How to be an ant on figs

Highlights

• Ants and figs are both regarded as providing keystone functions in many forests.

• On monoecious figs ants are often associated with hemipterans, whereas in dioecious figs ants predominantly prey on fig wasps.

• By preying on non-pollinating wasps, ants often have a positive effect on pollinator production.

• In hemi-epiphytic figs, ants may also play an important role as seed dispersers.

• Relatively few fig species are true myrmecophytes, with domatia or food rewards for ants.

Abstract

Mutualistic interactions are open to exploitation by one or other of the partners and a diversity of other organisms, and hence are best understood as being embedded in a complex network of biotic interactions. Figs participate in an obligate mutualism in that figs are dependent on agaonid fig wasps for pollination and the wasps are dependent on fig ovules for brood sites. Ants are common insect predators and abundant in tropical forests. Ants have been recorded on approximately 11% of fig species, including all six subgenera, and often affect the fig–fig pollinator interaction through their predation of either pollinating and parasitic wasps. On monoecious figs, ants are often associated with hemipterans, whereas in dioecious figs ants predominantly prey on fig wasps. A few fig species are true myrmecophytes, with domatia or food rewards for ants, and in at least one species this is linked to predation of parasitic fig wasps. Ants also play a role in dispersal of fig seeds and may be particularly important for hemi-epiphytic species, which require high quality establishment microsites in the canopy. The intersection between the fig–fig pollinator and ant–plant systems promises to provide fertile ground for understanding mutualistic interactions within the context of complex interaction networks.

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.