Paulo S. Oliveira

Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks

The structure of mutualistic networks provides clues to processes shaping biodiversity [1-10]. Among them, interaction intimacy, the degree of biological association between partners, leads to differences in specialization patterns [4, 11] and might affect network organization [12]. Here, we investigated potential consequences of interaction intimacy for the structure and coevolution of mutualistic networks. From observed processes of selection on mutualistic interactions, it is expected that symbiotic interactions (high-interaction intimacy) will form species-poor networks characterized by compartmentalization [12, 13], whereas nonsymbiotic interactions (low intimacy) will lead to species-rich, nested networks in which there is a core of generalists and specialists often interact with generalists [3, 5, 7, 12, 14]. We demonstrated an association between interaction intimacy and structure in 19 ant-plant mutualistic networks. Through numerical simulations, we found that network structure of different forms of mutualism affects evolutionary change in distinct ways. Change in one species affects primarily one mutualistic partner in symbiotic interactions but might affect multiple partners in nonsymbiotic interactions. We hypothesize that coevolution in symbiotic interactions is characterized by frequent reciprocal changes between few partners, but coevolution in nonsymbiotic networks might show rare bursts of changes in which many species respond to evolutionary changes in a single species.

Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity

Abstract We studied the association between the honeydew-producing membracid Guayaquila xiphias and its tending ants in the cerrado savanna of Brazil, during 1992 and 1993. Results showed that ants attack potential enemies of G. xiphias, and that increased ant density near the treehoppers affects the spatial distribution of parasitoid wasps on the host plant, keeping them away from brood-guarding G. xiphias females. Controlled ant-exclusion experiments revealed that ant presence (seven species) reduces the abundance of G. xiphias’ natural enemies (salticid spiders, syrphid flies, and parasitoid wasps) on the host plant. The data further showed that ant-tending not only increased homopteran survival, but also conferred a direct reproductive benefit to G. xiphias females, which may abandon the first brood to ants and lay an additional clutch next to the original brood. Two years of experimental manipulations, however, showed that the degree of protection conferred by tending ants varies yearly, and that at initially high abundance of natural enemies the ant species differ in their effects on treehopper survival. Ant effects on treehopper fecundity also varied with time, and with shifts in the abundance of natural enemies. This is the first study to simultaneously demonstrate conditionality in ant-derived benefits related to both protection and fecundity in an ant-tended Membracidae, and the first to show the combined action of these effects in the same system.

Ants as Selective Agents on Herbivore Biology: Effects on the Behaviour of a Non-Myrmecophilous Butterfly

Larvae of the nymphalid butterfly Eunica bechina feed on young leaves of Caryocar brasiliense, a shrub of the Brazilian savannah that is frequently visited by nectar-gathering ants. Eggs are not removed by ants, but ant occupation on plants affects the oviposition behaviour of the butterflies. Adult females avoid laying eggs on highly visited plant locations and visual cues were demonstrated to mediate oviposition by the butterflies. Plant branches with artificial rubber ants were significantly less infested than control branches with rubber circles. This is the first demonstration that ant presence per se can be enough to produce an avoidance response by ovipositing females in a non-myrmecophilous butterfly. Larval mortality was strongly affected by the level of ant visitation to the host plants, and vulnerability to ant predation decreased with larval size. Stick-like frass chains constructed by the larvae at leaf margins were demonstrated to be a safe refuge against ant attacks on the host plant. Live termites placed on leaves were attacked by foraging ants in significantly greater numbers than those placed on the frass chains. It is concluded that the behavioural biology of both immature and adult Eunica bechina is finely linked with the utilization of a host plant where ant visitation patterns strongly affect larval survival.

