Divvying up an incubator: How parasitic and mutualistic fig wasps use space within their nursery microcosm

Differential occupancy of space can lead to species coexistence. The fig-fig wasp pollination system hosts species-specific pollinating and parasitic wasps that develop within galls in a nursery comprising a closed inflorescence, the syconium. This microcosm affords excellent opportunities for investigating spatial partitioning since it harbours a closed community in which all wasp species are dependent on securing safe sites inside the syconium for their developing offspring while differing in life history, egg deposition strategies and oviposition times relative to nursery development. We determined ontogenetic changes in oviposition sites available to the seven-member fig wasp community of Ficus racemosa comprising pollinators, gallers and parasitoids. We used species distribution models (SDMs) for the first time at a microcosm scale to predict patterns of spatial occurrence of nursery occupants. SDMs gave high true-positive and low false-positive site occupancy rates for most occupants indicating species specificity in oviposition sites. The nursery microcosm itself changed with syconium development and sequential egg-laying by different wasp species. The number of sites occupied by offspring of the different wasp species was negatively related to the risk of syconium abortion by the plant host following oviposition. Since unpollinated syconia are usually aborted, parasitic wasps ovipositing into nurseries at the same time as the pollinator targeted many sites, suggesting response to lower risk of syconium abortion owing to reduced risk of pollination failure compared to those species ovipositing before pollination. Wasp life history and oviposition time relative to nursery development contributed to the co-existence of nursery occupants.

The chemical ecology of seed dispersal in monoecious and dioecious figs

In the nursery pollination system of figs (Ficus, Moraceae), flower-bearing receptacles called syconia breed pollinating wasps and are units of both pollination and seed dispersal. Pollinators and mammalian seed dispersers are attracted to syconia by volatile organic compounds (VOCs). In monoecious figs, syconia produce both wasps and seeds, while in (gyno)dioecious figs, male (gall) fig trees produce wasps and female (seed) fig trees produce seeds. VOCs were collected using dynamic headspace adsorption methods on freshly collected figs from different trees using Super Q® collection traps. VOC profiles were determined using gas chromatography–mass spectrometry (GC–MS).The VOC profile of receptive and dispersal phase figs were clearly different only in the dioecious mammal-dispersed Ficus hispida but not in dioecious bird-dispersed F. exasperata and monoecious bird-dispersed F. tsjahela. The VOC profile of dispersal phase female figs was clearly different from that of male figs only in F. hispida but not in F. exasperata, as predicted from the phenology of syconium production which only in F. hispida overlaps between male and female trees. Greater difference in VOC profile in F. hispida might ensure preferential removal of seed figs by dispersal agents when gall figs are simultaneously available.The VOC profile of only mammal-dispersed female figs of F. hispida had high levels of fatty acid derivatives such as amyl-acetates and 2-heptanone, while monoterpenes, sesquiterpenes and shikimic acid derivatives were predominant in the other syconial types. A bird- and mammal-repellent compound methyl anthranilate occurred only in gall figs of both dioecious species, as expected, since gall figs containing wasp pollinators should not be consumed by dispersal agents.

A hitchhiker's guide to a crowded syconium: how do fig nematodes find the right ride?

P>1Organisms with low mobility, living within ephemeral environments,need to find vehicles that can disperse them reliably to new environments. The requirement for specificity in this passenger-vehicle relationship is enhanced within a tritrophic interaction when the environment of passenger and vehicle is provided by a third organism. Such relationships pose many interesting questions about specificity within a tritrophic framework. 2. Central to understanding how these tritrophic systems have evolved, is knowing how they function now. Determining the proximal cues and sensory modalities used by passengers to find vehicles and to discriminate between reliable and non-reliable vehicles is, therefore, essential to this investigation. 3. The ancient, co-evolved and highly species-specific nursery pollination mutualism between figs and fig wasps is host to species-specific plant-parasitic nematodes which use fig wasps to travel between figs. Since individual globular fig inflorescences, i.e. syconia, serve as incubators for hundreds of developing pollinating and parasitic wasps, a dispersal-stage nematode within such a chemically,complex and physically crowded environment is faced with the dilemma of choosing the right vehicle for dispersal into a new fig. Such a system therefore affords excellent opportunities to investigate mechanisms that contribute to the evolution of specificity between the passenger and the vehicle. 4. In this study of fig-wasp-nematode tritrophic interactions in Ficus racemosa within which seven wasp species can breed, we demonstrate using two-choice as well as cafeteria assays that plant-parasitic nematodes (Schistonchus racemosa) do not hitch rides randomly on available eclosing wasps within the fig syconium, but are specifically attracted, at close range, i.e. 3 mm distance, to only that vehicle which can quickly, within a few hours, reliably transfer it to another fig. This vehicle is the female pollinating wasp. Male wasps and female parasitic wasps are inappropriate vehicles since the former are wingless and die within the fig, while the latter never enter another fig. Nematodes distinguished between female pollinating wasps and other female parasitic wasps using volatiles and cuticular hydrocarbons. Nematodes could not distinguish between cuticular hydrocarbons of male and female pollinators but used other cues, such as volatiles, at close range, to find female pollinating wasps with which they have probably had a long history of chemical adaptation. 5. This study opens up new questions and hypotheses about the evolution and maintenance of specificity in fig-wasp-nematode tritrophic interactions.

