The climatic drivers of long-term population changes in rainforest montane birds.

Climate-driven biodiversity erosion is escalating at an alarming rate. The pressure imposed by climate change is exceptionally high in tropical ecosystems, where species adapted to narrow environmental ranges exhibit strong physiological constraints. Despite the observed detrimental effect of climate change on ecosystems at a global scale, our understanding of the extent to which multiple climatic drivers affect population dynamics is limited. Here, we disentangle the impact of different climatic stressors on 47 rainforest birds inhabiting the mountains of the Australian Wet Tropics using hierarchical population models. We estimate the effect of spatiotemporal changes in temperature, precipitation, heatwaves, droughts and cyclones on the population dynamics of rainforest birds between 2000 and 2016. We find a strong effect of warming and changes in rainfall patterns across the elevational-segregated bird communities, with lowland populations benefiting from increasing temperature and precipitation, while upland species show an inverse strong negative response to the same drivers. Additionally, we find a negative effect of heatwaves on lowland populations, a pattern associated with the observed distribution of these extreme events across elevations. In contrast, cyclones and droughts have a marginal effect on spatiotemporal changes in rainforest bird communities, suggesting a species-specific response unrelated to the elevational gradient. This study demonstrated the importance of unravelling the drivers of climate change impacts on population changes, providing significant insight into the mechanisms accelerating climate-induced biodiversity degradation.

Estimating co-extinction threats in terrestrial ecosystems.

The biosphere is changing rapidly due to human endeavour. Because ecological communities underlie networks of interacting species, changes that directly affect some species can have indirect effects on others. Accurate tools to predict these direct and indirect effects are therefore required to guide conservation strategies. However, most extinction-risk studies only consider the direct effects of global change-such as predicting which species will breach their thermal limits under different warming scenarios-with predictions of trophic cascades and co-extinction risks remaining mostly speculative. To predict the potential indirect effects of primary extinctions, data describing community interactions and network modelling can estimate how extinctions cascade through communities. While theoretical studies have demonstrated the usefulness of models in predicting how communities react to threats like climate change, few have applied such methods to real-world communities. This gap partly reflects challenges in constructing trophic network models of real-world food webs, highlighting the need to develop approaches for quantifying co-extinction risk more accurately. We propose a framework for constructing ecological network models representing real-world food webs in terrestrial ecosystems and subjecting these models to co-extinction scenarios triggered by probable future environmental perturbations. Adopting our framework will improve estimates of how environmental perturbations affect whole ecological communities. Identifying species at risk of co-extinction (or those that might trigger co-extinctions) will also guide conservation interventions aiming to reduce the probability of co-extinction cascades and additional species losses.

Research priorities for natural ecosystems in a changing global climate.

Climate change poses significant emerging risks to biodiversity, ecosystem function and associated socioecological systems. Adaptation responses must be initiated in parallel with mitigation efforts, but resources are limited. As climate risks are not distributed equally across taxa, ecosystems and processes, strategic prioritization of research that addresses stakeholder-relevant knowledge gaps will accelerate effective uptake into adaptation policy and management action. After a decade of climate change adaptation research within the Australian National Climate Change Adaptation Research Facility, we synthesize the National Adaptation Research Plans for marine, terrestrial and freshwater ecosystems. We identify the key, globally relevant priorities for ongoing research relevant to informing adaptation policy and environmental management aimed at maximizing the resilience of natural ecosystems to climate change. Informed by both global literature and an extensive stakeholder consultation across all ecosystems, sectors and regions in Australia, involving thousands of participants, we suggest 18 priority research topics based on their significance, urgency, technical and economic feasibility, existing knowledge gaps and potential for cobenefits across multiple sectors. These research priorities provide a unified guide for policymakers, funding organizations and researchers to strategically direct resources, maximize stakeholder uptake of resulting knowledge and minimize the impacts of climate change on natural ecosystems. Given the pace of climate change, it is imperative that we inform and accelerate adaptation progress in all regions around the world.

Identifying conservation priorities for threatened Eastern Himalayan mammals.

