Vulnerability of Southern Hemisphere bats to white-nose syndrome based on global analysis of fungal host specificity and cave temperatures.

White-nose syndrome (WNS), a disease affecting hibernating bats, is caused by the fungal pathogen Pseudogymnoascus destructans (Pd). Since the initial introduction of Pd from Eurasia to the United States in 2006, WNS has killed millions of bats throughout the temperate parts of North America. There is concern that if Pd is accidentally introduced to the Southern Hemisphere, WNS could pose similar threats to the bat fauna of the Southern Hemisphere's more temperate regions. Efforts are required to better understand the vulnerability of bats globally to WNS. We examined phylogenetic distances among cave roosting bat species globally to estimate the probability of infection by Pd. We predicted cave thermal suitability for Pd for 441 cave-roosting bat species across the globe via spatial analysis. We used host specificity models based on 65 species tested for Pd to determine phylogenetic specificity of Pd. Phylogenetic distance was not an important predictor of Pd infection, confirming that Pd has low host specificity. We found extensive areas (i.e., South America, Africa, and Australia) in the Southern Hemisphere with caves that were suitable for cave-roosting bat species and for Pd growth. Hence, if Pd spreads to the Southern Hemisphere, the risk of exposure is widespread for cave-roosting bats, and infection is possible regardless of relatedness to infected species in the Northern Hemisphere. Predicting the consequences of infection remains difficult due to lack of species-specific information about bat winter biology. Nevertheless, WNS is an important threat to naive Southern Hemisphere bat populations. Hence, biosecurity measures and planning of management responses that can help prevent or minimize a potential WNS outbreak in the Southern Hemisphere are urgently needed.

Vulnerabilidad de los murciélagos del hemisferio sur ante el síndrome de nariz blanca con base en el análisis mundial de especificidad del hospedero fúngico y las temperaturas de las cuevas Resumen El síndrome de nariz blanca (SNB), una enfermedad que afecta a los murciélagos en hibernación es causado por el hongo patógeno Pseudogymnoascus destructans (Pd). Desde la introducción inicial del Pd desde Eurasia a Estados Unidos en 2006, el SNB ha matado a millones de murciélagos en las zonas templadas de Norteamérica. Existe la preocupación de que, si el Pd se introduce por accidente en el hemisferio sur, el SNB podría amenazar de forma similar a los murciélagos en las regiones más templadas de este hemisferio. Se requieren esfuerzos para comprender mejor la vulnerabilidad de los murciélagos ante el SNB a nivel mundial. Analizamos las distancias filogenéticas entre las especies de murciélagos de cuevas de todo el mundo para estimar la probabilidad de infección por Pd. Mediante un análisis espacial, predijimos la idoneidad térmica de las cuevas para el Pd en 441 especies de murciélagos de todo el mundo. Usamos modelos de especificidad de hospedero basados en 65 especies analizadas para determinar la especificidad filogenética de Pd. La distancia filogenética no fue un factor predictivo importante de la infección por Pd, lo que confirma que la especificidad de hospedero de Pd es baja. En el hemisferio sur encontramos amplias zonas (América del Sur, África y Australia) con cuevas adecuadas para especies de murciélagos que se refugian en cuevas y para el crecimiento de Pd. Por lo tanto, si Pd se propaga en el hemisferio sur, el riesgo de exposición es generalizado para los murciélagos que pernoctan en cuevas, y la infección es posible independientemente del parentesco con especies infectadas en el hemisferio norte. Sigue siendo difícil predecir las consecuencias de la infección debido a la falta de información específica sobre la biología invernal de los murciélagos. No obstante, el SNB es una amenaza importante para las poblaciones de murciélagos del hemisferio sur que no están preparadas para enfrentarla. Por ello se necesiten medidas urgentes de bioseguridad y planificación de respuestas de gestión que puedan ayudar a prevenir o minimizar un posible brote del SNB en el hemisferio sur.

Savviness of prey to introduced predators.