Extrafloral nectaries: their taxonomic distribution and abundance in the woody flora of cerrado vegetation in southeast Brazil

The taxonomic distribution and abundance of woody plants with extrafloral nectaries (EFNs) are reported for different areas of cerrado vegetation (subtropical savanna) in the state of Sao Paulo, southeast Brazil. Thirty-four plant species belonging to 15 families were found to have EFNs. The Mimosaceae (6 species) and Bignoniaceae and Vochysiaceae (4 species each) were the families most frequently bearing EFNs. Glands associated with vegetative parts (leaves, stem) were more common (91.2%) than those found near the bud or flower (20.6%). The percentage of EFN-bearing species within the woody floras of 5 cerrado areas in Sao Paulo ranged from 15.5 to 20.2. The abundance of plants with EFNs in these areas varied from 7.6 to 20.3 percent. These results are compared with data obtained from other similar studies undertaken in temperate and tropical habitats.

Foraging ecology of attine ants in a Neotropical savanna: seasonal use of fungal substrate in the cerrado vegetation of Brazil

Summary: In this study we identified the material collected as fungal substrate by attine ants in the cerrado vegetation of Southeast Brazil. A total of 313 colonies of the evolutionary more primitive (genera Cyphomyrmex, Mycetarotes, Mycocepurus, Myrmicocrypta) and transitional attines (genera Sericomyrmex and Trachymyrmex) were marked in the field and monitored monthly, during one year. Attines collected material from 53 plant species in 28 families. Items included leaves, flowers, fruits, seeds, wood, mosses, lichens, insect feces and corpses. Flowers and fruits were the items most frequently collected by all genera, especially during the wet season when these plant parts are more abundant in the cerrado. During the dry season, the ants diversified the material collected, and the frequency of different items varied across the ant genera. The most primitive genera collected mainly insect feces and corpses, while the intermediate ones relied on vegetative plant parts such as recently fallen leaflets. Seeds and other materials such as mosses, lichens, and wood were also more commonly used during dry months. The use of these resources was associated with greater foraging distances by all genera in dry months. The results indicate that lower attines present an opportunistic foraging behavior, by collecting items in the vicinity of their nests, and in accordance with the phenology of the cerrado vegetation. We briefly discuss some general evolutionary trends within the Attini.

Size and lipid content of nonmyrmecochorous diaspores: effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil

Ants are often attracted to diaspores not adapted for dispersal by ants. These diaspores may occasionally benefit from this interaction. We selected six nonmyrmecochorous plant species (Virola oleifera, Eugenia stictosepala, Cabralea canjerana, Citharexylum myrianthum, Alchornea glandulosa and Hyeronima alchorneoides) whose diaspores differ in size and lipid content, and investigated how these features affect the outcome of ant-diaspore interactions on the floor of a lowland Atlantic forest of Southeast Brazil. A total of 23 ant species were seen interacting with diaspores on the forest floor. Ants were generally rapid at discovering and cleaning the diaspore pulp or aril. Recruitment rate and ant attendance were higher for lipid-rich diaspores than for lipid-poor ones. Removal rate and displacement distance were higher for small diaspores. The large ponerine ant Pachycondyla striata, one of the most frequent attendants to lipid-rich arillate diaspores, transported the latter into their nests and discarded clean intact seeds on refuse piles outside the nest. Germination tests with cleaned and uncleaned diaspores revealed that the removal of pulp or aril may increase germination success in Virola oleifera, Cabralea canjerana, Citharexylum myrianthum and Alchornea glandulosa. Gas chromatography analyses revealed a close similarity in the fatty acid composition of the arils of the lipid-rich diaspores and the elaiosome of a typical myrmecochorous seed (Ricinus communis), corroborating the suggestion that some arils and elaiosomes are chemically similar. Although ant-derived benefits to diaspores – secondary dispersal and/or increased germination – varied among the six plant species studied, the results enhanced the role of ant-diaspore interactions in the post-dispersal fates of nonmyrmecochorous seeds in tropical forests. The size and the lipid-content of the diaspores were shown to be major determinants of the outcome of such interactions.

