Corrigendum: Reductions in global biodiversity loss predicted from conservation spending.

This corrects the article DOI: 10.1038/nature24295.

Reductions in global biodiversity loss predicted from conservation spending.

Halting global biodiversity loss is central to the Convention on Biological Diversity and United Nations Sustainable Development Goals, but success to date has been very limited. A critical determinant of success in achieving these goals is the financing that is committed to maintaining biodiversity; however, financing decisions are hindered by considerable uncertainty over the likely impact of any conservation investment. For greater effectiveness, we need an evidence-based model that shows how conservation spending quantitatively reduces the rate of biodiversity loss. Here we demonstrate such a model, and empirically quantify how conservation investment reduced biodiversity loss in 109 countries (signatories to the Convention on Biological Diversity and Sustainable Development Goals), by a median average of 29% per country between 1996 and 2008. We also show that biodiversity changes in signatory countries can be predicted with high accuracy, using a dual model that balances the effects of conservation investment against those of economic, agricultural and population growth (human development pressures). Decision-makers can use this model to forecast the improvement that any proposed biodiversity budget would achieve under various scenarios of human development pressure, and then compare these forecasts to any chosen policy target. We find that the impact of spending decreases as human development pressures grow, which implies that funding may need to increase over time. The model offers a flexible tool for balancing the Sustainable Development Goals of human development and maintaining biodiversity, by predicting the dynamic changes in conservation finance that will be needed as human development proceeds.

Parasite sharing in wild ungulates and their predators: Effects of phylogeny, range overlap, and trophic links.

Understanding factors that facilitate interspecific pathogen transmission is a central issue for conservation, agriculture, and human health. Past work showed that host phylogenetic relatedness and geographical proximity can increase cross-species transmission, but further work is needed to examine the importance of host traits, and species interactions such as predation, in determining the degree to which parasites are shared between hosts. Here we consider the factors that predict patterns of parasite sharing across a diverse assemblage of 116 wild ungulates (i.e., hoofed mammals in the Artiodactyla and Perissodactyla) and nearly 900 species of micro- and macroparasites, controlling for differences in total parasite richness and host sampling effort. We also consider the effects of trophic links on parasite sharing between ungulates and carnivores. We tested for the relative influence of range overlap, phylogenetic distance, body mass, and ecological dissimilarity (i.e., the distance separating species in a Euclidean distance matrix based on standardized traits) on parasite sharing. We also tested for the effects of variation in study effort as a potential source of bias in our data, and tested whether carnivores reported to feed on ungulates have more ungulate parasites than those that use other resources. As in other groups, geographical range overlap and phylogenetic similarity predicted greater parasite community similarity in ungulates. Ecological dissimilarity showed a weak negative relationship with parasite sharing. Counter to our expectations, differences, not similarity, in host body mass predicted greater parasite sharing between pairs of ungulate hosts. Pairs of well-studied host species showed higher overlap than poorly studied species, although including sampling effort did not reduce the importance of biological traits in our models. Finally, carnivores that feed on ungulates harboured a greater richness of ungulate helminths. Overall, we show that the factors that predict parasite sharing in wild ungulates are similar to those known for other mammal groups, and demonstrate the importance of controlling for heterogeneity in host sampling effort in future analyses of parasite sharing. We also show that ecological interactions, in this case trophic links via predation, can allow sharing of some parasite species among distantly related host species.

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts.

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Targeting global conservation funding to limit immediate biodiversity declines.

Inadequate funding levels are a major impediment to effective global biodiversity conservation and are likely associated with recent failures to meet United Nations biodiversity targets. Some countries are more severely underfunded than others and therefore represent urgent financial priorities. However, attempts to identify these highly underfunded countries have been hampered for decades by poor and incomplete data on actual spending, coupled with uncertainty and lack of consensus over the relative size of spending gaps. Here, we assemble a global database of annual conservation spending. We then develop a statistical model that explains 86% of variation in conservation expenditures, and use this to identify countries where funding is robustly below expected levels. The 40 most severely underfunded countries contain 32% of all threatened mammalian diversity and include neighbors in some of the world's most biodiversity-rich areas (Sundaland, Wallacea, and Near Oceania). However, very modest increases in international assistance would achieve a large improvement in the relative adequacy of global conservation finance. Our results could therefore be quickly applied to limit immediate biodiversity losses at relatively little cost.

The path to host extinction can lead to loss of generalist parasites.

