Process-explicit models reveal pathway to extinction for woolly mammoth using pattern-oriented validation.

Pathways to extinction start long before the death of the last individual. However, causes of early stage population declines and the susceptibility of small residual populations to extirpation are typically studied in isolation. Using validated process-explicit models, we disentangle the ecological mechanisms and threats that were integral in the initial decline and later extinction of the woolly mammoth. We show that reconciling ancient DNA data on woolly mammoth population decline with fossil evidence of location and timing of extinction requires process-explicit models with specific demographic and niche constraints, and a constrained synergy of climatic change and human impacts. Validated models needed humans to hasten climate-driven population declines by many millennia, and to allow woolly mammoths to persist in mainland Arctic refugia until the mid-Holocene. Our results show that the role of humans in the extinction dynamics of woolly mammoth began well before the Holocene, exerting lasting effects on the spatial pattern and timing of its range-wide extinction.

Dominant carnivore loss benefits native avian and invasive mammalian scavengers.

Scavenging by large carnivores is integral for ecosystem functioning by limiting the build-up of carrion and facilitating widespread energy flows. However, top carnivores have declined across the world, triggering trophic shifts within ecosystems. Here, we compare findings from previous work on predator decline against areas with recent native mammalian carnivore loss. Specifically, we investigate top-down control on utilization of experimentally placed carcasses by two mesoscavengers-the invasive feral cat and native forest raven. Ravens profited most from carnivore loss, scavenging for five times longer in the absence of native mammalian carnivores. Cats scavenged on half of all carcasses in the region without dominant native carnivores. This was eight times more than in areas where other carnivores were at high densities. All carcasses persisted longer than the three-week monitoring period in the absence of native mammalian carnivores, while in areas with high carnivore abundance, all carcasses were fully consumed. Our results reveal that top-carnivore loss amplifies impacts associated with carnivore decline-increased carcass persistence and carrion access for smaller scavengers. This suggests that even at low densities, native mammalian carnivores can fulfil their ecological functions, demonstrating the significance of global carnivore conservation and supporting management approaches, such as trophic rewilding.

Accidents alter animal fitness landscapes.

Animals alter their habitat use in response to the energetic demands of movement ('energy landscapes') and the risk of predation ('the landscape of fear'). Recent research suggests that animals also select habitats and move in ways that minimise their chance of temporarily losing control of movement and thereby suffering slips, falls, collisions or other accidents, particularly when the consequences are likely to be severe (resulting in injury or death). We propose that animals respond to the costs of an 'accident landscape' in conjunction with predation risk and energetic costs when deciding when, where, and how to move in their daily lives. We develop a novel theoretical framework describing how features of physical landscapes interact with animal size, morphology, and behaviour to affect the risk and severity of accidents, and predict how accident risk might interact with predation risk and energetic costs to dictate movement decisions across the physical landscape. Future research should focus on testing the hypotheses presented here for different real-world systems to gain insight into the relative importance of theorised effects in the field.

Quantifying 25 years of disease-caused declines in Tasmanian devil populations: host density drives spatial pathogen spread.

Infectious diseases are strong drivers of wildlife population dynamics, however, empirical analyses from the early stages of pathogen emergence are rare. Tasmanian devil facial tumour disease (DFTD), discovered in 1996, provides the opportunity to study an epizootic from its inception. We use a pattern-oriented diffusion simulation to model the spatial spread of DFTD across the species' range and quantify population effects by jointly modelling multiple streams of data spanning 35 years. We estimate the wild devil population peaked at 53 000 in 1996, less than half of previous estimates. DFTD spread rapidly through high-density areas, with spread velocity slowing in areas of low host densities. By 2020, DFTD occupied >90% of the species' range, causing 82% declines in local densities and reducing the total population to 16 900. Encouragingly, our model forecasts the population decline should level-off within the next decade, supporting conservation management focused on facilitating evolution of resistance and tolerance.

Roadkill islands: Carnivore extinction shifts seasonal use of roadside carrion by generalist avian scavenger.

