Humanity's diverse predatory niche and its ecological consequences.

Although humans have long been predators with enduring nutritive and cultural relationships with their prey, seldom have conservation ecologists considered the divergent predatory behavior of contemporary, industrialized humans. Recognizing that the number, strength and diversity of predator-prey relationships can profoundly influence biodiversity, here we analyze humanity's modern day predatory interactions with vertebrates and estimate their ecological consequences. Analysing IUCN 'use and trade' data for ~47,000 species, we show that fishers, hunters and other animal collectors prey on more than a third (~15,000 species) of Earth's vertebrates. Assessed over equivalent ranges, humans exploit up to 300 times more species than comparable non-human predators. Exploitation for the pet trade, medicine, and other uses now affects almost as many species as those targeted for food consumption, and almost 40% of exploited species are threatened by human use. Trait space analyses show that birds and mammals threatened by exploitation occupy a disproportionally large and unique region of ecological trait space, now at risk of loss. These patterns suggest far more species are subject to human-imposed ecological (e.g., landscapes of fear) and evolutionary (e.g., harvest selection) processes than previously considered. Moreover, continued overexploitation will likely bear profound consequences for biodiversity and ecosystem function.

History's legacy: Why future progress in ecology demands a view of the past.

History has profoundly affected the composition, distribution, and abundances of species in contemporary ecosystems. A full understanding of how ecosystems work and change must therefore take history into account. We offer four well-studied examples illustrating how a knowledge of history has strengthened interpretations of modern systems: the development of molluscan antipredatory defenses in relation to shell-breaking predators; the North Pacific kelp ecosystem with sea otters, smaller predators, sea urchins, and large herbivores; estuarine ecosystems affected by the decline in oysters and other suspension feeders; and the legacy of extinct large herbivores and frugivores in tropical American forests. Many current ecological problems would greatly benefit from a historical perspective. We highlight four of these: soil depletion and tree stunting in forests related to the disappearance of large consumers; the spread of anoxic dead zones in the ocean, which we argue could be mitigated by restoring predator and suspension-feeding guilds; ocean acidification, which would be alleviated by more nutrient recycling by consumers in the aerobic ecosystem; and the relation between species diversity and keystone predators, a foundational concept that is complicated by simplified trophic relationships in modern ecosystems.

Genomic basis for skin phenotype and cold adaptation in the extinct Steller's sea cow.

Steller's sea cow, an extinct sirenian and one of the largest Quaternary mammals, was described by Georg Steller in 1741 and eradicated by humans within 27 years. Here, we complement Steller's descriptions with paleogenomic data from 12 individuals. We identified convergent evolution between Steller's sea cow and cetaceans but not extant sirenians, suggesting a role of several genes in adaptation to cold aquatic (or marine) environments. Among these are inactivations of lipoxygenase genes, which in humans and mouse models cause ichthyosis, a skin disease characterized by a thick, hyperkeratotic epidermis that recapitulates Steller's sea cows' reportedly bark-like skin. We also found that Steller's sea cows' abundance was continuously declining for tens of thousands of years before their description, implying that environmental changes also contributed to their extinction.

Southeast Alaskan kelp forests: inferences of process from large-scale patterns of variation in space and time.

Humans were considered external drivers in much foundational ecological research. A recognition that humans are embedded in the complex interaction networks we study can provide new insight into our ecological paradigms. Here, we use time-series data spanning three decades to explore the effects of human harvesting on otter-urchin-kelp trophic cascades in southeast Alaska. These effects were inferred from variation in sea urchin and kelp abundance following the post fur trade repatriation of otters and a subsequent localized reduction of otters by human harvest in one location. In an example of a classic trophic cascade, otter repatriation was followed by a 99% reduction in urchin biomass density and a greater than 99% increase in kelp density region wide. Recent spatially concentrated harvesting of otters was associated with a localized 70% decline in otter abundance in one location, with urchins increasing and kelps declining in accordance with the spatial pattern of otter occupancy within that region. While the otter-urchin-kelp trophic cascade has been associated with alternative community states at the regional scale, this research highlights how small-scale variability in otter occupancy, ostensibly due to spatial variability in harvesting or the risk landscape for otters, can result in within-region patchiness in these community states.

Physical disturbance by recovering sea otter populations increases eelgrass genetic diversity.

Most knowledge regarding the role of predators is ecological in nature. Here, we report how disturbance generated by sea otters (Enhydra lutris) digging for infaunal prey in eelgrass (Zostera marina) meadows increases genetic diversity by promoting conditions for sexual reproduction of plants. Eelgrass allelic richness and genotypic diversity were, respectively, 30 and 6% higher in areas where recovering sea otter populations had been established for 20 to 30 years than in areas where they had been present <10 years or absent >100 years. The influence of sea otter occupancy on the aforementioned measures of genetic diversity was stronger than those of depth, temperature, latitude, or meadow size. Our findings reveal an underappreciated evolutionary process by which megafauna may promote genetic diversity and ecological resilience.