Host extinction can alter disease transmission dynamics, influence parasite extinction and ultimately change the nature of host-parasite systems. While theory predicts that single-host parasites are among the parasite species most susceptible to extinction following declines in their hosts, documented parasite extinctions are rare. Using a comparative approach, we investigate how the richness of single-host and multi-host parasites is influenced by extinction risk among ungulate and carnivore hosts. Host-parasite associations for free-living carnivores (order Carnivora) and terrestrial ungulates (orders Perissodactyla + Cetartiodactyla minus cetaceans) were merged with host trait data and IUCN Red List status to explore the distribution of single-host and multi-host parasites among threatened and non-threatened hosts. We find that threatened ungulates harbour a higher proportion of single-host parasites compared to non-threatened ungulates, which is explained by decreases in the richness of multi-host parasites. However, among carnivores threat status is not a significant predictor of the proportion of single-host parasites, or the richness of single-host or multi-host parasites. The loss of multi-host parasites from threatened ungulates may be explained by decreased cross-species contact as hosts decline and habitats become fragmented. Among carnivores, threat status may not be important in predicting patterns of parasite specificity because host decline results in equal losses of both single-host parasites and multi-host parasites through reduction in average population density and frequency of cross-species contact. Our results contrast with current models of parasite coextinction and highlight the need for updated theories that are applicable across host groups and account for both inter- and intraspecific contact.

Estimating the normal background rate of species extinction.

A key measure of humanity's global impact is by how much it has increased species extinction rates. Familiar statements are that these are 100-1000 times pre-human or background extinction levels. Estimating recent rates is straightforward, but establishing a background rate for comparison is not. Previous researchers chose an approximate benchmark of 1 extinction per million species per year (E/MSY). We explored disparate lines of evidence that suggest a substantially lower estimate. Fossil data yield direct estimates of extinction rates, but they are temporally coarse, mostly limited to marine hard-bodied taxa, and generally involve genera not species. Based on these data, typical background loss is 0.01 genera per million genera per year. Molecular phylogenies are available for more taxa and ecosystems, but it is debated whether they can be used to estimate separately speciation and extinction rates. We selected data to address known concerns and used them to determine median extinction estimates from statistical distributions of probable values for terrestrial plants and animals. We then created simulations to explore effects of violating model assumptions. Finally, we compiled estimates of diversification-the difference between speciation and extinction rates for different taxa. Median estimates of extinction rates ranged from 0.023 to 0.135 E/MSY. Simulation results suggested over- and under-estimation of extinction from individual phylogenies partially canceled each other out when large sets of phylogenies were analyzed. There was no evidence for recent and widespread pre-human overall declines in diversity. This implies that average extinction rates are less than average diversification rates. Median diversification rates were 0.05-0.2 new species per million species per year. On the basis of these results, we concluded that typical rates of background extinction may be closer to 0.1 E/MSY. Thus, current extinction rates are 1,000 times higher than natural background rates of extinction and future rates are likely to be 10,000 times higher.

The maximum rate of mammal evolution.

How fast can a mammal evolve from the size of a mouse to the size of an elephant? Achieving such a large transformation calls for major biological reorganization. Thus, the speed at which this occurs has important implications for extensive faunal changes, including adaptive radiations and recovery from mass extinctions. To quantify the pace of large-scale evolution we developed a metric, clade maximum rate, which represents the maximum evolutionary rate of a trait within a clade. We applied this metric to body mass evolution in mammals over the last 70 million years, during which multiple large evolutionary transitions occurred in oceans and on continents and islands. Our computations suggest that it took a minimum of 1.6, 5.1, and 10 million generations for terrestrial mammal mass to increase 100-, and 1,000-, and 5,000-fold, respectively. Values for whales were down to half the length (i.e., 1.1, 3, and 5 million generations), perhaps due to the reduced mechanical constraints of living in an aquatic environment. When differences in generation time are considered, we find an exponential increase in maximum mammal body mass during the 35 million years following the Cretaceous-Paleogene (K-Pg) extinction event. Our results also indicate a basic asymmetry in macroevolution: very large decreases (such as extreme insular dwarfism) can happen at more than 10 times the rate of increases. Our findings allow more rigorous comparisons of microevolutionary and macroevolutionary patterns and processes.

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing.

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.

Phylogenetically related and ecologically similar carnivores harbour similar parasite assemblages.

