Ant-plant Protection Mutualism Research Articles

Plant species specificity of ant–plant mutualistic interactions: Differential predation of termites by Camponotus crassus on five species of extrafloral nectaries plants

AbstractThere is increasing evidence that the outcomes of mutualistic interactions between ants and plants bearing extrafloral nectaries (EFNs) are context‐dependent. In particular, the total number, density, and size of EFNs, as well as the abundance and identity of ants attending host plants, are considered as key factors determining the nature and strength of ant–EFN‐bearing plant interaction. Although many previous studies have investigated context‐dependency in ant–plant protection mutualisms mediated by EFNs, few have tested whether the protective behavior of ants varies among sympatric plant species. In this study, we performed a field experiment to investigate the predatory behavior of a dominant ant species (Camponotus crassus, Formicinae) among five EFN‐bearing plant species growing in the Brazilian savanna. In particular, we studied the variation in the ant abundance, termite predation, and time spent to find termites of C. crassus among the plant species, and further analyzed whether this variation could be related to the extrafloral nectar volume and sugar concentration of each plant species. We found that abundance and termite predation of C. crassus markedly varied among plant species. Specifically, C. crassus ants were significantly more abundant, active, and protective in Qualea multiflora, the plant species that produced significantly higher volumes and sugar concentrations of nectar. Overall, our results suggest that variation in extrafloral nectar volume and sugar concentration can result in plant species specificity of defensive behavior of a dominant foliage‐dwelling ant in the Brazilian savanna.Abstract in Portuguese is available with online material.

Extrafloral nectaries in Leguminosae: phylogenetic distribution, morphological diversity and evolution

Extrafloral nectaries (EFNs) mediating ecologically important ant–plant protection mutualisms are especially common and unusually diverse in the Leguminosae. We present the first comprehensively curated list of legume genera with EFNs, detailing and illustrating their systematic and phylogenetic distributions, locations on the plant, morphology and anatomy, on the basis of a unified classification of EFN categories and a time-calibrated phylogeny, incorporating 710 of the 768 genera. This new synthesis, the first since Mckey (1989)’s seminal paper, increases the number of genera with EFNs to 153 (20% of legumes), distributed across subfamilies Cercidoideae (1), Detarioideae (19), Caesalpinioideae (87) and Papilionoideae (46). EFNs occur at nine locations, and are most prevalent on vegetative plant parts, especially leaves (74%) and inflorescence axes (26%). Four main categories (with eight subcategories) are recognised and include the following: formless, trichomatic (exposed, hollow), parenchymatic (embedded, pit, flat, elevated) and abscission zone EFNs (non-differentiated, swollen scars). Phylogenetic reconstruction of EFNs suggests independent evolutionary trajectories of different EFN types, with elevated EFNs restricted almost exclusively to Caesalpinioideae (where they underwent spectacular morphological disparification), flat EFNs in Detarioideae, swollen scar EFNs in Papilionoideae, and Cercidoideae is the only subfamily bearing intrastipular EFNs. We discuss the complex evolutionary history of EFNs and highlight future research directions.

PROTECTION MUTUALISM: AN OVERVIEW OF ANT-PLANT INTERACTIONS MEDIATED BY EXTRAFLORAL NECTARIES

Ants and plants bearing extrafloral nectaries (EFNs) are among the most abundant interacting organisms in the Neotropics, being considered excellent models for studies of ecological interactions. These mutualisms have been studied for more than 150 years. The first studies on this subject addressed the indirect benefit of the presence of ants on plants, reducing the foliar herbivory in most cases. Recently, the direct and indirect benefits of these interactions for ants and for EFNs-bearing plants survivorship, growth and reproduction, have shown conditionality to spatial and temporal variations. Here, we reviewed how the topic “protection mutualism in ant-plant interactions mediated by EFNs” has been approached more recently. A great number of papers dealing with this theme have been published in the last 30 years and new perspectives have emerged in the last decade. We showed how scientific and academic areas are working to improve the knowledge on protection mutualisms considering ant-plant ecological networks and how they can shape communities. Furthermore, we discuss some aspects related with the EFNs evolutionary hypotheses, the existence of conditionalities in ant-plant protection mutualism mediated by EFNs, and we provide some perspectives to inspire new studies that will help in the understanding of these fascinating ecological interactions.

Network reorganization and breakdown of an ant-plant protection mutualism with elevation.

