Macroevolutionary patterns in the origin of mutualisms involving ants

Ants are a diverse and abundant insect group that form mutualistic associations with a number of different organisms from fungi to insects and plants. Here, we use a phylogenetic approach to identify ecological factors that explain macroevolutionary trends in the mutualism between ants and honeydew-producing Homoptera. We also consider association between ant-Homoptera, ant-fungi and ant-plant mutualisms. Homoptera-tending ants are more likely to be forest dwelling, polygynous, ecologically dominant and arboreal nesting with large colonies of 10(4)-10(5) individuals. Mutualistic ants (including those that garden fungi and inhabit ant-plants) are found in under half of the formicid subfamilies. At the genus level, however, we find a negative association between ant-Homoptera and ant-fungi mutualisms, whereas there is a positive association between ant-Homoptera and ant-plant mutualisms. We suggest that species can only specialize in multiple mutualisms simultaneously when there is no trade-off in requirements from the different partners and no redundancy of rewards.

Avoidance responses of an aphidophagous ladybird, Adalia bipunctata, to aphid-tending ants

1. Insect predators often aggregrate to patches of high prey density and use prey chemicals as cues for oviposition. If prey have mutualistic guardians such as ants, however, then these patches may be less suitable for predators. 2. Ants often tend aphids and defend them against predators such as ladybirds. Here, we show that ants can reduce ladybird performance by destroying eggs and physically attacking larvae and adults. 3. Unless ladybirds are able to defend against ant attacks they are likely to have adaptations to avoid ants. We show that Adalia bipunctata ladybirds not only move away from patches with Lasius niger ants, but also avoid laying eggs in these patches. Furthermore, ladybirds not only respond to ant presence, but also detect ant semiochemicals and alter oviposition strategy accordingly. 4. Ant semiochemicals may signal the extent of ant territories allowing aphid predators to effectively navigate a mosaic landscape of sub-optimal patches in search of less well-defended prey. Such avoidance probably benefits both ants and ladybirds, and the semiochemicals could be regarded as a means of cooperative communication between enemies. 5. Overall, ladybirds respond to a wide range of positive and negative oviposition cues that may trade-off with each other and internal motivation to determine the overall oviposition strategy.

When are ant-attractant devices a worthwhile investment? Vicia faba extrafloral nectaries and Lasius niger ants

Most studies aiming to determine the beneficial effect of ants on plants simply consider the effects of the presence or exclusion of ants on plant yield. This approach is often inadequate, however, as ants interact with both non-tended herbivores and tended Homoptera. Moreover, the interaction with these groups of organisms is dependent on ant density, and these functional relationships are likely to be non-linear. A model is presented here that segregates plant herbivores into two categories depending on the sign of their numerical response to ants (myrmecophiles increase with ants, non-tended herbivores decline). The changes in these two components of herbivores with increasing ant density and the resulting implications for ant-plant mutualisms are considered. It emerges that a wide range of ant densities needs to be considered as the interaction sign (mutualism or parasitism) and strength is likely to change with ant density. The model is used to interpret the results of an experimental study that varied levels of Aphis fabae infestation and Lasius niger ant attendance on Vicia faba bean plants. Increasing ant density consistently reduced plant fitness and thus, in this location, the interaction between the ants and the plant can be considered parasitic. In the Vicia faba system, these costs of ants are unlikely to be offset by other beneficial agents (e.g., parasitoids), which also visit extrafloral nectaries.

Thorn-dwelling ants provide antiherbivore defence for camelthorn trees, Vachellia erioloba, in Namibia

Ants are widely employed by plants as an antiherbivore defence. A single host plant can associate with multiple, symbiotic ant species, although usually only a single ant species at a time. Different plant-ant species may vary in the degree to which they defend their host plant. In Kenya, ant–acacia interactions are well studied, but less is known about systems elsewhere in Africa. A southern African species, Vachellia erioloba, is occupied by thorn-dwelling ants from three different genera. Unusually, multiple colonies of all these ants simultaneously and stably inhabit trees. We investigated if the ants on V. erioloba (i) deter insect herbivores; (ii) differ in their effectiveness depending on the identity of the herbivore; and (iii) protect the tree against an important herbivore, the larvae of the lepidopteran Gonometa postica. We show that experimental exclusion of ants leads to greater levels of herbivory on trees. The ants inhabiting V. erioloba are an effective deterrent against hemipteran and coleopteran, but not lepidopteran herbivores. Defensive services do not vary among ant species, but only Crematogaster ants exhibit aggression towards G. postica. This highlights the potential of the V. erioloba–ant mutualism for studying ant–plant interactions that involve multiple, simultaneously resident thorn-dwelling ant species.