Global road networks facilitate habitat modification and are integral to human expansion. Many animals, particularly scavengers, use roads as they provide a reliable source of food, such as carrion left after vehicle collisions. Tasmania is often cited as the 'roadkill capital of Australia', with the isolated offshore islands in the Bass Strait experiencing similar, if not higher, levels of roadkill. However, native mammalian predators on the islands are extirpated, meaning the remaining scavengers are likely to experience lower interference competition. In this study, we used a naturally occurring experiment to examine how the loss of mammalian carnivores within a community impacts roadside foraging behaviour by avian scavengers. We monitored the locations of roadkill and forest ravens Corvus tasmanicus, an abundant scavenger species, on eight road transects across the Tasmanian mainland (high scavenging competition) and the Bass Strait islands (low scavenging competition). We represented raven observations as one-dimensional point patterns, using hierarchical Bayesian models to investigate the dependence of raven spatial intensity on habitat, season, distance to roadkill and route location. We found that roadkill carcasses were a strong predictor of raven presence along road networks. The effect of roadkill was amplified on roads on the Bass Strait islands, where roadside carrion was a predictor of raven presence across the entire year. In contrast, ravens were more often associated with roadkill on Tasmanian mainland roads in the autumn, when other resources were low. This suggests that in the absence of competing mammalian scavengers, ravens choose to feed on roadside carrion throughout the year, even in seasons when other resources are available. This lack of competition could be disproportionately benefiting forest ravens, leading to augmented raven populations and changes to the vertebrate community structure. Our study provides evidence that scavengers modify their behaviour in response to reduced scavenger species diversity, potentially triggering trophic shifts and highlighting the importance of conserving or reintroducing carnivores within ecosystems.

Analyzing linear spatial features in ecology.

The spatial analysis of dimensionless points (e.g., tree locations on a plot map) is common in ecology, for instance using point-process statistics to detect and compare patterns. However, the treatment of one-dimensional linear features (fiber processes) is rarely attempted. Here we appropriate the methods of vector sums and dot products, used regularly in fields like astrophysics, to analyze a data set of mapped linear features (logs) measured in 12 × 1-ha forest plots. For this demonstrative case study, we ask two deceptively simple questions: do trees tend to fall downhill, and if so, does slope gradient matter? Despite noisy data and many potential confounders, we show clearly that topography (slope direction and steepness) of forest plots does matter to treefall. More generally, these results underscore the value of mathematical methods of physics to problems in the spatial analysis of linear features, and the opportunities that interdisciplinary collaboration provides. This work provides scope for a variety of future ecological analyzes of fiber processes in space.

How complex should models be? Comparing correlative and mechanistic range dynamics models.

Criticism has been levelled at climate-change-induced forecasts of species range shifts that do not account explicitly for complex population dynamics. The relative importance of such dynamics under climate change is, however, undetermined because direct tests comparing the performance of demographic models vs. simpler ecological niche models are still lacking owing to difficulties in evaluating forecasts using real-world data. We provide the first comparison of the skill of coupled ecological-niche-population models and ecological niche models in predicting documented shifts in the ranges of 20 British breeding bird species across a 40-year period. Forecasts from models calibrated with data centred on 1970 were evaluated using data centred on 2010. We found that more complex coupled ecological-niche-population models (that account for dispersal and metapopulation dynamics) tend to have higher predictive accuracy in forecasting species range shifts than structurally simpler models that only account for variation in climate. However, these better forecasts are achieved only if ecological responses to climate change are simulated without static snapshots of historic land use, taken at a single point in time. In contrast, including both static land use and dynamic climate variables in simpler ecological niche models improve forecasts of observed range shifts. Despite being less skilful at predicting range changes at the grid-cell level, ecological niche models do as well, or better, than more complex models at predicting the magnitude of relative change in range size. Therefore, ecological niche models can provide a reasonable first approximation of the magnitude of species' potential range shifts, especially when more detailed data are lacking on dispersal dynamics, demographic processes underpinning population performance, and change in land cover.

Disentangling synergistic disease dynamics: Implications for the viral biocontrol of rabbits.

