Taal Levi

Collapse of the world's largest herbivores.

The collapsing populations of large herbivores will have extensive ecological and social consequences. Large wild herbivores are crucial to ecosystems and human societies. We highlight the 74 largest terrestrial herbivore species on Earth (body mass ≥100 kg), the threats they face, their important and often overlooked ecosystem effects, and the conservation efforts needed to save them and their predators from extinction. Large herbivores are generally facing dramatic population declines and range contractions, such that ~60% are threatened with extinction. Nearly all threatened species are in developing countries, where major threats include hunting, land-use change, and resource depression by livestock. Loss of large herbivores can have cascading effects on other species including large carnivores, scavengers, mesoherbivores, small mammals, and ecological processes involving vegetation, hydrology, nutrient cycling, and fire regimes. The rate of large herbivore decline suggests that ever-larger swaths of the world will soon lack many of the vital ecological services these animals provide, resulting in enormous ecological and social costs.

Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding

To manage and conserve biodiversity, one must know what is being lost, where, and why, as well as which remedies are likely to be most effective. Metabarcoding technology can characterise the species compositions of mass samples of eukaryotes or of environmental DNA. Here, we validate metabarcoding by testing it against three high-quality standard data sets that were collected in Malaysia (tropical), China (subtropical) and the United Kingdom (temperate) and that comprised 55,813 arthropod and bird specimens identified to species level with the expenditure of 2,505 person-hours of taxonomic expertise. The metabarcode and standard data sets exhibit statistically correlated alpha- and beta-diversities, and the two data sets produce similar policy conclusions for two conservation applications: restoration ecology and systematic conservation planning. Compared with standard biodiversity data sets, metabarcoded samples are taxonomically more comprehensive, many times quicker to produce, less reliant on taxonomic expertise and auditable by third parties, which is essential for dispute resolution.

Several scales of biodiversity affect ecosystem multifunctionality.

Society values landscapes that reliably provide many ecosystem functions. As the study of ecosystem functioning expands to include more locations, time spans, and functions, the functional importance of individual species is becoming more apparent. However, the functional importance of individual species does not necessarily translate to the functional importance of biodiversity measured in whole communities of interacting species. Furthermore, ecological diversity at scales larger than neighborhood species richness could also influence the provision of multiple functions over extended time scales. We created experimental landscapes based on whole communities from the world’s longest running biodiversity-functioning field experiment to investigate how local species richness (α diversity), distinctness among communities (β diversity), and larger scale species richness (γ diversity) affected eight ecosystem functions over 10 y. Using both threshold-based and unique multifunctionality metrics, we found that α diversity had strong positive effects on most individual functions and multifunctionality, and that positive effects of β and γ diversity emerged only when multiple functions were considered simultaneously. Higher β diversity also reduced the variability in multifunctionality. Thus, in addition to conserving important species, maintaining ecosystem multifunctionality will require diverse landscape mosaics of diverse communities.

Deer, predators, and the emergence of Lyme disease

Lyme disease is the most prevalent vector-borne disease in North America, and both the annual incidence and geographic range are increasing. The emergence of Lyme disease has been attributed to a century-long recovery of deer, an important reproductive host for adult ticks. However, a growing body of evidence suggests that Lyme disease risk may now be more dynamically linked to fluctuations in the abundance of small-mammal hosts that are thought to infect the majority of ticks. The continuing and rapid increase in Lyme disease over the past two decades, long after the recolonization of deer, suggests that other factors, including changes in the ecology of small-mammal hosts may be responsible for the continuing emergence of Lyme disease. We present a theoretical model that illustrates how reductions in small-mammal predators can sharply increase Lyme disease risk. We then show that increases in Lyme disease in the northeastern and midwestern United States over the past three decades are frequently uncorrelated with deer abundance and instead coincide with a range-wide decline of a key small-mammal predator, the red fox, likely due to expansion of coyote populations. Further, across four states we find poor spatial correlation between deer abundance and Lyme disease incidence, but coyote abundance and fox rarity effectively predict the spatial distribution of Lyme disease in New York. These results suggest that changes in predator communities may have cascading impacts that facilitate the emergence of zoonotic diseases, the vast majority of which rely on hosts that occupy low trophic levels.

Wolves—coyotes—foxes: a cascade among carnivores

Due to the widespread eradication of large canids and felids, top predators in many terrestrial ecosystems are now medium-sized carnivores such as coyotes. Coyotes have been shown to increase songbird and rodent abundance and diversity by suppressing populations of small carnivores such as domestic cats and foxes. The restoration of gray wolves to many parts of North America, however, could alter this interaction chain. Here we use a 30-year time series of wolf, coyote, and fox relative abundance from the state of Minnesota, USA, to show that wolves suppress coyote populations, which in turn releases foxes from top-down control by coyotes. In contrast to mesopredator release theory, which has often considered the consequence of top predator removal in a three-species interaction chain (e.g., coyote-fox-prey), the presence of the top predator releases the smaller predator in a four-species interaction chain. Thus, heavy predation by abundant small predators might be more similar to the historical ecosystem before top-predator extirpation. The restructuring of predator communities due to the loss or restoration of top predators is likely to alter the size spectrum of heavily consumed prey with important implications for biodiversity and human health.

Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests

Significance A standardized network of wildlife surveys across 166 Amazonian hunted and nonhunted forests, combined with basin-wide spatial modeling of central-place hunting pressure, reveal the degree to which arboreal frugivores have been extirpated by hunters and the spatial extent of overhunting for harvest-sensitive frugivore species across the Brazilian Amazon. Simulations based on data from 2,345 1-ha tree plots inventoried throughout Brazilian Amazonia then show widespread erosion of forest carbon stocks in the world’s largest tropical forest region. Tropical forests are the global cornerstone of biological diversity, and store 55% of the forest carbon stock globally, yet sustained provisioning of these forest ecosystem services may be threatened by hunting-induced extinctions of plant–animal mutualisms that maintain long-term forest dynamics. Large-bodied Atelinae primates and tapirs in particular offer nonredundant seed-dispersal services for many large-seeded Neotropical tree species, which on average have higher wood density than smaller-seeded and wind-dispersed trees. We used field data and models to project the spatial impact of hunting on large primates by ∼1 million rural households throughout the Brazilian Amazon. We then used a unique baseline dataset on 2,345 1-ha tree plots arrayed across the Brazilian Amazon to model changes in aboveground forest biomass under different scenarios of hunting-induced large-bodied frugivore extirpation. We project that defaunation of the most harvest-sensitive species will lead to losses in aboveground biomass of between 2.5–5.8% on average, with some losses as high as 26.5–37.8%. These findings highlight an urgent need to manage the sustainability of game hunting in both protected and unprotected tropical forests, and place full biodiversity integrity, including populations of large frugivorous vertebrates, firmly in the agenda of reducing emissions from deforestation and forest degradation (REDD+) programs.

Saving the World's Terrestrial Megafauna

From the late Pleistocene to the Holocene, and now the so called Anthropocene, humans have been driving an ongoing series of species declines and extinctions (Dirzo et al. 2014). Large-bodied mammals are typically at a higher risk of extinction than smaller ones (Cardillo et al. 2005). However, in some circumstances terrestrial megafauna populations have been able to recover some of their lost numbers due to strong conservation and political commitment, and human cultural changes (Chapron et al. 2014). Indeed many would be in considerably worse predicaments in the absence of conservation action (Hoffmann et al. 2015). Nevertheless, most mammalian megafauna face dramatic range contractions and population declines. In fact, 59% of the world’s largest carnivores (≥ 15 kg, n = 27) and 60% of the world’s largest herbivores (≥ 100 kg, n = 74) are classified as threatened with extinction on the International Union for the Conservation of Nature (IUCN) Red List (supplemental table S1 and S2). This situation is particularly dire in sub-Saharan Africa and Southeast Asia, home to the greatest diversity of extant megafauna (figure 1). Species at risk of extinction include some of the world’s most iconic animals—such as gorillas, rhinos, and big cats (figure 2 top row)—and, unfortunately, they are vanishing just as science is discovering their essential ecological roles (Estes et al. 2011). Here, our objectives are to raise awareness of how these megafauna are imperiled (species in supplemental table S1 and S2) and to stimulate broad interest in developing specific recommendations and concerted action to conserve them.

Bushmeat hunting and extinction risk to the world’s mammals

Terrestrial mammals are experiencing a massive collapse in their population sizes and geographical ranges around the world, but many of the drivers, patterns and consequences of this decline remain poorly understood. Here we provide an analysis showing that bushmeat hunting for mostly food and medicinal products is driving a global crisis whereby 301 terrestrial mammal species are threatened with extinction. Nearly all of these threatened species occur in developing countries where major coexisting threats include deforestation, agricultural expansion, human encroachment and competition with livestock. The unrelenting decline of mammals suggests many vital ecological and socio-economic services that these species provide will be lost, potentially changing ecosystems irrevocably. We discuss options and current obstacles to achieving effective conservation, alongside consequences of failure to stem such anthropogenic mammalian extirpation. We propose a multi-pronged conservation strategy to help save threatened mammals from immediate extinction and avoid a collapse of food security for hundreds of millions of people.

Life History and Demographic Drivers of Reservoir Competence for Three Tick-Borne Zoonotic Pathogens

Animal and plant species differ dramatically in their quality as hosts for multi-host pathogens, but the causes of this variation are poorly understood. A group of small mammals, including small rodents and shrews, are among the most competent natural reservoirs for three tick-borne zoonotic pathogens, Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum, in eastern North America. For a group of nine commonly-infected mammals spanning >2 orders of magnitude in body mass, we asked whether life history features or surrogates for (unknown) encounter rates with ticks, predicted reservoir competence for each pathogen. Life history features associated with a fast pace of life generally were positively correlated with reservoir competence. However, a model comparison approach revealed that host population density, as a proxy for encounter rates between hosts and pathogens, generally received more support than did life history features. The specific life history features and the importance of host population density differed somewhat between the different pathogens. We interpret these results as supporting two alternative but non-exclusive hypotheses for why ecologically widespread, synanthropic species are often the most competent reservoirs for multi-host pathogens. First, multi-host pathogens might adapt to those hosts they are most likely to experience, which are likely to be the most abundant and/or frequently bitten by tick vectors. Second, species with fast life histories might allocate less to certain immune defenses, which could increase their reservoir competence. Results suggest that of the host species that might potentially be exposed, those with comparatively high population densities, small bodies, and fast pace of life will often be keystone reservoirs that should be targeted for surveillance or management.

Using Grizzly Bears to Assess Harvest-Ecosystem Tradeoffs in Salmon Fisheries

Using grizzly bears as surrogates for “salmon ecosystem” function, the authors develop a generalizable ecosystem-based management framework that enables decision-makers to quantify ecosystem-harvest tradeoffs between wild and human recipients of natural resources like fish.