Jacob R. Goheen

Breakdown of an Ant-Plant Mutualism Follows the Loss of Large Herbivores from an African Savanna

Mutualisms are key components of biodiversity and ecosystem function, yet the forces maintaining them are poorly understood. We investigated the effects of removing large mammals on an ant-Acacia mutualism in an African savanna. Ten years of large-herbivore exclusion reduced the nectar and housing provided by plants to ants, increasing antagonistic behavior by a mutualistic ant associate and shifting competitive dominance within the plant-ant community from this nectar-dependent mutualist to an antagonistic species that does not depend on plant rewards. Trees occupied by this antagonist suffered increased attack by stem-boring beetles, grew more slowly, and experienced doubled mortality relative to trees occupied by the mutualistic ant. These results show that large mammals maintain cooperation within a widespread symbiosis and suggest complex cascading effects of megafaunal extinction.

Skin shedding and tissue regeneration in African spiny mice (Acomys)

Evolutionary modification has produced a spectrum of animal defence traits to escape predation, including the ability to autotomize body parts to elude capture. After autotomy, the missing part is either replaced through regeneration (for example, in urodeles, lizards, arthropods and crustaceans) or permanently lost (such as in mammals). Although most autotomy involves the loss of appendages (legs, chelipeds, antennae or tails, for example), skin autotomy can occur in certain taxa of scincid and gekkonid lizards. Here we report the first demonstration of skin autotomy in Mammalia (African spiny mice, Acomys). Mechanical testing showed a propensity for skin to tear under very low tension and the absence of a fracture plane. After skin loss, rapid wound contraction was followed by hair follicle regeneration in dorsal skin wounds. Notably, we found that regenerative capacity in Acomys was extended to ear holes, where the mice exhibited complete regeneration of hair follicles, sebaceous glands, dermis and cartilage. Salamanders capable of limb regeneration form a blastema (a mass of lineage-restricted progenitor cells) after limb loss, and our findings suggest that ear tissue regeneration in Acomys may proceed through the assembly of a similar structure. This study underscores the importance of investigating regenerative phenomena outside of conventional model organisms, and suggests that mammals may retain a higher capacity for regeneration than was previously believed. As re-emergent interest in regenerative medicine seeks to isolate molecular pathways controlling tissue regeneration in mammals, Acomys may prove useful in identifying mechanisms to promote regeneration in lieu of fibrosis and scarring.

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism.

Understanding cooperation is a central challenge in biology, because natural selection should favor “free-loaders” that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a “sterilization parasite” that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these “parasites” enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.

Worldwide evidence of a unimodal relationship between productivity and plant species richness

Grassland diversity and ecosystem productivity The relationship between plant species diversity and ecosystem productivity is controversial. The debate concerns whether diversity peaks at intermediate levels of productivity—the so-called humped-back model—or whether there is no clear predictable relationship. Fraser et al. used a large, standardized, and geographically diverse sample of grasslands from six continents to confirm the validity and generality of the humped-back model. Their findings pave the way for a more mechanistic understanding of the factors controlling species diversity. Science, this issue p. 302 The humped-back model of plant species diversity is confirmed by a global grassland survey. The search for predictions of species diversity across environmental gradients has challenged ecologists for decades. The humped-back model (HBM) suggests that plant diversity peaks at intermediate productivity; at low productivity few species can tolerate the environmental stresses, and at high productivity a few highly competitive species dominate. Over time the HBM has become increasingly controversial, and recent studies claim to have refuted it. Here, by using data from coordinated surveys conducted throughout grasslands worldwide and comprising a wide range of site productivities, we provide evidence in support of the HBM pattern at both global and regional extents. The relationships described here provide a foundation for further research into the local, landscape, and historical factors that maintain biodiversity.

