Ecological factors associated with pre-dispersal predation of fig seeds and wasps by fig-specialist lepidopteran larvae

In brood pollination mutualisms, predation of developing fruit can have large negative repercussions for both plant and pollinator population dynamics. The Sonoran Desert rock fig Ficus petiolaris and its highly-coevolved wasp pollinator are subject to frequent attack by lepidopteran larvae that consume fig fruit and the developing seeds and larval pollinators they contain. We used generalized linear mixed models to investigate how the phenology, quantity, and spatial distribution of fig fruits is associated with variation in lepidopteran damage intensity on individual trees at nine geographic locations spanning a 741 km latitudinal transect along Mexico's Baja California Peninsula. We found lepidopteran damage to be strongly positively associated with more synchronous fig crops and larger trees, and only weakly associated with lower local host tree density. These results imply that fruit production that is asynchronous within trees and spread out over time, as observed in several fig species, benefits female and male components of fitness (pollen disperser and seed production, respectively) by reducing pre-dispersal predation by frugivores.     

Limiting the cost of mutualism: the defensive role of elongated gynophore in the leafflower–moth mutualism

Mutualisms are interactions from which both partners benefit but may collapse if mutualists’ costs and benefits are not aligned. Host sanctions are one mechanism whereby hosts selectively allocate resources to the more cooperative partners and thereby reduce the fitness of overexploiters; however, many mutualisms lack apparent means of host sanctions. In mutualisms between plants and pollinating seed parasites, such as those between leafflowers and leafflower moths, pollinators consume subsets of the seeds as larval food in return for their pollination service. Plants may select against overexploiters by selectively aborting flowers with a heavy egg load, but in many leafflower species, seeds are fully eaten in some fruits, suggesting that such a mechanism is not present in all species. Instead, the fruits of Breynia vitis-idaea have stalk-like structures (gynophore) through which early-instar moth larvae must bore to reach seeds. Examination of moth mortality in fruits with different gynophore lengths suggested that fruits with longer gynophore had higher moth mortality and, therefore, less seed damage. Most moth mortality occurred at the egg stage or as early larval instar before moths reached the seeds, consistent with the view that gynophore functions to prevent moth access to seeds. Gynophore length was unaffected by plant size, extent of moth oviposition, or geography; thus, it is most likely genetically controlled. Because gynophores do not elongate in related species whose pollinators oviposit directly into the ovary, the gynophore in B. vitis-idaea may have evolved as a defense to limit the cost of the mutualism.     

Plant connectivity underlies plant‐pollinator‐exploiter distributions in Ficus petiolaris and associated pollinating and non‐pollinating fig wasps

Mutualism is ubiquitous in nature, and nursery pollination mutualisms provide a system well suited to quantifying the benefits and costs of symbiotic interactions. In nursery pollination mutualisms, pollinators reproduce within the inflorescence they pollinate, with benefits and costs being measured in the numbers of pollinator offspring and seeds produced. This type of mutualism is also typically exploited by seed‐consuming non‐pollinators that obtain resources from plants without providing pollination services. Theory predicts that the rate at which pollen‐bearing ‘foundresses’ visit a plant will strongly affect the plant's production of pollinator offspring, non‐pollinator offspring, and seeds. Spatially aggregated plants are predicted to have high rates of foundress visitation, increasing pollinator and seed production, and decreasing non‐pollinator production; very high foundress visitation may also decrease seed production indirectly through the production of pollinators. Working with a nursery mutualism comprised of the Sonoran Desert rock fig, Ficus petiolaris, and host‐specific pollinating and non‐pollinating fig wasps, we use linear models to evaluate four hypotheses linking species interactions to benefits and costs: 1) foundress density increases with host‐tree connectivity, 2) pollinator production increases with foundress density, and 3) non‐pollinator production and 4) seed production decrease with pollinator production. We also directly test how tree connectivity affects non‐pollinator production. We find strong support for our four hypotheses, and we conclude that tree connectivity is a key driver of foundress visitation, thereby strongly affecting spatial distributions in the F. petiolaris community. We also find that foundress visitation decreases at the northernmost edge of the F. petiolaris range. Finally, we find species‐specific effects of tree connectivity on non‐pollinators to be strongly correlated with previously estimated non‐pollinator dispersal abilities. We conclude that plant connectivity is highly important for predicting plant‐pollinator‐exploiter dynamics, and discuss the implications of our results for species coexistence and adaptation.     

