School of Biological Sciences

Hundreds of tropical plant species house ant colonies in specialized chambers called domatia. When, in 1873, Richard Spruce likened plant-ants to fleas and asserted that domatia are ant-created galls, he incited a debate that lasted almost a century. Although we now know that domatia are not galls and that most ant-plant interactions are mutualisms and not parasitisms, we revisit Spruce’s suggestion that ants can gall in light of our observations of the plant-ant Myrmelachista schumanni, which creates clearings in the Amazonian rain forest called “supay-chakras,” or “devil’s gardens.” We observed swollen scars on the trunks of nonmyrmecophytic canopy trees surrounding supay-chakras, and within these swellings, we found networks of cavities inhabited by M. schumanni. Here, we summarize the evidence supporting the hypothesis that M. schumanni ants make these galls, and we hypothesize that the adaptive benefit of galling is to increase the amount of nesting space available to M. schumanni colonies.

Manu National Park of southern Peru is one of the most renowned protected areas in the world, yet large-bodied vertebrate surveys conducted to date have been restricted to Cocha Cashu Biological Station, a research station covering < 0.06 percent of the 1.7 Mha park. Manu Park is occupied by 4 460 settled Matsigenka Amerindians, 300–400 isolated Matsigenka, and several, little-known groups of isolated hunter–gatherers, yet the impact of these native Amazonians on game vertebrate populations within the park remains poorly understood. On the basis of 1495 km of standardized line-transect censuses, we present density and biomass estimates for 23 mammal, bird, and reptile species for seven lowland and upland forest sites in Manu Park, including Cocha Cashu. We compare these estimates between hunted and nonhunted sites within Manu Park, and with other Neotropical forest sites. Manu Park safeguards some of the most species-rich and highest biomass assemblages of arboreal and terrestrial mammals ever recorded in Neotropical forests, most likely because of its direct Andean influence and high levels of soil fertility. Relative to Barro Colorado Island, seed predators and arboreal folivores in Manu are rare, and generalist frugivores specializing on mature fruit pulp are abundant. The impact of such a qualitative shift in the vertebrate community on the dynamics of plant regeneration, and therefore, on our understanding of tropical plant ecology, must be profound. Despite a number of external threats, Manu Park continues to serve as a baseline against which other Neotropical forests can be gauged.

Theory suggests that spatial structuring should select for intermediate levels of virulence in parasites, but empirical tests are rare and have never been conducted with castration (sterilizing) parasites. To test this theory in a natural landscape, we construct a spatially explicit model of the symbiosis between the ant-plant Cordia nodosa and its two, protecting ant symbionts, Allomerus and Azteca. Allomerus is also a castration parasite, preventing fruiting to increase colony fecundity. Limiting the dispersal of Allomerus and host plant selects for intermediate castration virulence. Increasing the frequency of the mutualist, Azteca, selects for higher castration virulence in Allomerus, because seeds from Azteca-inhabited plants are a public good that Allomerus exploits. These results are consistent with field observations and, to our knowledge, provide the first empirical evidence supporting the hypothesis that spatial structure can reduce castration virulence and the first such evidence in a natural landscape for either mortality or castration virulence.

1. Widespread hunting throughout Amazonia threatens the persistence of large primates and other vertebrates. Most studies have used models of limited validity and restricted spatial and temporal scales to assess the sustainability.
2. We use human-demographic, game-harvest and game-census data to parameterize a spatially explicit hunting model. We explore how population growth and spread, hunting technology and effort, and source–sink dynamics impact the density of black spider monkeys Ateles chamek over time and space in the rainforests of south-eastern Peru.
3. In all scenarios, spider monkey populations, which are vulnerable to hunting, persist in high numbers in much of Manu National Park over the next 50 years. Nonetheless, shotguns cause much more depletion than traditional bow hunting by Matsigenka (Machiguenga) indigenous people.
4. Maintenance of the current indigenous lifestyle (dispersed settlements, bow hunting) is unlikely to deplete spider monkeys and, by extension, other fauna, despite rapid human population growth. This helps explain why large, pre-Colombian human populations did not drive large primates to extinction. When guns are used, however, spider monkeys quickly become depleted around even small settlements, with depletion eventually reversing the short-term harvest advantage provided by shotgun hunting. Thus, our models show that when guns are used, limits on settlement numbers can reduce total depletion.
5. Synthesis and applications. Our framework lets us visualize the future effects of hunting, population growth, hunting technology and settlement spread in tropical forests. In Manu Park, the continued prohibition of firearms is important for ensuring long-term hunting sustainability. A complementary policy is to negotiate limits on new settlements in return for development aid in existing settlements. The advantage of the latter approach is that settlement numbers are more easily monitored than is hunting effort or technology. Similar policies could help to reduce landscape-scale depletion of prey species in human-occupied reserves and protected areas throughout the Amazon.

Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia (‘figs’) that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp- stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can ‘set the rules of the game’ to ensure mutualistic behavior in its symbionts.

In this study, we present the cumulative results of ongoing research into the landscape classification system of the Arawakan-speaking Baniwa people of the Upper Rio Negro, Brazil. After presenting a general overview of Baniwa land- scape classification, we provide more detailed analysis of the Baniwa’s sophisti- cated system for characterizing different vegetation types within the white-sand savanna-forest matrix, or campinarana, that dominates the northwest Amazon. Ten Baniwa informants provided a repertoire of 150 indigenous-language plant names (hereafter, “species”) during interviews about perceived botanical compo- sition in fourteen predominant white-sand vegetation types. Informant consen- sus regarding the presence of these species was used as a proxy for the species’ actual abundance for each vegetation type. Species assemblies and patterns of gradual floristic change across the fourteen vegetation types were analyzed using cluster analysis, indicator species analysis, and ordination by nonmetric multi-dimensional scaling. These tools from quantitative ecological community analy- sis confirm the ecological validity of Baniwa landscape knowledge while provid- ing further insights into how this knowledge is structured, and how it relates to specific biotic and abiotic elements of the campinarana landscape. The methods applied here would likewise prove useful for rapid, cost-effective assessment of conservation priorities of plant communities in regions where, as among the Baniwa, local populations maintain intimate knowledge of the environmental preferences of a large number of plant species.

We investigated sex allocation in the Neotropical ant Allomerus octoarticulatus var. demerarae. Because Allomerus is a plant symbiont, we could make geographically extensive collections of complete colonies and of foundresses in saplings, allowing us to estimate not only population- and colony-level sex allocation but also colony resource levels and the relatednesses of competing ant foundresses. This species exhibits a strongly split sex ratio, with 80% of mature colonies producing ≥90% of one sex or the other. Our genetic analyses (DNA microsatellites) reveal that Allomerus has a breeding system characterized by almost complete monogyny and a low frequency of polyandry. Contrary to theoretical explanations, we find no difference in worker relatedness asymmetries between female- and male-specialist colonies. Furthermore, no clear link was found between colony sex allocation and life history traits such as the number of mates per queen, or colony size, resource level, or fecundity. We also failed to find significant support for male production by workers, infection by Wolbachia, local resource competition, or local mate competition. We are left with the possibility that Allomerus exhibits split sex ratios because of the evolution of alternative biasing strategies in queens or workers, as recently proposed in the literature.

Manu National Park was founded in 1973 on a profound contradiction: the “untouchable” core area is in fact the homeland of a large Amerindian population, including the Matsigenka (Machiguenga). Some view the Westernization of native communities living in protected areas as a threat to biodiversity conservation and suggest that such populations should be enticed to resettle outside parks. Here, we present an overview of the indigenous populations of Manu, outline the history of the park and its anthropological policies, and discuss evolving park-Matsigenka conflicts as well as areas of common interest. Analysis reveals that resettlement has no political, legal, or practical viability. Thus, given the options available, we propose that long-term biodiversity conservation can best be achieved through a ‘tenure for defense’ trade: indigenous communities receive explicit benefits (direct and indirect) in exchange for helping to defend the park against incursion and managing vulnerable resources such as game animals.

