Commonly collected thermal performance data can inform species distributions in a data-limited invader.

Predicting potential distributions of species in new areas is challenging. Physiological data can improve interpretation of predicted distributions and can be used in directed distribution models. Nonnative species provide useful case studies. Panther chameleons (Furcifer pardalis) are native to Madagascar and have established populations in Florida, USA, but standard correlative distribution modeling predicts no suitable habitat for F. pardalis there. We evaluated commonly collected thermal traits- thermal performance, tolerance, and preference-of F. pardalis and the acclimatization potential of these traits during exposure to naturally-occurring environmental conditions in North Central Florida. Though we observed temperature-dependent thermal performance, chameleons maintained similar thermal limits, performance, and preferences across seasons, despite long-term exposure to cool temperatures. Using the physiological data collected, we developed distribution models that varied in restriction: time-dependent exposure near and below critical thermal minima, predicted activity windows, and predicted performance thresholds. Our application of commonly collected physiological data improved interpretations on potential distributions of F. pardalis, compared with correlative distribution modeling approaches that predicted no suitable area in Florida. These straightforward approaches can be applied to other species with existing physiological data or after brief experiments on a limited number of individuals, as demonstrated here.

Dermatomycosis Caused by Paranannizziopsis australasiensis in Nonnative Panther Chameleons (Furcifer pardalis) Captured in Central Florida, USA.

Emergent fungal pathogens in herpetofauna are a concern in both wild and captive populations. We diagnosed dermatomycosis by Paranannizziopsis australasiensis in two panther chameleons (Furcifer pardalis) and suspected it in eight others captured from an established free-living nonnative population in Florida, USA. Chameleons developed skin lesions following recent exposure to cold weather conditions while housed in captivity, approximately 10 mo after capture and 12 wk after being placed in outdoor enclosures. Affected animals were treated with oral voriconazole and terbinafine until most cases resolved; however, medications were ultimately discontinued. Paranannizziopsis australasiensis has not previously been described in chameleons, nor in animals originating from a free-ranging population in the USA. Although the source of P. australasiensis infection is uncertain, we discuss several scenarios related to the pet trade and unique situation of chameleon "ranching" present in the USA.

Divergent Serpentoviruses in Free-Ranging Invasive Pythons and Native Colubrids in Southern Florida, United States.

Burmese python (Python bivittatus) is an invasive snake that has significantly affected ecosystems in southern Florida, United States. Aside from direct predation and competition, invasive species can also introduce nonnative pathogens that can adversely affect native species. The subfamily Serpentovirinae (order Nidovirales) is composed of positive-sense RNA viruses primarily found in reptiles. Some serpentoviruses, such as shingleback nidovirus, are associated with mortalities in wild populations, while others, including ball python nidovirus and green tree python nidovirus can be a major cause of disease and mortality in captive animals. To determine if serpentoviruses were present in invasive Burmese pythons in southern Florida, oral swabs were collected from both free-ranging and long-term captive snakes. Swabs were screened for the presence of serpentovirus by reverse transcription PCR and sequenced. A total serpentovirus prevalence of 27.8% was detected in 318 python samples. Of the initial swabs from 172 free-ranging pythons, 42 (24.4%) were positive for multiple divergent viral sequences comprising four clades across the sampling range. Both sex and snout-vent length were statistically significant factors in virus prevalence, with larger male snakes having the highest prevalence. Sampling location was statistically significant in circulating virus sequence. Mild clinical signs and lesions consistent with serpentovirus infection were observed in a subset of sampled pythons. Testing of native snakes (n = 219, 18 species) in part of the python range found no evidence of python virus spillover; however, five individual native snakes (2.3%) representing three species were PCR positive for unique, divergent serpentoviruses. Calculated pairwise uncorrected distance analysis indicated the newly discovered virus sequences likely represent three novel genera in the subfamily Serpentovirinae. This study is the first to characterize serpentovirus in wild free-ranging pythons or in any free-ranging North America reptile. Though the risk these viruses pose to the invasive and native species is unknown, the potential for spillover to native herpetofauna warrants further investigation.

