Predator-induced collapse of niche structure and species coexistence.

Biological invasions are both a pressing environmental challenge and an opportunity to investigate fundamental ecological processes, such as the role of top predators in regulating biodiversity and food-web structure. In whole-ecosystem manipulations of small Caribbean islands on which brown anole lizards (Anolis sagrei) were the native top predator, we experimentally staged invasions by competitors (green anoles, Anolis smaragdinus) and/or new top predators (curly-tailed lizards, Leiocephalus carinatus). We show that curly-tailed lizards destabilized the coexistence of competing prey species, contrary to the classic idea of keystone predation. Fear-driven avoidance of predators collapsed the spatial and dietary niche structure that otherwise stabilized coexistence, which intensified interspecific competition within predator-free refuges and contributed to the extinction of green-anole populations on two islands. Moreover, whereas adding either green anoles or curly-tailed lizards lengthened food chains on the islands, adding both species reversed this effect-in part because the apex predators were trophic omnivores. Our results underscore the importance of top-down control in ecological communities, but show that its outcomes depend on prey behaviour, spatial structure, and omnivory. Diversity-enhancing effects of top predators cannot be assumed, and non-consumptive effects of predation risk may be a widespread constraint on species coexistence.

Inter- and intrapopulation resource use variation of marine subsidized western fence lizards.

Marine resource subsidies alter consumer dynamics of recipient populations in coastal systems. The response to these subsidies by generalist consumers is often not uniform, creating inter- and intrapopulation diet variation and niche diversification that may be intensified across heterogeneous landscapes. We sampled western fence lizards, Sceloporus occidentalis, from Puget Sound beaches and coastal and inland forest habitats, in addition to the lizards' marine and terrestrial prey items to quantify marine and terrestrial resource use with stable isotope analysis and mixing models. Beach lizards had higher average δ13C and δ15N values compared to coastal and inland forest lizards, exhibiting a strong mixing line between marine and terrestrial prey items. Across five beach sites, lizard populations received 20-51% of their diet from marine resources, on average, with individual lizards ranging between 7 and 86% marine diet. The hillslope of the transition zone between marine and terrestrial environments at beach sites was positively associated with marine-based diets, as the steepest sloped beach sites had the highest percent marine diets. Within-beach variation in transition zone slope was positively correlated with the isotopic niche space of beach lizard populations. These results demonstrate that physiography of transitional landscapes can mediate resource flow between environments, and variable habitat topography promotes niche diversification within lizard populations. Marine resource subsidization of Puget Sound beach S. occidentalis populations may facilitate occupation of the northwesternmost edge of the species range. Shoreline restoration and driftwood beach habitat conservation are important to support the unique ecology of Puget Sound S. occidentalis.

Faunal isotope records reveal trophic and nutrient dynamics in twentieth century Yellowstone grasslands.

Population sizes and movement patterns of ungulate grazers and their predators have fluctuated dramatically over the past few centuries, largely owing to overharvesting, land-use change and historic management. We used δ(13)C and δ(15)N values measured from bone collagen of historic and recent gray wolves and their potential primary prey from Yellowstone National Park to gain insight into the trophic dynamics and nutrient conditions of historic and modern grasslands. The diet of reintroduced wolves closely parallels that of the historic population. We suggest that a significant shift in faunal δ(15)N values over the past century reflects impacts of anthropogenic environmental changes on grassland ecosystems, including grazer-mediated shifts in grassland nitrogen cycle processes.

Cooperation and individuality among man-eating lions.

Cooperation is the cornerstone of lion social behavior. In a notorious case, a coalition of two adult male lions from Tsavo, southern Kenya, cooperatively killed dozens of railway workers in 1898. The "man-eaters of Tsavo" have since become the subject of numerous popular accounts, including three Hollywood films. Yet the full extent of the lions' man-eating behavior is unknown; estimates range widely from 28 to 135 victims. Here we use stable isotope ratios to quantify increasing dietary specialization on novel prey during a time of food limitation. For one lion, the delta(13)C and delta(15)N values of bone collagen and hair keratin (which reflect dietary inputs over years and months, respectively) reveal isotopic changes that are consistent with a progressive dietary specialization on humans. These findings not only support the hypothesis that prey scarcity drives individual dietary specialization, but also demonstrate that sustained dietary individuality can exist within a cooperative framework. The intensity of human predation (up to 30% reliance during the final months of 1898) is also associated with severe craniodental infirmities, which may have further promoted the inclusion of unconventional prey under perturbed environmental conditions.

Megafaunal extinctions and the disappearance of a specialized wolf ecomorph.

