An inquiline fig wasp using seeds as a resource for small male production: a potential first step for the evolution of new feeding habits?

The processes allowing evolutionary transitions in resources used by parasitic wasps are largely unknown. Microhymenopteran communities associated with figs could provide a model system to investigate such transitions. We investigate here a species of genus Idarnes . The larvae generally develop as inquilines of the pollinating wasp larvae. However, in figs where the parasitic pressure is high, eggs are laid in developing seeds. These eggs turn into small males. This is the first report of seed consumption by a fig wasp. Using an alternative resource to produce small males could provide a pathway to select for increased ability to use this resource and hence provide an intermediate step for evolving the capacity to use new resources.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 9–17.     

Exclusive rewards in mutualisms: ant proteases and plant protease inhibitors create a lock–key system to protect Acacia food bodies from exploitation

Myrmecophytic Acacia species produce food bodies (FBs) to nourish ants of the Pseudomyrmex ferrugineus group, with which they live in an obligate mutualism. We investigated how the FBs are protected from exploiting nonmutualists. Two‐dimensional gel electrophoresis of the FB proteomes and consecutive protein sequencing indicated the presence of several Kunitz‐type protease inhibitors (PIs). PIs extracted from Acacia FBs were biologically active, as they effectively reduced the trypsin‐like and elastase‐like proteolytic activity in the guts of seed‐feeding beetles (Prostephanus truncatus and Zabrotes subfasciatus), which were used as nonadapted herbivores representing potential exploiters. By contrast, the legitimate mutualistic consumers maintained high proteolytic activity dominated by chymotrypsin 1, which was insensitive to the FB PIs. Larvae of an exploiter ant (Pseudomyrmex gracilis) taken from Acacia hosts exhibited lower overall proteolytic activity than the mutualists. The proteases of this exploiter exhibited mainly elastase‐like and to a lower degree chymotrypsin 1‐like activity. We conclude that the mutualist ants possess specifically those proteases that are least sensitive to the PIs in their specific food source, whereas the congeneric exploiter ant appears partly, but not completely, adapted to consume Acacia FBs. By contrast, any consumption of the FBs by nonadapted exploiters would effectively inhibit their digestive capacities. We suggest that the term ‘exclusive rewards’ can be used to describe situations similar to the one that has evolved in myrmecophytic Acacia species, which reward mutualists with FBs but safeguard the reward from exploitation by generalists by making the FBs difficult for the nonadapted consumer to use.     

Production of food bodies on the reproductive organs of myrmecophytic Macaranga species (Euphorbiaceae): effects on interactions with herbivores and pollinators

In protective ant–plant mutualisms, plants offer ants food (such as extrafloral nectar and/or food bodies) and ants protect plants from herbivores. However, ants often negatively affect plant reproduction by deterring pollinators. The aggressive protection that mutualistic ants provide to some myrmecophytes may enhance this negative effect in comparison to plant species that are facultatively protected by ants. Because little is known about the processes by which myrmecophytes are pollinated in the presence of ant guards, we examined ant interactions with herbivores and pollinators on plant reproductive organs. We examined eight myrmecophytic and three nonmyrmecophytic Macaranga species in Borneo. Most of the species studied are pollinated by thrips breeding in the inflorescences. Seven of eight myrmecophytic species produced food bodies on young inflorescences and/or immature fruits. Food body production was associated with increased ant abundance on inflorescences of the three species observed. The exclusion of ants from inflorescences of one species without food rewards resulted in increased herbivory damage. In contrast, ant exclusion had no effect on the number of pollinator thrips. The absence of thrips pollinator deterrence by ants may be due to the presence of protective bracteoles that limit ants, but not pollinators, from accessing flowers. This unique mechanism may account for simultaneous thrips pollination and ant defense of inflorescences.     

Not all ants are equal: obligate acacia ants provide different levels of protection against mega‐herbivores

In obligate ant–plant mutualisms, the asymmetric engagement of a single plant species with multiple ant species provides the opportunity for partners to vary in their behaviour. Variation in behaviour has implications for the interactions with third‐party species such as herbivores. This study assessed the effect of obligate ant‐mutualists (Crematogaster mimosae, Crematogaster nigriceps and Tetraponera penzigi) inhabiting the African ant‐acacia (Acacia drepanolobium) on three mega‐herbivore browsers: the Maasai giraffe (Giraffa camelopardalis tippelskirchi), the reticulated giraffe (Giraffa c. reticulata) and the black rhino (Diceros bicornis). Giraffes are abundant and wide‐ranging herbivores of the acacias, whereas black rhinos are localized and perennial herbivores of the acacias. Multiyear field studies comparing the ants’ aggressive behaviour and browsing by mega‐herbivores suggested differences between the tending abilities of the primary ant species inhabiting A. drepanolobium. Trees occupied by the aggressive ant species C. mimosae had significantly less browsing by giraffes and black rhino than trees occupied by other ant species. The results of this study provide evidence that ant‐mutualists on African acacias can serve as deterrents to mega‐herbivores and that different ant species vary in their tending abilities.     

