Context dependency of rewards and services in an Indian ant-plant interaction: southern sites favour the mutualism between plants and ants

Protection-based ant-plant mutualisms may vary in strength due to differences in ant rewards, abundance of protective ants and herbivory pressure. We investigated geographical and temporal variation in host plant traits and herbivory pressure at five sites spanning the distribution range of the myrmecophyte Humboldtia brunonis (Fabaceae) in the Indian Western Ghats. Southern siteshad, onaverage, 2.4 times greater abundance of domatia-bearing individuals, 1.6 times greater extrafloral nectary numbers per leaf, 1.2 times larger extrafloral nectary sizes, 2.2 times greater extrafloral nectar (EFN) volumes and a two-fold increase in total amino acid and total sugar concentrations in EFN compared with northern sites. Astrong protection-based mutualismwith ants occurred at only one southern site where herbivory was highest, suggesting that investments in attracting ants correlate with anti-herbivore benefits gained from the presence of protective ants. Our results confirm a temporally stable north-south gradient in myrmecophytic traits in this ant-plant as several of these traits were re-sampled after a 5-y interval. However, the chemical composition of EFN varied at both spatial and short-term temporal scales suggesting that only repeated measurements of rewards such as EFN can reveal the real spectrum of trait variation in an ant-plant mutualistic system.

Nutritional benefits from domatia inhabitants in an ant-plant interaction: interlopers do pay the rent

1. How a symbiosis originates and is maintained are important evolutionary questions. Symbioses in myrmecophytes (plants providing nesting for ants) are believed to be maintained by protection and nutrients provided by specialist plant-ants in exchange for nesting spaces (called domatia) and nourishment offered by ant-plants. However, besides the benefits accrued from housing protective ants, the mechanisms contributing to the fitness advantages of bearing domatia have rarely been examined, especially because the domatia trait is usually constitutively expressed, and many myrmecophytes have obligate mutualisms with single ant species resulting in invariant conditions. 2. In the unspecialized ant-plant Humboldtia brunonis (Fabaceae) that offers extrafloral nectar to ants, only some plants produce domatia in the form of hollow internodes. These domatia have a self-opening slit making them more prone to interlopers and are occupied mostly by non-protective ants and other invertebrates, especially arboreal earthworms. The protection mutualism with ants is restricted in geographical extent, occurring only at a few sites in the southernmost part of this plant's range in the Western Ghats of India. 3. We examined nutrient flux from domatia residents to the plant using stable isotopes. We found that between 9% (earthworms) and 17% (protective or non-protective ants) of nitrogen of plant tissues nearest the domatium came from domatia inhabitants. Therefore, interlopers such as earthworms and non-protective ants contributed positively to the nitrogen budget of localized plant modules of this understorey tree. N-15-enriched feeding experiments with protective ants demonstrated that nutrients flowed from domatia inhabitants to nearby plant modules. Fruit set did not differ between paired hand-pollinated inflorescences on domatia and non-domatia bearing branches. This was possibly due to the nutrient flux from domatia to adjacent branches without domatia within localized modules. 4. This study has demonstrated the nutritive role of non-protective ants and non-ant invertebrates, hitherto referred to as interlopers, in an unspecialized myrmecophyte. Our study suggests that even before the establishment of a specialized ant-plant protection mutualism, nutritional benefits conferred by domatia inhabitants can explain the fitness benefits of bearing domatia, and thus the maintenance of a trait that facilitates the establishment of a specialized ant-plant symbiosis.

Foliar Extrafloral Nectar of Humboldtia brunonis (Fabaceae), a Paleotropic Ant-plant, is Richer than Phloem Sap and More Attractive than Honeydew

The ant-plant Humboldtia brunonis secretes extrafloral nectar (EFN) despite the lack of antiherbivore protection from most ants. EFN was richer in composition than phloem sap and honeydew from untended Hemiptera on the plant, suggesting that EFN could potentially distract ants from honeydew, since ants rarely tended Hemiptera on this plant.

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.

Abiotic factors shape temporal variation in the structure of an ant-plant network

Despite recognition of key biotic processes in shaping the structure of biological communities, few empirical studies have explored the influences of abiotic factors on the structural properties of mutualistic networks. We tested whether temperature and precipitation contribute to temporal variation in the nestedness of mutualistic ant-plant networks. While maintaining their nested structure, nestedness increased with mean monthly precipitation and, particularly, with monthly temperature. Moreover, some species changed their role in network structure, shifting from peripheral to core species within the nested network. We could summarize that abiotic factors affect plant species in the vegetation (e.g., phenology), meaning presence/absence of food sources, consequently an increase/decrease of associations with ants, and finally, these variations to fluctuations in nestedness. While biotic factors are certainly important, greater attention needs to be given to abiotic factors as underlying determinants of the structures of ecological networks.

Natural history of an ant-plant-butterfly interaction in a Neotropical savanna

Non-myrmecophilous lepidopteran larvae using plants bearing ant attractants such as extrafloral nectaries are good models for studying morphological and behavioural mechanisms against ant predation. Udranomia spitzi (Hesperiidae) is a butterfly whose larvae feed on leaves of Ouratea spectabilis (Ochnaceae), a plant with extrafloral nectaries. We described the early stages of U. spitzi, and used field observations and experiments to investigate the defensive strategies of caterpillars against predatory ants. Larvae pass through five instars and pupation occurs inside larval leaf shelters. Ant-exclusion experiments revealed that the presence of ants did not affect significantly caterpillar survival. Predation experiments showed that vulnerability to ant predation decreased with increase in larval size. The present study showed that predatory ants are not as relevant as demonstrated for other systems, and also illustrates how observational data and field experiments can contribute to a better understanding of the biology and ecology of a species of interest.