NET EFFECTS OF LARGE MAMMALS ON ACACIA SEEDLING SURVIVAL IN AN AFRICAN SAVANNA

Trees of the genus Acacia are widespread and important components of savanna ecosystems. Factors or organisms that influence the survival of Acacia seedlings are likely to affect tree recruitment and therefore community and ecosystem dynamics. In African savannas, large mammals, especially elephants, have been considered the most important agents of mortality for adult trees, but their impacts on tree seedlings are not well known. We investigated the effects of large mammals on Acacia seedling survival by excluding large mammals from replicated 4-ha plots. Approximately twice as many seedlings were killed in plots with large mammals absent as on plots with large mammals present. Rodents and some invertebrates were more abundant on plots without large mammals and were responsible for these higher predation rates. Seedlings in areas with large mammals were more likely to die of desiccation; however, net seedling survival was approximately twice as high in the presence of large mammals. Our results indicate that large mammals may indirectly increase Acacia seedling survival and thus accelerate, rather than inhibit, tree recruitment.

Zero-sum, the niche,and metacommunities: long-term dynamics of community assembly

Recent models of community assembly, structure, and dynamics have incorporated, to varying degrees, three mechanistic processes: resource limitation and interspecific competition, niche requirements of species, and exchanges between a local community and a regional species pool. Synthesizing 30 years of data from an intensively studied desert rodent community, we show that all of these processes, separately and in combination, have influenced the structural organization of this community and affected its dynamical response to both natural environmental changes and experimental perturbations. In addition, our analyses suggest that zero‐sum constraints, niche differences, and metacommunity processes are inextricably linked in the ways that they affect the structure and dynamics of this system. Explicit consideration of the interaction of these processes should yield a deeper understanding of the assembly and dynamics of other ecological communities. This synthesis highlights the role that long‐term data, especially when coupled with experimental manipulations, can play in assessing the fundamental processes that govern the structure and function of ecological communities.

Large carnivores make savanna tree communities less thorny

Understanding how predation risk and plant defenses interactively shape plant distributions is a core challenge in ecology. By combining global positioning system telemetry of an abundant antelope (impala) and its main predators (leopards and wild dogs) with a series of manipulative field experiments, we showed that herbivores’ risk-avoidance behavior and plants’ antiherbivore defenses interact to determine tree distributions in an African savanna. Well-defended thorny Acacia trees (A. etbaica) were abundant in low-risk areas where impala aggregated but rare in high-risk areas that impala avoided. In contrast, poorly defended trees (A. brevispica) were more abundant in high- than in low-risk areas. Our results suggest that plants can persist in landscapes characterized by intense herbivory, either by defending themselves or by thriving in risky areas where carnivores hunt. Changes to thorny plant defenses and high predator risk for impala determine density and distribution of savanna trees. A thorny defense keeps grazers at bay Fear and avoidance of predators are known to influence how and where herbivore prey species, such as impala, forage. This in turn has cascading effects on plant morphologies and communities. Plants, however, have their own defenses, and so may not just be hapless victims of the predator-prey “dance.” Ford et al. found that thorny Acacia trees are more common in areas where impala experience a low risk of predation by wild dogs. A related Acacia, without thorns, is most abundant in areas where risk of predation is high, and so the number of hungry impala is low. Science, this issue p. 346

INCIDENTAL NEST PREDATION IN SONGBIRDS: BEHAVIORAL INDICATORS DETECT ECOLOGICAL SCALES AND PROCESSES

Incidental predation occurs when secondary prey items are encountered and subsequently consumed, not through directed search for such prey, but through their con- sequential encounter by a predator engaged in search for primary prey. We developed a mathematical model that examines the relationships between the abundance of primary prey, patch exploitation (i.e., quitting harvest rates), and the rate of incidental predation on secondary prey items. The models predictions are dependent upon the spatial scale over which a forager integrates foraging costs and thus determines its quitting harvest rate (QHR). At local (i.e., foraging) spatial scales, we predicted that incidental predation should increase with local food abundance. Also at the foraging scale, local food abundance should not influence QHRs, but local predation risk (from higher trophic levels) should increase QHRs. Therefore, we predicted that incidental predation rates should be negatively correlated with QHRs. Over large (i.e., landscape) spatial scales, greater food abundance and predation risk increase QHRs, and we predicted that predation rates should vary inversely with QHR through two complementary mechanisms: foragers use a greater proportion of space and spend more time foraging as quitting harvest rates decrease. We experimentally tested the qualitative predictions of the theory in the field using artificial Veery (Catharus fuscescens) nests depredated by white-footed mice, Peromyscus leucopus, across three spatial scales. We used the technique of giving-up densities to measure QHRs and to determine the scale at which mice integrate different foraging costs. In accord with our predictions, nest predation was positively influenced by the local abundance of food at the foraging scale, and local predation risk to mice and perhaps interference com- petition from chipmunks resulted in higher giving-up densities and lower nest predation. At the landscape scale, there was an inverse relationship between giving-up densities and nest predation, which was probably the result of large-scale differences in resource abun- dance between plots. Our study demonstrates how linking theoretical development to the use of empirical behavioral indicators can help determine the relevant ecological scales and processes necessary for understanding predator-prey interactions.