European rabbits (Oryctolagus cuniculus) have been exposed to rabbit haemorrhagic disease virus (RHDV) and myxoma virus (MYXV) in their native and invasive ranges for decades. Yet, the long-term effects of these viruses on rabbit population dynamics remain poorly understood. In this context, we analysed 17 years of detailed capture-mark-recapture data (2000-2016) from Turretfield, South Australia, using a probabilistic state-space hierarchical modelling framework to estimate rabbit survival and epidemiological dynamics. While RHDV infection and disease-induced death were most prominent during annual epidemics in winter and spring, we found evidence for continuous infection of susceptible individuals with RHDV throughout the year. RHDV-susceptible rabbits had, on average, 25% lower monthly survival rates compared to immune individuals, while the average monthly force of infection in winter and spring was ~38%. These combined to result in an average infection-induced mortality rate of 69% in winter and spring. Individuals susceptible to MYXV and immune to RHDV had similar survival probabilities to those having survived infections from both viruses, whereas individuals susceptible to both RHDV and MYXV had higher survival probabilities than those susceptible to RHDV and immune to MYXV. This suggests that MYXV may reduce the future survival rates of individuals that endure initial MYXV infection. There was no evidence for long-term changes in disease-induced mortality and infection rates for either RHDV or MYXV. We conclude that continuous, year-round virus perpetuation (and perhaps heterogeneity in modes of transmission and infectious doses during and after epidemics) acts to reduce the efficiency of RHDV and MYXV as biocontrol agents of rabbits in their invasive range. However, if virulence can be maintained as relatively constant through time, RHDV and MYXV will likely continue realizing strong benefits as biocontrol agents.

Pattern, process, inference and prediction in extinction biology.

Extinction is a key feature of the evolutionary history of life, and assessments of extinction risk are essential for the effective protection of biodiversity. The goal in assembling this special issue of Biology Letters was to highlight problems and questions at the research frontier of extinction biology, with an emphasis on recent developments in the methodology of inferring the patterns and processes of extinction from a background of often noisy and sparse data. In selecting topics, we sought to illustrate how extinction is not simply a self-evident phenomenon, but the subject of a dynamic and quantitatively rigorous field of natural science, with practical applications to conservation.

Primary forests are irreplaceable for sustaining tropical biodiversity.

Human-driven land-use changes increasingly threaten biodiversity, particularly in tropical forests where both species diversity and human pressures on natural environments are high. The rapid conversion of tropical forests for agriculture, timber production and other uses has generated vast, human-dominated landscapes with potentially dire consequences for tropical biodiversity. Today, few truly undisturbed tropical forests exist, whereas those degraded by repeated logging and fires, as well as secondary and plantation forests, are rapidly expanding. Here we provide a global assessment of the impact of disturbance and land conversion on biodiversity in tropical forests using a meta-analysis of 138 studies. We analysed 2,220 pairwise comparisons of biodiversity values in primary forests (with little or no human disturbance) and disturbed forests. We found that biodiversity values were substantially lower in degraded forests, but that this varied considerably by geographic region, taxonomic group, ecological metric and disturbance type. Even after partly accounting for confounding colonization and succession effects due to the composition of surrounding habitats, isolation and time since disturbance, we find that most forms of forest degradation have an overwhelmingly detrimental effect on tropical biodiversity. Our results clearly indicate that when it comes to maintaining tropical biodiversity, there is no substitute for primary forests.

Human population reduction is not a quick fix for environmental problems.

The inexorable demographic momentum of the global human population is rapidly eroding Earth's life-support system. There are consequently more frequent calls to address environmental problems by advocating further reductions in human fertility. To examine how quickly this could lead to a smaller human population, we used scenario-based matrix modeling to project the global population to the year 2100. Assuming a continuation of current trends in mortality reduction, even a rapid transition to a worldwide one-child policy leads to a population similar to today's by 2100. Even a catastrophic mass mortality event of 2 billion deaths over a hypothetical 5-y window in the mid-21(st) century would still yield around 8.5 billion people by 2100. In the absence of catastrophe or large fertility reductions (to fewer than two children per female worldwide), the greatest threats to ecosystems--as measured by regional projections within the 35 global Biodiversity Hotspots--indicate that Africa and South Asia will experience the greatest human pressures on future ecosystems. Humanity's large demographic momentum means that there are no easy policy levers to change the size of the human population substantially over coming decades, short of extreme and rapid reductions in female fertility; it will take centuries, and the long-term target remains unclear. However, some reduction could be achieved by midcentury and lead to hundreds of millions fewer people to feed. More immediate results for sustainability would emerge from policies and technologies that reverse rising consumption of natural resources.