Secondary galling: a novel feeding strategy among ‘non‐pollinating’ fig wasps from Ficus curtipes

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Body size in a pollinating fig wasp and implications for stability in a fig‐pollinator mutualism

The fig–fig pollinator association is a classic case of an obligate mutualism. Fig‐pollinating wasps often have to fly long distances from their natal syconia to a receptive syconium and then must enter the narrow ostiole of the syconium to reproduce. Large wasps are expected to have a greater chance of reaching a receptive syconium. In this study, we tested this hypothesis and then examined whether the ostiole selectively prevented larger pollinators from entering the syconial cavity. In Xishuangbanna, China, Ceratosolen solmsi marchali Mayr (Hymenoptera: Agaonidae) pollinates the dioecious syconia of Ficus hispida L. (Moraceae). The body size of newly emerged wasps and wasps arriving at receptive syconia were compared. Wasps arriving at receptive syconia were significantly larger than newly emerged wasps. We also compared the size of wasps trapped in the ostiole with those in the cavity. Wasps trapped in the ostiole were significantly larger than those in the syconial cavity. Thus, in the case of F. hispida, large wasps were more likely to reach receptive syconia, but the ostiole limited maximum fig wasp size. This indicates that the ostiole, as a selective filter to pollinators, stabilizes pollinator size. Hence, it helps to maintain stability in the fig–fig pollinator mutualism.     

Characterization of microsatellite markers for plant‐ants of the genus Crematogaster subgenus Decacrema

We present primer sequences for five polymorphic microsatellite loci in ants of the genus Crematogaster subgenus Decacrema that live in obligate symbiosis with host plants of the euphorb genus Macaranga. Microsatellite loci were isolated with a highly efficient method of enrichment. The number of alleles ranged from 10 to 18 for Crematogaster morphospecies 2, for which these markers were developed, with an observed heterozygosity ranging from 0.6578 to 0.9474. The markers were designed for the study of the population as well as of the social structure of colonies.     

Insect responses to host plant provision beyond natural boundaries: latitudinal and altitudinal variation in a Chinese fig wasp community

Many plants are grown outside their natural ranges. Plantings adjacent to native ranges provide an opportunity to monitor community assembly among associated insects and their parasitoids in novel environments, to determine whether gradients in species richness emerge and to examine their consequences for host plant reproductive success. We recorded the fig wasps (Chalcidoidea) associated with a single plant resource (ovules of Ficus microcarpa) along a 1200 km transect in southwest China that extended for 1000 km beyond the tree's natural northern range margin. The fig wasps included the tree's agaonid pollinator and other species that feed on the ovules or are their parasitoids. Phytophagous fig wasps (12 species) were more numerous than parasitoids (nine species). The proportion of figs occupied by fig wasps declined with increasing latitude, as did the proportion of utilized ovules in occupied figs. Species richness, diversity, and abundance of fig wasps also significantly changed along both latitudinal and altitudinal gradients. Parasitoids declined more steeply with latitude than phytophages. Seed production declined beyond the natural northern range margin, and at high elevation, because pollinator fig wasps became rare or absent. This suggests that pollinator climatic tolerances helped limit the tree's natural distribution, although competition with another species may have excluded pollinators at the highest altitude site. Isolation by distance may prevent colonization of northern sites by some fig wasps and act in combination with direct and host‐mediated climatic effects to generate gradients in community composition, with parasitoids inherently more sensitive because of declines in the abundance of potential hosts.     

Interactions between pollinator and non‐pollinator fig wasps: correlations between their numbers can be misleading

Ficus and their species–specific pollinator fig wasps represent an obligate plant–insect mutualism, but figs also support a community of non‐pollinating fig wasps (NPFWs) that consist of phytophages and parasitoids or inquilines. We studied interactions between Kradibia tentacularis, the pollinator of a dioecious fig tree species Ficus montana, and an undescribed NPFW Sycoscapter sp. Members of Sycoscapter sp. oviposited 2–4 weeks after pollinator oviposition, when host larvae were present in the figs. No negative correlation was found between the numbers of the two wasp species emerging from figs in a semi‐natural population. However, in experiments where the numbers of pollinator foundresses entering a fig were controlled, Sycoscapter sp. significantly reduced the numbers of pollinator offspring. Consequently, it can be concluded that Sycoscapter sp. is a parasitoid of K. tentacularis (which may also feed on plant tissue). Sycoscapter females concentrate their oviposition in figs that contain more potential hosts, rendering invalid conclusions based on simple correlations of host and natural enemy numbers.     