Keystone predators govern the pathway and pace of climate impacts in a subarctic marine ecosystem.

Predator loss and climate change are hallmarks of the Anthropocene yet their interactive effects are largely unknown. Here, we show that massive calcareous reefs, built slowly by the alga Clathromorphum nereostratum over centuries to millennia, are now declining because of the emerging interplay between these two processes. Such reefs, the structural base of Aleutian kelp forests, are rapidly eroding because of overgrazing by herbivores. Historical reconstructions and experiments reveal that overgrazing was initiated by the loss of sea otters, Enhydra lutris (which gave rise to herbivores capable of causing bioerosion), and then accelerated with ocean warming and acidification (which increased per capita lethal grazing by 34 to 60% compared with preindustrial times). Thus, keystone predators can mediate the ways in which climate effects emerge in nature and the pace with which they alter ecosystems.

Size, growth, and density data for shallow-water sea urchins from Mexico to the Aleutian Islands, Alaska, 1956-2016.

Size, growth, and density have been studied for North American Pacific coast sea urchins Strongylocentrotus purpuratus, S. droebachiensis, S. polyacanthus, Mesocentrotus (Strongylocentrotus) franciscanus, Lytechinus pictus, Centrostephanus coronatus, and Arbacia stellata by various workers at diverse sites and for varying lengths of time from 1956 to present. Numerous peer-reviewed publications have used some of these data but some data have appeared only in graduate theses or the gray literature. There also are data that have never appeared outside original data sheets. Motivation for studies has included fisheries management and environmental monitoring of sewer and power plant outfalls as well as changes associated with disease epidemics. Studies also have focused on kelp restoration, community effects of sea otters, basic sea urchin biology, and monitoring. The data sets presented here are a historical record of size, density, and growth for a common group of marine invertebrates in intertidal and nearshore environments that can be used to test hypotheses concerning future changes associated with fisheries practices, shifts of predator distributions, climate and ecosystem changes, and ocean acidification along the Pacific Coast of North America and islands of the north Pacific. No copyright restrictions apply. Please credit this paper when using the data.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

A keystone ecologist: Robert Treat Paine, 1933-2016.

Robert T. Paine, who passed away on 13 June 2016, is among the most influential people in the history of ecology. Paine was an experimentalist, a theoretician, a practitioner, and proponent of the "ecology of place," and a deep believer in the importance of natural history to ecological understanding. His scientific legacy grew from the discovery of a link between top-down forcing and species diversity, a breakthrough that led to the ideas of both keystone species and trophic cascades, and to our early understanding of the mosaic nature of biological communities, causes of zonation across physical gradients, and the intermediate-disturbance hypothesis of species diversity. Paine's influence as a mentor was equally important to the growth of ecological thinking, natural resource conservation, and policy. He served ecology as an Ecological Society of America president, an editor of the Society's journals, a member of and contributor to the National Academy of Sciences and the National Research Council, and an in-demand advisor to various state and federal agencies. Paine's broad interests, enthusiasm, charisma, and humor deeply affected our lives and the lives of so many others.

What is a Trophic Cascade?

Few concepts in ecology have been so influential as that of the trophic cascade. Since the 1980s, the term has been a central or major theme of more than 2000 scientific articles. Despite this importance and widespread usage, basic questions remain about what constitutes a trophic cascade. Inconsistent usage of language impedes scientific progress and the utility of scientific concepts in management and conservation. Herein, we offer a definition of trophic cascade that is designed to be both widely applicable yet explicit enough to exclude extraneous interactions. We discuss our proposed definition and its implications, and define important related terms, thereby providing a common language for scientists, policy makers, conservationists, and other stakeholders with an interest in trophic cascades.

Sea otters, kelp forests, and the extinction of Steller's sea cow.

The late Pleistocene extinction of so many large-bodied vertebrates has been variously attributed to two general causes: rapid climate change and the effects of humans as they spread from the Old World to previously uninhabited continents and islands. Many large-bodied vertebrates, especially large apex predators, maintain their associated ecosystems through top-down forcing processes, especially trophic cascades, and megaherbivores also exert an array of strong indirect effects on their communities. Thus, a third possibility for at least some of the Pleistocene extinctions is that they occurred through habitat changes resulting from the loss of these other keystone species. Here we explore the plausibility of this mechanism, using information on sea otters, kelp forests, and the recent extinction of Steller's sea cows from the Commander Islands. Large numbers of sea cows occurred in the Commander Islands at the time of their discovery by Europeans in 1741. Although extinction of these last remaining sea cows during early years of the Pacific maritime fur trade is widely thought to be a consequence of direct human overkill, we show that it is also a probable consequence of the loss of sea otters and the co-occurring loss of kelp, even if not a single sea cow had been killed directly by humans. This example supports the hypothesis that the directly caused extinctions of a few large vertebrates in the late Pleistocene may have resulted in the coextinction of numerous other species.