Parasites exert conflicting selection pressures to affect reproductive asynchrony of their host plant in an obligate pollination mutualism

1. Plant reproductive phenology is generally viewed as an individual's strategy to maximize gamete exchange and propagule dispersal and is often considered largely dependent on patterns of floral initiation. Reproductive phenology, however, can be affected by proximate responses to pollinators, parasites and herbivores which could influence floral longevity or fruit development time. 2. We examined the influence of insect interactants on within-plant reproductive phenology in the fig-fig wasp nursery pollination mutualism in Ficus racemosa (Moraceae). Most figs support a wasp community comprised of a mutualistic pollinator, with several host-plant-specific non-pollinating herbivorous gallers and parasitoids. These wasps reproduce within enclosed inflorescences called syconia, which develop into fruit after pollination. While different wasp species oviposit into syconia at varying times during its ontogeny, all wasp progeny are constrained to exit syconia simultaneously just prior to fruit ripening. Developing larvae of early-ovipositing wasps may hasten syconium ontogeny through formation of earlier and larger nutrient sinks, whereas larvae of late-arriving parasites may lengthen syconium ontogeny to complete their development successfully. Seeds are also important nutrient sinks. The number of seeds and the type and number of developing wasps may therefore be expected to influence syconium development times, thereby affecting the reproductive synchrony of syconia on a plant. 3. Observations on naturally pollinated and parasitized syconia indicated that their seed and wasp content affected syconium development time. Experimental manipulations of syconia to produce only seeds or various combinations of wasps confirmed this finding. Early-ovipositing galler progeny reduced syconium development times, while gallers ovipositing concurrently with pollinators had no effect on syconium development. Late-ovipositing parasitoid progeny, the presence of only seeds within the syconium, or delayed pollination increased syconium development time. The differential development of syconia, which was influenced by mutualistic or parasitic progeny, accordingly contributed to within-tree reproductive asynchrony. 4. Synthesis. Individual reproductive units in fig trees called syconia, which also function as brood sites for pollinating and parasitic fig wasps, have plastic development durations dependent on pollination timing and species of wasps developing within them. Syconium development times are a likely compromise between conflicting demands from developing seeds and different wasp species.

High Temperatures Result in Smaller Nurseries which Lower Reproduction of Pollinators and Parasites in a Brood Site Pollination Mutualism

In a nursery pollination mutualism, we asked whether environmental factors affected reproduction of mutualistic pollinators, non-mutualistic parasites and seed production via seasonal changes in plant traits such as inflorescence size and within-tree reproductive phenology. We examined seasonal variation in reproduction in Ficus racemosa community members that utilise enclosed inflorescences called syconia as nurseries. Temperature, relative humidity and rainfall defined four seasons: winter; hot days, cold nights; summer and wet seasons. Syconium volumes were highest in winter and lowest in summer, and affected syconium contents positively across all seasons. Greater transpiration from the nurseries was possibly responsible for smaller syconia in summer. The 3-5 degrees C increase in mean temperatures between the cooler seasons and summer reduced fig wasp reproduction and increased seed production nearly two-fold. Yet, seed and pollinator progeny production were never negatively related in any season confirming the mutualistic fig-pollinator association across seasons. Non-pollinator parasites affected seed production negatively in some seasons, but had a surprisingly positive relationship with pollinators in most seasons. While within-tree reproductive phenology did not vary across seasons, its effect on syconium inhabitants varied with season. In all seasons, within-tree reproductive asynchrony affected parasite reproduction negatively, whereas it had a positive effect on pollinator reproduction in winter and a negative effect in summer. Seasonally variable syconium volumes probably caused the differential effect of within-tree reproductive phenology on pollinator reproduction. Within-tree reproductive asynchrony itself was positively affected by intra-tree variation in syconium contents and volume, creating a unique feedback loop which varied across seasons. Therefore, nursery size affected fig wasp reproduction, seed production and within-tree reproductive phenology via the feedback cycle in this system. Climatic factors affecting plant reproductive traits cause biotic relationships between plants, mutualists and parasites to vary seasonally and must be accorded greater attention, especially in the context of climate change.

How to be a fig wasp parasite on the fig-fig wasp mutualism

The nursery pollination mutualism between figs and pollinating fig wasps is based on adaptations that allow wasps to enter the enclosed inflorescences of figs, to facilitate seed set, and to have offspring that develop within the nursery and that leave to enter other inflorescences for pollination. This closed mutualistic system is not immune to parasitic fig wasps. Although the life histories and basic biology of the mutualists have been investigated, the biology of the fig wasp parasites has been severely neglected. This review brings together current knowledge of the many different ways in which parasites can enter the system, and also points to the serious lacunae in our understanding of the intricate interactions between gallers, kleptoparasites, seed eaters and parasitoids within this mutualism.

How to be a dioecious fig: Chemical mimicry between sexes matters only when both sexes flower synchronously

In nursery pollination mutualisms, which are usually obligate interactions, olfactory attraction of pollinators by floral volatile organic compounds (VOCs) is the main step in guaranteeing partner encounter. However, mechanisms ensuring the evolutionary stability of dioecious fig-pollinator mutualisms, in which female fig trees engage in pollination by deceit resulting in zero reproductive success of pollinators that visit them, are poorly understood. In dioecious figs, individuals of each sex should be selected to produce odours that their pollinating wasps cannot distinguish, especially since pollinators have usually only one choice of a nursery during their lifetime. To test the hypothesis of intersexual chemical mimicry, VOCs emitted by pollen-receptive figs of seven dioecious species were compared using headspace collection and gas chromatography-mass spectrometry analysis. First, fig-flower scents varied significantly among species, allowing host-species recognition. Second, in species in which male and female figs are synchronous, intersexual VOC variation was not significant. However, in species where figs of both sexes flower asynchronously, intersexual variation of VOCs was detectable. Finally, with one exception, there was no sexual dimorphism in scent quantity. We show that there are two ways to use scent to be a dioecious fig based on differences in flowering synchrony between the sexes.