Tick exposure and extreme climate events impact survival and threaten the persistence of a long-lived lizard.

Assessing the impacts of multiple, often synergistic, stressors on the population dynamics of long-lived species is becoming increasingly important due to recent and future global change. Tiliqua rugosa (sleepy lizard) is a long-lived skink (>30 years) that is adapted to survive in semi-arid environments with varying levels of parasite exposure and highly seasonal food availability. We used an exhaustive database of 30 years of capture-mark-recapture records to quantify the impacts of both parasite exposure and environmental conditions on the lizard's survival rates and long-term population dynamics. Lizard abundance was relatively stable throughout the study period; however, there were changing patterns in adult and juvenile apparent survival rates, driven by spatial and temporal variation in levels of tick exposure and temporal variation in environmental conditions. Extreme weather events during the winter and spring seasons were identified as important environmental drivers of survival. Climate models predict a dramatic increase in the frequency of extreme hot and dry winter and spring seasons in our South Australian study region; from a contemporary probability of 0.17 up to 0.47-0.83 in 2080 depending on the emissions scenario. Our stochastic population model projections showed that these future climatic conditions will induce a decline in the abundance of this long-lived reptile of up to 67% within 30 years from 2080, under worst case scenario modelling. The results have broad implications for future work investigating the drivers of population dynamics and persistence. We highlight the importance of long-term data sets and accounting for synergistic impacts between multiple stressors. We show that predicted increases in the frequency of extreme climate events have the potential to considerably and negatively influence a long-lived species, which might previously have been assumed to be resilient to environmental perturbations.

Extinction debt from climate change for frogs in the wet tropics.

The effect of twenty-first-century climate change on biodiversity is commonly forecast based on modelled shifts in species ranges, linked to habitat suitability. These projections have been coupled with species-area relationships (SAR) to infer extinction rates indirectly as a result of the loss of climatically suitable areas and associated habitat. This approach does not model population dynamics explicitly, and so accepts that extinctions might occur after substantial (but unknown) delays-an extinction debt. Here we explicitly couple bioclimatic envelope models of climate and habitat suitability with generic life-history models for 24 species of frogs found in the Australian Wet Tropics (AWT). We show that (i) as many as four species of frogs face imminent extinction by 2080, due primarily to climate change; (ii) three frogs face delayed extinctions; and (iii) this extinction debt will take at least a century to be realized in full. Furthermore, we find congruence between forecast rates of extinction using SARs, and demographic models with an extinction lag of 120 years. We conclude that SAR approaches can provide useful advice to conservation on climate change impacts, provided there is a good understanding of the time lags over which delayed extinctions are likely to occur.

Empirical tests of harvest-induced body-size evolution along a geographic gradient in Australian macropods.

Life-history theory predicts the progressive dwarfing of animal populations that are subjected to chronic mortality stress, but the evolutionary impact of harvesting terrestrial herbivores has seldom been tested. In Australia, marsupials of the genus Macropus (kangaroos and wallabies) are subjected to size-selective commercial harvesting. Mathematical modelling suggests that harvest quotas (c. 10-20% of population estimates annually) could be driving body-size evolution in these species. We tested this hypothesis for three harvested macropod species with continental-scale distributions. To do so, we measured more than 2000 macropod skulls sourced from wildlife collections spanning the last 130 years. We analysed these data using spatial Bayesian models that controlled for the age and sex of specimens as well as environmental drivers and island effects. We found no evidence for the hypothesized decline in body size for any species; rather, models that fit trend terms supported minor body size increases over time. This apparently counterintuitive result is consistent with reduced mortality due to a depauperate predator guild and increased primary productivity of grassland vegetation following European settlement in Australia. Spatial patterns in macropod body size supported the heat dissipation limit and productivity hypotheses proposed to explain geographic body-size variation (i.e. skull size increased with decreasing summer maximum temperature and increasing rainfall, respectively). There is no empirical evidence that size-selective harvesting has driven the evolution of smaller body size in Australian macropods. Bayesian models are appropriate for investigating the long-term impact of human harvesting because they can impute missing data, fit nonlinear growth models and account for non-random spatial sampling inherent in wildlife collections.

