Combining mesocosms with models reveals effects of global warming and ocean acidification on a temperate marine ecosystem.

Ocean warming and species exploitation have already caused large-scale reorganization of biological communities across the world. Accurate projections of future biodiversity change require a comprehensive understanding of how entire communities respond to global change. We combined a time-dynamic integrated food web modeling approach (Ecosim) with previous data from community-level mesocosm experiments to determine the independent and combined effects of ocean warming, ocean acidification and fisheries exploitation on a well-managed temperate coastal ecosystem. The mesocosm parameters enabled important physiological and behavioral responses to climate stressors to be projected for trophic levels ranging from primary producers to top predators, including sharks. Through model simulations, we show that under sustainable rates of fisheries exploitation, near-future warming or ocean acidification in isolation could benefit species biomass at higher trophic levels (e.g., mammals, birds, and demersal finfish) in their current climate ranges, with the exception of small pelagic fishes. However, under warming and acidification combined, biomass increases at higher trophic levels will be lower or absent, while in the longer term reduced productivity of prey species is unlikely to support the increased biomass at the top of the food web. We also show that increases in exploitation will suppress any positive effects of human-driven climate change, causing individual species biomass to decrease at higher trophic levels. Nevertheless, total future potential biomass of some fisheries species in temperate areas might remain high, particularly under acidification, because unharvested opportunistic species will likely benefit from decreased competition and show an increase in biomass. Ecological indicators of species composition such as the Shannon diversity index decline under all climate change scenarios, suggesting a trade-off between biomass gain and functional diversity. By coupling parameters from multilevel mesocosm food web experiments with dynamic food web models, we were able to simulate the generative mechanisms that drive complex responses of temperate marine ecosystems to global change. This approach, which blends theory with experimental data, provides new prospects for forecasting climate-driven biodiversity change and its effects on ecosystem processes.

Reconstructing colonization dynamics to establish how human activities transformed island biodiversity.

Drivers and dynamics of initial human migrations across individual islands and archipelagos are poorly understood, hampering assessments of subsequent modification of island biodiversity. We developed and tested a new statistical-simulation approach for reconstructing the pattern and pace of human migration across islands at high spatiotemporal resolutions. Using Polynesian colonisation of New Zealand as an example, we show that process-explicit models, informed by archaeological records and spatiotemporal reconstructions of past climates and environments, can provide new and important insights into the patterns and mechanisms of arrival and establishment of people on islands. We find that colonisation of New Zealand required there to have been a single founding population of approximately 500 people, arriving between 1233 and 1257 AD, settling multiple areas, and expanding rapidly over both North and South Islands. These verified spatiotemporal reconstructions of colonisation dynamics provide new opportunities to explore more extensively the potential ecological impacts of human colonisation on New Zealand's native biota and ecosystems.

Millennial processes of population decline, range contraction and near extinction of the European bison.

European bison (Bison bonasus) were widespread throughout Europe during the late Pleistocene. However, the contributions of environmental change and humans to their near extinction have never been resolved. Using process-explicit models, fossils and ancient DNA, we disentangle the combinations of threatening processes that drove population declines and regional extinctions of European bison through space and across time. We show that the population size of European bison declined abruptly at the termination of the Pleistocene in response to rapid environmental change, hunting by humans and their interaction. Human activities prevented populations of European bison from rebounding in the Holocene, despite improved environmental conditions. Hunting caused range loss in the north and east of its distribution, while land use change was responsible for losses in the west and south. Advances in hunting technologies from 1500 CE were needed to simulate low abundances observed in 1870 CE. While our findings show that humans were an important driver of the extinction of the European bison in the wild, vast areas of its range vanished during the Pleistocene-Holocene transition because of post-glacial environmental change. These areas of its former range have been climatically unsuitable for millennia and should not be considered in reintroduction efforts.

Impact of Holocene environmental change on the evolutionary ecology of an Arctic top predator.

The Arctic is among the most climatically sensitive environments on Earth, and the disappearance of multiyear sea ice in the Arctic Ocean is predicted within decades. As apex predators, polar bears are sentinel species for addressing the impact of environmental variability on Arctic marine ecosystems. By integrating genomics, isotopic analysis, morphometrics, and ecological modeling, we investigate how Holocene environmental changes affected polar bears around Greenland. We uncover reductions in effective population size coinciding with increases in annual mean sea surface temperature, reduction in sea ice cover, declines in suitable habitat, and shifts in suitable habitat northward. Furthermore, we show that west and east Greenlandic polar bears are morphologically, and ecologically distinct, putatively driven by regional biotic and genetic differences. Together, we provide insights into the vulnerability of polar bears to environmental change and how the Arctic marine ecosystem plays a vital role in shaping the evolutionary and ecological trajectories of its inhabitants.