The prey naivety hypothesis posits that prey are vulnerable to introduced predators because many generations in slow gradual coevolution are needed for appropriate avoidance responses to develop. It predicts that prey will be more responsive to native than introduced predators and less responsive to introduced predators that differ substantially from native predators and from those newly established. To test these predictions, we conducted a global meta-analysis of studies that measured the wariness responses of small mammals to the scent of sympatric mammalian mesopredators. We identified 26 studies that met our selection criteria. These studies comprised 134 experiments reporting on the responses of 36 small mammal species to the scent of six introduced mesopredators and 12 native mesopredators. For each introduced mesopredator, we measured their phylogenetic and functional distance to local native mesopredators and the number of years sympatric with their prey. We used predator and prey body mass as a measure of predation risk. Globally, small mammals were similarly wary of the scent of native and introduced mesopredators; phylogenetic and functional distance between introduced mesopredators and closest native mesopredators had no effect on wariness; and wariness was unrelated to the number of prey generations, or years, since first contact with introduced mesopredators. Small mammal wariness was associated with predator-prey body mass ratio, regardless of the nativity. The one thing animals do not seem to recognize is whether their predators are native.

La hipótesis de la ingenuidad de la presa plantea que ésta es vulnerable a los depredadores introducidos porque se requiere que muchas generaciones atraviesen una coevolución lenta y gradual para que se desarrollen las respuestas de evasión adecuadas. La hipótesis supone que la presa será más sensible a los depredadores introducidos que difieren notoriamente de los nativos y de aquellos recién establecidos. Realizamos un metaanálisis global de estudios que midieron las respuestas cautelosas de mamíferos pequeños ante el rastro de meso depredadores simpátricos para probar estas suposiciones. Identificamos 26 estudios que cumplieron con nuestro criterio de selección. Estos estudios estuvieron conformados por 134 experimentos que reportaban las respuestas de 36 especies de mamíferos pequeños ante el rastro de seis meso depredadores introducidos y 12 nativos. Medimos la distancia funcional y filogenética entre cada meso depredador introducido y los meso depredadores locales nativos y el número de años simpátricos con su presa. Usamos la masa corporal del depredador y la presa como medida del riesgo de depredación. A nivel mundial, los mamíferos pequeños compartieron la cautela ante el rastro de los meso depredadores nativos e introducidos; la distancia funcional y la filogenética entre los meso depredadores introducidos y el meso depredador nativo más cercano no tuvieron efecto sobre la cautela; y la cautela no estuvo relacionada con el número de generaciones de la presa, o años, desde el primer contacto con los meso depredadores introducidos. La cautela de los mamíferos pequeños estuvo asociada con las proporciones de masa corporal entre el depredador y la presa, sin importar el origen. Lo único que los animales parecen no reconocer es si el depredador es nativo o no.

Restoring vertebrate predator populations can provide landscape-scale biological control of established invasive vertebrates: Insights from pine marten recovery in Europe.

Invasive species pose one of the greatest global threats to biodiversity. There has been a long history of importing coevolved natural enemies to act as biological control agents to try to suppress densities of invasive species, with historically limited success and frequent adverse impacts on native biodiversity. Our understanding of the processes and drivers of successful biological control has been focussed on invertebrates and is evidently limited and potentially ill-suited with respect to biological control of vertebrate populations. The restoration of native vertebrate predator populations provides a promising nature-based solution for slowing, halting, or even reversing the spread of some invasive vertebrates over spatial scales relevant to the management of wildlife populations. Here, we first review the growing literature and data from the pine marten-red and grey squirrel system in Europe. We synthesise a multi-decadal dataset to show that the recovery of a native predator has resulted in rapid, landscape-scale declines of an established invasive species. We then use the model system, predator-prey interaction theory, and examples from the literature to develop ecological theory relating to natural biological control in vertebrates and evolutionary processes in native-invasive predator-prey interactions. We find support for the hypotheses that evolutionary naivety of invasive species to native predators and lack of local refuges results in higher predation of naive compared to coevolved prey. We apply lessons learnt from the marten-squirrel model system to examine the plausibility of specific native predator solutions to some of the Earth's most devastating invasive vertebrates. Given the evidence, we conclude that depletion of vertebrate predator populations has increased ecosystem vulnerability to invasions and thus facilitated the spread of invasive species. Therefore, restoration of vertebrate predator populations is an underappreciated, fundamental, nature-based solution to the crisis of invasive species and should be a priority for vertebrate invasive species management globally.