Face-off: Novel depredation and nest defense behaviors between an invasive and a native predator in the Greater Everglades Ecosystem, Florida, USA.

We describe several photo-documented novel interactions between intraguild predators in southern Florida-the native bobcat (Lynx rufus) and the invasive Burmese python (Python bivittatus). Over several days we documented a bobcat's depredation of an unguarded python nest and subsequent python nest defense behavior following the return of both animals to the nest. This is the first documentation of any animal in Florida preying on python eggs, and the first evidence or description of such antagonistic interactions at a python nest.

Physiological effects of capture and short-term captivity in an invasive snake species, the Burmese python (Python bivittatus) in Florida.

It is important to evaluate the role of captivity as a potential stressor. An understanding of stress responses to capture and transition to captivity may inform the limitations of laboratory studies on wild animals, aid in understanding the consequences of introducing animals into captive environments, and help predict which species may be successful invasives. We investigated physiological effects of captivity by comparing at-capture blood variables in wild Burmese pythons (Python bivittatus) in Florida to pythons recently brought into captivity (1-109 days). We conducted an acute restraint test by collecting samples at baseline (immediately at handling) and one hour post-restraint across wild field-sampled (n = 19) and recently-captive (n = 33) pythons to evaluate fluctuations in plasma corticosterone, bacterial killing ability, antibody response, leukogram, and serpentovirus infection. We observed higher baseline plasma corticosterone and monocytes in recently captive compared to wild snakes, which both subsided in snakes held for a longer time in captivity, and a mild decrease in lymphocytes in the middle of the captivity period. Functional immunity and viral infection were not affected by captivity, and pythons maintained restraint-induced responses in corticosterone, heterophil to lymphocyte ratio, and monocyte counts throughout captivity. Prevalence for serpentovirus was 50%, though infection status was related to sampling date rather than captivity, indicating that viral infection may be seasonal. The history of Burmese python as a common captive animal for research and pet trade, as well as its general resilience to effects of capture and short-term captivity, may contribute to its invasion success in Florida.

The International Vertebrate Pet Trade Network and Insights from US Imports of Exotic Pets.

The international trade in exotic vertebrate pets provides key social and economic benefits but also drives associated ecological, ethical, and human health impacts. However, despite its clear importance, we currently lack a full understanding of the structure of the pet trade, hampering efforts to optimize its benefits while mitigating its negative effects. In the present article, we represent and review the structure of the pet trade as a network composed of different market actors (nodes) and trade flows (links). We identify key data gaps in this network that, if filled, would enable network analyses to pinpoint targets for management. As a case study of how data-informed networks can realize this goal, we quantified spatial and temporal patterns in pets imported to the United States. Our framework and case study illustrate how network approaches can help to inform and manage the effects of the growing demand for exotic pets.

A tale of two islands: evidence for impaired stress response and altered immune functions in an insular pit viper following ecological disturbance.

The frequency and intensity of ecological perturbations affecting wild animal populations is expected to increase in the future with animals facing numerous global threats. Seahorse Key is a continental island off mainland Florida that has historically been a major rookery for several species of waterbirds. As a result of an unknown disturbance, the entire rookery abandoned Seahorse Key in April 2015 and shifted nesting activities to nearby Snake Key, resulting in an influx of food resources in the form of fish carrion to resident Florida cottonmouth snakes (Agkistrodon conanti), while snakes on Seahorse Key experienced a drastic reduction in food resources. Our objective was to assess plasma corticosterone concentrations, corticosterone negative feedback using dexamethasone, blood glucose, body condition, packed cell volume, natural antibody agglutination, white blood cell counts and ratios and erythrocyte sedimentation rate to characterize the long-term effects of differential resource availability in these two snake populations 3 years after this major ecological disturbance. We collected blood samples at three time points from cottonmouths on Seahorse Key (n = 6 individuals) and Snake Key (n = 13 individuals) in fall 2018. In due consideration of the small sample size, our study shows evidence that 3 years after the shift in waterbird nesting Seahorse Key cottonmouths exhibit a dampened acute stress response and presumptive impaired innate immune functions relative to cottonmouths on Snake Key. These results highlight the context-dependent nature of biomarkers and implicate the significant decrease in food resources on Seahorse Key in altering hormonal stress responses and innate immune functions, possibly leading to unknown long-term downstream effects. This study assessed the response of a wild population of pit viper to ecological disturbance in situ with the aim to improve our understanding of how animals cope with such perturbations and improve our capacity to make informed decisions for conservation.