To augment mammal conservation in the Eastern Himalayan region, we assessed the resident 255 terrestrial mammal species and identified the 50 most threatened species based on conservation status, endemism, range size, and evolutionary distinctiveness. By using the spatial analysis package letsR and the complementarity core-area method in the conservation planning software Zonation, we assessed the current efficacy of their protection and identified priority conservation areas by comparing protected areas (PAs), land cover, and global ecoregion 2017 maps at a 100 × 100 m spatial scale. The 50 species that were most threatened, geographically restricted, and evolutionarily distinct faced a greater extinction risk than globally nonthreatened and wide-ranging species and species with several close relatives. Small, medium-sized, and data-deficient species faced extinction from inadequate protection in PAs relative to wide-ranging charismatic species. There was a mismatch between current PA distribution and priority areas for conservation of the 50 most endangered species. To protect these species, the skewed regional PA distribution would require expansion. Where possible, new PAs and transboundary reserves in the 35 priority areas we identified should be established. There are adequate remaining natural areas in which to expand current Eastern Himalayan PAs. Consolidation and expansion of PAs in the EH requires strengthening national and regional transboundary collaboration, formulating comprehensive regional land-use plans, diversifying conservation funding, and enhancing information sharing through a consolidated regional database.

Rare species contribute disproportionately to the functional structure of species assemblages.

There is broad consensus that the diversity of functional traits within species assemblages drives several ecological processes. It is also widely recognized that rare species are the first to become extinct following human-induced disturbances. Surprisingly, however, the functional importance of rare species is still poorly understood, particularly in tropical species-rich assemblages where the majority of species are rare, and the rate of species extinction can be high. Here, we investigated the consequences of local and regional extinctions on the functional structure of species assemblages. We used three extensive datasets (stream fish from the Brazilian Amazon, rainforest trees from French Guiana, and birds from the Australian Wet Tropics) and built an integrative measure of species rarity versus commonness, combining local abundance, geographical range, and habitat breadth. Using different scenarios of species loss, we found a disproportionate impact of rare species extinction for the three groups, with significant reductions in levels of functional richness, specialization, and originality of assemblages, which may severely undermine the integrity of ecological processes. The whole breadth of functional abilities within species assemblages, which is disproportionately supported by rare species, is certainly critical in maintaining ecosystems particularly under the ongoing rapid environmental transitions.

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.

Microhabitats reduce animal's exposure to climate extremes.

Extreme weather events, such as unusually hot or dry conditions, can cause death by exceeding physiological limits, and so cause loss of population. Survival will depend on whether or not susceptible organisms can find refuges that buffer extreme conditions. Microhabitats offer different microclimates to those found within the wider ecosystem, but do these microhabitats effectively buffer extreme climate events relative to the physiological requirements of the animals that frequent them? We collected temperature data from four common microhabitats (soil, tree holes, epiphytes, and vegetation) located from the ground to canopy in primary rainforests in the Philippines. Ambient temperatures were monitored from outside of each microhabitat and from the upper forest canopy, which represent our macrohabitat controls. We measured the critical thermal maxima (CTmax ) of frog and lizard species, which are thermally sensitive and inhabit our microhabitats. Microhabitats reduced mean temperature by 1-2 °C and reduced the duration of extreme temperature exposure by 14-31 times. Microhabitat temperatures were below the CTmax of inhabitant frogs and lizards, whereas macrohabitats consistently contained lethal temperatures. Microhabitat temperatures increased by 0.11-0.66 °C for every 1 °C increase in macrohabitat temperature, and this nonuniformity in temperature change influenced our forecasts of vulnerability for animal communities under climate change. Assuming uniform increases of 6 °C, microhabitats decreased the vulnerability of communities by up to 32-fold, whereas under nonuniform increases of 0.66 to 3.96 °C, microhabitats decreased the vulnerability of communities by up to 108-fold. Microhabitats have extraordinary potential to buffer climate and likely reduce mortality during extreme climate events. These results suggest that predicted changes in distribution due to mortality and habitat shifts that are derived from macroclimatic samples and that assume uniform changes in microclimates relative to macroclimates may be overly pessimistic. Nevertheless, even nonuniform temperature increases within buffered microhabitats would still threaten frogs and lizards.

