pipiens) had a significantly different mortality response from one or more of the native prey species (Anolis carolinensis, Peromyscus gossypinus, Lithobates sphenocephalus, Hyla cinerea, and Hyla squirella) that the models were meant to represent. Two features of our results suggest an importance of evolutionary history in understanding these differences. First, there was a phylogenetic component to prey responses to venom in that in each group, non-native models and congeneric native prey showed more similar responses than prey from other genera suggesting that venom may act on common prey targets that result from common ancestry. Second, native prey generally showed higher LD50 values than their non-native counterparts, suggesting greater resistance to venom from a predator with which they interact in nature. Our results suggest that researchers should use native prey to generate measures of venom toxicity that are ecologically and evolutionarily relevant. If this is not possible using "model" prey species that are close taxonomic relatives to natural prey may be a reasonable alternative.
Asunto(s)
Venenos de Crotálidos/toxicidad , Crotalinae , Especificidad de la Especie , Animales , Anuros/fisiología , Dosificación Letal Mediana , Lagartos/fisiología , Ratones , Peromyscus/fisiología , Filogenia , Conducta Predatoria/fisiologíaRESUMEN
Snake fungal disease (SFD) is an emerging threat to snake populations in the United States. Fungal pathogens are often associated with a physiological stress response mediated by the hypothalamo-pituitary-adrenal axis (HPA), and afflicted individuals may incur steep coping costs. The severity of SFD can vary seasonally; however, little is known regarding (1) how SFD infection relates to HPA activity and (2) how seasonal shifts in environment, life history, or HPA activity may interact to drive seasonal patterns of infection severity and outcomes. To test the hypothesis that SFD is associated with increased HPA activity and to identify potential environmental or physiological drivers of seasonal infection, we monitored baseline corticosterone, SFD infection severity, foraging success, body condition, and reproductive status in a field-active population of pigmy rattlesnakes. Both plasma corticosterone and the severity of clinical signs of SFD peaked in the winter. Corticosterone levels were also elevated in the fall before the seasonal rise in SFD severity. Severely symptomatic snakes were in low body condition and had elevated corticosterone levels compared to moderately infected and uninfected snakes. The monthly mean severity of SFD in the population was negatively related to population-wide estimates of body condition and temperature measured in the precedent month and positively correlated with corticosterone levels measured in the precedent month. Symptomatic females were less likely to enter reproductive bouts compared to asymptomatic females. We propose the hypothesis that the seasonal interplay among environment, host energetics, and HPA activity initiates trade-offs in the fall that drive the increase in SFD prevalence, symptom severity, and decline in condition observed in the population through winter.
Asunto(s)
Corticosterona/sangre , Crotalus , Micosis/veterinaria , Estrés Fisiológico , Animales , Enfermedades Transmisibles Emergentes , Femenino , Micosis/sangre , Reacción en Cadena en Tiempo Real de la Polimerasa , Reproducción , Estaciones del AñoRESUMEN
In the past decade, snake fungal disease (SFD) has been identified as an emerging threat to snake populations throughout the eastern USA. Snake fungal disease is caused by the fungus Ophidiomyces ophiodiicola. Little is known regarding the environmental or physiological variables that affect host vulnerability and O. ophiodiicola virulence in wild snake populations. Understanding the intrinsic and extrinsic factors that correlate with infection severity is a key first step in understanding host-pathogen dynamics. Host vulnerability may vary seasonally as a result of thermal conditions or energetic trade-offs, and pathogen growth rates or dispersal may be tied to seasonal trends in climate. To determine whether season, environmental temperature or energetic trade-offs associated with life-history stage influence an individual's susceptibility to infection, we monitored the severity of clinical signs of SFD, surface air temperature, reproductive status, body condition and serum complement activity (plasma bactericidal ability) in free-ranging pigmy rattlesnakes, Sistrurus miliarius, over the course of 18 months. Seasonal increases in the severity of clinical signs of SFD were correlated negatively with monthly air surface temperature and the mean body condition of the population. Bactericidal ability varied seasonally, but pigmy rattlesnakes suffering from active SFD infections did not exhibit deficits in innate immune function. Infected snakes were in significantly lower body condition when compared with the general population, but seasonal patterns in the mean body condition of the population were not driven by seasonal patterns of infection severity. Our results highlight the potential importance of the thermal environment and energetic status in determining infection severity and outcomes and the need for managers and researchers to consider seasonality of symptom presentation when the goal is to identify the prevalence or incidence of SFD in populations.
