A castration parasite of an ant-plant mutualism

Exploring the factors governing the maintenance and breakdown of cooperation between mutualists is an intriguing and enduring problem for evolutionary ecology, and symbioses between ants and plants can provide useful experimental models for such studies. Hundreds of tropical plant species have evolved structures to house and feed ants, and these ant–plant symbioses have long been considered classic examples of mutualism. Here, we report that the primary ant symbiont, Allomerus cf. demerarae, of the most abundant ant-plant found in south-east Peru, Cordia nodosa Lam., castrates its host plant. Allomerus workers protect new leaves and their associated domatia from herbivory, but destroy flowers, reducing fruit production to zero in most host plants. Castrated plants occupied by Allomerus provide more domatia for their associated ants than plants occupied by three species of Azteca ants that do not castrate their hosts. Allomerus colonies in larger plants have higher fecundity. As a consequence, Allomerus appears to benefit from its castration behaviour, to the detriment of C. nodosa. The C. nodosa–ant system exhibits none of the retaliatory or filtering mechanisms shown to stabilize cheating in other cooperative systems, and appears to persist because some of the plants, albeit a small minority, are inhabited by the three species of truly mutualistic Azteca ants.     

Caterpillars and fungal pathogens: two co-occurring parasites of an ant-plant mutualism

In mutualisms, each interacting species obtains resources from its partner that it would obtain less efficiently if alone, and so derives a net fitness benefit. In exchange for shelter (domatia) and food, mutualistic plant-ants protect their host myrmecophytes from herbivores, encroaching vines and fungal pathogens. Although selective filters enable myrmecophytes to host those ant species most favorable to their fitness, some insects can by-pass these filters, exploiting the rewards supplied whilst providing nothing in return. This is the case in French Guiana for Cecropia obtusa (Cecropiaceae) as Pseudocabima guianalis caterpillars (Lepidoptera, Pyralidae) can colonize saplings before the installation of their mutualistic Azteca ants. The caterpillars shelter in the domatia and feed on food bodies (FBs) whose production increases as a result. They delay colonization by ants by weaving a silk shield above the youngest trichilium, where the FBs are produced, blocking access to them. This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants. However, once incipient ant colonies are able to develop, they prevent further colonization by the caterpillars. Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants. Therefore, the Cecropia treelets can be parasitized by two often overlooked species: the caterpillars that shelter in the domatia and feed on FBs, delaying colonization by mutualistic ants, and the fungal pathogen that develops on old trichilia. The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.     

Carbon and nitrogen isotopes trace nutrient exchange in an ant-plant mutualism

By combining and reanalysing data from two independent field experiments we explore whether food limitation at the brood stage affects habitat selection in nesting mallards (Anas platyrhynchos). In an introduction experiment we found that, independent of treatment, some study lakes remained empty of wild mallard pairs (”empty lakes”), whereas on other lakes introduced birds attracted wild mallards (”attractive lakes”). In the other experiment we used mallard ducklings to address brood-stage food limitation by studying mass change of ducklings. We found that ducklings foraging on lakes that did not attract wild mallard pairs in the introduction experiment gained much less mass than those foraging on attractive lakes. In most cases ducklings even lost mass in the empty-lake foraging trials, providing strong evidence for food limitation. Therefore, lakes that remained empty of wild mallard pairs in the introduction experiment proved to be inferior brood habitats, particularly in terms of food. Our results give insight into the mechanisms underlying the general habitat selection hypotheses, specifically the ideal preemptive and conspecific attraction rules. The results further support our earlier conclusion that mallards do not use the ideal preemptive rule when selecting nesting lakes. However, conspecific attraction may not be generally applicable either, because, independent of the presence of introduced conspecifics, wild mallards somehow anticipated the low quality of the empty lakes as brood-rearing habitats and made their habitat-selection decision accordingly. Received: 22 March 1999 / Accepted: 7 October 1999     

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.     