Interactions between ants, fruits and seeds in a restinga forest in south-eastern Brazil

Fleshy diaspores (fruits, seeds) comprise a large portion of the litter on the floor of tropical forests, and interactions involving litter-foraging ants and diaspores are common in these areas. In this study, the interactions between ants and non-myrmecochorous diaspores (i.e. not adapted to dispersal by ants) were surveyed along a 1.4-km transect in a restinga forest (sandy soil) on the coast of south-eastern Brazil. During 2 y of monthly samplings, 562 interactions involving 48 ant species and 44 species of diaspore (0.02-11.10 g) were recorded. Ant-diaspore associations involved a considerable part of the ground-dwelling ant community. Large ponerine ants individually removed the diaspores up to 13 m, whereas small ants (myrmicines) normally recruited workers and consumed the diaspore on the spot. Ant- derived benefits to diaspores of non-myrmecochorous plants included secondary dispersal (small to medium-sized diaspores), and increased germination success after seed cleaning by ants. Large ponerine ants such as Odontomachus chelifer and Pachycondyla striata were the main seed vectors. Seedlings of three species were associated with nests of O. chelifer. The results indicate that ants play an important role in fruit/seed biology in the restinga forest.

The Use of Fruits and Seeds by Ants in the Atlantic Forest of Southeast Brazil1

Given the abundance of litter-foraging ants and fallen fleshy diaspores on the floor of tropical forests, interactions involving them should be common and may render important consequences for the biology of the diaspores. In this study, we surveyed the interactions between ants and non-myrmecochorous diaspores along a 5-km transect in a lowland Atlantic rain forest of southeast Brazil. A diaspore is defined as any seed, fruit, or infructescence that constitutes the unit of dispersal of the plant. During two years of monthly samplings of naturally fallen diaspores, 886 ant– diaspore interactions involving 36 ant species and 56 different species of diaspores (range 0.05–29.5 g) were recorded. The number of interactions was significantly and positively correlated with rainfall but not with mean temperature. The number of ant species recorded in the interactions was positively associated with both rainfall and temperature. Lipid-rich diaspores attracted a larger ant assemblage than those with lower contents of lipids. The seasonal pattern for ant–diaspore interactions in the Atlantic rain forest is predicted by well known seasonal patterns in ant activity and diaspore production. Other factors that also may affect the observed pattern are the massive and episodic fruiting of some plant species in which diaspores are especially attractive to ants, and a preference for lipidrich arillate seeds. Interactions between ants and fallen non-myrmecochorous diaspores may be especially common in lowland rain forests in which the abundance of ants is coupled with the year-round availability of fleshy diaspores.

Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in cerrado vegetation: ants as potential antiherbivore agents

SummaryQualea grandiflora is a typical tree of Brazilian cerrados (savanna-like vegetation) that bears paired extrafloral nectaries (EFNs) along its stems. Results show that possession of EFNs increases ant density on Q. grandiflora shrubs over that of neighbouring non-nectariferous plants. Frequency of ant occupancy and mean number of ants per plant were much higher on Qualea than on plants lacking EFNs. These differences resulted in many more live termitebaits being attacked by foraging ants on Qualea than on neighbours without EFNs. Termites were attacked in equal numbers and with equal speeds on different-aged leaves of Qualea. The greatest potential for herbivore deterrence was presented by Camponotus ants (C. crassus, C. rufipes and C. aff. blandus), which together attacked significantly more termites than nine other ant species grouped. EFNs are regarded as important promoters of ant activity on cerado plants.

Egg-laying butterflies distinguish predaceous ants by sight.

Information about predation risks is critical for herbivorous insects, and natural selection favors their ability to detect predators before oviposition and to select enemy‐free foliage when offspring mortality risk is high. Food plants are selected by ovipositing butterflies, and offspring survival frequently varies among plants because of variation in the presence of predators. Eunica bechina butterflies oviposit on Caryocar brasiliense, an ant‐defended plant. Experiments with dried Camponotus and Cephalotes ants pinned to leaves revealed that butterflies use ant size and form as visual cues to avoid ovipositing on plant parts occupied by ants more likely to kill larval offspring. Presence of sap‐sucking bugs did not affect butterfly oviposition. This is the first demonstration that visual recognition of predators can mediate egg‐laying decisions by an insect herbivore and that an insect will discriminate among different species of potential predators. This unusual behavioral capability permits specialization on a risky, ant‐defended food plant.