Original articleHow to be an ant on figs
Introduction
Mutualistic interactions are ubiquitous in nature, and are ecologically and evolutionarily important. However, the long-term exchange of resources between mutualistic partners attracts a large variety of other organisms that exploit the mutualism (Bronstein, 2001; Yu, 2001; Morris et al., 2003; Schatz et al., 2008). Hence, instead of isolated interactions, mutualisms are increasingly seen as being integrated within complex interaction networks (Blüthgen and Klein, 2011).
Among mutualistic interactions, the fig (Ficus) – fig pollinator interaction is often considered a model system (Herre and Jandér, 2010; Hossaert-McKey et al., 2010) and recent advances in the taxonomy of figs (Berg and Corner, 2005), their pollinators and non-pollinating fig wasps (NPFWs) (Cruaud et al., 2010, 2011) render easier investigations of the interactions among insect communities supported by figs. The interaction between figs and their pollinators have frequently been the subject of both evolutionary (Weiblen, 2002; Cook and Rasplus, 2003; Kjellberg et al., 2005; Dunn et al., 2008; Cruaud et al., 2010; Herre and Jandér, 2010) and ecological study (Harrison, 2005; Hossaert-McKey et al., 2010).
Figs are primarily tropical taxa and are an important component of tropical plant assemblages (Harrison, 2005). Ficus is also a globally diverse genus with at least 700 species (Berg, 1989; Berg and Corner, 2005). Several authors have suggested that figs are keystone resources in tropical forest because of the diversity of vertebrates that depend on their year-round production of fruits (Shanahan et al., 2001). Their ecological success is presumed to have arisen from the mutualistic association between figs and their pollinators; an interaction that is at least 60 Myrs old (Rønsted et al., 2005).
Mutualistic interactions are special cases of mutual exploitation in which both partners receive a net benefit in terms of reproductive success from the exchange (McKey and Hossaert-McKey, 2008). However, within the interacting populations, different individuals may receive net positive or negative payoffs. Moreover, the payoffs between mutualistic partners are often affected by other organisms (Yu, 2001; Bronstein, 2001, 2003; Morris et al., 2003; Ashman and King, 2005; Nahas et al., 2012).
In this review we focus on the interactions between figs and ants (Hymenoptera: Formicidae). Ants are a ubiquitous component of tropical forests and constitute a diversity of interactions with plants that range from obligate mutualism through parasitism. Ants occur widely on figs and are known to affect the interactions between figs and other symbionts, in particular their pollinating wasps. We explored the different types of interactions that have been studied between ants and figs, and discuss how these interactions may have affected coevolutionary processes between figs and their other symbionts.
There are over 12,000 ant species (Bolton et al., 2006) and these display an incredible range of feeding habits, associations with others species, in particular plants and other insects, and live in diverse habitats (Hölldobler and Wilson, 1990). It has been suggested that the radiation and success of ants in various ecosystems is due to the rise of the angiosperms, which released ants from a dependence on predation (Wilson and Hölldobler, 2005). In exchange for food rewards, ants often protect plants (Hölldobler and Wilson, 1990), but the interaction can be more complex when the same ants are tending sap-sucking insects (Huxley and Cutler, 1991; Moreira and Del-Claro, 2005). With respect to Ficus, ants are mobile actors that through their predatory behavior can alter the proportions of different wasp species that develop in fig syconia (Bronstein, 1988, 1991; Compton and Robertson, 1988, 1991; Zachariades, 1994; Cushman et al., 1998; Schatz et al., 2006; Harrison, 2014). Ants may also reduce herbivore pressure on fig leaves, act as seed dispersers or reduce seed dispersal through inhibiting feeding by vertebrate frugivores (Thomas, 1988). Ants are often observed on fig trees by researchers, but ecological studies have been limited.
Section snippets
The players
All fig species are engaged in an obligate and highly specific mutualistic interaction with agaonid wasps (Cruaud et al., 2010). Fig pollinators (Hymenoptera, Agaonidae, Agaoninae) are, with a few minor exceptions (Jouselline et al., 2001), the only pollen dispersers of the fig trees. Conversely, fig pollinators can only reproduce inside the inflorescence of their host fig (Galil and Eisikowitch, 1968; Cook and Rasplus, 2003; Harrison, 2005; Kjellberg et al., 2005). The fig has a unique closed
The presence of ants on Ficus
Ants and angiosperms are both the ecologically and numerically dominant groups in many environments, and have evolved alongside each other for 140–168 million years (Rico-Gray and Oliveira, 2007). Thus the ancestors of modern figs were probably already interacting with ants long before the fig pollination mutualism arose.