Key role for nuclear energy in global biodiversity conservation.

Modern society uses massive amounts of energy. Usage rises as population and affluence increase, and energy production and use often have an impact on biodiversity or natural areas. To avoid a business-as-usual dependence on coal, oil, and gas over the coming decades, society must map out a future energy mix that incorporates alternative sources. This exercise can lead to radically different opinions on what a sustainable energy portfolio might entail, so an objective assessment of the relative costs and benefits of different energy sources is required. We evaluated the land use, emissions, climate, and cost implications of 3 published but divergent storylines for future energy production, none of which was optimal for all environmental and economic indicators. Using multicriteria decision-making analysis, we ranked 7 major electricity-generation sources (coal, gas, nuclear, biomass, hydro, wind, and solar) based on costs and benefits and tested the sensitivity of the rankings to biases stemming from contrasting philosophical ideals. Irrespective of weightings, nuclear and wind energy had the highest benefit-to-cost ratio. Although the environmental movement has historically rejected the nuclear energy option, new-generation reactor technologies that fully recycle waste and incorporate passive safety systems might resolve their concerns and ought to be more widely understood. Because there is no perfect energy source however, conservation professionals ultimately need to take an evidence-based approach to consider carefully the integrated effects of energy mixes on biodiversity conservation. Trade-offs and compromises are inevitable and require advocating energy mixes that minimize net environmental damage. Society cannot afford to risk wholesale failure to address energy-related biodiversity impacts because of preconceived notions and ideals.

Predictors of contraction and expansion of area of occupancy for British birds.

Geographical range dynamics are driven by the joint effects of abiotic factors, human ecosystem modifications, biotic interactions and the intrinsic organismal responses to these. However, the relative contribution of each component remains largely unknown. Here, we compare the contribution of life-history attributes, broad-scale gradients in climate and geographical context of species' historical ranges, as predictors of recent changes in area of occupancy for 116 terrestrial British breeding birds (74 contractors, 42 expanders) between the early 1970s and late 1990 s. Regional threat classifications demonstrated that the species of highest conservation concern showed both the largest contractions and the smallest expansions. Species responded differently to climate depending on geographical distribution-northern species changed their area of occupancy (expansion or contraction) more in warmer and drier regions, whereas southern species changed more in colder and wetter environments. Species with slow life history (larger body size) tended to have a lower probability of changing their area of occupancy than species with faster life history, whereas species with greater natal dispersal capacity resisted contraction and, counterintuitively, expansion. Higher geographical fragmentation of species' range also increased expansion probability, possibly indicating a release from a previously limiting condition, for example through agricultural abandonment since the 1970s. After accounting statistically for the complexity and nonlinearity of the data, our results demonstrate two key aspects of changing area of occupancy for British birds: (i) climate is the dominant driver of change, but direction of effect depends on geographical context, and (ii) all of our predictors generally had a similar effect regardless of the direction of the change (contraction versus expansion). Although we caution applying results from Britain's highly modified and well-studied bird community to other biogeographic regions, our results do indicate that a species' propensity to change area of occupancy over decadal scales can be explained partially by a combination of simple allometric predictors of life-history pace, average climate conditions and geographical context.

An ecological regime shift resulting from disrupted predator-prey interactions in Holocene Australia.

The mass extinction events during human prehistory are striking examples of ecological regime shifts, the causes of which are still hotly debated. In Australia, human arrival approximately 50 thousand years ago was associated with the continental-scale extinction of numerous marsupial megafauna species and a permanent change in vegetation structure. An alternative stable state persisted until a second regime shift occurred during the late Holocene, when the largest two remaining marsupial carnivores, the thylacine and devil, disappeared from mainland Australia. These extinctions have been widely attributed to the human-assisted invasion of a competing predator, the dingo. In this unusual case, the simultaneous effects of human "intensification" (population growth and technological advances) and climate change (particularly increased ENSO variability) have been largely overlooked. We developed a dynamic model system capable of simulating the complex interactions between the main predators (humans, thylacines, devils, dingoes) and their marsupial prey (macropods), which we coupled with reconstructions of human population growth and climate change for late-Holocene Australia. Because the strength of important interspecific interactions cannot be estimated directly, we used detailed scenario testing and sensitivity analysis to identify robust model outcomes and investigate competing explanations for the Holocene regime shift. This approach identified human intensification as the most probable cause, while also demonstrating the potential importance of synergies with the effects of climate change. Our models indicate that the prehistoric impact of humans on Australian mammals was not limited to the late Pleistocene (i.e., the megafaunal extinctions) but extended into the late Holocene.