Safeguarding nutrients from coral reefs under climate change.

The sustainability of coral reef fisheries is jeopardized by complex and interacting socio-ecological stressors that undermine their contribution to food and nutrition security. Climate change has emerged as one of the key stressors threatening coral reefs and their fish-associated services. How fish nutrient concentrations respond to warming oceans remains unclear but these responses are probably affected by both direct (metabolism and trophodynamics) and indirect (habitat and species range shifts) effects. Climate-driven coral habitat loss can cause changes in fish abundance and biomass, revealing potential winners and losers among major fisheries targets that can be predicted using ecological indicators and biological traits. A critical next step is to extend research focused on the quantity of available food (fish biomass) to also consider its nutritional quality, which is relevant to progress in the fields of food security and malnutrition. Biological traits are robust predictors of fish nutrient content and thus potentially indicate how climate-driven changes are expected to impact nutrient availability within future food webs on coral reefs. Here, we outline future research priorities and an anticipatory framework towards sustainable reef fisheries contributing to nutrition-sensitive food systems in a warming ocean.

Process-explicit models reveal the structure and dynamics of biodiversity patterns.

With ever-growing data availability and computational power at our disposal, we now have the capacity to use process-explicit models more widely to reveal the ecological and evolutionary mechanisms responsible for spatiotemporal patterns of biodiversity. Most research questions focused on the distribution of diversity cannot be answered experimentally, because many important environmental drivers and biological constraints operate at large spatiotemporal scales. However, we can encode proposed mechanisms into models, observe the patterns they produce in virtual environments, and validate these patterns against real-world data or theoretical expectations. This approach can advance understanding of generalizable mechanisms responsible for the distributions of organisms, communities, and ecosystems in space and time, advancing basic and applied science. We review recent developments in process-explicit models and how they have improved knowledge of the distribution and dynamics of life on Earth, enabling biodiversity to be better understood and managed through a deeper recognition of the processes that shape genetic, species, and ecosystem diversity.

Spatiotemporal influences of climate and humans on muskox range dynamics over multiple millennia.

Processes leading to range contractions and population declines of Arctic megafauna during the late Pleistocene and early Holocene are uncertain, with intense debate on the roles of human hunting, climatic change, and their synergy. Obstacles to a resolution have included an overreliance on correlative rather than process-explicit approaches for inferring drivers of distributional and demographic change. Here, we disentangle the ecological mechanisms and threats that were integral in the decline and extinction of the muskox (Ovibos moschatus) in Eurasia and in its expansion in North America using process-explicit macroecological models. The approach integrates modern and fossil occurrence records, ancient DNA, spatiotemporal reconstructions of past climatic change, species-specific population ecology, and the growth and spread of anatomically modern humans. We show that accurately reconstructing inferences of past demographic changes for muskox over the last 21,000 years require high dispersal abilities, large maximum densities, and a small Allee effect. Analyses of validated process-explicit projections indicate that climatic change was the primary driver of muskox distribution shifts and demographic changes across its previously extensive (circumpolar) range, with populations responding negatively to rapid warming events. Regional analyses show that the range collapse and extinction of the muskox in Europe (~13,000 years ago) was likely caused by humans operating in synergy with climatic warming. In Canada and Greenland, climatic change and human activities probably combined to drive recent population sizes. The impact of past climatic change on the range and extinction dynamics of muskox during the Pleistocene-Holocene transition signals a vulnerability of this species to future increased warming. By better establishing the ecological processes that shaped the distribution of the muskox through space and time, we show that process-explicit macroecological models have important applications for the future conservation and management of this iconic species in a warming Arctic.

Faster ocean warming threatens richest areas of marine biodiversity.