Both the abiotic environment and the composition of animal and plant communities change with elevation. For mutualistic species, these changes are expected to result in altered partner availability, and shifts in context-dependent benefits for partners. To test these predictions, we assessed the network structure of terrestrial ant-plant mutualists and how the benefits to plants of ant inhabitation changed with elevation in tropical forest in Papua New Guinea. At higher elevations, ant-plants were rarer, species richness of both ants and plants decreased, and the average ant or plant species interacted with fewer partners. However, networks became increasingly connected and less specialized, more than could be accounted for by reductions in ant-plant abundance. On the most common ant-plant, ants recruited less and spent less time attacking a surrogate herbivore at higher elevations, and herbivory damage increased. These changes were driven by turnover of ant species rather than by within-species shifts in protective behaviour. We speculate that reduced partner availability at higher elevations results in less specialized networks, while lower temperatures mean that even for ant-inhabited plants, benefits are reduced. Under increased abiotic stress, mutualistic networks can break down, owing to a combination of lower population sizes, and a reduction in context-dependent mutualistic benefits.

Thermal tolerance affects mutualist attendance in an ant-plant protection mutualism.

Mutualism is an often complex interaction among multiple species, each of which may respond differently to abiotic conditions. The effects of temperature on the formation, dissolution, and success of these and other species interactions remain poorly understood. We studied the thermal ecology of the mutualism between the cactus Ferocactus wislizeni and its ant defenders (Forelius pruinosus, Crematogaster opuntiae, Solenopsis aurea, and Solenopsis xyloni) in the Sonoran Desert, USA. The ants are attracted to extrafloral nectar produced by the plants and, in exchange, protect the plants from herbivores; there is a hierarchy of mutualist effectiveness based on aggression toward herbivores. We determined the relationship between temperature and ant activity on plants, the thermal tolerance of each ant species, and ant activity in relation to the thermal environment of plants. Temperature played a role in determining which species interact as mutualists. Three of the four ant species abandoned the plants during the hottest part of the day (up to 40 °C), returning when surface temperature began to decrease in the afternoon. The least effective ant mutualist, F. pruinosus, had a significantly higher critical thermal maximum than the other three species, was active across the entire range of plant surface temperatures observed (13.8-57.0 °C), and visited plants that reached the highest temperatures. F. pruinosus occupied some plants full-time and invaded plants occupied by more dominant species when those species were thermally excluded. Combining data on thermal tolerance and mutualist effectiveness provides a potentially powerful tool for predicting the effects of temperature on mutualisms and mutualistic species.

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

Summary 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. 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. 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. 15N‐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. 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.

Protection Mutualisms and the Community: Geographic Variation in an Ant-Plant Symbiosis and the Consequences for Herbivores

Protection mutualisms mediate trophic interactions in many systems, but their effects on the surrounding community are rarely studied. Ant-plant symbioses are classic examples of protection mutualisms: myrmecophytic plants provide nesting space and food for symbiotic ants in exchange for ant defense. Ant defense should thus reduce the abundance of herbivores, but studies of ant-plant symbioses usually measure damage to the plant without quantifying the herbivores themselves. In this study, we investigated whether geographic variation in the quality of ant defense in a symbiotic mutualism between Cordia alliodora trees and Azteca ants was associated with the abundance and species richness of plant herbivore communities. In three tropical-dry-forest sites in Middle America, we found that the density of Azteca ants within trees was negatively associated with the levels of leaf herbivory. At sites where ants were effective tree defenders, tree herbivores were less abundant and herbivore assemblages on trees exhibited lower species richness than at a site where ants were poor defenders. In addition, in a site where ants reduced herbivory, herbivore communities were less abundant and diverse in the presence of ants than in their absence, where as in a site where ants did not reduce herbivory, there were no differences in herbivore abundance or richness between trees with or without ants. We conclude that geographic variation in the quality of ant defense drives variation in myrmecophytic-plant herbivore communities. Moreover, ant-plant protection mutualisms should have important but rarely considered effects on herbivore population dynamics and food-plant specialization.

An ant’s-eye view of an ant-plant protection mutualism

Ant protection of extrafloral nectar (EFN)-secreting plants is a common form of mutualism found in most habitats around the world. However, very few studies have considered these mutualisms from the ant, rather than the plant, perspective. In particular, a whole-colony perspective that takes into account the spatial structure and nest arrangement of the ant colonies that visit these plants has been lacking, obscuring when and how colony-level foraging decisions might affect tending rates on individual plants. Here, we experimentally demonstrate that recruitment of Crematogaster opuntiae (Buren) ant workers to the EFN-secreting cactus Ferocactus wislizeni (Englem) is not independent between plants up to 5 m apart. Colony territories of C. opuntiae are large, covering areas of up to 5,000 m(2), and workers visit between five and 34 EFN-secreting barrel cacti within the territories. These ants are highly polydomous, with up to 20 nest entrances dispersed throughout the territory and interconnected by trail networks. Our study demonstrates that worker recruitment is not independent within large polydomous ant colonies, highlighting the importance of considering colonies rather than individual workers as the relevant study unit within ant/plant protection mutualisms.