Ants suppressing plant pathogens: a review

Ant–plant mutualisms are usually regarded as driven by ants defending plants against herbivores in return for plant‐produced food rewards and housing. However, ants may provide additional services. In a review of published studies on ant–pathogen–plant interactions, we investigated whether ants’ extensive hygiene measures, including the use of ant‐produced antibiotics, extend to their host plants and reduce plant pathogen loads. From 30 reported species combinations, we found that the presence of ants lead to reduced pathogen levels in 18 combinations and to increased levels in 6. On average, ants significantly reduced pathogen incidence with 59%. This effect size did not differ significantly from effect sizes reported from meta‐analyses on herbivore protection. Thus, pathogen and herbivore protection could be of equal importance in ant–plant mutualisms. Considering the abundance of these interactions, ecological impacts are potentially high. Furthermore, awareness of this service may stimulate the development of new measures to control plant diseases in agriculture. It should be noted, though, that studies were biased toward tropical ant–plant symbioses and that the literature in the field is limited at present. Future research on plant pathogens is needed to enhance our understanding of ant–plant mutualisms and their evolution.     

Figs (Ficus spp.) and fig wasps (Chalcidoidea, Agaonidae): hypotheses for an ancient symbiosis

Figs and their pollinating fig wasps are dependent on one another for propagation of their own kinds. The wasps reproduce by ovipositing through the styles of female flowers within the closed fig receptacles (syconia). About half of the female flowers within the syconia of monoecious figs have styles which are longer than the ovipositors of the wasp, and they will therefore produce seeds rather than wasp larvae. Since a longer ovipositor would enable a wasp to reach more ovules and deposit more eggs, the question arises at to why longer ovipositors have not evolved.
In an attempt to answer this question, four seemingly plausible hypotheses are examined but each is shown to be problematical in some way. Consideration is then given to a fifth hypothesis which proposes that ovipositor length is constrained by abortion of syconia with relatively few seed embryos and many agaonid larvae. It is argued first that this pattern of abortion will be selected during a sustained period of heavy wasp infestation because seeds will then become scarce relative to pollen-carrying wasps. Increased expenditure by the fig on seed production would therefore be favoured by natural selection. A greater expenditure on seeds would occur if young syconia with exceptionally heavy wasp infestations were dropped and the saved nutrients invested in syconia of a subsequent crop containing average levels of wasp larvae and seeds. Provided that the energy and nutrient cost of dropping young syconia is small, the selective advantage to the wasp of longer ovipositors is eliminated in this way. A stable coexistence of figs and wasps is therefore possible. The paper concludes by discussing two general predictions of the abortion hypothesis, and how these may be tested.     

Infiltration of a facultative ant–plant mutualism by the introduced Argentine ant: effects on mutualist diversity and mutualism benefits

1. Ant–plant mutualisms have been the focus of considerable empirical research, but few studies have investigated how introduced ants affect these interactions. Using 2 years of survey data, this study examines how the introduced Argentine ant [Linepithema humile (Mayr)] differs from native ants with respect to its ability to protect the extrafloral nectary‐bearing coast barrel cactus (Ferocactus viridescens) in Southern California. 2. Eighteen native ant species visited cacti in uninvaded areas, but cacti in invaded areas were primarily visited by the Argentine ant. The main herbivore of the coast barrel cactus present at the study sites is a leaf‐footed bug (Narnia wilsoni). 3. Herbivore presence (the fraction of surveys in which leaf‐footed bugs were present on individual cacti) was negatively related to ant presence (the fraction of surveys in which ants were present on individual cacti). Compared with cacti in uninvaded areas, those in invaded areas were less likely to have herbivores and when they did had them less often. 4. Seed mass was negatively related to herbivore presence, and this relationship did not differ for cacti in invaded areas versus those in uninvaded areas. 5. Although the Argentine ant might provide superior protection from herbivores, invasion‐induced reductions in ant mutualist diversity could potentially compromise plant reproduction. The cumulative number of ant species on individual cacti over time was lower in invaded areas and was associated with a shortened seasonal duration of ant protection and reduced seed mass. These results support the hypothesis that multiple partners may enhance mutualism benefits.     