Selection for protection in an ant-plant mutualism: host sanctions, host modularity, and the principal-agent game

Retaliation against cheaters can prevent the breakdown of cooperation. Here we ask whether the ant-plant Cordia nodosa is able to apply retaliatory sanctions against its ant symbiont Allomerus octoarticulatus, which patrols new shoots to prevent herbivory. We test the hypothesis that the modular design of C. nodosa physiologically ties the growth of housing (stem swellings known as domatia) to the successful development of the attached leaves. We experimentally simulated herbivory by cutting leaves from patrolled shoots and found that the domatia on such 'cheated' shoots suffered higher mortality and lower growth than did controls, evidence for a host sanction. On the other hand, patrolling is costly to the ant, and experiment shows that non-patrollers run a low risk of being sanctioned because most leaves (and the attached domatia) escape heavy herbivory even when patrollers are absent. This suggests that cheaters might enjoy a higher fitness than do mutualists, despite sanctions, but we find that patrolling provides a net fecundity benefit when the colony and plant exceed a minimum size, which requires sustained ant investment in patrolling. These results map directly onto the principal-agent (P-A) game from economics, which we suggest can be used as a framework for studying stability in mutualisms, where high sampling costs and cheating do not allow market effects to select for mutual benefits.     

Distinguishing coevolution from covicariance in an obligate pollination mutualism: asynchronous divergence in Joshua tree and its pollinators

Obligate pollination mutualisms--in which both plants and their pollinators are reliant upon one another for reproduction--represent some of the most remarkable coevolutionary interactions in the natural world. The intimacy and specificity of these interactions have led to the prediction that the plants and their pollinators may be prone to cospeciation driven by coevolution. Several studies have identified patterns of phylogenetic congruence that are consistent with this prediction, but it is difficult to determine the evolutionary process that underlies these patterns. Phylogenetic congruence might also be produced by extrinsic factors, such as a shared biogeographic history. We examine the biogeographic history of a putative case of codivergence in the obligate pollination mutualism between Joshua trees (Yucca brevifolia) and two sister species of pollinating yucca moths (Tegeticula spp.) We employ molecular phylogenetic methods and coalescent-based approaches, in combination with relaxed-clock estimates of absolute rates of molecular evolution, to analyze multi-locus sequence data from more than 30 populations of Y. brevifolia and its pollinators. The results indicate that the moth species diverged significantly (p < 0.01) more recently than their corresponding host populations, suggesting that the apparent codivergence is not an artifact of a shared biogeographic history.     

The geographical mosaic of coevolution in a plant-pollinator mutualism.

Although coevolution is widely accepted as a concept, its importance as a driving factor in biological diversification is still being debated. Because coevolution operates mainly at the population level, reciprocal coadaptations should result in trait covariation among populations of strongly interacting species. A long-tongued fly (Prosoeca ganglbaueri) and its primary floral food plant (Zaluzianskya microsiphon) were studied across both of their geographical ranges. The dimensions of the fly's proboscis and the flower's corolla tube length varied significantly among sites and were strongly correlated with each other. In addition, the match between tube length of flowers and tongue length of flies was found to affect plant fitness. The relationship between flower tube length and fly proboscis length remained significant in models that included various alternative environmental (altitude, longitude, latitude) and allometric (fly body size, flower diameter) predictor variables. We conclude that coevolution is a compelling explanation for the geographical covariation in flower depth and fly proboscis length.     

Food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions in an arid environment

In this study, we conducted a series of experiments in a population of Vachellia constricta (Fabaceae) in the arid Tehuacan-Cuicatláan valley, Mexico, in order to evaluate if the food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions. Using an experiment with artificial nectaries, we observed that ants foraging on food sources with higher concentration of sugar are quicker in finding and attacking potential herbivorous insects. More specifically, we found that the same ant species may increase their defence effectiveness according to the quality of food available. These findings indicate that ant effectiveness in plant protection is context-dependent and may vary according to specific individual characteristics of plants. In addition, we showed that competitively superior ant species tend to dominate plants in periods with high nectar activity, emphasizing the role of the dominance hierarchy structuring ant-plant interactions. However, when high sugar food sources were experimentally available ad libitum, the nocturnal and competitively superior ant species, Camponotus atriceps, did not dominate the artificial nectaries during the day possibly due to limitation of its thermal tolerance. Therefore, temporal niche partitioning may be allowing the coexistence of two dominant ant species (Camponotus rubritorax during the day and C. atriceps at night) on V. constricta. Our findings indicate that the quality of the food source, and temporal shifts in ant dominance are key factors which structure the biotic plant defences in an arid environment.     

Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus

Abstract.— The interaction between Ficus (Moraceae) and their pollinating wasps (Chalcidoidea: Agaonidae; more than 700 species-specific couples) is one of the most specialized mutualisms found in nature. Both partners of this interaction show extensive variation in their respective biology. Here we investigate Ficus life-history trait evolution and fig/fig wasp coadaptation in the context of a well-resolved molecular phylogeny. Mapping out variations in Ficus life-history traits on an independently derived phylogeny constructed from ribosomal DNA sequences (external and internal transcribed spacer) reveals several parallel transitions in Ficus growth habit and breeding system. Convergent trait evolution might explain the discrepancies between morphological analyses and our molecular reconstruction of the genus. Morphological characters probably correlate with growth habit and breeding system and could therefore be subject to convergent evolution. Furthermore, we reconstruct the evolution of Ficus inflorescence characters that are considered adaptations to the pollinators. Our phylogeny reveals convergences in ostiole shape, stigma morphology, and stamen:ovule ratio. Statistical tests taking into account the phylogenetic relationship of the species show that transitions in ostiole shape are correlated with variation in wasp pollinator head shape, and evolutionary changes in stigma morphology and stamen:ovule ratio correlate with changes in the pollination behavior of the associated wasp. These correlations provide evidence for reciprocal adaptations of morphological characters between these mutualistic partners that have interacted over a long evolutionary time. In light of previous ecological studies on mutualism, we discuss the adaptive significance of these correlations and what they can tell us about the coevolutionary process occurring between figs and their pollinators.     

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores. 2. We conducted field and greenhouse experiments in which we manipulated the presence and absence of cotton aphids (Aphis gossypii) on cotton plants to test the hypothesis that a mutualism between cotton aphids and an invasive ant, the red imported fire ant (Solenopsis invicta), benefits cotton plants by increasing fire ant suppression of caterpillars. We also manipulated caterpillar abundance to test whether the benefit of the mutualism varied with caterpillar density. 3. We found that more fire ants foraged on plants with cotton aphids than on plants without cotton aphids, which resulted in a significant reduction in caterpillar survival and caterpillar herbivory of leaves, flower buds, and bolls on plants with aphids. Consequently, cotton aphids indirectly increased cotton reproduction: plants with cotton aphids produced 16% more bolls, 25% more seeds, and 10% greater seedcotton mass than plants without aphids. The indirect benefit of cotton aphids, however, varied with caterpillar density: the number of bolls per plant at harvest was 32% greater on plants with aphids than on plants without aphids at high caterpillar density, versus just 3% greater at low caterpillar density. 4. Our results highlight the potential benefit to plants that host ant–hemipteran mutualisms and provide the first experimental evidence that the consequences to plants of an ant–aphid mutualism vary at different densities of non‐aphid herbivores.     

Origin of caulinary ant domatia and timing of their onset in plant ontogeny: evolution of a key trait in horizontally transmitted ant-plant symbioses

Many ant plants possess caulinary domatia, hollow and usually swollen stems. What are the evolutionary origins of this key trait of ant‐plant symbioses? In a single lineage, myrmecophytes often differ in the timing of the first appearance of domatia. What processes have led to diversification in the timing of expression of domatia in ontogeny? We suggest that an approach based on the analysis of leaf‐ stem size correlations, that appear general in trees, can supply answers to both these questions. Traits associated with increased primary diameter of twigs may have facilitated the evolution of domatia. Among lineages, differences in stem diameter may help to explain why domatia appeared in some, and not in others. Within species, because twig primary diameter increases over plant ontogeny, initially ants may have colonized only plants at later stages of development, whose twigs had reached a minimum size. We thus postulate that expression of domatia later in development is the primitive condition in lineages with domatia, and that increasing specialization of ants and plants enhanced both the probability of establishment and ant protection, favouring precocity of onset of domatia and other myrmccophytic characters. In the language of heterochrony, these characters are affected by prc‐displacement.     

Plant coevolution: evidences and new challenges

Abstract

Coevolution has been defined as the reciprocal genetic change in interacting species owing to natural selection imposed by each on the other. The process of coevolution between plants and the surrounding biota – including viruses, fungi, bacteria, nematodes, insects, and mammals – is considered by many biologists to have generated much of the earth's biological diversity. While much of the discussion on plant coevolution focuses on single plant–enemy interactions, a wide array of other micro and macro coevolutive processes co-occur in the same individual plant, posing the question whether we should talk about plant coevolutions. In this review article, I begin by briefly discussing the framework of coevolution theory and explore the complexities of studying coevolution in natural conditions. Then I analyze the difference between plants, microbes and animal coevolution, by exploring the above- and below-ground behaviors.     

