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Temporal Associations in Fig–Wasp–Ant Interactions

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Temporal Associations in Fig–Wasp–Ant Interactions DOI: 10.1111/j.1570-7458.2010.01038.x Temporal associations in fig–wasp–ant interactions: diel and phenological patterns Yuvaraj Ranganathan§, Mahua Ghara§ & Renee M. Borges* Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India Accepted: 24 June 2010 Key words: Apocrypta, Apocryptophagus, Ficus racemosa,gallers,Oecophylla smaragdina, Myrmicaria brunnea, parasitoids, predatory ants, resource partitioning, resource pulse, Technomyrmex albipes, tritrophic interactions Abstract In a complex multitrophic plant–animal interaction system in which there are direct and indirect interactions between species, comprehending the dynamics of these multiple partners is very impor- tant for an understanding of how the system is structured. We investigated the plant Ficus racemosa L. (Moraceae) and its community of obligatory mutualistic and parasitic fig wasps (Hymenoptera: Chalcidoidea) that develop within the fig inflorescence or syconium, as well as their interaction with opportunistic ants. We focused on temporal resource partitioning among members of the fig wasp community over the development cycle of the fig syconia during which wasp oviposition and devel- opment occur and we studied the activity rhythm of the ants associated with this community. We found that the seven members of the wasp community partitioned their oviposition across fig syco- nium development phenology and showed interspecific variation in activity across the day–night cycle. The wasps presented a distinct sequence in their arrival at fig syconia for oviposition, with the parasitoid wasps following the galling wasps. Although fig wasps are known to be largely diurnal, we documented night oviposition in several fig wasp species for the first time. Ant activity on the fig syconia was correlated with wasp activity and was dependent on whether the ants were predatory or trophobiont-tending species; only numbers of predatory ants increased during peak arrivals of the wasps. especially that of Springate & Basset (1996) who also inves- Introduction tigated taxa involved in multitrophic plant–insect interac- Spatio-temporal heterogeneity in resource availability and tions (e.g., parasitoids and ants preying upon insect quality can provide suitable axes for niche differentiation herbivores), seem to indicate that the night is a niche and thus coexistence of species (Schoener, 1974a). dimension that is not completely exploited. Even ephem- Although spatial resource partitioning has been investi- eral plant-based resources can support a diverse commu- gated to a considerable extent theoretically and empirically nity of insect species through a variety of coexistence (Schoener, 1974a; Amarasekare, 2003, 2008), the temporal mechanisms, which can include partitioning the same axis has received far less attention, whether across a resource at the same time (Haigh & Maynard Smith, 1972; resource’s life cycle or on a diel time scale (Schoener, Richards et al., 2000) or at different developmental stages 1974b; Carothers & Jaksic´, 1984; Kronfeld-Schor & Dayan, of the resource (Hackett-Jones et al., 2009). Thus, by tem- 2003). poral differentiation, the coexistence of mutualistic and In interactions between plants and insects, whether antagonistic insect species has been recorded in some spec- pollination or herbivory, the diel scale has rarely been ialised and ephemeral plant–seed predator systems which examined (Springate & Basset, 1996; Somanathan & Bor- include yucca ⁄ yucca moth (Pellmyr et al., 1996; Marr ges, 2001; Basset et al., 2003; Somanathan et al., 2006, et al., 2001), globeflower ⁄ globeflower fly (Pellmyr, 1989; 2008, 2009a,b; Wcislo & Tierney, 2009). These studies, Despre´s & Cherif, 2004; Pompanon et al., 2006), lar- ch⁄ larch fly (Sachet et al., 2006, 2009), and fig ⁄ fig wasp *Correspondence: E-mail: [email protected] interactions (Bronstein, 1991; Law et al., 2001; Cook & §Contributed equally to the paper. Rasplus, 2003; Herre et al., 2008; Ghara & Borges, 2010). Ó 2010 The Authors Entomologia Experimentalis et Applicata 137: 50–61, 2010 50 Journal compilation Ó 2010 The Netherlands Entomological Society 156 Temporal partitioning in fig–wasp–ant interactions 51 The fig⁄ fig wasp system is characterised by mutualistic species-specific (Cook & Rasplus, 2003; Marussich & and antagonistic wasp species developing within fig infl- Machado, 2007). The fig inflorescence (syconium) is typi- orescences called syconia (Cook & Rasplus, 2003; Herre cally globular; its development is divided into five phases et al., 2008). Although spatial and temporal patterns of (A–E) (Galil & Eisikowitch, 1968). In a typical fig, syconia resource utilisation in such ephemeral systems have been in the pre-receptive