Population genomics of a predatory mammal reveals patterns of decline and impacts of exposure to toxic toads.

Mammal declines across northern Australia are one of the major biodiversity loss events occurring globally. There has been no regional assessment of the implications of these species declines for genomic diversity. To address this, we conducted a species-wide assessment of genomic diversity in the northern quoll (Dasyurus hallucatus), an Endangered marsupial carnivore. We used next generation sequencing methods to genotype 10,191 single nucleotide polymorphisms (SNPs) in 352 individuals from across a 3220-km length of the continent, investigating patterns of population genomic structure and diversity, and identifying loci showing signals of putative selection. We found strong heterogeneity in the distribution of genomic diversity across the continent, characterized by (i) biogeographical barriers driving hierarchical population structure through long-term isolation, and (ii) severe reductions in diversity resulting from population declines, exacerbated by the spread of introduced toxic cane toads (Rhinella marina). These results warn of a large ongoing loss of genomic diversity and associated adaptive capacity as mammals decline across northern Australia. Encouragingly, populations of the northern quoll established on toad-free islands by translocations appear to have maintained most of the initial genomic diversity after 16 years. By mapping patterns of genomic diversity within and among populations, and investigating these patterns in the context of population declines, we can provide conservation managers with data critical to informed decision-making. This includes the identification of populations that are candidates for genetic management, the importance of remnant island and insurance/translocated populations for the conservation of genetic diversity, and the characterization of putative evolutionarily significant units.

Fire as a driver and mediator of predator-prey interactions.

Both fire and predators have strong influences on the population dynamics and behaviour of animals, and the effects of predators may either be strengthened or weakened by fire. However, knowledge of how fire drives or mediates predator-prey interactions is fragmented and has not been synthesised. Here, we review and synthesise knowledge of how fire influences predator and prey behaviour and interactions. We develop a conceptual model based on predator-prey theory and empirical examples to address four key questions: (i) how and why do predators respond to fire; (ii) how and why does prey vulnerability change post-fire; (iii) what mechanisms do prey use to reduce predation risk post-fire; and (iv) what are the outcomes of predator-fire interactions for prey populations? We then discuss these findings in the context of wildlife conservation and ecosystem management before outlining priorities for future research. Fire-induced changes in vegetation structure, resource availability, and animal behaviour influence predator-prey encounter rates, the amount of time prey are vulnerable during an encounter, and the conditional probability of prey death given an encounter. How a predator responds to fire depends on fire characteristics (e.g. season, severity), their hunting behaviour (ambush or pursuit predator), movement behaviour, territoriality, and intra-guild dynamics. Prey species that rely on habitat structure for avoiding predation often experience increased predation rates and lower survival in recently burnt areas. By contrast, some prey species benefit from the opening up of habitat after fire because it makes it easier to detect predators and to modify their behaviour appropriately. Reduced prey body condition after fire can increase predation risk either through impaired ability to escape predators, or increased need to forage in risky areas due to being energetically stressed. To reduce risk of predation in the post-fire environment, prey may change their habitat use, increase sheltering behaviour, change their movement behaviour, or use camouflage through cryptic colouring and background matching. Field experiments and population viability modelling show instances where fire either amplifies or does not amplify the impacts of predators on prey populations, and vice versa. In some instances, intense and sustained post-fire predation may lead to local extinctions of prey populations. Human disruption of fire regimes is impacting faunal communities, with consequences for predator and prey behaviour and population dynamics. Key areas for future research include: capturing data continuously before, during and after fires; teasing out the relative importance of changes in visibility and shelter availability in different contexts; documenting changes in acoustic and olfactory cues for both predators and prey; addressing taxonomic and geographic biases in the literature; and predicting and testing how changes in fire-regime characteristics reshape predator-prey interactions. Understanding and managing the consequences for predator-prey communities will be critical for effective ecosystem management and species conservation in this era of global change.

Animal mortality during fire.