Host-specific phenotypic variation of a parasite co-introduced with invasive Burmese pythons.

Invasive Burmese pythons (Python bivittatus Kuhl, 1820) have introduced a lung parasite, Raillietiella orientalis, (Hett, 1915) from the python's native range in Southeast Asia to its introduced range in Florida, where parasite spillover from pythons to two families and eight genera of native snakes has occurred. Because these novel host species present a diversity of ecological and morphological traits, and because these parasites attach to their hosts with hooks located on their cephalothorax, we predicted that R. orientalis would exhibit substantial, host-associated phenotypic plasticity in cephalothorax shape. Indeed, geometric morphometric analyses of 39 parasites from five host species revealed significant variation among host taxa in R. orientalis cephalothorax shape. We observed differences associated with host ecology, where parasites from semi-aquatic and aquatic snakes exhibited the greatest morphological similarity. Morphological analyses of R. orientalis recovered from invasive pythons, native pit vipers, and terrestrial snakes each revealed distinct shapes. Our results suggest R. orientalis can exhibit significant differences in morphology based upon host species infected, and this plasticity may facilitate infection with this non-native parasite in a wide array of novel squamate host species.

Parasite spillover: indirect effects of invasive Burmese pythons.

Identification of the origin of parasites of nonindigenous species (NIS) can be complex. NIS may introduce parasites from their native range and acquire parasites from within their invaded range. Determination of whether parasites are non-native or native can be complicated when parasite genera occur within both the NIS' native range and its introduced range. We explored potential for spillover and spillback of lung parasites infecting Burmese pythons (Python bivittatus) in their invasive range (Florida). We collected 498 indigenous snakes of 26 species and 805 Burmese pythons during 2004-2016 and examined them for lung parasites. We used morphology to identify three genera of pentastome parasites, Raillietiella, a cosmopolitan form, and Porocephalus and Kiricephalus, both New World forms. We sequenced these parasites at one mitochondrial and one nuclear locus and showed that each genus is represented by a single species, R. orientalis, P. crotali, and K. coarctatus. Pythons are host to R. orientalis and P. crotali, but not K. coarctatus; native snakes are host to all three species. Sequence data show that pythons introduced R. orientalis to North America, where this parasite now infects native snakes. Additionally, our data suggest that pythons are competent hosts to P. crotali, a widespread parasite native to North and South America that was previously hypothesized to infect only viperid snakes. Our results indicate invasive Burmese pythons have affected parasite-host dynamics of native snakes in ways that are consistent with parasite spillover and demonstrate the potential for indirect effects during invasions. Additionally, we show that pythons have acquired a parasite native to their introduced range, which is the initial condition necessary for parasite spillback.

Reduced innate immunity of Cuban Treefrogs at leading edge of range expansion.