Most parasites infect multiple hosts, but what factors determine the range of hosts a given parasite can infect? Understanding the broad scale determinants of parasite distributions across host lineages is important for predicting pathogen emergence in new hosts and for estimating pathogen diversity in understudied host species. In this study, we used a new data set on 793 parasite species reported from free-ranging populations of 64 carnivore species to examine the factors that influence parasite sharing between host species. Our results showed that parasites are more commonly shared between phylogenetically related host species pairs. Additionally, host species with higher similarity in biological traits and greater geographic range overlap were also more likely to share parasite species. Of three measures of phylogenetic relatedness considered here, the number divergence events that separated host species pairs most strongly influenced the likelihood of parasite sharing. We also showed that viruses and helminths tend to infect carnivore hosts within more restricted phylogenetic ranges than expected by chance. Overall, our results underscore the importance of host evolutionary history in determining parasite host range, even when simultaneously considering other factors such as host ecology and geographic distribution.

Global trends in emerging infectious diseases.

Emerging infectious diseases (EIDs) are a significant burden on global economies and public health. Their emergence is thought to be driven largely by socio-economic, environmental and ecological factors, but no comparative study has explicitly analysed these linkages to understand global temporal and spatial patterns of EIDs. Here we analyse a database of 335 EID 'events' (origins of EIDs) between 1940 and 2004, and demonstrate non-random global patterns. EID events have risen significantly over time after controlling for reporting bias, with their peak incidence (in the 1980s) concomitant with the HIV pandemic. EID events are dominated by zoonoses (60.3% of EIDs): the majority of these (71.8%) originate in wildlife (for example, severe acute respiratory virus, Ebola virus), and are increasing significantly over time. We find that 54.3% of EID events are caused by bacteria or rickettsia, reflecting a large number of drug-resistant microbes in our database. Our results confirm that EID origins are significantly correlated with socio-economic, environmental and ecological factors, and provide a basis for identifying regions where new EIDs are most likely to originate (emerging disease 'hotspots'). They also reveal a substantial risk of wildlife zoonotic and vector-borne EIDs originating at lower latitudes where reporting effort is low. We conclude that global resources to counter disease emergence are poorly allocated, with the majority of the scientific and surveillance effort focused on countries from where the next important EID is least likely to originate.

Interconnecting global threats: climate change, biodiversity loss, and infectious diseases.

The concurrent pressures of rising global temperatures, rates and incidence of species decline, and emergence of infectious diseases represent an unprecedented planetary crisis. Intergovernmental reports have drawn focus to the escalating climate and biodiversity crises and the connections between them, but interactions among all three pressures have been largely overlooked. Non-linearities and dampening and reinforcing interactions among pressures make considering interconnections essential to anticipating planetary challenges. In this Review, we define and exemplify the causal pathways that link the three global pressures of climate change, biodiversity loss, and infectious disease. A literature assessment and case studies show that the mechanisms between certain pairs of pressures are better understood than others and that the full triad of interactions is rarely considered. Although challenges to evaluating these interactions-including a mismatch in scales, data availability, and methods-are substantial, current approaches would benefit from expanding scientific cultures to embrace interdisciplinarity and from integrating animal, human, and environmental perspectives. Considering the full suite of connections would be transformative for planetary health by identifying potential for co-benefits and mutually beneficial scenarios, and highlighting where a narrow focus on solutions to one pressure might aggravate another.

Effects of allometry, productivity and lifestyle on rates and limits of body size evolution.

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow-fast life-history continuum, and the allometric scaling of generation time to predict a clade's evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow-fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.

The delayed rise of present-day mammals.

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals.

Traits, trees and taxa: global dimensions of biodiversity in mammals.

Measures of biodiversity encompass variation along several dimensions such as species richness (SR), phylogenetic diversity (PD) and functional/trait diversity (TD). At the global scale, it is widely recognized that SR and PD are strongly correlated, but the extent to which either tends to capture variation in TD is unclear. Here, we assess relationships among PD, SR and TD for a number of traits both across clades and regional assemblages of mammals. We also contrast results using two different measures of TD, trait variance and a new measure we refer to as trait bin filling (the number of orders of magnitude of variation that contain at least one species). When TD is defined as trait variance, PD is a much stronger correlate of TD than SR across clades, consistent with hypotheses about the conservation value of PD. However, when TD is defined as bin filling, PD and SR show similar correlations with TD across clades and space. We also investigate potential losses of SR, PD and TD if species that are currently threatened were to go extinct, and find that threatened PD is often a similar predictor of threatened TD as SR.

How global extinctions impact regional biodiversity in mammals.

Phylogenetic diversity (PD) represents the evolutionary history of a species assemblage and is a valuable measure of biodiversity because it captures not only species richness but potentially also genetic and functional diversity. Preserving PD could be critical for maintaining the functional integrity of the world's ecosystems, and species extinction will have a large impact on ecosystems in areas where the ecosystem cost per species extinction is high. Here, we show that impacts from global extinctions are linked to spatial location. Using a phylogeny of all mammals, we compare regional losses of PD against a model of random extinction. At regional scales, losses differ dramatically: several biodiversity hotspots in southern Asia and Amazonia will lose an unexpectedly large proportion of PD. Global analyses may therefore underestimate the impacts of extinction on ecosystem processes and function because they occur at finer spatial scales within the context of natural biogeography.