Earth's rapidly warming climate is propelling us towards an increasingly fire-prone future. Currently, knowledge of the extent and characteristics of animal mortality rates during fire remains rudimentary, hindering our ability to predict how animal populations may be impacted in the future. To address this knowledge gap, we conducted a global systematic review of the direct effects of fire on animal mortality rates, based on studies that unequivocally determined the fate of animals during fire. From 31 studies spanning 1984-2020, we extracted data on the direct impacts of fire on the mortality of 31 species from 23 families. From these studies, there were 43 instances where direct effects were measured by reporting animal survival from pre- to post-fire. Most studies were conducted in North America (52%) and Oceania (42%), focused largely on mammals (53%) and reptiles (30%), and reported mostly on animal survival in planned (82%) and/or low severity (70%) fires. We found no studies from Asia, Europe or South America. Although there were insufficient data to conduct a formal meta-analysis, we tested the effect of fire type, fire severity, fire regime, animal body mass, ecological attributes and class on survival. Only fire severity affected animal mortality, with a higher proportion of animals being killed by high than low severity fires. Recent catastrophic fires across the globe have drawn attention to the plight of animals exposed to wildfire. Yet, our systematic review suggests that a relatively low proportion of animals (mean predicted mortality [95% CI] = 3% [1%-9%]) are killed during fire. However, our review also underscores how little we currently know about the direct effects of fire on animal mortality, and highlights the critical need to understand the effects of high severity fire on animal populations.

Welcome to the Pyrocene: Animal survival in the age of megafire.

Planet Earth is entering the age of megafire, pushing ecosystems to their limits and beyond. While fire causes mortality of animals across vast portions of the globe, scientists are only beginning to consider fire as an evolutionary force in animal ecology. Here, we generate a series of hypotheses regarding animal responses to fire by adopting insights from the predator-prey literature. Fire is a lethal threat; thus, there is likely strong selection for animals to recognize the olfactory, auditory, and visual cues of fire, and deploy fire avoidance behaviours that maximize survival probability. If fire defences are costly, it follows that intraspecific variation in fire avoidance behaviours should correspond with variation in fire behaviour and regimes. Species and populations inhabiting ecosystems that rarely experience fire may lack these traits, placing 'fire naive' populations and species at enhanced extinction risk as the distribution of fire extends into new ecosystem types. We outline a research agenda to understand behavioural responses to fire and to identify conservation interventions that could be used to overcome fire naivety.

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.

Slow life history leaves endangered snake vulnerable to illegal collecting.

Global wildlife trade is a multibillion-dollar industry and a significant driver of vertebrate extinction risk. Yet, few studies have quantified the impact of wild harvesting for the illicit pet trade on populations. Long-lived species, by virtue of their slow life history characteristics, may be unable to sustain even low levels of collecting. Here, we assessed the impact of illegal collecting on populations of endangered broad-headed snakes (Hoplocephalus bungaroides) at gated (protected) and ungated (unprotected) sites. Because broad-headed snakes are long-lived, grow slowly and reproduce infrequently, populations are likely vulnerable to increases in adult mortality. Long-term data revealed that annual survival rates of snakes were significantly lower in the ungated population than the gated population, consistent with the hypothesis of human removal of snakes for the pet trade. Population viability analysis showed that the ungated population has a strongly negative population growth rate and is only prevented from ultimate extinction by dispersal of small numbers of individuals from the gated population. Sensitivity analyses showed that the removal of a small number of adult females was sufficient to impose negative population growth and suggests that threatened species with slow life histories are likely to be especially vulnerable to illegal collecting.

Effects of learning and adaptation on population viability.

Cultural adaptation is one means by which conservationists may help populations adapt to threats. A learned behavior may protect an individual from a threat, and the behavior can be transmitted horizontally (within generations) and vertically (between generations), rapidly conferring population-level protection. Although possible in theory, it remains unclear whether such manipulations work in a conservation setting; what conditions are required for them to work; and how they might affect the evolutionary process. We examined models in which a population can adapt through both genetic and cultural mechanisms. Our work was motivated by the invasion of highly toxic cane toads (Rhinella marina) across northern Australia and the resultant declines of endangered northern quolls (Dasyurus hallucatus), which attack and are fatally poisoned by the toxic toads. We examined whether a novel management strategy in which wild quolls are trained to avoid toads can reduce extinction probability. We used a simulation model tailored to quoll life history. Within simulations, individuals were trained and a continuous evolving trait determined innate tendency to attack toads. We applied this model in a population viability setting. The strategy reduced extinction probability only when heritability of innate aversion was low (<20%) and when trained mothers trained >70% of their young to avoid toads. When these conditions were met, genetic adaptation was slower, but rapid cultural adaptation kept the population extant while genetic adaptation was completed. To gain insight into the evolutionary dynamics (in which we saw a transitory peak in cultural adaptation over time), we also developed a simple analytical model of evolutionary dynamics. This model showed that the strength of natural selection declined as the cultural transmission rate increased and that adaptation proceeded only when the rate of cultural transmission was below a critical value determined by the relative levels of protection conferred by genetic versus cultural mechanisms. Together, our models showed that cultural adaptation can play a powerful role in preventing extinction, but that rates of cultural transmission need to be high for this to occur.