The perils of paradise: an endangered species conserved on an island loses antipredator behaviours within 13 generations.

When imperilled by a threatening process, the choice is often made to conserve threatened species on offshore islands that typically lack the full suite of mainland predators. While keeping the species extant, this releases the conserved population from predator-driven natural selection. Antipredator traits are no longer maintained by natural selection and may be lost. It is implicitly assumed that such trait loss will happen slowly, but there are few empirical tests. In Australia, northern quolls (Dasyurus hallucatus) were moved onto a predator-free offshore island in 2003 to protect the species from the arrival of invasive cane toads on the mainland. We compared the antipredator behaviours of wild-caught quolls from the predator-rich mainland with those from this predator-free island. We compared the responses of both wild-caught animals and their captive-born offspring, to olfactory cues of two of their major predators (feral cats and dingoes). Wild-caught, mainland quolls recognized and avoided predator scents, as did their captive-born offspring. Island quolls, isolated from these predators for only 13 generations, showed no recognition or aversion to these predators. This study suggests that predator aversion behaviours can be lost very rapidly, and that this may make a population unsuitable for reintroduction to a predator-rich mainland.

Does despotic behavior or food search explain the occurrence of problem brown bears in Europe?

Bears foraging near human developments are often presumed to be responding to food shortage, but this explanation ignores social factors, in particular despotism in bears. We analyzed the age distribution and body condition index (BCI) of shot brown bears in relation to densities of bears and people, and whether the shot bears were killed by managers (i.e., problem bears; n = 149), in self-defense (n = 51), or were hunter-killed nonproblem bears (n = 1,896) during 1990-2010. We compared patterns between areas with (Slovenia) and without supplemental feeding (Sweden) of bears relative to 2 hypotheses. The food-search/food-competition hypothesis predicts that problem bears should have a higher BCI (e.g., exploiting easily accessible and/or nutritious human-derived foods) or lower BCI (e.g., because of food shortage) than nonproblem bears, that BCI and human density should have a positive correlation, and problem bear occurrence and seasonal mean BCI of nonproblem bears should have a negative correlation (i.e., more problem bears during years of low food availability). Food competition among bears additionally predicts an inverse relationship between BCI and bear density. The safety-search/naivety hypothesis (i.e., avoiding other bears or lack of human experience) predicts no relationship between BCI and human density, provided no dietary differences due to spatiotemporal habitat use among bears, no relationship between problem bear occurrence and seasonal mean BCI of nonproblem bears, and does not necessarily predict a difference between BCI for problem/nonproblem bears. If food competition or predation avoidance explained bear occurrence near settlements, we predicted younger problem than nonproblem bears and a negative correlation between age and human density. However, if only food search explained bear occurrence near settlements, we predicted no relation between age and problem or nonproblem bear status, or between age and human density. We found no difference in BCI or its variability between problem and nonproblem bears, no relation between BCI and human density, and no correlation between numbers of problem bears shot and seasonal mean BCI for either country. The peak of shot problem bears occurred from April to June in Slovenia and in June in Sweden (i.e., during the mating period when most intraspecific predation occurs and before fall hyperphagia). Problem bears were younger than nonproblem bears, and both problem and nonproblem bears were younger in areas of higher human density. These age differences, in combination with similarities in BCI between problem and nonproblem bears and lack of correlation between BCI and human density, suggested safety-search and naïve dispersal to be the primary mechanisms responsible for bear occurrence near settlements. Younger bears are less competitive, more vulnerable to intraspecific predation, and lack human experience, compared to adults. Body condition was inversely related to the bear density index in Sweden, whereas we found no correlation in Slovenia, suggesting that supplemental feeding may have reduced food competition, in combination with high bear harvest rates. Bears shot in self-defense were older and their BCI did not differ from that of nonproblem bears. Reasons other than food shortage apparently explained why most bears were involved in encounters with people or viewed as problematic near settlements in our study.

Phenotypic and Transcriptomic Analysis Revealed a Lack of Risk Perception by Native Tadpoles Toward Novel Non-Native Fish.