phase (A) are small and have imma- described (Kerdelhue´ & Rasplus, 1996; Anstett, 2001; ture flowers; in the B phase, PFWs enter the syconium, Proffit et al., 2007; Dunn et al., 2008; Elias et al., 2008; pollinate some female flowers, and oviposit into others to Ghara & Borges, 2010), the temporal associations form galls. Seeds and pollinators develop in galled flowers between all interacting species (mutualists, parasites, and in the inter-floral (C) phase. In the wasp dispersal (D) predators) have never been quantified, and their diel phase, pollinator males and females eclose, mate, and the activity patterns never investigated. For example, we do wingless pollinator males chew an exit hole for winged not know whether fig wasp species parasitising the same females who leave the syconium with pollen from male development stage of the fig syconium partition their flowers to enter another receptive syconium (usually on activity in the diel time axis, and thereby avoid competi- another tree, as developmental phases of fig syconia are tion. Furthermore, the temporal activity of mutualists generally synchronised within a tree) to re-commence the and antagonists in these systems may also be influenced cycle. Males usually die within their natal syconium. After by the activity of opportunistic predators such as ants pollinators disperse, syconial properties (colour, odour) (or vice versa) (Schatz et al., 2008; Ranganathan & change (E phase) to attract seed dispersers (Borges et al., Borges, 2009). This makes the inclusion of several trophic 2008). During development, the syconium and syconial levels important in the analysis of activity patterns of spe- wall change from small, thin-walled syconia in the A phase cies comprising such a community on an ephemeral to large, thick-walled syconia in later phases. resource. This development cycle is subject to parasitism by Because multitrophic temporal activity patterns and other chalcidoid wasps. These non-pollinating fig wasps associations in such ephemeral plant–seed predator ⁄ para- (NPFWs) are also highly host-specific (Jousselin et al., site systems have rarely been simultaneously examined and 2008; but see Marussich & Machado, 2007; Silvieus et al., quantified (Snell & Addicott, 2008), we investigated the 2008). Non-pollinating fig wasps usually oviposit into the possibility of temporal niche partitioning across short- syconium from the outside using long ovipositors; they term (diel) and long-term (resource phenology) scales in a are flower-gallers, inquilines, or parasitoids of other fig fig–wasp–ant interaction system. Using a reasonably spe- wasps or of each other, and can attack syconia at various cies-rich community of fig wasps and ant predators in a developmental stages (Proffit et al., 2007; Elias et al., common fig species, Ficus racemosa L. (Moraceae, Section 2008; Wang & Zheng, 2008; Ghara & Borges, 2010). Thus, Sycomorus) in India, which has been a model system in several wasp species compete for brood space in the syco- our laboratory (e.g., Ranganathan & Borges, 2009; Ghara nium. Details of the type of parasitism are scarcely known & Borges, 2010; Krishnan et al., 2010), we asked the fol- and the hosts of most parasites still remain speculative lowing questions: (1) What is the arrival pattern of fig (Cook & Rasplus, 2003; Herre et al., 2008). Non-pollinat- wasps across the fig syconium (inflorescence) develop- ing fig wasp females usually leave the syconium in the mental cycle? (2) What is the diel activity pattern of fig D phase through the exit hole chewed by wingless polli- wasps and ants on the fig syconia? (3) What are the tempo- nator males, although there are exceptions to this pattern. ral associations between wasps and between wasps and Pollinators and NPFWs use, at long distances, volatile ants over the syconium developmental phases? and (4) compounds produced by syconia to locate figs appropri- Does the association between wasp and ant activity pat- ate for oviposition (Grison-Pige´ et al., 2002; Proffit et al., terns translate into greater predation by ants on certain 2007). The nature of the short-distance cues used by wasp species? To our knowledge this is the first study to externally ovipositing NPFWs to locate potential hosts simultaneously examine arrival sequence in fig wasps and within syconia is still unknown. ants over 24 h of the day, as well as across the entire devel- opment of fig syconia. The study system The study was conducted on six trees of the monoecious F. racemosa within the campus of the Indian Institute of Materials and methods Science (12°58¢N, 77°35¢E), Bangalore, India. This fig spe- Natural history of the fig wasp community cies bears cauliflorous syconia and produces 5–6 flower ⁄ The interaction between figs and their pollinating fig wasps fruit crops each year with the phenology of the syconium (PFWs)
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