Analysis and modeling of ants’ behavior from single to multi-body

In order to shed light on the collective behavior of social insects, we analyzed the behavior of ants from single to multi-body. In an experimental set-up, ants are placed in hemisphere without a nest and food. Trajectory of ants is recorded. From this bottom-up approach, we found that collective behavior of ants as follows: 1. Activity of single ant increases and decreases periodically. 2. Spontaneous meeting process is observed between two ants and meeting spot of two ants is localized in hemisphere. 3. Result on division of labor is obtained between two ants.

Arboreal thorn-dwelling ants use domatia morphology to partition nest sites on the savanna ant-plant, Vachellia erioloba

Nest site selection in arboreal, domatia-dwelling ants, particularly those coexisting on a single host plant, is little understood. To examine this phenomenon we studied the African savannah tree Vachellia erioloba, which hosts ants in swollen-thorn domatia. We found four ant species from different genera (Cataulacus intrudens, Tapinoma subtile, Tetraponera ambigua and an unidentified Crematogaster species). In contrast to other African ant plants, many V. erioloba trees (41 % in our survey) were simultaneously co-occupied by more than one ant species. Our study provides quantitative field data describing: (1) aspects of tree and domatia morphology relevant to supporting a community of mutualist ants, (2) how ant species occupancy varies with domatia morphology and (3) how ant colony size varies with domatia size and species. We found that Crematogaster sp. occupy the largest thorns, followed by C. intrudens, with T. subtile in the smallest thorns. Thorn age, as well as nest entrance hole size correlated closely with ant species occupant. These differing occupancy patterns may help to explain the unusual coexistence of three ant species on individual myrmecophytic trees. In all three common ant species, colony size, as measured by total number of ants, increased with domatia size. Additionally, domatia volume and species identity interact to predict ant numbers, suggesting differing responses between species to increased availability of nesting space. The proportion of total ants in nests that were immatures varied with thorn volume and species, highlighting the importance of domatia morphology in influencing colony structure.

A trophic cascade induced by predatory ants in a fig-fig wasp mutualism

Summary 1. A trophic cascade occurs when predators directly decrease the densities, or change the behaviour, of herbivores and thus indirectly increase plant productivity. The predator–herbivore– plant context is well known, but some predators attack species beneficial to plants (e.g. pollinators) and/or enemies of herbivores (e.g. parasites), and their role in the dynamics of mutualisms remains largely unexplored. 2. We surveyed the predatory ant species and studied predation by the dominant ant species, the weaver ant Oecophylla smaragdina, associated with the fig tree Ficus racemosa in southwest China. We then tested the effects of weaver ants on the oviposition behaviour of pollinating and non-pollinating fig wasps in an ant-exclusion experiment. The effects of weaver ants on fig wasp community structure and fig seed production were then compared between trees with and without O. smaragdina. 3. Oecophylla smaragdina captured more non-pollinating wasps (Platyneura mayri) than pollinators as the insects arrived to lay eggs. When ants were excluded, more non-pollinators laid eggs into figs and fewer pollinators entered figs. Furthermore, trees with O. smaragdina produced more pollinator offspring and fewer non-pollinator offspring, shifting the community structure significantly. In addition, F. racemosa produced significantly more seeds on trees inhabited by weaver ants. 4. Oecophylla smaragdina predation reverses the dominance of the two commonest wasp species at the egg-laying stage and favours the pollinators. This behavioural pattern is mirrored by wasp offspring production, with pollinators’ offspring dominating figs produced by trees inhabited by weaver ants, and offspring of the non-pollinator P. mayri most abundant in figs on trees inhabited by other ants. 5. Overall, our results suggest that predation by weaver ants limits the success of the non-pollinating P. mayri and therefore indirectly benefits the mutualism by increasing the reproductive success of both the pollinators and the plant. Predation is thus a key functional factor that can shape the community structure of a pollinator-plant mutualistic system. Key-words: competitive release, fig wasp, mutualism, predation, predator-exclusion experiment, trophic cascade

A Plant Needs Ants like a Dog Needs Fleas: Myrmelachista schumanni Ants Gall Many Tree Species to Create Housing

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.