The vulnerability of marine biodiversity to accelerated rates of climatic change is poorly understood. By developing a new method for identifying extreme oceanic warming events during Earth's most recent deglaciation, and comparing these to 21st century projections, we show that future rates of ocean warming will disproportionately affect the most speciose marine communities, potentially threatening biodiversity in more than 70% of current-day global hotspots of marine species richness. The persistence of these richest areas of marine biodiversity will require many species to move well beyond the biogeographic realm where they are endemic, at rates of redistribution not previously seen. Our approach for quantifying exposure of biodiversity to past and future rates of oceanic warming provides new context and scalable information for deriving and strengthening conservation actions to safeguard marine biodiversity under climate change.

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.

Climate change negates positive CO2 effects on marine species biomass and productivity by altering the strength and direction of trophic interactions.

One of the biggest challenges in more accurately forecasting the effects of climate change on future food web dynamics relates to how climate change affects multi-trophic species interactions, particularly when multiple interacting stressors are considered. Using a dynamic food web model, we investigate the individual and combined effect of ocean warming and acidification on changes in trophic interaction strengths (both direct and indirect) and the consequent effects on biomass structure of food web functional groups. To do this, we mimicked a species-rich multi-trophic-level temperate shallow-water rocky reef food web and integrated empirical data from mesocosm experiments on altered species interactions under warming and acidification, into food-web models. We show that a low number of strong temperature-driven changes in direct trophic interactions (feeding and competition) will largely determine the magnitude of biomass change (either increase or decrease) of high-order consumers, with increasing consumer biomass suppressing that of prey species. Ocean acidification, in contrast, alters a large number of weak indirect interactions (e.g. cascading effects of increased or decreased abundances of other groups), enabling a large increase in consumer and prey biomass. The positive effects of ocean acidification are driven by boosted primary productivity, with energy flowing up to higher trophic levels. We show that warming is a much stronger driver of positive as well as negative modifications of species biomass compared to ocean acidification. Warming affects a much smaller number of existing trophic interactions, though, with direct consumer-resource effects being more important than indirect effects. We conclude that the functional role of consumers in future food webs will be largely regulated by alterations in the strength of direct trophic interactions under ocean warming, with ensuing effects on the biomass structure of marine food webs.

Identifying island safe havens to prevent the extinction of the World's largest lizard from global warming.

The Komodo dragon (Varanus komodoensis) is an endangered, island-endemic species with a naturally restricted distribution. Despite this, no previous studies have attempted to predict the effects of climate change on this iconic species. We used extensive Komodo dragon monitoring data, climate, and sea-level change projections to build spatially explicit demographic models for the Komodo dragon. These models project the species' future range and abundance under multiple climate change scenarios. We ran over one million model simulations with varying model parameters, enabling us to incorporate uncertainty introduced from three main sources: (a) structure of global climate models, (b) choice of greenhouse gas emission trajectories, and (c) estimates of Komodo dragon demographic parameters. Our models predict a reduction in range-wide Komodo dragon habitat of 8%-87% by 2050, leading to a decrease in habitat patch occupancy of 25%-97% and declines of 27%-99% in abundance across the species' range. We show that the risk of extirpation on the two largest protected islands in Komodo National Park (Rinca and Komodo) was lower than other island populations, providing important safe havens for Komodo dragons under global warming. Given the severity and rate of the predicted changes to Komodo dragon habitat patch occupancy (a proxy for area of occupancy) and abundance, urgent conservation actions are required to avoid risk of extinction. These should, as a priority, be focused on managing habitat on the islands of Komodo and Rinca, reflecting these islands' status as important refuges for the species in a warming world. Variability in our model projections highlights the importance of accounting for uncertainties in demographic and environmental parameters, structural assumptions of global climate models, and greenhouse gas emission scenarios when simulating species metapopulation dynamics under climate change.

StableClim, continuous projections of climate stability from 21000 BP to 2100 CE at multiple spatial scales.

Paleoclimatic data are used in eco-evolutionary models to improve knowledge of biogeographical processes that drive patterns of biodiversity through time, opening windows into past climate-biodiversity dynamics. Applying these models to harmonised simulations of past and future climatic change can strengthen forecasts of biodiversity change. StableClim provides continuous estimates of climate stability from 21,000 years ago to 2100 C.E. for ocean and terrestrial realms at spatial scales that include biogeographic regions and climate zones. Climate stability is quantified using annual trends and variabilities in air temperature and precipitation, and associated signal-to-noise ratios. Thresholds of natural variability in trends in regional- and global-mean temperature allow periods in Earth's history when climatic conditions were warming and cooling rapidly (or slowly) to be identified and climate stability to be estimated locally (grid-cell) during these periods of accelerated change. Model simulations are validated against independent paleoclimate and observational data. Projections of climatic stability, accessed through StableClim, will improve understanding of the roles of climate in shaping past, present-day and future patterns of biodiversity.