How interactions between animal movement and landscape processes modify local range dynamics and extinction risk.

Forecasts of range dynamics now incorporate many of the mechanisms and interactions that drive species distributions. However, connectivity continues to be simulated using overly simple distance-based dispersal models with little consideration of how the individual behaviour of dispersing organisms interacts with landscape structure (functional connectivity). Here, we link an individual-based model to a niche-population model to test the implications of this omission. We apply this novel approach to a turtle species inhabiting wetlands which are patchily distributed across a tropical savannah, and whose persistence is threatened by two important synergistic drivers of global change: predation by invasive species and overexploitation. We show that projections of local range dynamics in this study system change substantially when functional connectivity is modelled explicitly. Accounting for functional connectivity in model simulations causes the estimate of extinction risk to increase, and predictions of range contraction to slow. We conclude that models of range dynamics that simulate functional connectivity can reduce an important source of bias in predictions of shifts in species distributions and abundances, especially for organisms whose dispersal behaviours are strongly affected by landscape structure.

A non-invasive approach to measuring body dimensions of wildlife with camera traps: A felid field trial.

Dimensions of body size are an important measurement in animal ecology, although they can be difficult to obtain due to the effort and cost associated with the invasive nature of these measurements. We avoid these limitations by using camera trap images to derive dimensions of animal size. To obtain measurements of object dimensions using this method, the size of the object in pixels, the focal length of the camera, and the distance to that object must be known. We describe a novel approach of obtaining the distance to the object through the creation of a portable distance marker, which, when photographed, creates a "reference image" to determine the position of the animal within an image. This method allows for the retrospective analysis of existing datasets and eliminates the need for permanent in-field distance markers. We tested the accuracy of this methodology under controlled conditions with objects of known size resembling Felis catus, our study species, validating the legitimacy of our method of size estimation. We then apply our method to measure feral cat body size using images collected in Tasmania, Australia. The precision of our methodology was evaluated by comparing size estimates across individual cats, revealing consistent and reliable results. The average height (front paw to shoulder) of the feral cats sampled was 25.25 cm (CI = 24.4, 26.1) and the average length (base of tail to nose) was 47.48 cm (CI = 46.0, 48.9), suggesting wild feral cats in our study area are no larger than their domestic counterparts. Given the success of its application within our study, we call for further trails with this method across a variety of species.

Population dynamics can be more important than physiological limits for determining range shifts under climate change.

Evidence is accumulating that species' responses to climate changes are best predicted by modelling the interaction of physiological limits, biotic processes and the effects of dispersal-limitation. Using commercially harvested blacklip (Haliotis rubra) and greenlip abalone (Haliotis laevigata) as case studies, we determine the relative importance of accounting for interactions among physiology, metapopulation dynamics and exploitation in predictions of range (geographical occupancy) and abundance (spatially explicit density) under various climate change scenarios. Traditional correlative ecological niche models (ENM) predict that climate change will benefit the commercial exploitation of abalone by promoting increased abundances without any reduction in range size. However, models that account simultaneously for demographic processes and physiological responses to climate-related factors result in future (and present) estimates of area of occupancy (AOO) and abundance that differ from those generated by ENMs alone. Range expansion and population growth are unlikely for blacklip abalone because of important interactions between climate-dependent mortality and metapopulation processes; in contrast, greenlip abalone should increase in abundance despite a contraction in AOO. The strongly non-linear relationship between abalone population size and AOO has important ramifications for the use of ENM predictions that rely on metrics describing change in habitat area as proxies for extinction risk. These results show that predicting species' responses to climate change often require physiological information to understand climatic range determinants, and a metapopulation model that can make full use of this data to more realistically account for processes such as local extirpation, demographic rescue, source-sink dynamics and dispersal-limitation.