Evolution of cuticular hydrocarbon diversity in ants

The cuticular hydrocarbons (CHCs) of ants provide important cues for nestmate and caste recognition. There is enormous diversity in the composition of these CHCs, but the manner in which this diversity has evolved is poorly understood. We gathered data on CHC profiles for 56 ant species, relating this information to their phylogeny. We deduced the mode of evolution of CHC profiles by reconstructing character evolution and then relating the number of changes in CHC components along each branch of the phylogeny to the length of the branch. There was a strong correlation between branch length and number of component changes, with fewer changes occurring on short branches. Our analysis thereby indicated a gradual mode of evolution. Different ant species tend to use specific CHC structural types that are exclusive of other structural types, indicating that species differences may be generated in part by switching particular biosynthetic pathways on or off in different lineages. We found limited, and contradictory, evidence for abiotic factors (temperature and rainfall) driving change in CHC profiles.

Effects of leaves of Ipomoea batatas (Convolvulaceae) on nest development and on respiratory metabolism of leaf-cutting ants Atta sexdens L. (Hym., Formicidae)

Laboratory colonies of the leaf-cutting ants Atta sexdens feed daily with leaves of Ipomoea batatas showed ant mortality and a significant decrease in the size of the fungal garden after the second week, with complete depletion of nests after 5 weeks of treatment. The mean oxygen consumption rate of these ants was higher than the control (ants collected from nests feed with leaves of Eucalyptus alba), suggesting a physiological action of the leaves of I. batatas on the ants in addition to the effect of inhibiting the growth of the fungal garden.

Nesting biology of the fungus growing ants Mycetarotes Emery (Attini, Formicidae)

Fungus-growing ants of the genus Mycetarotes are among the least studied in the tribe Attini. This report documents nest architecture and worker population numbers for 19 nests of M. parallelus and 5 nests of M. acutus, including the first such report for M. acutus. This new information is integrated with the scant biological information reported on Mycetarotes to date. The resulting picture of Mycetarotes life history, as well as the relative ease with which large numbers of nests can be collected and observed in the field, suggest that Mycetarotes (particularly M. parallelus) is an ideal model system for the study of coevolution of lower-attine ants and their cultivated fungi.

Starch metabolism in Leucoagaricus gongylophorus, the symbiotic fungus of leaf-cutting ants

Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ants, degrades starch, this degradation being supposed to occur in the plant material which leafcutters forage to the nests, generating most of the glucose which the ants utilize for food. In the present investigation, we show that laboratory cultures of L. gongylophorus produce extracellular alpha-amylase and maltase which degrade starch to glucose, reinforcing that the ants can obtain glucose from starch through the symbiotic fungus. Glucose was found to repress a-amylase and, more severely, maltase activity, thus repressing starch degradation by L. gongylophorus, so that we hypothesize that: (1) glucose down-regulation of starch degradation also occurs in the Atta sexdens fungus garden; (2) glucose consumption from the fungus garden by A. sexdens stimutates degradation of starch from plant material by L. gongylophorus, which may represent a mechanism by which Leafcutters can control enzyme production by the symbiotic fungus. Since glucose is found in the fungus garden inside the nests, down-regulation of starch degradation by glucose is supposed to occur in the nest and play a part in the control of fungal enzyme production by leafcutters. (c) 2005 Elsevier GmbH. All rights reserved.

Respiratory metabolism of Camponotus rufipes ants: Brood and adults

The respiratory metabolism of immature forms (eggs, larvae, prepupae and pupae) of Camponotus rufipes (Hymenoptera: Formicidae) was studied at 25 degrees C, using a Warburg respirometer. Mean respiratory rates (mu l O gamma mg(-1) live weight.hr(-1)) for eggs, first instars, second instars, third instars, fourth instars, prepupae, and pupae were respectively: 2.53, 5.07, 1.23, 0.32, 0.22, 0.19 and 0.13. Adult workers with body mass between 20 and 30 mg had a mean respiratory rate of 0.43. The high respiratory rate in first instars probably reflects, besides the size influence, the metabolic costs of differentiation that occurs in this phase. (C) 1998 Published by Elsevier B.V.

Substrate Preparation Behaviors for the Cultivation of the Symbiotic Fungus in Leaf-Cutting Ants of the Genus Atta (Hymenoptera: Formicidae)

Our findings revealed two distinct patterns of substrate preparation: the pattern of leaf-cutting ants foraging on dicotyledons is marked by highly fragmented substrate resulting in a more advanced initial decomposition. The pattern of leaf-cutting ants harvesting grasses is characterized by large pieces of substrate, resulting in little initial decomposition. Ants foraging on both types of plants are apparently intermediary between the two patterns, although more similar to the patterns of those foraging on dicotyledons. Also, the behavior of scraping the substrate was described for the first time, it is very important for the removal of the epicuticular wax layer of the leaves helping the growth of the symbiotic fungus.