Developmental Changes in Direct and Indirect Defenses in the Young Leaves of the Neotropical Tree Genus Inga (Fabaceae)

Plant fitness is affected by herbivory, and in moist tropical forests, 70 percent of herbivore damage occurs on young leaves. Thus, to understand the effects of herbivory on tropical plant fitness, it is necessary to understand how tropical young leaves survive the brief, but critical, period of susceptibility. In this study, we surveyed three species of Inga during young leaf expansion. Three classes of toxic secondary metabolites (phenolics, saponins, and tyrosine), extrafloral nectar production, leaf area, and extrafloral nectary area were measured at randomly assigned young leaf sizes. In addition, all defenses were compared for potential trade‐offs during leaf expansion. No trade‐offs among defenses were found, and the concentration of all defenses, except tyrosine, decreased during leaf expansion. We suggest that plants continued to increase phenolic and saponin content, but at a rate that resulted in decreasing concentrations. In contrast, tyrosine content per leaf steadily increased such that a constant concentration was maintained regardless of young leaf size. Nectar production remained constant during leaf expansion, but, because young leaf area increased by tenfold, the investment in extrafloral nectar per leaf area significantly decreased. In addition, nectary area did not change during leaf expansion and therefore the relative size of the nectary significantly decreased during young leaf expansion. These results support the predictions of the optimal defense hypothesis and demonstrate that the youngest leaves have the highest investment in multiple defenses, most likely because they have the highest nitrogen content and are most susceptible to a diversity of herbivores.     

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.     

Predation on the pollinating fig wasp of Ficus erecta by larvae of Silba sp. (Diptera: Lonchaeidae)

This study examined the insect assemblage within the syconium of the dioecious fig Ficus erecta Thunb., 1786 (Moraceae) on Kii‐Oshima Island, Wakayama Prefecture, Japan. Species present included pollinating and non‐pollinating fig wasps Blastophaga nipponica Grandi, 1921 and Sycoscapter inubiae Ishii, 1934, respectively, as well as an undetermined species of Silba Macquart, 1851 (Diptera: Lonchaeidae). Larvae of Silba sp. were found only in fig syconia containing B. nipponica. Observations revealed that larvae of Silba sp. fed on female adults of B. nipponica within fig galls by thrusting their heads through the intersegmental membrane. Furthermore, larvae of Silba sp. had a high predation rate (90%). These observations suggest that larvae of Silba sp. are specialized for feeding on B. nipponica and have a negative effect on populations of this species.     

Partner manipulation stabilises a horizontally transmitted mutualism

Mutualisms require protection from non‐reciprocating exploiters. Pseudomyrmex workers that engage in an obligate defensive mutualism with Acacia hosts feed exclusively on the sucrose‐free extrafloral nectar (EFN) that is secreted by their hosts, a behaviour linking ant energy supply directly to host performance and thus favouring reciprocating behaviour. We tested the hypothesis that Acacia hosts manipulate this digestive specialisation of their ant mutualists. Invertase (sucrose hydrolytic) activity in the ant midguts was inhibited by chitinase, a dominant EFN protein. The inhibition occurred quickly in cell‐free gut liquids and in native gels and thus likely results from an enzyme–enzyme interaction. Once a freshly eclosed worker ingests EFN as the first diet available, her invertase becomes inhibited and she, thus, continues feeding on host‐derived EFN. Partner manipulation acts at the phenotypic level and means that one partner actively controls the phenotype of the other partner to enhance its dependency on host‐derived rewards.     

Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism

Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative‐fitness‐based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best‐studied mutualisms. We find that although there are numerous observations of low‐quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative‐fitness‐based definition of cheating.     

Effects of planting method on the recovery of arboreal ant activity on revegetated farmland

Ecological restoration aims to re‐establish both biodiversity and ecological function in damaged ecosystems. Ants are important drivers of ecological functions and are early colonizers of restored ecosystems. Rates at which ants perform functions are thought to be fuelled by access to plant sugars. In revegetated farmland in south‐eastern Australia, I tested if ant activity on trees, which reflects use of arboreal sugars, follows a predictable trajectory of recovery towards a remnant‐like state. Additionally, I examined whether planting method alters this trajectory by comparing tube stock (TS), which results in low Eucalyptus densities, with direct seeding (DS), which results in high Eucalyptus densities. Replicate sites (n = 5) of young (planted between 1998 and 2001) and old (planted between 1989 and 1994) TS and DS revegetation, pastures and remnants were compared. Activity on trunks was significantly positively correlated with ant tending of Hemiptera in young and old revegetation. In DS plantings, activity and estimated liquid loads on Eucalyptus trees were low and rapidly approached that in remnants, while TS sites remained similar to high values observed in pastures with trees. Patterns for Acacia were less clear, reflecting consistent densities for this species between TS and DS. At the whole‐of‐field scale, planting methods did not differ. Importantly, although trajectories differed, neither TS nor DS sites approached the low activity or estimated liquid loads observed in remnants. Rates of ant use of arboreal sugars and associated sugar‐fuelled processes may thus take considerably longer to recover than the period covered by this study. This finding suggests planting method may affect the trajectory and outcome of revegetation for plant health, as well as sugar‐fuelled ecosystem functions performed by ants.