The introduction of alien species poses a serious threat to native biodiversity, and mountain lake systems in the southwest of China are particularly vulnerable to the introduction of non-native fish. The prey naivety hypothesis states that native species may not be able to recognize novel introduced species due to a lack of common evolutionary background and therefore become easy targets, so the impacts of non-native fish on mountain endemic amphibians need to be urgently assessed. In an ex-situ experiment, we exposed the tadpoles of the Chaochiao Brown Frog (Rana chaochiaoensis), endemic to western China, to kairomones of both native and translocated fish species, and their phenotypic and genetic response patterns were compared. The results revealed significant phenotypic plasticity responses in total length (TOL), tail length (TL), and tail muscle width (TW) of tadpoles induced by native fish kairomone, while tadpoles exposed to translocated fish kairomone exhibited weaker phenotypic changes. At the transcriptional level, the number of differently expressed genes (DEGs) in the native fish treatment was 3.1-fold (liver) and 52.6-fold (tail muscle) higher than in the translocated fish treatment, respectively. There were more unique DEGs in the native fish treatment, primarily enriched in terms and pathways related to stress response, energy metabolism, and muscle development. The study revealed a lack of risk perception by native tadpoles toward novel non-native fish, providing new evidence for the prey naivety hypothesis from both phenotypic and molecular perspectives. Future conservation efforts should prioritize assessing the impacts of non-native fish on alpine and subalpine threatened and narrowly distributed amphibians. Additionally, prevention, early warning, monitoring, and removal of non-native fish should be carried out as soon as possible.

Relaxed predation theory: size, sex and brains matter.

Australia's wildlife is being considerably impacted by introduced mammalian predators such as cats (Felis catus), dogs (Canis lupus familiaris), and foxes (Vulpes vulpes). This is often attributed to native wildlife being naïve to these introduced predators. A systematic review of the literature reveals that native metatherians (body mass range 0.02-25 kg) do not recognise, and show relaxed antipredator behaviours towards, native and some introduced mammalian predators. Native eutherians (all with body mass < 2 kg), however, do appear to recognise and exhibit antipredator behaviours towards both native and introduced predators. Based on our findings, we propose a novel theory, the 'Relaxed Predation Theory'. Our new theory is based on the absence of large mammalian predators leading to reduced predation pressure in Australia during the past 40000-50000 years, and on three key differences between Australian metatherians and eutherians: size, sex, and brains. In light of this Relaxed Predation Theory, we make a number of recommendations for the conservation of Australian wildlife: (i) predator avoidance training of suitable species; (ii) exclusion fencing to exclude some, but not all, predators to facilitate the development of antipredator behaviours; (iii) captive breeding programs to prevent the extinction of some species; and (iv) reintroduction of Australia's larger predators, potentially to compete with and displace introduced predators. A more detailed understanding of the responses of Australian mammals to predators will hopefully contribute to the improved conservation of susceptible species.

Trophic cascade driven by behavioral fine-tuning as naïve prey rapidly adjust to a novel predator.

The arrival of novel predators can trigger trophic cascades driven by shifts in prey numbers. Predators also elicit behavioral change in prey populations, via phenotypic plasticity and/or rapid evolution, and such changes may also contribute to trophic cascades. Here, we document rapid demographic and behavioral changes in populations of a prey species (grassland melomys Melomys burtoni, a granivorous rodent) following the introduction of a novel marsupial predator (northern quoll Dasyurus hallucatus). Within months of quolls appearing, populations of melomys exhibited reduced survival and population declines relative to control populations. Quoll-invaded populations were also significantly shyer than nearby, quoll-free populations of conspecifics. This rapid but generalized response to a novel threat was replaced over the following 2 yr with more threat-specific antipredator behaviors (i.e., predator-scent aversion). Predator-exposed populations, however, remained more neophobic than predator-free populations throughout the study. These behavioral responses manifested rapidly in changed rates of seed predation by melomys across treatments. Quoll-invaded melomys populations exhibited lower per-capita seed take rates, and rapidly developed an avoidance of seeds associated with quoll scent, with discrimination playing out over a spatial scale of tens of meters. Presumably the significant and novel predation pressure induced by quolls drove melomys populations to fine-tune behavioral responses to be more predator specific through time. These behavioral shifts could reflect individual plasticity (phenotypic flexibility) in behavior or may be adaptive shifts from natural selection imposed by quoll predation. Our study provides a rare insight into the rapid ecological and behavioral shifts enacted by prey to mitigate the impacts of a novel predator and shows that trophic cascades can be strongly influenced by behavioral as well as numerical responses.