Tolerance traits and the stability of mutualism

Identifying factors which allow the evolution and persistence of cooperative interactions between species is a fundamental issue in evolutionary ecology. Various hypotheses have been suggested which generally focus on mechanisms that allow cooperative genotypes in different species to maintain interactions over space and time. Here, we emphasise the fact that even within mutualisms (interactions with net positive fitness effects for both partners), there may still be inherent costs, such as the occasional predation by ants upon aphids. Individuals engaged in mutualisms benefit from minimising these costs as long as it is not at the expense of breaking the interspecific interaction, which offers a net positive benefit. The most common and obvious defence traits to minimise interspecific interaction costs are resistance traits, which act to reduce encounter rate between two organisms. Tolerance traits, in contrast, minimise fitness costs to the actor, but without reducing encounter rate. Given that, by definition, it is beneficial to remain in mutualistic interactions, the only viable traits to minimise costs are tolerance-based 'defence' strategies. Thus, we propose that tolerance traits are an important factor promoting stability in mutualisms. Furthermore, because resistance traits tend to propagate coevolutionary arms races between antagonists, whilst tolerance traits do not, we also suggest that tolerance-based defence strategies may be important in facilitating the transition from antagonistic interactions into mutualisms. For example, the mutualism between ants and aphids has been suggested to have evolved from parasitism. We describe how phenotypic plasticity in honeydew production may be a tolerance trait that has prevented escalation into an antagonistic arms race and instead led to mutualistic coevolution.     

Genetic architecture of multiple mutualisms and mating system in Turnera ulmifolia

Plants often associate with multiple arthropod mutualists. These partners provide important services to their hosts, but multiple interactions can constrain a plant's ability to respond to complex, multivariate selection. Here, we quantified patterns of genetic variance and covariance among rewards for pollination, biotic defence and seed dispersal mutualisms in multiple populations of Turnera ulmifolia to better understand how the genetic architecture of multiple mutualisms might influence their evolution. We phenotyped plants cultivated from 17 Jamaican populations for several mutualism and mating system-related traits. We then fit genetic variance–covariance (G) matrices for the island metapopulation and the five largest individual populations. At the metapopulation level, we observed significant positive genetic correlations among stigma–anther separation, floral nectar production and extrafloral nectar production. These correlations have the potential to significantly constrain or facilitate the evolution of multiple mutualisms in T. ulmifolia and suggest that pollination, seed dispersal and defence mutualisms do not evolve independently. In particular, we found that positive genetic correlations between floral and extrafloral nectar production may help explain their stable coexistence in the face of physiological trade-offs and negative interactions between pollinators and ant bodyguards. Locally, we found only small differences in G among our T. ulmifolia populations, suggesting that geographic variation in G may not shape the evolution of multiple mutualisms.     

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

1. Mutualisms are relationships of mutual exploitation, in which interacting species receive a net benefit from their association. In obligate pollination mutualisms (OPMs), female pollinators move pollen between the flowers of a single plant species and oviposit eggs within the female flowers that they visit. 2. Competition between co‐occurring pollinator species is predicted to increase pollinator virulence, i.e. laying more eggs or consuming more seeds per fruit. Plants involved in OPMs frequently host various non‐pollinating seed parasites and parasitoids that may influence the outcome of the mutualism. Quantifying the prevalence of parasites and parasitoids and competition between pollinators is important for understanding the factors that influence OPM evolutionary stability. 3. This study investigated the pollination mutualism occurring between the leaf flower plant, Breynia oblongifolia, and its co‐pollinating Epicephala moths. A third moth, Herpystis, also occurs in B. oblongifolia fruits as a non‐pollinating seed parasite. 4. Breynia oblongifolia fruits were collected to quantify seed predation and compare seed predation costs between the three moth species. Results showed that the larvae of the two pollinator species consume similar numbers of seeds, and that adults deposit similar numbers of eggs per flower. As such, no evidence of increases in virulent behaviours was detected as a result of competition between co‐pollinators. 5. By contrast, the seed parasite Herpystis consumed more seeds than either pollinator species, and fruit crops with a high proportion of Herpystis had significantly lower net seed production. 6. This work adds to the growing understanding of the ecology and dynamics of plant–pollinator mutualisms.     