Microhabitats in the tropics buffer temperature in a globally coherent manner.

Vegetated habitats contain a variety of fine-scale features that can ameliorate temperate extremes. These buffered microhabitats may be used by species to evade extreme weather and novel climates in the future. Yet, the magnitude and extent of this buffering on a global scale remains unknown. Across all tropical continents and using 36 published studies, we assessed temperature buffering from within microhabitats across various habitat strata and structures (e.g. soil, logs, epiphytes and tree holes) and compared them to non-buffered macro-scale ambient temperatures (the thermal control). Microhabitats buffered temperature by 3.9 °C and reduced maximum temperatures by 3.5 °C. Buffering was most pronounced in tropical lowlands where temperatures were most variable. With the expected increase in extreme weather events, microhabitats should provide species with a local layer of protection that is not captured by traditional climate assessments, which are typically derived from macro-scale temperatures (e.g. satellites). Our data illustrate the need for a next generation of predictive models that account for species' ability to move within microhabitats to exploit favourable buffered microclimates.

Increasing arboreality with altitude: a novel biogeographic dimension.

Biodiversity is spatially organized by climatic gradients across elevation and latitude. But do other gradients exist that might drive biogeographic patterns? Here, we show that rainforest's vertical strata provide climatic gradients much steeper than those offered by elevation and latitude, and biodiversity of arboreal species is organized along this gradient. In Philippine and Singaporean rainforests, we demonstrate that rainforest frogs tend to shift up in the rainforest strata as altitude increases. Moreover, a Philippine-wide dataset of frog distributions shows that frog assemblages become increasingly arboreal at higher elevations. Thus, increased arboreality with elevation at broad biogeographic scales mirrors patterns we observed at local scales. Our proposed 'arboreality hypothesis' suggests that the ability to exploit arboreal habitats confers the potential for larger geographical distributions because species can shift their location in the rainforest strata to compensate for shifts in temperature associated with elevation and latitude. This novel finding may help explain patterns of species richness and abundance wherever vegetation produces a vertical microclimatic gradient. Our results further suggest that global warming will 'flatten' the biodiversity in rainforests by pushing arboreal species towards the cooler and wetter ground. This 'flattening' could potentially have serious impacts on forest functioning and species survival.

Recent speciation and limited phylogeographic structure in Mixophyes frogs from the Australian Wet Tropics.

Through a combination of macroecological, paleoecological, and phylogeographical analyses, the rainforests of the Australian Wet Tropics (AWT) have emerged as a useful model for understanding sensitivity of species to past climatic change and, hence, for predicting vulnerability to future change. To extend the ecological breadth of comparative phylogeographic analyses, we investigate a clade of myobatrachid frogs, Mixophyes, a genus of large, stream-breeding but terrestrial frogs, three species of which are endemic to rainforests of the AWT. Here we (i) combine mtDNA, allozyme, and morphological data to refine knowledge of the geographic and environmental distribution of each taxon, (ii) resolve relationships among species, and (iii) use mtDNA phylogeography to infer responses of the three taxa to late-Pleistocene and Holocene climatic change. Each of the three species (Mixophyes carbinensis, Mixophyes coggeri, and Mixophyes schevilli) is effectively diagnosed by mtDNA, with the two small-bodied, allopatric species (M. carbinensis and M. schevilli) being sister-taxa. Mixophyes have a very different history from other AWT amphibians, with more recent speciation (net divergences <5%) and much lower and geographically unstructured mtDNA diversity within each species. The combination of low diversity (θ(Π)<0.36%) and strong signals of recent population expansion (Fu's Fs<0) suggests very high sensitivity to climate-driven rainforest dynamics, perhaps due to their large body size, low population density, and their requirement for both wet forest-floor litter and streams suitable for breeding. The results further emphasize the heterogeneity of species' responses to climate change and suggest that species dependent on multiple habitat types could be especially vulnerable.