Global distribution and conservation of rare and threatened vertebrates.

Global conservation strategies commonly assume that different taxonomic groups show congruent geographical patterns of diversity, and that the distribution of extinction-prone species in one group can therefore act as a surrogate for vulnerable species in other groups when conservation decisions are being made. The validity of these assumptions remains unclear, however, because previous tests have been limited in both geographical and taxonomic extent. Here we use a database on the global distribution of 19,349 living bird, mammal and amphibian species to show that, although the distribution of overall species richness is very similar among these groups, congruence in the distribution of rare and threatened species is markedly lower. Congruence is especially low among the very rarest species. Cross-taxon congruence is also highly scale dependent, being particularly low at the finer spatial resolutions relevant to real protected areas. 'Hotspots' of rarity and threat are therefore largely non-overlapping across groups, as are areas chosen to maximize species complementarity. Overall, our results indicate that 'silver-bullet' conservation strategies alone will not deliver efficient conservation solutions. Instead, priority areas for biodiversity conservation must be based on high-resolution data from multiple taxa.

Colloquium paper: phylogenetic trees and the future of mammalian biodiversity.

Phylogenies describe the origins and history of species. However, they can also help to predict species' fates and so can be useful tools for managing the future of biodiversity. This article starts by sketching how phylogenetic, geographic, and trait information can be combined to elucidate present mammalian diversity patterns and how they arose. Recent diversification rates and standing diversity show different geographic patterns, indicating that cradles of diversity have moved over time. Patterns in extinction risk reflect both biological differences among mammalian lineages and differences in threat intensity among regions. Phylogenetic comparative analyses indicate that for small-bodied mammals, extinction risk is governed mostly by where the species live and the intensity of the threats, whereas for large-bodied mammals, ecological differences also play an important role. This modeling approach identifies species whose intrinsic biology renders them particularly vulnerable to increased human pressure. We outline how the approach might be extended to consider future trends in anthropogenic drivers, to identify likely future battlegrounds of mammalian conservation, and the likely casualties. This framework could help to highlight consequences of choosing among different future climatic and socioeconomic scenarios. We end by discussing priority-setting, showing how alternative currencies for diversity can suggest very different priorities. We argue that aiming to maximize long-term evolutionary responses is inappropriate, that conservation planning needs to consider costs as well as benefits, and that proactive conservation of largely intact systems should be part of a balanced strategy.

Quaternary climate change and the geographic ranges of mammals.

A species' range can be a proxy for its ecological well-being. Species with small and shrinking range distributions are particularly vulnerable to extinction. Future climate change scenarios are predicted to affect species' geographical extents, but data on how species' distributions respond to changing climate are largely anecdotal, and our understanding of the determinants and limits to species geographic ranges is surprisingly poor. Here we show that mammal species in more historically variable environments have larger geographical ranges. However, the relationship between range size and long-term climate trends cannot be explained by variation in our estimates of habitat specificity. We suggest that large oscillations in Quaternary temperatures may have shaped the contemporary distribution of range sizes via the selective extirpation of small-ranged species during glacial expansion and/or recolonization by good dispersers after glacial retreats. The effect of current climate change on species' distributions and extinctions may therefore be determined by the geographical coincidence between historical and future climate scenarios, the "mesh size" of the extinction/dispersal filter imposed by past climate change, and whether similar ecological and evolutionary responses to historical climatic change are appropriate in an increasingly transformed and fragmented landscape.

Global patterns in the phylogenetic structure of island mammal assemblages.

Assemblage-level phylogenies carry the signature of ecological and evolutionary processes, which may provide useful information on modes of assemblage formation. We present a global-scale analysis of the emergent phylogenetic properties of mammal assemblages on islands, in which we compared the structure of 595 island assemblages with null models constructed under four alternative definitions of regional source pools. Although most assemblages had a structure indistinguishable from random samples, for some mammal taxa, up to 40% of island assemblages were phylogenetically overdispersed. This suggests that in at least some cases, the processes that shape island faunas are not independent of phylogeny. Furthermore, measures of phylogenetic structure were associated in some cases with island geographical features (size, maximum elevation and habitat diversity). Our results suggest that part of the signal of assemblage formation processes is detectable in the phylogenies of contemporary island mammal faunas, though much is obscured by the complexity of these processes.