Divided They Stay : Species Coexistence In A Community Of Mutualists And Exploiters

Abstract

The fig–fig wasp interaction is a classic example of obligate mutualism and coevolution. It is also a nursery pollination mutualism and supports a diversity of exploiter/parasite/non-pollinating fig wasp species. Mutualists and exploiters comprise the fig wasp community. All the wasp community members are obligately dependent on the fig syconium (a globular closed structure comprising of hundreds to thousands of uniovulate florets) for completing their life cycle. The fig florets can be sessile (without a stalk) or pedicellate (stalked) and can support a community comprising 3–30 wasp species. Fig wasps can access the floral resources for oviposition directly by entering into the syconium (internal oviposition) or by penetration of the syconium surface (external oviposition). Most studies on the fig–fig wasp interaction have investigated the stability of the interaction, pollination biology, pollen dispersal, co-evolution or the effect of exploiters on this mutualism. However, studies dealing with community ecology and species coexistence mechanisms in these communities are rare. Factors contributing to coexistence of mutualists and exploiters in a fig wasp community were studied using a reasonably speciose fig wasp community associated with Ficus racemosa in south India. The wasp community of Ficus racemosa comprises a single species of pollinator and six species of exploiters; together they represent three genera of fig wasp species. The community members show differences in their feeding habit; they could be 1) gallers (feed on floral tissue after pollination and/or after inducing abnormal tissue development of the floret that is also called the gall), 2) inquilines (feed on gall tissue but cannot induce galling; survive by feeding on gall tissue and starving the host larva to death), or 3) parasitoids (lay eggs in or on developing offspring of a galler or inquiline species; develop by feeding on host tissue). Resource partitioning across temporal and spatial axes on this fig wasp community have been quantified. Ovipositor traits of each community member were also investigated since variation in ovipositor traits might facilitate resource partitioning. Finally, the role of life-history traits in species coexistence in this community was also explored. Temporal resource partitioning among members of the fig wasp community was studied (1) across the resource phenology, i.e. over the development phases of the fig syconium, and (2) on a diel scale. The seven members of the wasp community were found to partition their oviposition periods across fig syconium development phenology; some species used very young syconia (soft and smaller in size) for oviposition whereas others used mature (hard and bigger in size) syconia for oviposition. The first species to colonise the syconia were gallers and these were followed by parasitoids in a definite oviposition sequence. Pollinators arrived concurrently with an exploiter galler species and had the shortest oviposition window in terms of days. Although fig wasps are known to be largely diurnal, night oviposition in several fig wasp species was documented for the first time. Wasp species showed a peak in their activity period across the diel cycle and phenology. This is probably the first study to simultaneously investigate temporal partitioning across the syconium phenology as well as the diel scale in a fig wasp community. Partitioning of syconium space was investigated by quantifying the quality (type of floret—sessile or pedicellate) of floral resources. The number of individuals of each species developing in a syconium was quantified along with host accessibility during oviposition by each wasp species. The association between community members developing within a syconium was also tested. The differential occupancy of florets by each species based on their distance from the base of the syconium was evaluated. For the first time the relative distribution of males and females of the entire fig wasp community was quantified. The wasp community members used similar types of florets for oviposition. Seeds were found mostly in sessile florets and wasps were present in large numbers in pedicellate florets. Except for one wasp species, all others occurred uniformly within the syconium with respect to the distance from the base of the syconium. Species distribution models revealed higher prediction ability for the location of mutualists (seed and pollinator) within the syconium compared to exploiters. Within a syconium, all species pairs exhibited positive associations indicating either an absence of or low competitive exclusion. Some florets were modified by their gall occupants such that they were longer in length indicating the possibility of creation of an enemy-free zone by the gall occupant. Yet, most florets were accessible to ovipositing wasps based on ovipositor lengths and flexibility. The probability of finding a male decreased with increase in floret length when all wasp species were grouped together; however, this trend did not hold true when males and females of species were tested individually. Based on these results, the fig wasps of F. racemosa could be grouped into—(1) Early-arriving galler species which used immature florets, inducing large galls that protruded into the cavity, and with fewer individuals per syconium, (2) Galler species arriving concurrently with the pollinator, inducing galls that were morphologically indistinguishable from those of the pollinator, and with many individuals developing per fig syconium, and (3) Parasitoids and/or inquilines of the galler species, with variable abundance per syconium. Thus, these results show that the wasp species do not clearly partition floral resources between syconia and within syconium but they can modify their oviposition sites and also differ in the proportion of florets within a syconium used for oviposition. Oviposition sites of the fig wasps can be reached only by using their ovipositor. The resources for oviposition are hidden and hence might require tools for resource location and utilisation. The frequency and diversity of sensilla on the ovipositor, as well as ovipositor structure (morphology and sclerotisation of the tip) was documented for the entire wasp community. The internally-ovipositing pollinator had the simplest ovipositor, negligible sclerotisation and only one type of sensillum on its ovipositor; the externally ovipositing exploiter species had teeth on their ovipositors, sclerotisation and various types of ovipositor sensilla. Ovipositor sclerotisation and lateness of arrival for oviposition in syconium development were positively correlated. Ovipositor teeth height increased from gallers to parasitoids. Presence of different types of sensilla was noted which included mechano- and chemosensilla, as well as combined mechano-chemosensilla. Chemosensilla were most concentrated at ovipositor tips while mechanoreceptors were more widely distributed. Ovipositor traits of one putative parasitoid/inquiline species differed from those of its syntopic galler congeners and clustered with those of parasitoids within a different wasp subfamily. Thus ovipositor tools show lability based on adaptive necessity, and are not constrained by phylogeny. Life-history traits such as fecundity, pre-adult and adult lifespan were studied for each wasp member of the community. Trade-offs in life-history traits were also investigated. Interspecific variation in life-history traits was observed. Gallers were pro-ovigenic (all eggs were mature upon adult emergence) whereas parasitoids were synovigenic (eggs matured progressively during adult lifespan). Initial egg load was correlated with body size for some species, and there was a trade-off between egg number and egg size across all species. Although all species completed their development and left the syconium concurrently, they differed in their adult and preadult lifespans. Providing sucrose solutions increased parasitoid lifespan but had no effect on the longevity of some galler species. While feeding regimes and body size affected longevity in most species, an interaction effect between these variables was detected for only one species. Life-history traits of wasp species exhibited a continuum in relation to their arrival sequence at syconia for oviposition during syconium development, and therefore reflected their ecology. The largest number of eggs, smallest egg sizes, and shortest longevities were characteristic of the earliest-arriving galling wasps at the smallest, immature syconia; the converse characterised the later-arriving parasitoids at the larger, already exploited syconia. Thus life-history is an important correlate of community resource partitioning and can be used to understand community structure. The comparative approach revealed constraints and flexibility in trait evolution. This is probably the first comprehensive study of life-history traits in a fig wasp community.