Defensive Plant-Ants Stabilize Megaherbivore-Driven Landscape Change in an African Savanna

Tree cover in savanna ecosystems is usually regarded as unstable, varying with rainfall, fire, and herbivory. In sub-Saharan Africa, elephants (Loxodonta africana) suppress tree cover, thereby maintaining landscape heterogeneity by promoting tree-grass coexistence. In the absence of elephants, tree encroachment may convert savannas into closed-canopy woodlands; when elephants increase in abundance, intensified browsing pressure can transform savannas into open grasslands. We show that symbiotic ants stabilize tree cover across landscapes in Kenya by protecting a dominant tree from elephants. In feeding trials, elephants avoided plants with ants and did not distinguish between a myrmecophyte (the whistling-thorn tree [Acacia drepanolobium]) from which ants had been removed and a highly palatable, nonmyrmecophytic congener. In field experiments, elephants inflicted severe damage on whistling-thorn trees from which ants had been removed. Across two properties on which elephants increased between 2003 and 2008, cover of whistling-thorn did not change significantly inside versus outside large-scale elephant exclusion fences; over the same period of time, cover of nonmyrmecophytes differed profoundly inside versus outside exclusion fences. These results highlight the powerful role that symbioses and plant defense play in driving tree growth and survival in savannas, ecosystems of global economic and ecological importance.

Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna

1. Herbivores influence the structure and composition of terrestrial plant communities. However, responses of plant communities to herbivory are variable and depend on environmental conditions, herbivore identity and herbivore abundance. As anthropogenic impacts continue to drive large declines in wild herbivores, understanding the context dependence of herbivore impacts on plant communities becomes increasingly important. 2. Exclosure experiments are frequently used to assess how ecosystems reorganize in the face of large wild herbivore defaunation. Yet in many landscapes, declines in large wildlife are often accompanied by other anthropogenic activities, especially land conversion to livestock production. In such cases, exclosure experiments may not reflect typical outcomes of human-driven extirpations of wild herbivores. 3. Here, we examine how plant community responses to changes in the identity and abundance of large herbivores interact with abiotic factors (rainfall and soil properties). We also explore how effects of wild herbivores on plant communities differ between large-scale herbivore exclosures and landscape sites where anthropogenic activity has caused wildlife declines, often accompanied by livestock increases. 4. Abiotic context modulated the responses of plant communities to herbivore declines with stronger effect sizes in lower-productivity environments. Also, shifts in plant community structure, composition and species richness following wildlife declines differed considerably between exclosure experiments and landscape sites in which wild herbivores had declined and were often replaced by livestock. Plant communities in low wildlife landscape sites were distinct in both composition and physical structure from both exclosure and control sites in experiments. The power of environmental (soil and rainfall) gradients in influencing plant response to herbivores was also greatly dampened or absent in the landscape sites. One likely explanation for these observed differences is the compensatory effect of livestock associated with the depression or extirpation of wildlife. 5. Synthesis. Our results emphasize the importance of abiotic environmental heterogeneity in modulating the effects of mammalian herbivory on plant communities and the importance of such covariation in understanding effects of wild herbivore declines. They also suggest caution when extrapolating results from exclosure experiments to predict the consequences of defaunation as it proceeds in the Anthropocene.