Todd M. Palmer

Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis

Plants and their associated fungi reward partners that offer the best resources to sustain mutualism in complex systems. Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be “enslaved.” Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.

Accelerated modern human–induced species losses: Entering the sixth mass extinction

Humans are causing a massive animal extinction without precedent in 65 million years. The oft-repeated claim that Earth’s biota is entering a sixth “mass extinction” depends on clearly demonstrating that current extinction rates are far above the “background” rates prevailing between the five previous mass extinctions. Earlier estimates of extinction rates have been criticized for using assumptions that might overestimate the severity of the extinction crisis. We assess, using extremely conservative assumptions, whether human activities are causing a mass extinction. First, we use a recent estimate of a background rate of 2 mammal extinctions per 10,000 species per 100 years (that is, 2 E/MSY), which is twice as high as widely used previous estimates. We then compare this rate with the current rate of mammal and vertebrate extinctions. The latter is conservatively low because listing a species as extinct requires meeting stringent criteria. Even under our assumptions, which would tend to minimize evidence of an incipient mass extinction, the average rate of vertebrate species loss over the last century is up to 100 times higher than the background rate. Under the 2 E/MSY background rate, the number of species that have gone extinct in the last century would have taken, depending on the vertebrate taxon, between 800 and 10,000 years to disappear. These estimates reveal an exceptionally rapid loss of biodiversity over the last few centuries, indicating that a sixth mass extinction is already under way. Averting a dramatic decay of biodiversity and the subsequent loss of ecosystem services is still possible through intensified conservation efforts, but that window of opportunity is rapidly closing.

Mutualisms in a changing world: an evolutionary perspective

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.

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.

Competition and Coexistence: Exploring Mechanisms That Restrict and Maintain Diversity within Mutualist Guilds

Mutualistic interactions are diverse and widespread and often involve multispecies guilds of mutualists competing for access to one or more partner species. Despite the ubiquity of these interactions, we know little about the dynamics of competition and coexistence within these guilds or how interactions between mutualists and their shared resource (the partner species) may influence these dynamics. In this article, we review the evidence for interspecific competition for partners within mutualist guilds in both plant‐pollinator and ant‐myrmecophyte systems. We then review evidence for the operation of different coexistence mechanisms within these guilds and discuss how the dynamics of competition and coexistence may be uniquely shaped by multispecies mutualist interactions. In particular, we note that adaptive and plastic responses by mutualists to variation in partner quality are likely to play an important role in determining these dynamics. We summarize by considering the ecological conditions that are likely to restrict or promote species coexistence within mutualist guilds. We suggest that these guilds may provide powerful model systems for exploring multiple mechanisms of species coexistence, and we discuss how these mechanisms may be modified by evolutionary adaptation.

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.

Spatial Pattern Enhances Ecosystem Functioning in an African Savanna

Termites indirectly enhance plant and animal productivity near their mounds, and the uniform spatial patterning of these mounds enhances the overall productivity of the entire landscape.

The influences of patch shape and boundary contrast on insect response to fragmentation in California grasslands

Landscape ecologists typically identify boundaries to demarcate habitatpatches. The boundary between two habitat types may be abrupt, such as thetransition between a grassland and a parking lot, or more gradual, such as theshift between successional forest stages. Two key aspects of landscapeboundaries, their shape and contrast, are predicted to influence movement ofmaterials, plants, and animals. Ecological theory suggests that a patch’sperimeter-to-area ratio should strongly influence animal emigration when patchboundaries are relatively permeable, but not when boundaries are more severe.Weinvestigated the interactive effects of patch shape and boundary contrast onmovement of ground-dwelling beetles (Carabidae and Tenebrionidae) in nativegrassland habitat at Jepson Prairie, Solano County, California, USA. Weconducted a field experiment with two patch shape treatments, square andrectangle, that held patch area constant, and two boundary contrast treatmentscreated by mowing grass surrounding each plot at two different heights. Wemonitored the number of beetles leaving each patch over a three-week periodfollowing treatment establishment. We observed a significant effect of boundarycontrast on net movement of beetles, with low contrast boundaries exhibitingnetimmigration and high contrast boundaries experiencing net emigration. Moreover,the importance of patch shape appeared to be greater for low contrast versushigh contrast boundaries, consistent with theoretical expectations. Ourcombinedobservations indicate that these ground-dwelling beetles were more likely tomove into patches that were rectangular and surrounded by a low contrast matrixthan patches that were square or surrounded by a high contrast matrix. Weconclude that net movement of beetles across patch boundaries is stronglyinfluenced by boundary contrast and may be affected by patch shape whenboundarycontrast is low.

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.