Arboreality drives heat tolerance while elevation drives cold tolerance in tropical rainforest ants.

Determining how species thermal limits correlate with climate is important for understanding biogeographic patterns and assessing vulnerability to climate change. Such analyses need to consider thermal gradients at multiple spatial scales. Here we relate thermal traits of rainforest ants to microclimate conditions from ground to canopy (microgeographic scale) along an elevation gradient (mesogeographic scale) and calculate warming tolerance to assess climate change vulnerability in the Australian Wet Tropics Bioregion. We test the thermal adaptation and thermal niche asymmetry hypotheses to explain interspecific patterns of thermal tolerance at these two spatial scales. We tested cold tolerance (CTmin ), heat tolerance (CTmax ), and calculated thermal tolerance range (CTrange ), using ramping assays for 74 colonies of 40 ant species collected from terrestrial and arboreal habitats at lowland and upland elevation sites and recorded microclimatic conditions for one year. Within sites, arboreal ants were exposed to hotter microclimates and on average had a 4.2°C (95% CI: 2.7-5.6°C) higher CTmax and 5.3°C (95% CI: 3.5-7°C) broader CTrange than ground-dwelling ants. This pattern was consistent across the elevation gradient, whether it be the hotter lowlands or the cooler uplands. Across elevation, upland ants could tolerate significantly colder temperatures than lowland ants, whereas the change in CTmax was less pronounced, and CTrange did not change over elevation. Differential exposure to microclimates, due to localized niche preferences, drives divergence in CTmax , while environmental temperatures along the elevation gradient drive divergence in CTmin . Our results suggest that both processes of thermal adaptation and thermal niche asymmetry are at play, depending on the spatial scale of observation, and we discuss potential mechanisms underlying these patterns. Despite the broad thermal tolerance range of arboreal rainforest ants, lowland arboreal ants had the lowest warming tolerance and may be most vulnerable to climate change.

Laying low: Rugged lowland rainforest preferred by feral cats in the Australian Wet Tropics.

Invasive mesopredators are responsible for the decline of many species of native mammals worldwide. Feral cats have been causally linked to multiple extinctions of Australian mammals since European colonization. While feral cats are found throughout Australia, most research has been undertaken in arid habitats, thus there is a limited understanding of feral cat distribution, abundance, and ecology in Australian tropical rainforests. We carried out camera-trapping surveys at 108 locations across seven study sites, spanning 200 km in the Australian Wet Tropics. Single-species occupancy analysis was implemented to investigate how environmental factors influence feral cat distribution. Feral cats were detected at a rate of 5.09 photographs/100 days, 11 times higher than previously recorded in the Australian Wet Tropics. The main environmental factors influencing feral cat occupancy were a positive association with terrain ruggedness, a negative association with elevation, and a higher affinity for rainforest than eucalypt forest. These findings were consistent with other studies on feral cat ecology but differed from similar surveys in Australia. Increasingly harsh and consistently wet weather conditions at higher elevations, and improved shelter in topographically complex habitats may drive cat preference for lowland rainforest. Feral cats were positively associated with roads, supporting the theory that roads facilitate access and colonization of feral cats within more remote parts of the rainforest. Higher elevation rainforests with no roads could act as refugia for native prey species within the critical weight range. Regular monitoring of existing roads should be implemented to monitor feral cats, and new linear infrastructure should be limited to prevent encroachment into these areas. This is pertinent as climate change modeling suggests that habitats at higher elevations will become similar to lower elevations, potentially making the environment more suitable for feral cat populations.

Persistence in peripheral refugia promotes phenotypic divergence and speciation in a rainforest frog.

