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.

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.

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.

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.

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.

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.

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.

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.

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.

Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters.

Studies of consumer-resource interactions suggest that individual diet specialisation is empirically widespread and theoretically important to the organisation and dynamics of populations and communities. We used weighted networks to analyze the resource use by sea otters, testing three alternative models for how individual diet specialisation may arise. As expected, individual specialisation was absent when otter density was low, but increased at high-otter density. A high-density emergence of nested resource-use networks was consistent with the model assuming individuals share preference ranks. However, a density-dependent emergence of a non-nested modular network for 'core' resources was more consistent with the 'competitive refuge' model. Individuals from different diet modules showed predictable variation in rank-order prey preferences and handling times of core resources, further supporting the competitive refuge model. Our findings support a hierarchical organisation of diet specialisation and suggest individual use of core and marginal resources may be driven by different selective pressures.

Assessing the effects of large mobile predators on ecosystem connectivity.

Large predators are often highly mobile and can traverse and use multiple habitats. We know surprisingly little about how predator mobility determines important processes of ecosystem connectivity. Here we used a variety of data sources drawn from Palmyra Atoll, a remote tropical marine ecosystem where large predators remain in high abundance, to investigate how these animals foster connectivity. Our results indicate that three of Palmyra's most abundant large predators (e.g., two reef sharks and one snapper) use resources from different habitats creating important linkages across ecosystems. Observations of cross-system foraging such as this have important implications for the understanding of ecosystem functioning, the management of large-predator populations, and the design of conservation measures intended to protect whole ecosystems. In the face of widespread declines of large, mobile predators, it is important that resource managers, policy makers, and ecologists work to understand how these predators create connectivity and to determine the impact that their depletions may be having on the integrity of these linkages.

Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system.

The processes promoting disease in wild animal populations are highly complex, yet identifying these processes is critically important for conservation when disease is limiting a population. By combining field studies with epidemiologic tools, we evaluated the relationship between key factors impeding southern sea otter (Enhydra lutris nereis) population growth: disease and resource limitation. This threatened population has struggled to recover despite protection, so we followed radio-tagged sea otters and evaluated infection with 2 disease-causing protozoal pathogens, Toxoplasma gondii and Sarcocystis neurona, to reveal risks that increased the likelihood of pathogen exposure. We identified patterns of pathogen infection that are linked to individual animal behavior, prey choice, and habitat use. We detected a high-risk spatial cluster of S. neurona infections in otters with home ranges in southern Monterey Bay and a coastal segment near San Simeon and Cambria where otters had high levels of infection with T. gondii. We found that otters feeding on abalone, which is the preferred prey in a resource-abundant marine ecosystem, had a very low risk of infection with either pathogen, whereas otters consuming small marine snails were more likely to be infected with T. gondii. Individual dietary specialization in sea otters is an adaptive mechanism for coping with limited food resources along central coastal California. High levels of infection with protozoal pathogens may be an adverse consequence of dietary specialization in this threatened species, with both depleted resources and disease working synergistically to limit recovery.

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.

Predicting community responses to perturbations in the face of imperfect knowledge and network complexity.

How best to predict the effects of perturbations to ecological communities has been a long-standing goal for both applied and basic ecology. This quest has recently been revived by new empirical data, new analysis methods, and increased computing speed, with the promise that ecologically important insights may be obtainable from a limited knowledge of community interactions. We use empirically based and simulated networks of varying size and connectance to assess two limitations to predicting perturbation responses in multispecies communities: (1) the inaccuracy by which species interaction strengths are empirically quantified and (2) the indeterminacy of species responses due to indirect effects associated with network size and structure. We find that even modest levels of species richness and connectance (-25 pairwise interactions) impose high requirements for interaction strength estimates because system indeterminacy rapidly overwhelms predictive insights. Nevertheless, even poorly estimated interaction strengths provide greater average predictive certainty than an approach that uses only the sign of each interaction. Our simulations provide guidance in dealing with the trade-offs involved in maximizing the utility of network approaches for predicting dynamics in multispecies communities.

Food limitation leads to behavioral diversification and dietary specialization in sea otters.

Dietary diversity often varies inversely with prey resource abundance. This pattern, although typically measured at the population level, is usually assumed to also characterize the behavior of individual animals within the population. However, the pattern might also be produced by changes in the degree of variation among individuals. Here we report on dietary and associated behavioral changes that occurred with the experimental translocation of sea otters from a food-poor to a food-rich environment. Although the diets of all individuals were broadly similar in the food-rich environment, a behaviorally based dietary polymorphism existed in the food-poor environment. Higher dietary diversity under low resource abundance was largely driven by greater variation among individuals. We further show that the dietary polymorphism in the food-poor environment included a broad suite of correlated behavioral variables and that the individuals that comprised specific behavioral clusters benefited from improved foraging efficiency on their individually preferred prey. Our findings add to the growing list of examples of extreme individuality in behavior and prey choice within populations and suggest that this phenomenon can emerge as a behavioral manifestation of increased population density. Individuality in foraging behavior adds complexity to both the fitness consequences of prey selection and food web dynamics, and it may figure prominently as a diversifying process over evolutionary timescales.

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.