Nutrient loading alters the performance of key nutrient exchange mutualisms

Nutrient exchange mutualisms between phototrophs and heterotrophs, such as plants and mycorrhizal fungi or symbiotic algae and corals, underpin the functioning of many ecosystems. These relationships structure communities, promote biodiversity and help maintain food security. Nutrient loading may destabilise these mutualisms by altering the costs and benefits each partner incurs from interacting. Using meta‐analyses, we show a near ubiquitous decoupling in mutualism performance across terrestrial and marine environments in which phototrophs benefit from enrichment at the expense of their heterotrophic partners. Importantly, heterotroph identity, their dependence on phototroph‐derived C and the type of nutrient enrichment (e.g. nitrogen vs. phosphorus) mediated the responses of different mutualisms to enrichment. Nutrient‐driven changes in mutualism performance may alter community organisation and ecosystem processes and increase costs of food production. Consequently, the decoupling of nutrient exchange mutualisms via alterations of the world's nitrogen and phosphorus cycles may represent an emerging threat of global change.     

Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees

The obligate mutualisms between flowering plants and their seed-parasitic pollinators constitute fascinating examples of interspecific mutualisms, which are often characterized by high levels of species diversity and reciprocal species specificity. The diversification in these mutualisms has been thought to occur through simultaneous speciation of the partners, mediated by tight reciprocal adaptation; however, recent studies cast doubt over this general view. In this study, we examine the diversity and species specificity of Epicephala moths (Gracillariidae) that pollinate Glochidion trees (Phyllanthaceae), using analysis of mitochondrial and nuclear gene sequences. Phylogenetic analysis of Epicephala moths associated with five Glochidion species in Japan and Taiwan reveal six genetically isolated species that are also distinguishable by male genital morphology: (i) two species specific to single host species (G. acuminatum and G. zeylanicum, respectively); (ii) two species that coexist on G. lanceolatum; and (iii) two species that share two, closely-related parapatric hosts (G. obovatum and G. rubrum). Statistical analysis shows that the two species associated with G. lanceolatum are not sister species, indicating the colonization of novel Glochidion host in at least one lineage. Behavioural observations suggest that all six species possess the actively-pollinating habit, thus none of the studied species has become a nonmutualistic 'cheater' that exploits the benefit resulting from pollination by other species. Our results parallel recent findings in ecologically similar associations, namely the fig-fig wasp and yucca-yucca moth mutualisms, and contribute to a more general understanding of the factors that determine ecological and evolutionary outcomes in these mutualisms.     

Why do fig wasps actively pollinate monoecious figs?

Active pollination, although rare, has been documented in a few pollination mutualisms. Such behaviour can only evolve if it benefits the pollinator in some way. The wasps that pollinate Ficus inflorescences can be active or passive pollinators. They lay their eggs in fig flowers, so that a proportion of flowers will host a wasp larva instead of a seed. We show in an actively pollinated monoecious fig that lack of pollination does not induce fig abortion or affect wasp offspring size but results in smaller numbers of offspring. Hence, conversely to other active pollination systems, seed formation is not obligatory to sustain developing pollinator larvae; however there is a direct fitness cost to active pollinators not to pollinate. We then compared the locations of eggs and fertilised flowers of three actively pollinated Ficus species and one passively pollinated species. We found that more flowers containing wasp eggs were fertilised in the actively pollinated species relative to those of the passively pollinated one. These results along with comparison with similar studies on dioecious figs, support the hypothesis that active pollination has evolved in fig wasps to ensure that more flowers containing wasp eggs are fertilised as this may increase the chances of successful gall development. The stigmatic platform characterising actively pollinated figs is probably an adaptation to increase pollen dispersion within the fig.     