It is well established from the fossil record and phylogeographic analyses that late Quaternary climate fluctuations led to substantial changes in species' distribution, but whether and how these fluctuations resulted in phenotypic divergence and speciation is less clear. This question can be addressed through detailed analysis of traits relevant to ecology and mating within and among intraspecific lineages that persisted in separate refugia. In a biogeographic system (the Australian Wet Tropics [AWT]) with a well-established history of refugial isolation during Pleistocene glacial periods, we tested whether climate-mediated changes in distribution drove genetic and phenotypic divergence in the rainforest frog Cophixalus ornatus. We combined paleomodeling and multilocus genetics to demonstrate long-term persistence within, and isolation among, one central and two peripheral refugia. In contrast to other AWT vertebrates, the three major lineages differ in ecologically relevant morphology and in mating call, reflecting divergent selection and/or genetic drift in the peripheral isolates. Divergence in mating call and contact zone analyses suggest that the lineages now represent distinct species. The results show that climate shifts can promote genetic and phenotypic divergence and, potentially, speciation and direct attention toward incorporating adaptive traits into phylogeographic studies to better resolve the mechanisms of speciation.

Long-term changes in populations of rainforest birds in the Australia Wet Tropics bioregion: A climate-driven biodiversity emergency.

Many authors have suggested that the vulnerability of montane biodiversity to climate change worldwide is significantly higher than in most other ecosystems. Despite the extensive variety of studies predicting severe impacts of climate change globally, few studies have empirically validated the predicted changes in distribution and population density. Here, we used 17 years (2000-2016) of standardised bird monitoring across latitudinal/elevational gradients in the rainforest of the Australian Wet Tropics World Heritage Area to assess changes in local abundance and elevational distribution. We used relative abundance in 1977 surveys across 114 sites ranging from 0-1500m above sea level and utilised a trend analysis approach (TRIM) to investigate elevational shifts in abundance of 42 species. The local abundance of most mid and high elevation species has declined at the lower edges of their distribution by >40% while lowland species increased by up to 190% into higher elevation areas. Upland-specialised species and regional endemics have undergone dramatic population declines of almost 50%. The "Outstanding Universal Value" of the Australian Wet Tropics World Heritage Area, one of the most irreplaceable biodiversity hotspots on Earth, is rapidly degrading. These observed impacts are likely to be similar in many tropical montane ecosystems globally.

Patterns of persistence and isolation indicate resilience to climate change in montane rainforest lizards.

Globally, montane tropical diversity is characterized by extraordinary local endemism that is not readily explained by current environmental variables indicating a strong imprint of history. Montane species often exist as isolated populations under current climatic conditions and may have remained isolated throughout recent climatic cycles, leading to substantial genetic and phenotypic divergence. Alternatively, populations may have become contiguous during colder climates resulting in less divergence. Here we compare responses to historical climate fluctuation in a montane specialist skink, Lampropholis robertsi, and its more broadly distributed congener, L. coggeri, both endemic to rainforests of northeast Australia. To do so, we combine spatial modelling of potential distributions under representative palaeoclimates, multi-locus phylogeography and analyses of phenotypic variation. Spatial modelling of L. robertsi predicts strong isolation among disjunct montane refugia during warm climates, but with potential for localized exchange during the most recent glacial period. In contrast, predicted stable areas are more widespread and connected in L. coggeri. Both species exhibit pronounced phylogeographic structuring for mitochondrial and nuclear genes, attesting to low dispersal and high persistence across multiple isolated regions. This is most prominent in L. robertsi, for which coalescent analyses indicate that most populations persisted in isolation throughout the climate cycles of the Pleistocene. Morphological divergence, principally in body size, is more evident among isolated populations of L. robertsi than L. coggeri. These results highlight the biodiversity value of isolated montane populations and support the general hypothesis that tropical montane regions harbour high levels of narrow-range taxa because of their resilience to past climate change.

Extinction risk from climate change.

