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.

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.

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.

The curious case of the camelthorn: competition, coexistence and nest-site limitation in a multispecies mutualism

Myrmecophyte plants house ants in domatia in exchange for protection from herbivores. Ant-myrmecophyte mutualisms exhibit two general patterns due to competition between ants for plant occupancy: i) domatia nest-sites are a limiting resource and ii) each individual plant hosts one ant species at a time. However, individual camelthorn trees (Vachellia erioloba) typically host two to four ant species simultaneously, often coexisting in adjacent domatia on the same branch. Such fine-grain spatial coexistence brings into question the conventional wisdom on ant-myrmecophyte mutualisms. Camelthorn ants appear not to be nest-site limited, despite low abundance of suitable domatia, and have random distributions of nest-sites within and across trees. These patterns suggest a lack of competition between ants for domatia and contrast strongly with other ant-myrmecophyte systems. Comparison of this unusual case with others suggests that spatial scale is crucial to coexistence or competitive exclusion involving multiple ant species. Furthermore, coexistence may be facilitated when co-occurring ant species diverge strongly on at least one niche axis. Our conclusions provide recommendations for future ant-myrmecophyte research, particularly in utilising multispecies systems to further our understanding of mutualism biology.

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

Floral volatiles controlling ant behaviour

P>1. Ants show complex interactions with plants, both facultative and mutualistic, ranging from grazers through seed predators and dispersers to herders of some herbivores and guards against others. But ants are rarely pollinators, and their visits to flowers may be detrimental to plant fitness. 2. Plants therefore have various strategies to control ant distributions, and restrict them to foliage rather than flowers. These 'filters' may involve physical barriers on or around flowers, or 'decoys and bribes' sited on the foliage (usually extrafloral nectaries - EFNs). Alternatively, volatile organic compounds (VOCs) are used as signals to control ant behaviour, attracting ants to leaves and/or deterring them from functional flowers. Some of the past evidence that flowers repel ants by VOCs has been equivocal and we describe the shortcomings of some experimental approaches, which involve behavioural tests in artificial conditions. 3. We review our previous study of myrmecophytic acacias, which used in situ experiments to show that volatiles derived from pollen can specifically and transiently deter ants during dehiscence, the effects being stronger in ant-guarded species and more effective on resident ants, both in African and Neotropical species. In these plants, repellence involves at least some volatiles that are known components of ant alarm pheromones, but are not repellent to beneficial bee visitors. 4. We also present new evidence of ant repellence by VOCs in temperate flowers, which is usually pollen-based and active on common European ants. We use these data to indicate that across a wide range of plants there is an apparent trade-off in ant-controlling filter strategies between the use of defensive floral volatiles and the alternatives of decoying EFNs or physical barriers.

Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps

Diversification of insect herbivores is often associated with coevolution between plant toxins and insect countermeasures, resulting in a specificity that restricts host plant shifts. Gall inducers, however, bypass plant toxins and the factors influencing host plant associations in these specialized herbivores remain unclear. We reconstructed the evolution of host plant associations in Western Palaearctic oak gallwasps (Cynipidae: Cynipini), a species-rich lineage of specialist herbivores on oak (Quercus). (1) Bayesian analyses of sequence data for three genes revealed extreme host plant conservatism, with inferred shifts between major oak lineages (sections Cerris and Quercus) closely matching the minimum required to explain observed diversity. It thus appears that the coevolutionary demands of gall induction constrain host plant shifts, both in cases of mutualism (e.g., fig wasps, yucca moths) and parasitism (oak gallwasps). (2) Shifts between oak sections occurred independently in sexual and asexual generations of the gallwasp lifecycle, implying that these can evolve independently. (3) Western Palaearctic gallwasps associated with sections Cerris and Quercus diverged at least 20 million years ago (mya), prior to the arrival of oaks in the Western Palaearctic from Asia 5-7 mya. This implies an Asian origin for Western Palaearctic gallwasps, with independent westwards range expansion by multiple lineages.

A role for parasites in stabilising the fig-pollinator mutualism

Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics, leading to mutualism instability. Monoecious figs (Ficus) are pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their "fruits'' (syconia). Female pollinating wasps oviposit directly into Ficus ovules from inside the receptive syconium. Across Ficus species, there is a widely documented segregation of pollinator galls in inner ovules and seeds in outer ovules. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, and this results in mutualism stability. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. We report that in Ficus rubiginosa, offspring in outer ovules are vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases towards the centre of the syconium, where inner ovules provide enemy-free space for pollinator offspring. We suggest that the resulting gradient in offspring viability is likely to contribute to selection on pollinators to avoid outer ovules, and by forcing wasps to focus on a subset of ovules, reduces their galling rates. This previously unidentified mechanism may therefore contribute to mutualism persistence independent of additional factors that invoke plant defences against pollinator oviposition, or physiological constraints on pollinators that prevent oviposition in all available ovules.

The role of biotic and abiotic factors in evolution of ant dispersal in the milkwort family (Polygalaceae)

A phylogenetic approach was taken to investigate the evolutionary history of seed appendages in the plant family Polygalaceae (Fabales) and determine which factors might be associated with evolution of elaiosomes through comparisons to abiotic (climate) and biotic (ant species number and abundance) timelines. Molecular datasets from three plastid regions representing 160 species were used to reconstruct a phylogenetic tree of the order Fabales, focusing on Polygalaceae. Bayesian dating methods were used to estimate the age of the appearance of ant-dispersed elaiosomes in Polygalaceae, shown by likelihood optimizations to have a single origin in the family. Topology-based tests indicated a diversification rate shift associated with appearance of caruncular elaiosomes. We show that evolution of the caruncular elaiosome type currently associated with ant dispersal occurred 54.0-50.5 million year ago. This is long after an estimated increase in ant lineages in the Late Cretaceous based on molecular studies, but broadly concomitant with increasing global temperatures culminating in the Late Paleocene-Early Eocene thermal maxima. These results suggest that although most major ant clades were present when elaiosomes appeared, the environmental significance of elaiosomes may have been an important factor in success of elaiosome-bearing lineages. Ecological abundance of ants is perhaps more important than lineage numbers in determining significance of ant dispersal. Thus, our observation that elaiosomes predate increased ecological abundance of ants inferred from amber deposits could be indicative of an initial abiotic environmental function.

Ant semiochemicals limit apterous aphid dispersal

Some organisms can manipulate the nervous systems of others or alter their physiology in order to obtain benefit. Ants are known to limit alate aphid dispersal by physically removing wings and also through chemical manipulation of the alate developmental pathway. This results in reduced dispersal and higher local densities of aphids, which benefit ants in terms of increased honeydew and prey availability. Here, we show that the walking movement of mutualistic apterous aphids is also reduced by ant semiochemicals. Aphids walk slower and their dispersal from an unsuitable patch is hampered by ants. If aphid walking dispersal has evolved as a means of natural enemy escape, then ant chemicals may act as a signal indicating protection; hence, reduced dispersal could be adaptive for aphids. If, however, dispersal is primarily a means to reduce competition or to maintain persistent metapopulations, then manipulation by ants could be detrimental. Such manipulation strategies, common in host-parasite and predator-prey interactions, may be more common in mutualism than expected.

An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale co-phylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on average, wasps had sequences from 77% of six genes (5.6kb), figs had sequences from 60% of five genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based co-phylogenetic analyses further support the co-diversification hypothesis. Biogeographic analyses indicate that the presentday distribution of fig and pollinator lineages is consistent with an Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term co-diversification.

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.