Composition of Extrafloral Nectar Influences Interactions between the Myrmecophyte Humboldtia brunonis and its Ant Associates

Ant-plant interactions often are mediated by extrafloral nectar (EFN) composition that may influence plant visitation by ants. Over a 300 km range in the Indian Western Ghats, we investigated the correlation between the EFN composition of the myrmecophytic ant-plant Humboldtia brunonis (Fabaceae) and the number and species of ants visiting EFN. EFN composition varied among H. brunonis populations and between plant organs (floral bud vs. young leaf EFN). In general, EFN was rich in sugars with small quantities of amino acids, especially essential amino acids, and had moderate invertase activity. In experiments at the study sites with sugar and amino acid solutions and with leaf or floral bud EFN mimics, dominant EFN-feeding ants differentiated between solutions as well as between mimics. The castration parasite Crematogaster dohrni (northern study site) was the least selective and did not exhibit any clear feeding preferences, while the largely trophobiont-tending non-protective Myrmicaria brunnea (middle study site) preferred higher sucrose concentrations and certain essential/non-essential amino acid mixtures. The mutualistic Technomyrmex albipes (southern study site) preferred sucrose over glucose or fructose solutions and consumed the leaf EFN mimic to a greater extent than the floral bud EFN mimic. This young leaf EFN mimic had low sugar concentrations, the lowest viscosity and sugar: amino acid ratio, was rich in essential amino acids, and appeared ideally suited to the digestive physiology of T. albipes. This preference for young leaf EFN may explain the greater protection afforded to young leaves than to floral buds by T. albipes, and may also help to resolve ant-pollinator conflicts. The differential response of dominant ants to sugar, amino acids, or solution viscosity suggests that plants can fine-tune their interactions with local ants via EFN composition. Thus, EFN can mediate local partner-choice mechanisms in ant-plant interactions.

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. Alth

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.

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.

Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado

Extrafloral nectaries are nectar-secreting structures that are especially common among the woody flora of the Brazilian cerrado, a savanna-like vegetation. In this study, we provide morphological and anatomical descriptions of extrafloral nectaries (EFNs) occurring on vegetative and reproductive organs of several plant species from the cerrado, and discuss their function and ecological relevance. We describe the morphology and anatomy of EFNs of 40 species belonging to 15 woody families using scanning electron microscopy and light microscopy. We categorise EFNs following a structural-topographical classification, and characterise the vascularised and complex nectaries, amorphous nectaries and secretory trichomes. Fabaceae, Bignoniaceae, Malpighiaceae and Vochysiaceae were the plant families with the majority of species having EFNs. Ten species possess more than one morphotype of gland structure. Observations and experimental field studies in the cerrado support the anti-herbivore role of EFN-gathering ants in this habitat. Additional morphological studies of EFNs-bearing plants, including other growth forms (e.g. herbs and lianas), are being undertaken and will hopefully cast further light on the ecological relevance of these glands in the cerrado, especially with respect to their attractiveness to multiple visitors.

Colonization pattern of Cecropia by Azteca ants: Influence of plant ontogeny, environment and host plant choice by queens

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Ant exclusion and reproduction of Croton sarcopetalus (Euphorbiaceae)

A total of 20 insect species were observed on the extrafloral nectaries (EFNs) of Croton sarcopetalus. The most frequent ant species were Zacryptocerus sp., Crematogaster brevispinosa, C. scelerata, and Linepithema humile. Ants continuously patrolled the plants taking extrafloral nectar. Experimental data showed that there were no significant differences in either the degree of herbivory or in the reproductive output between control stems (with ants) and treated ones (without ants). We found no significant evidence of protection by ants mediated by EFNs in C. sarcopetalus. It is possible that the plant has other mechanisms than ant protection to prevent herbivore damage (e.g., hairs, latex, chemical defense). As this species occupies the southernmost distribution for the genus, the presence of EFNs in this species may be the remnant of a mutualistic interaction with the ants in tropical regions, where the abundance and diversity of ants and herbivores are comparatively higher. To draw accurate patterns in the genus Croton, further investigations in other species from tropical regions of South America are needed.

The effect of plant diversity on fungus garden development and foraging behavior of leaf-cutting ants (Hymenoptera: Formicidae)

The leaf-cutting ants forage a wide variety of plant species, used for symbiotic fungus cultivation. To better understand this tripartite complex interaction, 24 colonies of Acromyrmex subterraneus brunneus were conditioned for 4 months to 6 different plants (Citrus spp., Ligustrum spp., Acalypha spp., Eucalyptus spp., Alchornea triplinervia, Melia spp.), to verify the influence of conditioning on foraging behavior of workers. The effect of plants on symbiotic fungus development was studied separately, through macerated plants in Agar and culture medium A as the control. During foraging, workers presented polyphagic foraging behavior, refusing the plants to which they were conditioned. The selection of plants is not correlated with the plant substrate that promotes good development of symbiotic fungus. Such results demonstrate the importance of plant diversity for fungus garden maintenance.

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.