Benefits for Plants in Ant-Plant Protective Mutualisms: A Meta-Analysis

Costs and benefits for partners in mutualistic interactions can vary greatly, but surprisingly little is known about the factors that drive this variation across systems. We conducted a meta-analysis of ant-plant protective mutualisms to quantify the effects of ant defenders on plant reproductive output, to evaluate if reproductive effects were predicted from reductions in herbivory and to identify characteristics of the plants, ants and environment that explained variation in ant protection. We also compared our approach with two other recent meta-analyses on ant-plant mutualisms, emphasizing differences in our methodology (using a weighted linear mixed effects model) and our focus on plant reproduction rather than herbivore damage. Based on 59 ant and plant species pairs, ant presence increased plant reproductive output by 49% and reduced herbivory by 62%. The effects on herbivory and reproduction within systems were positively correlated, but the slope of this relationship (0.75) indicated that tolerance to foliar herbivory may be a common plant response to absence of ant guards. Furthermore, the relationship between foliar damage and reproduction varied substantially among systems, suggesting that herbivore damage is not a reliable surrogate for fitness consequences of ant protection. Studies that experimentally excluded ants reported a smaller effect of ant protection on plant reproduction than studies that relied upon natural variation in ant presence, suggesting that study methods can affect results in these systems. Of the ecological variables included in our analysis, only plant life history (i.e., annual or perennial) explained variation in the protective benefit of mutualistic ants: presence of ants benefitted reproduction of perennials significantly more than that of annuals. These results contrast with other quantitative reviews of these relationships that did not include plant life history as an explanatory factor and raise several questions to guide future research on ant-plant protection mutualisms.

Polygynous supercolonies of the acacia‐antPseudomyrmex peperi, an inferior colony founder

In ant-plant protection mutualisms, plants provide nesting space and nutrition to defending ants. Several plant-ants are polygynous. Possessing more than one queen per colony can reduce nestmate relatedness and consequently the inclusive fitness of workers. Here, we investigated the colony structure of the obligate acacia-ant Pseudomyrmex peperi, which competes for nesting space with several congeneric and sympatric species. Pseudomyrmex peperi had a lower colony founding success than its congeners and thus, appears to be competitively inferior during the early stages of colony development. Aggression assays showed that P. peperi establishes distinct, but highly polygynous supercolonies, which can inhabit large clusters of host trees. Analysing queens, workers, males and virgin queens from two supercolonies with eight polymorphic microsatellite markers revealed a maximum of three alleles per locus within a colony and, thus, high relatedness among nestmates. Colonies had probably been founded by one singly mated queen and supercolonies resulted from intranidal mating among colony-derived males and daughter queens. This strategy allows colonies to grow by budding and to occupy individual plant clusters for time spans that are longer than an individual queen's life. Ancestral states reconstruction indicated that polygyny represents the derived state within obligate acacia-ants. We suggest that the extreme polygyny of Pseudomyrmex peperi, which is achieved by intranidal mating and thereby maintains high nestmate relatedness, might play an important role for species coexistence in a dynamic and competitive habitat.

Quantitative synthesis of context dependency in ant–plant protection mutualisms

Context dependency, variation in the outcome of species interactions with biotic and abiotic conditions, is increasingly considered ubiquitous among mutualisms. Despite several qualitative reviews of many individual empirical studies, there has been little quantitative synthesis examining the generality of context dependency, or conditions that may promote it. We conducted a meta-analysis of ant-plant protection mutualisms to examine the generality of context-dependent effects of ants on herbivory and plant performance (growth, reproduction). Our results show that ant effects on plants are not generally context dependent, but instead are routinely positive and rarely neutral, as overall effect sizes of ants in reducing herbivory and increasing plant performance were positive and significantly greater than 0. The magnitude of these positive effects did vary, however. Variation in plant performance was not explained by the type of biotic or abiotic factor examined, including plant rewards (extrafloral nectar, food bodies, domatia), ant species richness, plant growth form, or latitude. With the exception of plant growth form, these factors did contribute to the effects of ants in reducing herbivory. Reductions in herbivory were greater for plants with than without domatia, and greatest for plants with both domatia and food bodies. Effect sizes of ants in reducing herbivory decreased, but remained positive, with latitude and ant species richness. Effect sizes in reducing herbivory were greater in tropical vs. temperate systems. Although ant-plant interactions have been pivotal in the study of context dependency of mutualisms, our results, along with other recent meta-analyses, indicate that context dependency may not be a general feature of mutualistic interactions. Rather, ant-plant protection mutualisms appear to be routinely positive for plants, and only occasionally neutral.