One of the main problems impeding the evolution of cooperation between species is partner choice. When information is asymmetric (the quality of the potential partners is known only to themselves), an interaction with high-quality partners can be established if they can signal their quality. If signaling is not possible, or if hosts cannot actively choose, it may seem that partner choice is not possible. Many mutualisms, however, exist without signaling, and the mechanisms by which hosts might select the right partners are unclear. For example, can an animal exclude parasitic bacteria from its gut, and can a plant favor colonization by beneficial ants, bacteria, or fungi? Here we propose a very general mechanism of partner choice, ‘screening,’ that is taken from the economic theory of mechanism design. If a host evolves an appropriate entry cost for potential partners, such that the ability to pay the cost is correlated with their quality as symbionts, then only high-quality partners will find it profitable to accept the interaction, and low-quality partners will screen themselves out of the interaction, or not evolve to colonize the host. Several types of biological symbioses are good candidates for screening, including bobtail squid, ant-plants, gut microbiomes, and the many animal and plant species that produce reactive oxygen species while paradoxically also hosting beneficial bacteria. We describe a series of diagnostic tests for screening. Screening games can apply to the difficult cases where by-products, partner fidelity feedback, or host sanctions do not apply, therefore explaining the evolution of mutualism in systems that are not repeated games or vertically transmitted, where it is impossible for potential symbionts to signal their cooperativeness beforehand, and where the host does not punish symbiont misbehavior.

Although mutualisms are common in all ecological communities and have played key roles in the diversification of life, our current understanding of the evolution of cooperation applies mostly to social behavior within a species. A central question is whether mutualisms persist because hosts have evolved costly punishment of cheaters. Here, we use the economic theory of employment contracts to formulate and distinguish between two mechanisms that have been proposed to prevent cheating in host–symbiont mutualisms, partner fidelity feedback (PFF) and host sanctions (HS). Under PFF, positive feedback between host fitness and symbiont fitness is sufficient to prevent cheating; in contrast, HS posits the necessity of costly punishment to maintain mutualism. A coevolutionary model of mutualism finds that HS are unlikely to evolve de novo, and published data on legume–rhizobia and yucca–moth mutualisms are consistent with PFF and not with HS. Thus, in systems considered to be textbook cases of HS, we find poor support for the theory that hosts have evolved to punish cheating symbionts; instead, we show that even horizontally transmitted mutualisms can be stabilized via PFF. PFF theory may place previously underappreciated constraints on the evolution of mutualism and explain why punishment is far from ubiquitous in nature.

Retaliation against cheaters can prevent the breakdown of cooperation. Here we ask whether the ant–plant Cordia nodosa is able to apply retaliatory sanctions against its ant symbiont Allomerus octoarticulatus, which patrols new shoots to prevent herbivory. We test the hypothesis that the modular design of C. nodosa physiologically ties the growth of housing (stem swellings known as domatia) to the successful development of the attached leaves. We experimentally simulated herbivory by cutting leaves from patrolled shoots and found that the domatia on such ‘cheated’ shoots suffered higher mortality and lower growth than did controls, evidence for a host sanction. On the other hand, patrolling is costly to the ant, and experiment shows that non-patrollers run a low risk of being sanctioned because most leaves (and the attached domatia) escape heavy herbivory even when patrollers are absent. This suggests that cheaters might enjoy a higher fitness than do mutualists, despite sanctions, but we find that patrolling provides a net fecundity benefit when the colony and plant exceed a minimum size, which requires sustained ant investment in patrolling. These results map directly onto the principal–agent (P–A) game from economics, which we suggest can be used as a framework for studying stability in mutualisms, where high sampling costs and cheating do not allow market effects to select for mutual benefits.

Exploring the factors governing the maintenance and breakdown of cooperation between mutualists is an intriguing and enduring problem for evolutionary ecology, and symbioses between ants and plants can provide useful experimental models for such studies. Hundreds of tropical plant species have evolved structures to house and feed ants, and these ant^plant symbioses have long been considered classic exam- ples of mutualism. Here, we report that the primary ant symbiont, Allomerus cf. demerarae, of the most abundant ant-plant found in south-east Peru, Cordia nodosa Lam., castrates its host plant. Allomerus workers protect new leaves and their associated domatia from herbivory, but destroy £owers, reducing fruit production to zero in most host plants. Castrated plants occupied by Allomerus provide more domatia for their associated ants than plants occupied by three species of Azteca ants that do not castrate their hosts. Allomerus colonies in larger plants have higher fecundity. As a consequence, Allomerus appears to bene¢t from its castration behaviour, to the detriment of C. nodosa. The C. nodosa^ant system exhibits none of the retaliatory or ¢ltering mechanisms shown to stabilize cheating in other cooperative systems, and appears to persist because some of the plants, albeit a small minority, are inhabited by the three species of truly mutualistic Azteca ants.