Using paleo-archives to safeguard biodiversity under climate change.

Strategies for 21st-century environmental management and conservation under global change require a strong understanding of the biological mechanisms that mediate responses to climate- and human-driven change to successfully mitigate range contractions, extinctions, and the degradation of ecosystem services. Biodiversity responses to past rapid warming events can be followed in situ and over extended periods, using cross-disciplinary approaches that provide cost-effective and scalable information for species' conservation and the maintenance of resilient ecosystems in many bioregions. Beyond the intrinsic knowledge gain such integrative research will increasingly provide the context, tools, and relevant case studies to assist in mitigating climate-driven biodiversity losses in the 21st century and beyond.

Evolutionary history and past climate change shape the distribution of genetic diversity in terrestrial mammals.

Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life. Yet, global patterns of GD and its drivers remain elusive. Here we assess existing biodiversity theories to explain and predict the global distribution of GD in terrestrial mammal assemblages. We find a strong positive covariation between GD and interspecific diversity, with evolutionary time, reflected in phylogenetic diversity, being the best predictor of GD. Moreover, we reveal the negative effect of past rapid climate change and the positive effect of inter-annual precipitation variability in shaping GD. Our models, explaining almost half of the variation in GD globally, uncover the importance of deep evolutionary history and past climate stability in accumulating and maintaining intraspecific diversity, and constitute a crucial step towards reducing the Wallacean shortfall for an important dimension of biodiversity.

Models of spatiotemporal variation in rabbit abundance reveal management hot spots for an invasive species.

The European rabbit (Oryctolagus cuniculus) is a notorious economic and environmental pest species in its invasive range. To better understand the population and range dynamics of this species, 41 yr of abundance data have been collected from 116 unique sites across a broad range of climatic and environmental conditions in Australia. We analyzed this time series of abundance data to determine whether interannual variation in climatic conditions can be used to map historic, contemporary, and potential future fluctuations in rabbit abundance from regional to continental scales. We constructed a hierarchical Bayesian regression model of relative abundance that corrected for observation error and seasonal biases. The corrected abundances were regressed against environmental and disease variables in order to project high spatiotemporal resolution, continent-wide rabbit abundances. We show that rabbit abundance in Australia is highly variable in space and time, being driven primarily by internnual variation in temperature and precipitation in concert with the prevalence of a non-pathogenic virus. Moreover, we show that internnual variation in local spatial abundances can be mapped effectively at a continental scale using highly resolved spatiotemporal predictors, allowing "hot spots" of persistently high rabbit abundance to be identified. Importantly, cross-validated model performance was fair to excellent within and across distinct climate zones. Long-term monitoring data for invasive species can be used to map fine-scale spatiotemporal fluctuations in abundance patterns when accurately accounting for inherent sampling biases. Our analysis provides ecologists and pest managers with a clearer understanding of the determinants of rabbit abundance in Australia, offering an important new approach for predicting spatial abundance patterns of invasive species at the near-term temporal scales that are directly relevant to resource management.

Modeling the distribution of a wide-ranging invasive species using the sampling efforts of expert and citizen scientists.

In its invasive range in Australia, the European rabbit threatens the persistence of native flora and fauna and damages agricultural production. Understanding its distribution and ecological niche is critical for developing management plans to reduce populations and avoid further biodiversity and economic losses.We developed an ensemble of species distribution models (SDMs) to determine the geographic range limits and habitat suitability of the rabbit in Australia. We examined the advantage of incorporating data collected by citizens (separately and jointly with expert data) and explored issues of spatial biases in occurrence data by implementing different approaches to generate pseudo-absences. We evaluated the skill of our model using three approaches: cross-validation, out-of-region validation, and evaluation of the covariate response curves according to expert knowledge of rabbit ecology.Combining citizen and expert occurrence data improved model skill based on cross-validation, spatially reproduced important aspects of rabbit ecology, and reduced the need to extrapolate results beyond the studied areas.Our ensemble model projects that rabbits are distributed across approximately two thirds of Australia. Annual maximum temperatures >25°C and annual minimum temperatures >10°C define, respectively, the southern and northern most range limits of its distribution. In the arid and central regions, close access to permanent water (≤~ 0.4 km) and reduced clay soil composition (~20%-50%) were the major factors influencing the probability of occurrence of rabbits. Synthesis and applications. Our results show that citizen science data can play an important role in managing invasive species by providing missing information on occurrences in regions not surveyed by experts because of logistics or financial constraints. The additional sampling effort provided by citizens can improve the capacity of SDMs to capture important elements of a species ecological niche, improving the capacity of statistical models to accurately predict the geographic range of invasive species.