The gray wolf (Canis lupus) is one of the few large predators to survive the Late Pleistocene megafaunal extinctions [1]. Nevertheless, wolves disappeared from northern North America in the Late Pleistocene, suggesting they were affected by factors that eliminated other species. Using skeletal material collected from Pleistocene permafrost deposits of eastern Beringia, we present a comprehensive analysis of an extinct vertebrate by exploring genetic (mtDNA), morphologic, and isotopic (delta(13)C, delta(15)N) data to reveal the evolutionary relationships, as well as diet and feeding behavior, of ancient wolves. Remarkably, the Late Pleistocene wolves are genetically unique and morphologically distinct. None of the 16 mtDNA haplotypes recovered from a sample of 20 Pleistocene eastern-Beringian wolves was shared with any modern wolf, and instead they appear most closely related to Late Pleistocene wolves of Eurasia. Moreover, skull shape, tooth wear, and isotopic data suggest that eastern-Beringian wolves were specialized hunters and scavengers of extinct megafauna. Thus, a previously unrecognized, uniquely adapted, and genetically distinct wolf ecomorph suffered extinction in the Late Pleistocene, along with other megafauna. Consequently, the survival of the species in North America depended on the presence of more generalized forms elsewhere.

Termites create spatial structure and govern ecosystem function by affecting N2 fixation in an East African savanna.

The mechanisms by which even the clearest of keystone or dominant species exert community-wide effects are only partially understood in most ecosystems. This is especially true when a species or guild influences community-wide interactions via changes in the abiotic landscape. Using stable isotope analyses, we show that subterranean termites in an East African savanna strongly influence a key ecosystem process: atmospheric nitrogen fixation by a monodominant tree species and its bacterial symbionts. Specifically, we applied the 15N natural abundance method in combination with other biogeochemical analyses to assess levels of nitrogen fixation by Acacia drepanolobium and its effects on co-occurring grasses and forbs in areas near and far from mounds and where ungulates were or were not excluded. We find that termites exert far stronger effects than do herbivores on nitrogen fixation. The percentage of nitrogen derived from fixation in Acacia drepanolobium trees is higher (55-80%) away from mounds vs. near mounds (40-50%). Mound soils have higher levels of plant available nitrogen, and Acacia drepanolobium may preferentially utilize soil-based nitrogen sources in lieu of fixed nitrogen when these sources are readily available near termite mounds. At the scale of the landscape, our models predict that termite/soil derived nitrogen sources influence >50% of the Acacia drepanolobium trees in our system. Further, the spatial extent of these effects combine with the spacing of termite mounds to create highly regular patterning in nitrogen fixation rates, resulting in marked habitat heterogeneity in an otherwise uniform landscape. In summary, we show that termite-associated effects on nitrogen processes are not only stronger than those of more apparent large herbivores in the same system, but also occur in a highly regular spatial pattern, potentially adding to their importance as drivers of community and ecosystem structure.

Termites, vertebrate herbivores, and the fruiting success of Acacia drepanolobium.

In African savannas, vertebrate herbivores are often identified as key determinants of plant growth, survivorship, and reproduction. However, plant reproduction is likely to be the product of responses to a suite of abiotic and biotic factors, including nutrient availability and interactions with antagonists and mutualists. In a relatively simple system, we examined the role of termites (which act as ecosystem engineers--modifying physical habitat and creating islands of high soil fertility), vertebrate herbivores, and symbiotic ants, on the fruiting success of a dominant plant, Acacia drepanolobium, in East African savannas. Using observational data, large-scale experimental manipulations, and analysis of foliar N, we found that Acacia drepanolobium trees growing at the edge of termite mounds were more likely to reproduce than those growing farther away, in off-mound soils. Although vertebrate herbivores preferentially used termite mounds as demonstrated by dung deposits, long-term exclusion of mammalian grazers did not significantly reduce A. drepanolobium fruit production. Leaf N was significantly greater in trees growing next to mounds than in those growing farther away, and this pattern was unaffected by exclusion of vertebrates. Thus, soil enrichment by termites, rather than through dung and urine deposition by large herbivores, is of primary importance to fruit production near mounds. Across all mound-herbivore treatment combinations, trees that harbored Crematogaster sjostedti were more likely to fruit than those that harbored one of the other three ant species. Although C. sjostedti is less aggressive than the other ants, it tends to inhabit large, old trees near termite mounds which are more likely to fruit than smaller ones. Termites play a key role in generating patches of nutrient-rich habitat important to the reproductive success of A. drepanolobium in East African savannas. Enhanced nutrient acquisition from termite mounds appears to allow plants to tolerate herbivory and the reduced defense by a relatively ineffective ant partner. Our results underscore the importance of simultaneously examining top-down and bottom-up effects to understand those factors most important to plant reproductive success.

Reply to Van Valkenburgh et al.

DeSantis et al. respond to the concerns raised by Van Valkenburgh et al. on their original study.

Causes and Consequences of Pleistocene Megafaunal Extinctions as Revealed from Rancho La Brea Mammals.