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.     

Selection on fruit traits is mediated by the interplay between frugivorous birds,fruit flies,parasitoid wasps and seed‐dispersing ants

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy‐fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.     

Ecological and evolutionary conditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproduction

Coevolved mutualisms, such as those between senita cacti, yuccas, and their respective obligate pollinators, benefit both species involved in the interaction. However, in these pollination mutualisms the pollinator's larvae impose a cost on plants through consumption of developing seeds and fruit. The effects of pollinators on benefits and costs are expected to vary with the abundance of pollinators, because large population sizes result in more eggs and larval seed-eaters. Here, we develop the hypothesis that fruit abortion, which is common in yucca, senita, and plants in general, could in some cases have the function of limiting pollinator abundance and, thereby, increasing fruit production. Using a general steady-state model of fruit production and pollinator dynamics, we demonstrate that plants involved in pollinating seed-eater mutualisms can increase their fecundity by randomly aborting fruit. We show that the ecological conditions under which fruit abortion can improve plants fecundity are not unusual. They are best met when the plant is long-lived, the population dynamics of the pollinator are much faster than those of the plant, the loss of one fruit via abortion kills a larva that would have the expectation of destroying more than one fruit through its future egg laying as an adult moth, and the effects of fruit abortion on pollinator abundance are spatially localized. We then use the approach of adaptive dynamics to find conditions under which a fruit abortion strategy based on regulating the pollinator population could feasibly evolve in this type of plant-pollinator interaction.     

Decreasing water availability across the globe improves the effectiveness of protective ant–plant mutualisms: a meta‐analysis

Abiotic conditions can increase the costs of services and/or the benefits of rewards provided by mutualistic partners. Consequently, in some situations, the outcome of mutualisms can move from beneficial to detrimental for at least one partner. In the case of protective mutualisms between ant bodyguards and plants bearing extrafloral nectaries (EFNs), plants from arid environments face a trade‐off between EFN production and maintenance and water and carbon economy. This trade‐off may increase EFN costs and decrease their value as a defensive strategy to plants in such environments. Despite this, the presence of EFNs is an ubiquitous trait in plants from arid environments, suggesting that they provide greater benefits to plants in these environments to compensate for their higher costs. We used a meta‐analysis to investigate if such benefits do increase with decreasing water availability and the possible underlying causes (such as ant behaviour or ant diversity). As predicted, ant effect on EFN plants performance increased as mean annual precipitation decreased. We also found that the frequency of dominant ants on EFN plants increased in drier areas. Due to the more aggressive behaviour of dominant ants, we suggest that they represent an important factor shaping the adaptive value of EFNs to plants in arid environments.     

Detecting the elusive cost of parasites on fig seed production

Mutualisms provide essential ecosystem functions such as pollination and contribute considerably to global biodiversity. However, they are also exploited by parasites that remove resources and thus impose costs on one or both of the mutualistic partners. The fig/pollinator interaction is a classic obligate mutualism; it is pantropical and involves >750 Ficus species and their host-specific pollinating wasps (family Agaonidae). Figs also host parasites of the mutualism that should consume pollinators or seeds, depending on their larval ecology. We collected data from a large crop of figs on Ficus glandifera var. brachysyce in a Sulawesi rainforest with an unusually high number of Eukoebelea sp. parasites. We found that these parasites have a significant negative correlation with fig seed production as well as with pollinator offspring production. Eukoebelea wasps form the basal genus in subfamily Sycophaginae (Chalcidoidea) and their larval biology is considered unknown. Our analysis suggests that they feed as flower gallers and impose direct costs on the fig tree, but a strategy including the consumption of pollinator larvae cannot be ruled out. We also present baseline data on the composition of the fig wasp community associated with F. glandifera var brachysyce and light trap catch data.     