Cradles of diversity are unlikely relics of regional climate stability.

The stability of regional climates on millennial timescales is theorised to be a primary determinant of nearby diversification [1-5]. Using simulated patterns of past temperature change at monthly timescales [6], we show that the locations of climatically stable regions are likely to have varied considerably across and within millennia during glacial-interglacial cycles of the Late Quaternary. This result has important implications for the role of regional climate stability in theories of speciation, because long-term climate refugia are typically presumed to be 'cradles' of diversity (areas of high speciation) only if they remain stable across Milankovitch climate oscillations [1-5], which operate on multi-millennial time scales [7].

The Australian National Rabbit Database: 50 yr of population monitoring of an invasive species.

With ongoing introductions into Australia since the 1700s, the European rabbit (Oryctolagus cuniculus) has become one of the most widely distributed and abundant vertebrate pests, adversely impacting Australia's biodiversity and agroeconomy. To understand the population and range dynamics of the species and its impacts better, occurrence and abundance data have been collected by researchers and citizens from sites covering a broad spectrum of climatic and environmental conditions in Australia. The lack of a common and accessible repository for these data has, however, limited their use in determining important spatiotemporal drivers of the structure and dynamics of the geographical range of rabbits in Australia. To meet this need, we created the Australian National Rabbit Database, which combines more than 50 yr of historical and contemporary survey data collected from throughout the range of the species in Australia. The survey data, obtained from a suite of complementary monitoring methods, were combined with high-resolution weather, climate, and environmental information, and an assessment of data quality. The database provides records of rabbit occurrence (689,265 records) and abundance (51,241 records, >120 distinct sites) suitable for identifying the spatiotemporal drivers of the rabbit's distribution and for determining spatial patterns of variation in its key life-history traits, including maximum rates of population growth. Because all data are georeferenced and date stamped, they can be coupled with information from other databases and spatial layers to explore the potential effects of rabbit occurrence and abundance on Australia's native wildlife and agricultural production. The Australian National Rabbit Database is an important tool for understanding and managing the European rabbit in its invasive range and its effects on native biodiversity and agricultural production. It also provides a valuable resource for addressing questions related to the biology, success, and impacts of invasive species more generally. No copyright or proprietary restrictions are associated with the use of this data set other than citation of this Data Paper.

Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts.

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high-resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown-of-thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km2 , predicting a mean annual coral loss of -0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner-shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no-take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.

Exploring mechanisms and origins of reduced dispersal in island Komodo dragons.

Loss of dispersal typifies island biotas, but the selective processes driving this phenomenon remain contentious. This is because selection via, both indirect (e.g. relaxed selection or island syndromes) and direct (e.g. natural selection or spatial sorting) processes may be involved, and no study has yet convincingly distinguished between these alternatives. Here, we combined observational and experimental analyses of an island lizard, the Komodo dragon (Varanus komodoensis, the world's largest lizard), to provide evidence for the actions of multiple processes that could contribute to island dispersal loss. In the Komodo dragon, concordant results from telemetry, simulations, experimental translocations, mark-recapture, and gene flow studies indicated that despite impressive physical and sensory capabilities for long-distance movement, Komodo dragons exhibited near complete dispersal restriction: individuals rarely moved beyond the valleys they were born/captured in. Importantly, lizard site-fidelity was insensitive to common agents of dispersal evolution (i.e. indices of risk for inbreeding, kin and intraspecific competition, and low habitat quality) that consequently reduced survival of resident individuals. We suggest that direct selection restricts movement capacity (e.g. via benefits of spatial philopatry and increased costs of dispersal) alongside use of dispersal-compensating traits (e.g. intraspecific niche partitioning) to constrain dispersal in island species.