Effects of historically familiar and novel predator odors on the physiology of an introduced prey.

Predator odors can elicit fear responses in prey and predator odor recognition is generally associated with physiological responses. Prey species are often more likely to respond to the odor of familiar rather than alien predators. However, predator naïvety in an introduced prey species has rarely been investigated. We examined the physiological response, as shown by changes in ventilatory variables, of an introduced terrestrial herbivore, the European rabbit Oryctolagus cuniculus, in Australia, to the odor of potential predators and to control odors (distilled water and horse), to explore if responses were limited to historical (cat and fox) predators, or extended to historically novel predators (snake and quoll). All odors except distilled water elicited a response, with rabbits showing long-term higher respiratory frequencies and lower tidal volumes after introduction of the odors, indicating an increase in alertness. However, the intensity of the rabbits' reaction could not be directly linked to any pattern of response with respect to the history of predator-prey relationships. Rabbits exhibited significantly stronger reactions in response to both cat and quoll odors than they did to distilled water, but responses to horse, fox, and snake odor were similar to that of water. Our results show that the introduced rabbit can respond to both historical and novel predators in Australia, and suggest that shared evolutionary history is not necessarily a prerequisite to predator odor recognition.

Phantoms of the forest: legacy risk effects of a regionally extinct large carnivore.

The increased abundance of large carnivores in Europe is a conservation success, but the impact on the behavior and population dynamics of prey species is generally unknown. In Europe, the recolonization of large carnivores often occurs in areas where humans have greatly modified the landscape through forestry or agriculture. Currently, we poorly understand the effects of recolonizing large carnivores on extant prey species in anthropogenic landscapes. Here, we investigated if ungulate prey species showed innate responses to the scent of a regionally exterminated but native large carnivore, and whether the responses were affected by human-induced habitat openness. We experimentally introduced brown bear Ursus arctos scent to artificial feeding sites and used camera traps to document the responses of three sympatric ungulate species. In addition to controls without scent, reindeer scent Rangifer tarandus was used as a noncarnivore, novel control scent. Fallow deer Dama dama strongly avoided areas with bear scent. In the presence of bear scent, all ungulate species generally used open sites more than closed sites, whereas the opposite was observed at sites with reindeer scent or without scent. The opening of forest habitat by human practices, such as forestry and agriculture, creates a larger gradient in habitat openness than available in relatively unaffected closed forest systems, which may create opportunities for prey to alter their habitat selection and reduce predation risk in human-modified systems that do not exist in more natural forest systems. Increased knowledge about antipredator responses in areas subjected to anthropogenic change is important because these responses may affect prey population dynamics, lower trophic levels, and attitudes toward large carnivores. These aspects may be of particular relevance in the light of the increasing wildlife populations across much of Europe.

Naïve prey exhibit reduced antipredator behavior and survivorship.

Prey naiveté has been hypothesized to be one of the major driving forces behind population declines following the introduction of novel predators or release of inexperienced prey into predator rich environments. In these cases, naïve prey may lack sufficient antipredator behavior and, as a result, suffer increased mortality. Despite this, some evidence suggests that many prey utilize a generalized response to predators. Here, the naiveté hypothesis is tested using a predator-prey pair sharing an evolutionary history: the red swamp crayfish (Procambarus clarkii Girard, 1852) and largemouth bass (Micropterus salmoides Lacépède, 1802). Using farm-reared, naïve crayfish and wild-caught, experienced individuals, laboratory experiments demonstrated that naïve, farmed crayfish lack behavioral responses to chemical cues from bass, both in terms of movement and use of structural refuge. In contrast, experienced crayfish responded strongly to the same cues. In a subsequent field tethering experiment, these naïve individuals suffered a three-fold increase in predation rate. Based on these results, recognition of predators may not be innate in all prey, and previous experience and learning likely play a key role in the development of antipredator behavior.