Hand pollination of global crops – A systematic review

Global pollinator declines and land-use change can lead to pollination limitation with implications for agricultural productivity. Hand pollination is used in agricultural production as a technique to manually pollinate crops. But the prevalence of hand pollination, as well as benefits and costs, remain unknown. We systematically reviewed the literature for examples, methods, drivers, and economic motivations of hand pollination. Furthermore, we discuss the risks, constraints, and opportunities of hand pollination. We found evidence for 20 hand-pollinated crops, including minor but also economically important crops (e.g. apple, oil palm, cacao). The lack of pollinators was the most important reason for the application of hand pollination (50% of crops), while insufficient proportion or proximity of pollinizers (8% of crops) and skewed sex ratio or dichogamy (8% of crops) were second most important. The main economic motivations for practicing or recommending hand pollination were to increase fruit set, and/or fruit quality (78% of crops). Hand pollination is practiced in large- and small-scale farming, home gardens, and greenhouses. Opportunities of hand pollination are the control of pollen origin and quantity, pollination timing and frequency as well as independence from environmental fluctuations. Farmers can increase yields, improve fruit quality, avoid fruit abortion, increase employment, and secure subsistence food. The main constraints of hand pollination are high labor inputs, high material costs, and required skills. Major risks of hand pollination include management ignoring pollinator conservation, high food prices, over-pollination, labor accidents, and unfair labor. We conclude that in the face of global change, hand pollination allows improved control of pollination and is likely to increase in importance. The benefits of hand pollination need to outweigh the costs and fair labor is essential. Altogether, hand pollination can be a valuable tool for crop systems where pollinators are absent or are not reliable for sustaining high-quality crop production.     

Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae)

About half a dozen obligate pollination mutualisms between plants and their seed-consuming pollinators are currently recognized, including fig-fig wasp, yucca-yucca moth, and the recently discovered Glochidion tree-Epicephala moth mutualisms. A common principle among these interactions is that the pollinators consume only a limited amount of the seed crop within a developing fruit (or fig in the case of fig-fig wasp mutualism), thereby ensuring a net benefit to plant reproduction. A novel obligate, seed-parasitic pollination mutualism between two species of New Caledonian Phyllanthus (Euphorbiaceae), a close relative of Glochidion, and Epicephala moths (Gracillariidae) is an exception to this principle. The highly specialized flowers of Phyllanthus are actively and exclusively pollinated by species-specific Epicephala moths, whose larvae consume all six ovules of the developing fruit. Some flowers pollinated by the moths remain untouched, and thus a fraction of the fruits is left intact. Additional evidence for a similar association of Epicephala moths in other Phyllanthus species suggests that this interaction is a coevolved, species-specific pollination mutualism. Implications for the evolutionary stability of the system, as well as differences in mode of interaction with respect to the Glochidion-Epicephala mutualism, are discussed.     

Floral visitation by the Argentine ant reduces pollinator visitation and seed set in the coast barrel cactus, Ferocactus viridescens

Mounting evidence indicates that trade-offs between plant defense and reproduction arise not only from resource allocation but also from interactions among mutualists. Indirect costs of plant defense by ants, for example, can outweigh benefits if ants deter pollinators. Plants can dissuade ants from occupying flowers, but such arrangements may break down when novel ant partners infiltrate mutualisms. Here, we examine how floral visitation by ants affects pollination services when the invasive Argentine ant (Linepithema humile) replaces a native ant species in a food-for-protection mutualism with the coast barrel cactus (Ferocactus viridescens), which, like certain other barrel cacti, produces extrafloral nectar. We compared the effects of floral visitation by the Argentine ant with those of the most prevalent native ant species (Crematogaster californica). Compared to C. californica, the Argentine ant was present in higher numbers in flowers. Cactus bees (Diadasia spp.), the key pollinators in this system, spent less time in flowers when cacti were occupied by the Argentine ant compared to when cacti were occupied by C. californica. Presumably as a consequence of decreased duration of floral visits by Diadasia, cacti occupied by L. humile set fewer seeds per fruit and produced fewer seeds overall compared to cacti occupied by C. californica. These data illustrate the importance of mutualist identity in cases where plants balance multiple mutualisms. Moreover, as habitats become increasingly infiltrated by introduced species, the loss of native mutualists and their replacement by non-native species may alter the shape of trade-offs between plant defense and reproduction.     