The cost of reproduction: differential resource specialization in female and male California sea otters.

Intraspecific variation in behavior and diet can have important consequences for population and ecosystem dynamics. Here, we examine how differences in reproductive investment and spatial ecology influence individual diet specialization in male and female southern sea otters (Enhydra lutris nereis). We hypothesize that greater reproductive constraints and smaller home ranges of females lead to more pronounced intraspecific competition and increased specialization. We integrate stable carbon (δ(13)C) and nitrogen (δ(15)N) isotope analysis of sea otter vibrissae with long-term observational studies of five subpopulations in California. We define individual diet specialization as low ratios of within-individual variation (WIC) to total population niche width (TNW). We compare isotopic and observational based metrics of WIC/TNW for males and females to data on population densities, and movement patterns using both general linear and linear mixed-effects models. Consistent with our hypothesis, increasing population density is associated with increased individual diet specialization by females but not by males. Additionally, we find the amount of coastline in a sea otter's home range positively related with individual dietary variability, with increased range span resulting in weaker specialization for both males and females. We attribute our results to sex-based differences in movement, with females needing to specialize in their small ranges to maximize energy gain, and posit that the paradigm of individual prey specialization in sea otters with increased intraspecific competition may be a pattern driven largely by females. Our work highlights a potentially broader role of sex in the mechanistic pressures promoting and maintaining diet specialization.

Marine defaunation: animal loss in the global ocean.

Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only hundreds of years ago, whereas terrestrial defaunation has been occurring far longer. Though humans have caused few global marine extinctions, we have profoundly affected marine wildlife, altering the functioning and provisioning of services in every ocean. Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine defaunation rates will rapidly intensify as human use of the oceans industrializes. Though protected areas are a powerful tool to harness ocean productivity, especially when designed with future climate in mind, additional management strategies will be required. Overall, habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive intervention can avert a marine defaunation disaster of the magnitude observed on land.

Status and ecological effects of the world's largest carnivores.

Large carnivores face serious threats and are experiencing massive declines in their populations and geographic ranges around the world. We highlight how these threats have affected the conservation status and ecological functioning of the 31 largest mammalian carnivores on Earth. Consistent with theory, empirical studies increasingly show that large carnivores have substantial effects on the structure and function of diverse ecosystems. Significant cascading trophic interactions, mediated by their prey or sympatric mesopredators, arise when some of these carnivores are extirpated from or repatriated to ecosystems. Unexpected effects of trophic cascades on various taxa and processes include changes to bird, mammal, invertebrate, and herpetofauna abundance or richness; subsidies to scavengers; altered disease dynamics; carbon sequestration; modified stream morphology; and crop damage. Promoting tolerance and coexistence with large carnivores is a crucial societal challenge that will ultimately determine the fate of Earth's largest carnivores and all that depends upon them, including humans.

Integrating the invisible fabric of nature into fisheries management.

Overfishing and environmental change have triggered many severe and unexpected consequences. As existing communities have collapsed, new ones have become established, fundamentally transforming ecosystems to those that are often less productive for fisheries, more prone to cycles of booms and busts, and thus less manageable. We contend that the failure of fisheries science and management to anticipate these transformations results from a lack of appreciation for the nature, strength, complexity, and outcome of species interactions. Ecologists have come to understand that networks of interacting species exhibit nonlinear dynamics and feedback loops that can produce sudden and unexpected shifts. We argue that fisheries science and management must follow this lead by developing a sharper focus on species interactions and how disrupting these interactions can push ecosystems in which fisheries are embedded past their tipping points.

Predicting and detecting reciprocity between indirect ecological interactions and evolution.

Living nature can be thought of as a tapestry, defined not only by its constituent parts but also by how these parts are woven together. The weaving of this tapestry is a metaphor for species interactions, which can be divided into three broad classes: competitive, mutualistic, and consumptive. Direct interactions link together as more complex networks, for example, the joining of consumptive interactions into food webs. Food web dynamics are driven, in turn, by changes in the abundances of web members, whose numbers or biomass respond to bottom-up (resource limitation) and top-down (consumer limitation) forcing. The relative strengths of top-down and bottom-up forcing on the abundance of a given web member depend on its ecological context, including its topological position within the food web. Top-down effects by diverse consumers are nearly ubiquitous, in many cases influencing the structure and operation of ecosystems. While the ecological effects of such interactions are well known, far less is known of their evolutionary consequences. In this essay, we describe sundry consequences of these interaction chains on species and ecosystem processes, explain several known or suspected evolutionary effects of consumer-induced interaction chains, and identify areas where reciprocity between ecology and evolution involving the indirect effects of consumer-prey interaction chains might be further explored.