RESUMEN
Parental care is a complex social behavior that is widespread among vertebrates. The neuroendocrine regulation of parent-offspring social behavior has been well-described in mammals, and to a lesser extent, in birds and fish. However, little is known regarding the underlying mechanisms that mediate the expression of care behaviors in squamate reptiles. In mammalian model species and humans, posterior pituitary hormones of the oxytocin and vasopressin families mediate parental care behaviors. To test the hypothesis that the regulatory role of posterior pituitary neuropeptides is conserved in a viviparous squamate reptile, we pharmacologically blocked the vasotocin receptor in post-parturient pigmy rattlesnakes, Sistrurus miliarius, and monitored the spatial relationship between mothers and offspring relative to controls. Mothers in the control group demonstrated spatial aggregation with offspring, with mothers having greater post-parturient energy stores aggregating more closely with their offspring. Blockade of vasotocin receptors eliminated evidence of spatial aggregation between mothers and offspring and eliminated the relationship between maternal energetic status and spatial aggregation. Our results are the first to implicate posterior pituitary neuropeptides in the regulation of maternal behavior in a squamate reptile and are consistent with the hypothesis that the neuroendocrine mechanisms underlying social behaviors are broadly conserved among vertebrates.
RESUMEN
The level of parental investment in free-living offspring varies greatly within and among vertebrate taxa, and the mechanisms that mediate investment are likely targets of selection in the evolution of reproductive strategies. In mammalian and avian systems, individual investment is adjusted according to parental energetic status, and regulatory mechanisms have been described. Parental care is also a component of the life history of several groups of squamates and archosaurs, but little to nothing is known regarding the mechanisms that underlie individual variation in parental investment in these groups. Therefore, we examined the relationships among maternal body condition, corticosterone, arginine vasotocin (AVT), and maternal care in postparturient pigmy rattlesnakes. Energetic status was manipulated in pregnant females by supplemental feeding, and AVT was manipulated in postparturient mothers by intraperitoneal injection. Circulating corticosterone and body condition were recorded in postparturient mothers. Mother-offspring spatial relationships were analyzed to determine the closeness of mother-offspring associations. No significant relationship between maternal body condition and baseline corticosterone was observed in mothers, and no significant relationship was found between corticosterone and the level of maternal association with offspring. Manipulation of AVT did not stimulate maternal care. There was a strong and repeatable positive relationship between maternal postparturient body condition and the level of maternal association with offspring. The lack of a significant correlation between body condition and corticosterone does not support the hypothesis that a postparturient glucocorticoid response drives the observed condition-dependence of maternal offspring association.
Asunto(s)
Composición Corporal/fisiología , Corticosterona/sangre , Crotalus/fisiología , Conducta Materna/fisiología , Ovoviviparidad/fisiología , Vasotocina/metabolismo , Animales , Metabolismo Energético , FemeninoRESUMEN
Since 2006, there has been a marked increase in the number of reports of severe and often fatal fungal skin infections in wild snakes in the eastern USA. The emerging condition, referred to as snake fungal disease (SFD), was initially documented in rattlesnakes, where the infections were believed to pose a risk to the viability of affected populations. The disease is caused by Ophidiomyces ophiodiicola, a fungus recently split from a complex of fungi long referred to as the Chrysosporium anamorph of Nannizziopsis vriesii (CANV). Here we review the current state of knowledge about O. ophiodiicola and SFD. In addition, we provide original findings which demonstrate that O. ophiodiicola is widely distributed in eastern North America, has a broad host range, is the predominant cause of fungal skin infections in wild snakes and often causes mild infections in snakes emerging from hibernation. This new information, together with what is already available in the scientific literature, advances our knowledge of the cause, pathogenesis and ecology of SFD. However, additional research is necessary to elucidate the factors driving the emergence of this disease and develop strategies to mitigate its impacts.This article is part of the themed issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'.
Asunto(s)
Ascomicetos/fisiología , Chrysosporium/fisiología , Dermatomicosis/veterinaria , Serpientes , Animales , Canadá/epidemiología , Dermatomicosis/epidemiología , Dermatomicosis/microbiología , Especificidad del Huésped , Prevalencia , Estados Unidos/epidemiologíaRESUMEN
The stability of a high rocky intertidal community was assessed in a controlled field experiment in which the most common consumers, limpets, were temporarily removed. Compared to the unmanipulated plots, the exclusion plots developed greater algal abundance and altered species composition of both algae and barnacles. The community was not perturbed beyond its capacity to recover, since the community structure of the limpet-removal plots converged on the structure of the unmanipulated plots following limpet reintroduction. Different components of the community recovered at different rates, depending on whether or not the species had a size-related escape from the limpets. Algae had no size-related escape from limpets. The difference in algal abundance between manipulated and unmanipulated plots lasted less than six months after limpet reintroduction. Barnacles, however, had a size-related escape from limpets and therefore recovered more slowly. The difference in barnacle species composition between the perturbed and unperturbed plots lasted for 17 months after limpet reintroduction. The length of the limpet removal period (16 or 28 months) did not appear to affect the rate of community recovery.