Codiversification in an ant-plant mutualism: stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae)

We investigate the evolution of host association in a cryptic complex of mutualistic Crematogaster (Decacrema) ants that inhabits and defends Macaranga trees in Southeast Asia. Previous phylogenetic studies based on limited samplings of Decacrema present conflicting reconstructions of the evolutionary history of the association, inferring both cospeciation and the predominance of host shifts. We use cytochrome oxidase I (COI) to reconstruct phylogenetic relationships in a comprehensive sampling of the Decacrema inhabitants of Macaranga. Using a published Macaranga phylogeny, we test whether the ants and plants have cospeciated. The COI phylogeny reveals 10 well-supported lineages and an absence of cospeciation. Host shifts, however, have been constrained by stem traits that are themselves correlated with Macaranga phylogeny. Earlier lineages of Decacrema exclusively inhabit waxy stems, a basal state in the Pachystemon clade within Macaranga, whereas younger species of Pachystemon, characterized by nonwaxy stems, are inhabited only by younger lineages of Decacrema. Despite the absence of cospeciation, the correlated succession of stem texture in both phylogenies suggests that Decacrema and Pachystemon have diversified in association, or codiversified. Subsequent to the colonization of the Pachystemon clade, Decacrema expanded onto a second clade within Macaranga, inducing the development of myrmecophytism in the Pruinosae group. Confinement to the aseasonal wet climate zone of western Malesia suggests myrmecophytic Macaranga are no older than the wet forest community in Southeast Asia, estimated to be about 20 million years old (early Miocene). Our calculation of COI divergence rates from several published arthropod studies that relied on tenable calibrations indicates a generally conserved rate of approximately 1.5% per million years. Applying this rate to a rate-smoothed Bayesian chronogram of the ants, the Decacrema from Macaranga are inferred to be at least 12 million years old (mid-Miocene). However, using the extremes of rate variation in COI produces an age as recent as 6 million years. Our inferred timeline based on 1.5% per million years concurs with independent biogeographical events in the region reconstructed from palynological data, thus suggesting that the evolutionary histories of Decacrema and their Pachystemon hosts have been contemporaneous since the mid-Miocene. The evolution of myrmecophytism enabled Macaranga to radiate into enemy-free space, while the ants' diversification has been shaped by stem traits, host specialization, and geographic factors. We discuss the possibility that the ancient and exclusive association between Decacrema and Macaranga was facilitated by an impoverished diversity of myrmecophytes and phytoecious (obligately plant inhabiting) ants in the region.     

Leaf volatile compounds and the distribution of ant patrollingin an ant-plant protection mutualism: Preliminary results onLeonardoxa (Fabaceae: Caesalpinioideae) andPetalomyrmex(Formicidae: Formicinae)

While observations suggest that plant chemicals could be important in maintaining the specificity and permitting the functioning of ant-plant symbioses, they have been little studied. We report here the strongest evidence yet for chemical signalling between ants and plants in a specific ant-plant protection symbiosis. In the mutualism between Leonardoxa africana subsp. africana and Petalomyrmex phylax, ants continuously patrol young leaves, which are vulnerable to attacks by phytophagous insects. We provide experimental evidence for chemical mediation of ant attraction to young leaves in this system. By a comparative analysis of the related non-myrmecophytic tree L. africana subsp. gracilicaulis, we identify likely candidates for attractant molecules, and suggest they may function not only as signals but also as resources. We also propose hypotheses on the evolutionary origin of these plant volatiles, and of the responses to them by mutualistic ants.     

Aphid–ant mutualism: how honeydew sugars influence the behaviour of ant scouts

Honeydew is the keystone on which ant–aphid mutualism is built. The present study investigates how each sugar identified in Aphis fabae Scopoli honeydew acts upon the feeding and the laying of a recruitment trail by scouts of the aphid‐tending ant Lasius niger Linnaeus, and thus may enhance collective exploitation by the ant mutualists. The feeding preferences shown by L. niger for honeydew sugars are: melezitose = sucrose = raffinose > glucose = fructose > maltose = trehalose = melibiose = xylose. Although feeding is a prerequisite to the launching of trail recruitment, the reverse is not necessarily true: not all ingested sugar solutions elicit a trail‐laying behaviour among fed scouts. Trail mark laying is only triggered by raffinose, sucrose or melezitose, with the latter sugar being specific to honeydew. By comparing gustatory and recruitment responses of ant foragers to sugar food sources, the present study clarifies the role of honeydew composition both as a source of energy and as a mediator in ant–aphid interactions. Lasius niger feeding preferences can be related to the physiological suitability of each sugar (i.e. their detection by gustatory receptors as well as their ability to be digested and converted into energy). Regarding recruitment, the aphid‐synthesized oligosaccharide (melezitose) could be used by ant scouts as a cue indicative of a long‐lasting productive resource that is worthy of collective exploitation and defence against competitors or aphid predators.     

Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association

The pioneer tree Macaranga in SE Asia has developed manyfold associations with ants. The genus comprises all stages of interaction with ants, from facultative relationships to obligate myrmecophytes. Only myrmecophytic Macaranga offer nesting space for ants and are associated with a specific ant partner. The nonmyrmecophytic species are visited by a variety of different ant species which are attracted by extrafloral nectaries (EFN) and food bodies. Transitional Macaranga species like M. hosei are colonized later in their development due to their stem structure. Before the colonization by their specific Crematogaster partner the young plants are visited by different ant species attracted by EFN. These nectaries are reduced and food body production starts as soon as colonization becomes possible. We demonstrated earlier that obligate ant partners can protect their Macaranga plants against herbivore damage and vine cover. In this study we focused on nonspecific interactions and studied M. tanarius and M. hosei, representing a non-myrmecophyte and a transitional species respectively. In ant exclusion experiments both M. tanarius and M. hosei suffered significantly higher mean leaf damage than controls, 37% versus 6% in M. hosei, 16% versus 7% in M. tanarius. M. tanarius offers both EFN and food bodies so that tests for different effects of these two food rewards could be conducted. Plants with food bodies removed but with EFN remaining had the lowest mean increase of herbivore damage of all experimental groups. Main herbivores on M. hosei were mites and caterpillars. Many M. tanarius plants were infested by a shootborer. Both Macaranga species were visited by various ant species, Crematogaster spp. being the most abundant. We found no evidence for any specific relationships. The results of this study strongly support the hypothesis that non-specific, facultative associations with ants can be advantageous for Macaranga plants. Food bodies appear to have lower attractive value for opportunistic ants than EFN and may require a specific dietary adaptation. This is also indicated by the fact that food body production in the transitional M. hosei does not start before stem structure allows a colonization by the obligate Crematogaster species. M. hosei thus benefits from facultative association with a variety of ants until it produces its first domatia and can be colonized by its obligate mutualist.     

Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant-plant

Abstract.  1. The simultaneous occupation of a rare understorey ant-acacia Acacia mayana by its guarding ant Pseudomyrmex ferrugineus , and an apparent opportunist parasite of the mutualism, the generalist ant Camponotus planatus is described. The two ant species occur together in 30.7% of the 26 mature A. mayana plants [23.5% of all trees ( n  = 34)] surveyed, but C. planatus is absent from saplings below 1 m in height ( n  = 8).
2. While P. ferrugineus shows behaviour compatible with effective host-tree defence, C. planatus does not attack phytophagous insects and appears ineffective as an ant-guard. Camponotus planatus does, however, occupy swollen thorns (pseudogalls) on the host tree, and harvests nectar from extrafloral leaf nectaries. It is proposed that C. planatus is a parasite of the Acacia–Pseudomyrmex mutualism.
3. Camponotus planatus does not harvest the second trophic reward produced by the tree for its Pseudomyrmex ant-guards, protein-rich food (Beltian) bodies. Camponotus planatus lack the specialised larval adaptations needed to use Beltian bodies as brood food, suggesting that this resource is potentially more resistant to exploitation by generalists than extrafloral nectar.
4. In competition for access to nectaries, C. planatus effectively displaced P. ferrugineus in 99.8% of encounters. These results suggest not only that C. planatus is a parasite of this mutualism, but also that it is able to effectively counteract the aggression shown to other insects by the resident ant-guards.     

Evolution of a unique seed maturity pattern in Croton bonplandianum Baill strengthens ant-plant mutualism for seed dispersal

Summary The female flowers of Croton bonplandianum bear nectar glands which become active during fruit maturation and attain peak activity just prior to the splitting of fruits. This temporal specificity of nectar gland activity is shown to facilitate seed dispersal by ants, which are attracted to the plant only during the fruit maturation period. The nectar glands establish a nectar influence zone with a radius of 60 cm around the plant within which seed dispersal by ants is effective. Seed dispersal by ants is facilitated only if the seeds are placed within this nectar influence zone. This is accomplished by an intriguing evolutionary shift in the maturation pattern of the fruits. Unlike the usual acropetal development, fruit maturation in Croton is temporally asymmetrical, with the fruits nearer the parental axis maturing early. This unique pattern of fruit development together with the polychasial branching system leads to a concentration of seeds within the nectar influence zone and enhances seed dispersal by ants. The proximate factors responsible for this asynchronous fruit maturity were investigated.