Ecological theory has long supported the idea that species coexistence in a homogeneous habitat is promoted by spatial structure, but empirical evidence for this hypothesis has lagged behind theory. Here we describe a Neotropical ant–plant symbiosis that is ideally suited for testing spatial models of coexistence. Two genera of ants, Allomerus cf. demerarae and three species of Azteca are specialized to live on a single species of ant- plant, Cordia nodosa, in a Western Amazonian tropical rain forest. Empirically, using census data from widely separated localities, we show that the relative colonization abilities of the two ant genera are a function of plant density. A parameterized model shows that this pattern alone is sufficiently robust to explain coexistence in the system. Census and ex- perimental data suggest that Azteca queens are better long-distance flyers, but that Allomerus colonies are more fecund. Thus, Azteca can dominate in areas where host-plant densities are low (and parent colony–sapling distances are long), and Allomerus can dominate in areas where host-plant densities are high. Existing spatial heterogeneity in host-plant den- sities therefore can allow regional coexistence, and intersite dispersal can produce local mixing. In conclusion, a dispersal–fecundity trade-off appears to allow the two genera to treat spatial heterogeneity in patch density as a niche axis. This study further suggests that a spatially structured approach is essential in understanding the persistence of some mu- tualisms in the presence of parasites

The Matsigenka (or Machiguenga) Indians of the Peruvian Amazon describe and define rain forest habitats according to a complex system of ecological classification based on vegetative adn other biotic features as well as abiotic features such as topography, hydrology, edaphic characteristics and disturbance regimes. The Matsigenka distinguish some 69 vegetationally-defined habitats (some of which overlap) and 29 abiotically-defined habitats, as well as ten soil types and at least seven habitats associated with specific faunal indicators. Palms and other Monocots are particularly important as indicator species in Matsigenka habitat classification. The Matsigenka consider various subcategories of biotic and abiotic features somewhat independently when assessing forest habitats. Though not organized into a single, unified hierarchy, the multiple systems of habitat description intersect to define forest types. Comparing Matsigenka habitat classification with that of several other Amazonian indigenous groups, a number of common features are observed. Given the scientific validity of indigenous and local knowledge about habitat diversity, and given the accelerating rates of cultural and environmental degradation, it is important that ethnobiologists, tropical biologist, conservationists and indigenous communities collaborate in studies of Amazonian biodiversity.

In this study, we draw on the ecological knowledge of the Matsigenka indigenous people of the Peruvian Amazon as a template for interpreting satellite images and assessing rain forest habitat diversity, in a process we have dubbed “ethnobotanical ground-truthing.” Recent assessments of LANDSAT images of the Peruvian Amazon suggest rain forest habitat diversity may have been historically underestimated. Yet there exists little empirical evidence to support this assertion, and satellite images alone prove problematic in accurately distinguishing habitats on the ground. An ethnoecological study among the Matsigenka reveals a complex system of habitat classification based on vegetative and other biotic features as well as topographic, hydrological, and edaphic characteristics, and disturbance regimes. The Matsigenka distinguish some 69 vegetationally-defined habitats (some of which overlap) and 29 abiotically-defined habitats, as well as ten soil types and at least seven habitats associated with specific faunal indicators. The Matsigenka recognize all forest types currently known to ecologists working in the region, and also distinguish some types not apparently known to ecologists. Several forest types recognized by the Matsigenka have, as their dominant species, trees previously considered rare. Estimates of forest diversity based on indigenous knowledge suggest forty to fifty distinct natural habitat and micro-habitat types for the Manu river alone, at least triple the number previously recognized. Scientists working in this and other tropical forest areas with indigenous populations might benefit from collaboration with ethnobiologists and local communities. Ethnobotanical ground-truthing may ultimately contribute to our understanding of the diversity and dynamics of tropical forests.