Simulated herbivory induces extrafloral nectary production in Prunus avium

1. Induced chemical responses to herbivory have been widely documented, however less attention has been given to the induced morphological defences, particularly those that mediate protection mutualisms. One of the most widely studied mutualisms is the ant-plant protection mutualism, in which ants and other predatory arthropods defend plants against herbivores in exchange for food or housing. 2. Chemical and morphological traits that mediate this protection mutualism attract beneficial partners to plants. Thus induction of traits can lead to greater protection by mutualists when herbivores are present. In this study we examined whether extrafloral nectaries (EFNs) are induced in response to simulated herbivory in Prunus avium. 3. In a greenhouse experiment, continuous damage to seedlings was simulated in two treatments intended to mimic different types of herbivores: (i) 50% of the area of each leaf was removed using a paper hole punch (e.g. insect herbivore simulation), and (ii) 50% of the area of each leaf was removed using scissors (e.g. browsing mammal simulation). Seedlings in the control group were not damaged. 4. Post-treatment, damaged plants produced significantly more EFNs per leaf on pre-existing leaves, as well as those that emerged following the onset of damage, than plants in the control group. Regardless of treatment, leaves emerging earlier supported fewer EFNs than leaves emerging later in the experiment. 5. Allocation to defence by seedlings, which have limited resources available, suggests the protection mutualism could be important to plant fitness in the field. Further study of patterns of EFN induction in P. avium seedlings is needed to better understand the significance of this induced response.

Integrating phenological, chemical and biotic defences in ant-plant protection mutualisms: a case study of two myrmecophyte lineages

We examined the role of plant phenology in the evolution of anti-herbivore defence in symbiotic ant-plant protection mutualisms. Phenology of the host-plant affects traits of its herbivores, including size, growth rate, development time, and gregariousness. Traits of herbivores in turn determine what traits ants must have to protect their host. Diversity in plant phenological traits could thus help explain the great ecological diversity of coevolved ant-plant mutualisms. We explored the postulated causal chain linking phenology of the plant, herbivore adaptations to phenology, and ant adaptations for protection, by comparing two myrmecophytes presenting strong contrasts in phenology. In Leonardoxa africana, a slow-growing understory tree, growth at each twig terminal is intermittent, the rapid flushing of a single leaf-bearing internode being followed by a pause of several months. In contrast, axes of Barteria nigritana, a tree of open areas, grow continuously. Analysis of the phenology (kinetics of expansion) and chemistry of leaf development (contents of chlorophylls, lignin, and nitrogen during leaf growth) showed that these two species exhibit strongly contrasting strategies. Leonardoxa exhibited a delayed greening strategy, with rapid expansion of leaves during a short period, followed by synthesis of chlorophylls and lignins only after final leaf size has been reached. In contrast, leaves of Barteria expanded more slowly, with chlorophylls and lignin gradually synthesised throughout development. Differences in the phenology of leaf development are reflected in differences in the duration of larval development, and thereby in size, of the principal lepidopteran herbivores observed on these two plants. This difference may in turn have led to different requirements for effective defence by ants. The strategy of phenological defence may thus affect the evolution of biotic defence.

Variation in the effectiveness of biotic defence: the case of an opportunistic ant-plant protection mutualism.

Benefits to plants in facultative ant protection mutualisms are highly variable. This allows examination of the sources of this variation and the mechanisms by which ants protect plants. We studied opportunistic interactions between ants and an extrafloral nectary-bearing vine, Dioscorea praehensilis, during 3 different years. Variation in plant protection among years was striking. Several factors affected the effectiveness of the biotic defence. Stems recently emerged from the underground tuber were self-supporting, contacting no other plants and encountering few foraging ants. Stems then became lianescent, and contact with supporting plants greatly increased ant recruitment. Both species and number of ant workers influenced the effect of ants on the major herbivore, the chrysomelid beetle Lilioceris latipennis. Protective actions included limitation of oviposition (reduction in the number of eggs laid on the plant) and predation, leading to increased larval mortality. The probability of successful predation was strongly dependent on larval size. If temporarily low ant-patrolling activity allows larvae to grow beyond a critical size, their mechanical (thick integument) or chemical (plant-derived compounds in a fecal shield) defences become more effective against ants. Secondary metabolites derived from the host plant thus appear to be important for the anti-predator mechanisms of this beetle, being necessary for its survival and reproduction on a host plant that actively recruits ants as a biotic defence against herbivores.