During geographic range expansion, populations of non-indigenous species at the invasion front may benefit from directing resources away from immune defense. To test this hypothesis, we investigated the strength of two innate immune components in populations of invasive Cuban Treefrogs (Osteopilus septentrionalis) in a long-colonized area (core region) and at the invasion front (leading-edge region). First, we compared the region-specific metabolic response of frogs injected with an endotoxin that induces systemic inflammation (lipopolysaccharide, LPS) to sham-injected control frogs pooled from both regions. Males and females were analyzed independently because we detected a sex-related difference in mass-independent metabolism of control frogs, with males exhibiting a significantly higher metabolic rate (F1, 21  = 29.02, P < 0.001) than females. We observed a significantly higher metabolic rate in LPS-injected core frogs compared with control frogs for both males (P = 0.041) and females (P = 0.007). Conversely, in leading-edge populations, there was no significant difference in the metabolic rate of LPS-injected and control frogs (males, P  = 0.195; females, P  = 0.132). Second, we directly compared bacterial killing ability of frog blood plasma between regions. Bactericidal ability of plasma was significantly greater in frogs from the core region in comparison with those at the leading edge (F1, 26   = 28.67, P < 0.001). For both immune components that we examined, populations from the core exhibited stronger immune responses. Our findings support hypotheses predicting an inverse relationship between immunity and range expansion.

Integrating invasion and disease in the risk assessment of live bird trade.

AIM: International trade in plants and animals generates significant economic benefits. It also leads to substantial unintended impacts when introduced species become invasive, causing environmental disturbance or transmitting diseases that affect people, livestock, other wildlife or the environment. Policy responses are usually only implemented after these species become established and damages are already incurred. International agreements to control trade are likewise usually based on selection of species with known impacts. We aim to further develop quantitative invasive species risk assessment for bird imports and extend the tool to explicitly address disease threats. LOCATION: United States of America. METHODS: We use a two-step approach for rapid risk assessment based on the expected biological risks due to both the environmental and health impact of a potentially invasive wildlife species in trade. We assess establishment probability based on a model informed by historical observations and then construct a model of emerging infectious disease threat based on economic and ecological characteristics of the exporting country. RESULTS: We illustrate how our rapid assessment tool can be used to identify high-priority species for regulation based on a combination of the threat they pose for becoming established and vectoring emerging infectious diseases. MAIN CONCLUSIONS: Our approach can be executed for a species in a matter of days and is nested in an economic decision-making framework for determining whether the biological risk is justified by trade benefits.

Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park.

Invasive species represent a significant threat to global biodiversity and a substantial economic burden. Burmese pythons, giant constricting snakes native to Asia, now are found throughout much of southern Florida, including all of Everglades National Park (ENP). Pythons have increased dramatically in both abundance and geographic range since 2000 and consume a wide variety of mammals and birds. Here we report severe apparent declines in mammal populations that coincide temporally and spatially with the proliferation of pythons in ENP. Before 2000, mammals were encountered frequently during nocturnal road surveys within ENP. In contrast, road surveys totaling 56,971 km from 2003-2011 documented a 99.3% decrease in the frequency of raccoon observations, decreases of 98.9% and 87.5% for opossum and bobcat observations, respectively, and failed to detect rabbits. Road surveys also revealed that these species are more common in areas where pythons have been discovered only recently and are most abundant outside the python's current introduced range. These findings suggest that predation by pythons has resulted in dramatic declines in mammals within ENP and that introduced apex predators, such as giant constrictors, can exert significant top-down pressure on prey populations. Severe declines in easily observed and/or common mammals, such as raccoons and bobcats, bode poorly for species of conservation concern, which often are more difficult to sample and occur at lower densities.

Contribution of the live-vertebrate trade toward taxonomic homogenization.

The process of taxonomic homogenization occurs through two mechanisms, extinctions and introductions, and leads to a reduction of global biodiversity. We used available U.S. trade data as a proxy for global trade in live vertebrates to assess the contribution of trade to the process of taxonomic homogenization. Data included all available U.S. importation and exportation records, estimation of extinction risk, and reports of establishment outside the native range for species within six vertebrate groups. Based on Monte Carlo sampling, the number of species traded, established outside of the native range, and threatened with extinction was not randomly distributed among vertebrate families. Twenty-eight percent of vertebrate families that were traded preferentially were also established or threatened with extinction, an unusually high percentage compared with the 7% of families that were not traded preferentially but that became established or threatened with extinction. The importance of trade in homogenization of vertebrates suggests that additional efforts should be made to prevent introductions and extinctions through this medium.