Eighty-two publications have described 48 ant genera present on 83 Ficus species (Table 1). Most records of ants on fig trees have come from Asia–Australasia (28 publications,
Ants nesting in fig trees
Arboreal ants are the most abundant and diverse arthropods in the tropics (Davidson and Pattrel-Kim, 1996). About 700 fig species are mainly tropical (Berg and Corner, 2005) However, of the total of 83 Ficus species covered in this review, only 19 species (23%) had reports of ants nesting. Subgenus Sycomorus had the highest proportion of species with records of nesting ants (5 species, 26% of the trees with nesting ants), followed by Urostigma and Sycidium (4 species each, 21%). No observations
Insect predation
Ants are considered to be omnivorous, but the proportion of the diet that is derived from animal prey varies hugely among ant subfamilies and genera. Ponerine ants feed more on animals than Formicine ants (Lach et al., 2010). Seventeen ant genera, predominantly belonging to the Pseudomyrmecinae and Ponerinae, have been recorded preying on fig wasps (Table 4). Ants have been recorded capturing pollinators and NPFWss during the emergence phase (Fig. 1d–e, Fig. 2b–c, Table 4). These include
Figs as ant–plants
Myrmecophytic plants have been defined as those offering specialized domatia or direct food rewards through specialized structures to ants (Webber et al., 2007). F. pisifera has hollow twigs with slit-like openings that are sometimes occupied by ants and can be defined as domatia (Fig. 2a, Maschwitz et al., 1994). Other species such as F. subpisocarpa (Bain et al., 2012) and F. paraensis (Davidson and Epstein, 1989) have a particular branch morphology that appears to encourage ant nesting, but
How figs may influence the behavior of ants
Ants can potentially provide a number of different services to figs, including protection of fig leaves against herbivory, dispersal of fig seeds and, perhaps most significantly for figs, protection of syconia against NPFWs (Dawkins and Krebs, 1979; Bronstein, 1991; Maschwitz et al., 1994; Schatz et al., 2006, 2008; Bain et al., 2012). Fig leaves are protected by latex and herbivore pressure appears to be low on most species in most places, although exceptions are sometimes observed. No
Chemical mediation of ant–fig interactions
Fig volatile signals change with syconia development and these changes are used by pollinating fig wasps and NPFWs to locate syconia at the correct phase of development for oviposition (Proffit et al., 2007, 2009; Ranganathan et al., 2010; Soler et al., 2012). This variation in odors emitted by figs can also potentially be used by ants to synchronize and enhance their predatory activity. In F. carica, F. fistulosa and F. racemosa ants learned to use the volatile organic compounds emitted by
Conclusions
Ants are a common component of invertebrate assemblages on fig trees in all tropical regions and across major evolutionary lineages. A broad diversity of ant subfamilies (48 genera) has been recorded on figs and at least 16 genera also nest in figs. Ants have been reported from about 11% of fig species (83 out of 735 species (Berg and Corner, 2005)) and about 3% (19 species) have records of ant nesting. However, these statistics are strongly constrained by the relative paucity of studies. At
Acknowledgments
Many thanks to several collaborators who participate to discussion around this work: Lien-Siang Chou, Bruno Di Giusto Martine Hossaert-McKey, Finn Kjellberg, Shang-Yang Lin, Samhan Nyawa, Magali Proffit, Jean-Yves Rasplus, Fabien Ravary and Catherine Soler. We also acknowledge the University of Brunei Darussalam for facilities of the National Taiwan University and CNRS (PICS N°935) and the ANR-NSC (ANR-09-BLAN-0392-CSD 7, NSC 99-2923-B-002-001-MY3) for grants permitting this study. RH was
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2018, Acta OecologicaCitation Excerpt :Considering the food rewards provided by fig trees and the heterogeneity of the ant colonization within a single studied population (Lin et al., 2016), F. benguetensis can be the first Ficus species to be categorized as a myrmecophilic species. Ant nests have been observed in approximately 24% of 86 studied species across all the Ficus subgenera (updated from Bain et al., 2014). Moreover, FEFNs are probably more common than are currently reported in the literature.
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2017, Advances in Botanical ResearchCitation Excerpt :Unfortunately, no studies have investigated the possible role of chemical mediation in this system. The OPM between figs and fig wasps is associated with numerous resources (galls, larvae, various insects used as prey, carbohydrates, etc.), which are exploited by many insect species, building a complex network of interactions (Fig. 4) (Bain et al., 2014; Bronstein, 1988; Schatz et al., 2006, 2008; Schatz, Proffit, et al., 2013; Wang et al., 2014; Zachariades, 1994). The majority of insects flying above the tropical forest canopy are linked to figs, and notably fig wasps (Harrison, 1996).