The fossils preserved in the Rancho La Brea "tar" seeps in southern California span the past ∼50,000 years and provide a rare opportunity to assess the ecology of predators (e.g., the American lion, sabertooth cats, cougars, dire wolves, gray wolves, and coyotes), including clarifying the causes and consequences of the terminal Pleistocene extinction event. Here, a multi-proxy approach elucidates dietary responses of carnivorans to changing climates and megafaunal extinctions. Using sample sizes that are unavailable anywhere else in the world, including hundreds of carnivoran and herbivore specimens, we clarify the paleobiology of the extinct sabertooth cats and dire wolves-overturning the idea that they heavily competed for similar prey. Canids (especially the dire wolf) consumed prey from more open environments than felids, demonstrating minimal competition for prey throughout the latest Pleistocene and largely irrespective of changing climates, including just prior to their extinction. Coyotes experienced a dramatic shift in dietary behavior toward increased carcass utilization and the consumption of forest resources (prey and/or plant resources) after the terminal Pleistocene megafaunal extinction. Extant predators' ability to effectively hunt smaller prey and/or utilize carcasses may have been a key to their survival, especially after a significant reduction in megafaunal prey resources. Collectively, these data suggest that dietary niches of carnivorans are not always static and can instead be substantially affected by the removal of top predators and abundant prey resources.

Coupling of canopy and understory food webs by ground-dwelling predators.

Understanding food-web dynamics requires knowing whether species assemblages are compartmentalized into distinct energy channels, and, if so, how these channels are structured in space. We used isotopic analyses to reconstruct the food web of a Kenyan wooded grassland. Insect prey were relatively specialized consumers of either C3 (trees and shrubs) or C4 (grasses) plants. Arboreal predators (arthropods and geckos) were also specialized, deriving c. 90% of their diet from C3-feeding prey. In contrast, ground-dwelling predators preyed considerably upon both C3- and C4-feeding prey. This asymmetry suggests a gravity-driven subsidy of the terrestrial predator community, whereby tree-dwelling prey fall and are consumed by ground-dwelling predators. Thus, predators in general couple the C3 and C4 components of this food web, but ground-dwelling predators perform this ecosystem function more effectively than tree-dwelling ones. Although prey subsidies in vertically structured terrestrial habitats have received little attention, they are likely to be common and important to food-web organization.

Stable isotopes, ecological integration and environmental change: wolves record atmospheric carbon isotope trend better than tree rings.

Large-scale patterns of isotope ratios are detectable in the tissues of organisms, but the variability in these patterns often obscures detection of environmental trends. We show that plants and animals at lower trophic levels are relatively poor indicators of the temporal trend in atmospheric carbon isotope ratios (delta13C) when compared with animals at higher trophic levels. First, we tested how differences in atmospheric delta13C values were transferred across three trophic levels. Second, we compared contemporary delta13C trends (1961-2004) in atmospheric CO2 to delta13C patterns in a tree species (jack pine, Pinus banksiana), large herbivore (moose, Alces alces) and large carnivore (grey wolf, Canis lupus) from North America. Third, we compared palaeontological (approx. 30000 to 12000 14C years before present) atmospheric CO2 trends to delta13C patterns in a tree species (Pinus flexilis, Juniperus sp.), a megaherbivore (bison, Bison antiquus) and a large carnivore (dire wolf, Canis dirus) from the La Brea tar pits (southern California, USA) and Great Basin (western USA). Contrary to previous expectations, we found that the environmental isotope pattern is better represented with increasing trophic level. Our results indicate that museum specimens of large carnivores would best reflect large-scale spatial and temporal patterns of carbon isotopes in the palaeontological record because top predators can act as ecological integrators of environmental change.

Probabilistic patterns of interaction: the effects of link-strength variability on food web structure.

Patterns of species interactions affect the dynamics of food webs. An important component of species interactions that is rarely considered with respect to food webs is the strengths of interactions, which may affect both structure and dynamics. In natural systems, these strengths are variable, and can be quantified as probability distributions. We examined how variation in strengths of interactions can be described hierarchically, and how this variation impacts the structure of species interactions in predator-prey networks, both of which are important components of ecological food webs. The stable isotope ratios of predator and prey species may be particularly useful for quantifying this variability, and we show how these data can be used to build probabilistic predator-prey networks. Moreover, the distribution of variation in strengths among interactions can be estimated from a limited number of observations. This distribution informs network structure, especially the key role of dietary specialization, which may be useful for predicting structural properties in systems that are difficult to observe. Finally, using three mammalian predator-prey networks (two African and one Canadian) quantified from stable isotope data, we show that exclusion of link-strength variability results in biased estimates of nestedness and modularity within food webs, whereas the inclusion of body size constraints only marginally increases the predictive accuracy of the isotope-based network. We find that modularity is the consequence of strong link-strengths in both African systems, while nestedness is not significantly present in any of the three predator-prey networks.