Climate change over the past approximately 30 years has produced numerous shifts in the distributions and abundances of species and has been implicated in one species-level extinction. Using projections of species' distributions for future climate scenarios, we assess extinction risks for sample regions that cover some 20% of the Earth's terrestrial surface. Exploring three approaches in which the estimated probability of extinction shows a power-law relationship with geographical range size, we predict, on the basis of mid-range climate-warming scenarios for 2050, that 15-37% of species in our sample of regions and taxa will be 'committed to extinction'. When the average of the three methods and two dispersal scenarios is taken, minimal climate-warming scenarios produce lower projections of species committed to extinction ( approximately 18%) than mid-range ( approximately 24%) and maximum-change ( approximately 35%) scenarios. These estimates show the importance of rapid implementation of technologies to decrease greenhouse gas emissions and strategies for carbon sequestration.

Potential for mountaintop boulder fields to buffer species against extreme heat stress under climate change.

Species may circumvent or minimize some impacts resulting from climate change by utilizing microhabitats that buffer against extreme events (e.g., heat waves). Boulder field habitats are considered to have functioned as important refugia for rainforest fauna during historical climate fluctuations. However, quantitative data on microhabitat buffering potential in these habitats is lacking. We characterized temperature buffering over small distances (i.e., depths) within an exposed and forested boulder field on a tropical mountain. We demonstrate that temperatures are cooler and become more stable at increasing depths within boulder fields. The magnitude of difference is most pronounced in exposed situations where temperatures within boulder fields can be as much as 10 degrees C lower than near surface conditions. Our data provide a first step toward building models that more realistically predict exposure to heat stress for fauna that utilize rocky habitats.

Abundance and the environmental niche: environmental suitability estimated from niche models predicts the upper limit of local abundance.

Ecologists seek to understand patterns of distribution and abundance of species. Studies of distribution often use occurrence data to build models of the environmental niche of a species. Environmental suitability (ES) derived from such models may be used to predict the potential distributions of species. The ability of such models to predict spatial patterns in abundance is unknown; we argue that there should be a positive relationship between ES and local abundance. This will be so if ES reflects how well the species' physiological and ecological requirements are met at a site and if those factors also determine local abundance. However, the presence of other factors may indicate that potential abundance is not attained at all sites. Therefore, ES should predict the upper limit of abundance, and the observed relationship with ES should be wedge shaped. We tested the relationship of ES with local abundance for 69 rain forest vertebrates in the Australian wet tropics. Ordinary least squares and quantile regressions revealed a positive relationship between ES and local abundance for most species (>84%). The relationships for these species were wedge shaped. We conclude that ES modeled from presence-only data provides useful information on spatial patterns of abundance, and we discuss implications of this in addressing important problems in ecology.

Variable responses of skinks to a common history of rainforest fluctuation: concordance between phylogeography and palaeo-distribution models.

There is a growing appreciation of impacts of late-Quaternary climate fluctuations on spatial patterns of species and genetic diversity. A major challenge is to understand how and why species respond individualistically to a common history of climate-induced habitat fluctuation. Here, we combine modelling of palaeo-distributions and mitochondrial-DNA phylogeographies to compare spatial patterns of population persistence and isolation across three species of rainforest skinks (Saproscincus spp.) with varying climatic preferences. Using Akaike Information Criterion model-averaged projections, all three species are predicted to have maintained one or more small populations in the northern Wet Tropics, multiple or larger populations in the central region, and few if any in the south. For the high-elevation species, Saproscincus czechurai, the warm-wet climate of the mid Holocene was most restrictive, whereas for the generalist S. basiliscus and lower-elevation S. tetradactyla, the cool-dry last glacial maximum was most restrictive. As expected, S. czechurai was the most genetically structured species, although relative to modelled distributions, S. basiliscus had surprisingly deep phylogeographical structure among southern rainforest isolates, implying long-term isolation and persistence. For both S. basiliscus and S. tetradactyla, there was high genetic diversity and complex phylogeographical patterns in the central Wet Tropics, reflecting persistence of large, structured populations. A previously identified vicariant barrier separating northern and central regions is supported, and results from these species also emphasize a historical persistence of populations south of another biogeographical break, the Tully Gorge. Overall, the results support the contention that in a topographically heterogeneous landscape, species with broader climatic niches may maintain higher and more structured genetic diversity due to persistence through varying climates.

Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being.

Distributions of Earth's species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation's Sustainable Development Goals.