La adaptación cultural es un medio mediante el cual los conservacionistas pueden ayudar a las poblaciones a adaptarse a las amenazas. Un comportamiento aprendido puede proteger a un individuo de las amenazas y este comportamiento puede transmitirse horizontalmente (dentro de las generaciones) y verticalmente (entre generaciones), lo que otorga rápidamente una protección a nivel poblacional. Aunque esto es posible en teoría, aún no está claro si dichas manipulaciones funcionan dentro de un escenario de conservación; cuáles son las condiciones requeridas para que funcionen las manipulaciones; y cómo pueden afectar el proceso evolutivo. Examinamos modelos en los cuales una población puede adaptarse tanto con mecanismos genéticos como culturales. Nuestro trabajo estuvo motivado por la invasión de sapos altamente tóxicos (Rhinella marina) en todo el norte de Australia y las declinaciones resultantes de cuoles norteños (Dasyurus hallucatus), los cuales atacan y mueren envenenados por los sapos tóxicos. Analizamos si una estrategia de manejo novedoso en la cual los cuoles silvestres son entrenados para evitar a los sapos puede reducir la probabilidad de extinción. Usamos un modelo de simulación diseñado alrededor de la historia de vida de los cuoles. Dentro de las simulaciones, se entrenó a cuoles individuales y una característica en continua evolución determinó la tendencia innata para atacar a los sapos. Aplicamos este modelo en un escenario de viabilidad poblacional. La estrategia redujo la probabilidad de extinción sólo cuando la heredabilidad de la aversión innata fue baja (<20%) y cuando las madres entrenadas entrenaron a más del 70% de sus crías para evitar a los sapos. Cuando ambas condiciones fueron cumplidas, la adaptación genética fue más lenta pero la adaptación cultural rápida mantuvo a la población vigente mientras se completaba la adaptación genética. Para ganar conocimiento sobre las dinámicas evolutivas (en las cuales vimos un pico transitorio en la adaptación cultural a lo largo del tiempo) también desarrollamos un modelo analítico simple de las dinámicas evolutivas. Este modelo mostró que la fuerza de la selección natural declinó conforme incrementó la tasa de transmisión cultural y que la adaptación procedió solamente cuando la tasa de transmisión cultural estuvo por debajo de un valor crítico determinado por los niveles relativos de protección otorgados por los mecanismos genéticos contra los mecanismos evolutivos. En conjunto, nuestros modelos mostraron que la adaptación cultural puede jugar un papel importante en la prevención de la extinción, pero las tasas de transmisión cultural necesitan ser altas para que esto ocurra.

A new velvet gecko (Oedura: Diplodactylidae) from Groote Eylandt, Northern Territory.

Over the last decade, the combination of biological surveys, genetic diversity assessments and systematic research has revealed a growing number of previously unrecognised vertebrate species endemic to the Australian Monsoonal Tropics. Here we describe a new species of saxicoline velvet gecko in the Oedura marmorata complex from Groote Eylandt, a large island off the eastern edge of the Top End region of the Northern Territory. Oedura nesos sp. nov. differs from all congeners in combination of moderate size, and aspects of tail morphology and colouration. It has not been reported from the nearby mainland regions (eastern Arnhem Land) suggesting it may be an insular endemic, although further survey work is required to confirm this. While Groote Eylandt is recognised as a contemporary ecological refuge for declining mammal species of northern Australia, newly detected endemic species suggest it may also be of significance as an evolutionary refuge for many taxa, especially those associated with sandstone escarpments.

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.