Repeated independent evolution of obligate pollination mutualism in the Phyllantheae-Epicephala association

The well-known fig-fig wasp and yucca-yucca moth mutualisms are classic examples of obligate mutualisms that have been shaped by millions of years of coevolution. Pollination systems involving obligate seed parasites are only expected to evolve under rare circumstances where their positive effects are not swamped by abundant co-pollinators and heavy costs resulting from seed destruction. Here, we show that, in Phyllantheae, specialization to pollination by Epicephala moths evolved at least five times, involving more than 500 Phyllantheae species in this obligate association. Active pollination behaviour evolved once in Epicephala, 10-20 Myr after the initial divergence of their host plants. The pollinating Epicephala moths thus radiated on an already-diverged host lineage and successively colonized new Phyllantheae hosts, thereby giving rise to repeated independent evolution of the specialized pollination system in Phyllantheae. The present evolutionary success of this association rests entirely upon active pollination by Epicephala, making this a distinct example of an evolutionary key innovation. Overall, our findings provide a clear empirical demonstration of how a combination of evolutionary innovation and partner shifts facilitates the spread of mutualism in a coevolving species interaction.     

Complex interactions on fig trees: ants capturing parasitic wasps as possible indirect mutualists of the fig–fig wasp interaction

Like other mutualisms, pollination mutualisms attract parasites, as well as opportunistic and specialist predators of the pollinators and parasites. These associated species influence the evolutionary dynamics of pairwise mutualisms. Predatory ants are frequent associates of pollination mutualisms, but their effects on the complex interactions between plants, pollinators and parasites have not yet been clearly established, even in the case of the well-described obligate interaction between figs and fig wasps. We attempted to quantify such effects for ants associated with three fig species, two dioecious ( Ficus condensa [Bruneï], F . carica [France]) and one monoecious ( F . racemosa [India]). In all these cases, ant presence on a fig tree strongly reduced the number of parasitic wasps on the figs. Experimental exclusion of ants resulted in an increase in the number of non-pollinating fig wasps on F . condensa and F . racemosa . Experimental ant supplementation led to a decrease in the number of non-pollinating fig wasps on F . carica . Moreover, on F . condensa , the level of reduction of the number of parasitic wasps depended on the number and identity of the ants. On F . carica , non-pollinating fig wasps even avoided trees occupied by the dominant predatory ant. The consistency of the effect of ants in these three cases, representing a geographically, ecologically, and taxonomically broad sample of figs, argues for the generality of the effect we observed. Because reduction of parasitism benefits the pollinator, ants may be considered as indirect mutualists of plants and pollinators in the network of complex interactions supported by fig trees.     

Synchrony between fruit maturation and effective dispersers' foraging activity increases seed protection against seed predators

The evolution of pollination and seed dispersal mutualisms is conditioned by the spatial and temporal co-occurrence of animals and plants. In the present study we explore the timing of seed release of a myrmecochorous plant (Helleborus foetidus) and ant activity in two populations in southern Spain during 2 consecutive years. The results indicate that fruit dehiscence and seed shedding occur mostly in the morning and correspond to the period of maximum foraging activity of the most effective ant dispersers. By contrast, ant species that do not transport seeds and/or that do not abound near the plants are active either before or after H. foetidus diaspores are released. Experimental analysis of diet preference for three kinds of food shows that effective ant dispersers are mostly scavengers that readily feed on insect corpses and sugars. Artificial seed depots suggest that seeds deposited on the ground out of the natural daily time window of diaspore releasing are not removed by ants and suffer strong predation by nocturnal rodents Apodemus sylvaticus. Nevertheless, important inter-annual variations in rodent populations cast doubts on their real importance as selection agents. We argue that traits allowing synchrony between seed presentation and effective partners may constitute a crucial pre-adaptation for the evolution of plant-animal mutualisms involving numerous animal partners.