Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant

Abstract

We studied the relationship between Hirtella myrmecophila (Chrysobalanaceae), a common but littlestudied Amazonian ant-plant that produces leaf-pouches as domatia, and its obligate ant partner, Allomerus octoarticulatus. Field observations revealed that H. myrmecophila drops domatia from older leaves, a characteristic that is unique among myrmecophytes. The physiological mechanism for abortion of domatia is currently unknown, but this characteristic allows for the existence, within the same plant, of branches with and without ants. Older branches generally bear only old leaves with no domatia and therefore have no ants, whereas younger branches have leaves of various ages. Ants forage mainly on new leaves, and experimental removal of ants showed that A. octoarticulatus is crucial for defense of these leaves against insect herbivores. However, A. octoarticulatus also acts as a castration parasite, severing the plant's inflorescences. Mature flowers and fruits were only found on older branches with no ants, and flower production was 8 times greater on plants whose ants were experimentally removed than on control plants. Given the reproductive costs inflicted by its mutualistic partner, we suggest that abortion of domatia is a strategy developed by H. myrmecophila to minimize the effects of cheating by A. octoarticulatus. These results support the view that evolutionary conflicts of interest between mutualistic species often impose selection for cheating on the partner, as well as for mechanisms to retaliate or to prevent super-exploitation. Opposing selection pressures, operating independently on the two partners, probably help to maintain the evolutionary stability of this mutualistic relationship.

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism

“…Our work further demonstrates that some "parasites" are actually beneficial partners when considered within the broader context of the mutualist assemblage. In our system, as in others (22,46), ant species identified as sterilizing "parasites" nonetheless can confer valuable protective benefits to host plants, often occupy host plants earlier in ontogeny, and are likely to be replaced by nonsterilizing ants as plants grow older. We show that when followed by nonsterilizing species later in ontogeny, these putative parasites can confer complementary benefits to plants.…”

“…In most ant-plant mutualisms, multiple ant species compete for housing and/or food provided by host plants in exchange for protecting those plants from herbivores, pathogens, or encroaching vegetation (18). In A. drepanolobium, as in many other ant-plant systems, the quality of services provided by individual ant associates is variable: Some species appear to exploit plants by taking up residence while providing little or no protection (19)(20)(21), and others sterilize their hosts (22)(23)(24)(25).…”

The Direct and Ecological Costs of an Ant-Plant Symbiosis

“…In Brazil, ants identified as A. octoarticulatus have been collected from Duroia saccifera, Hirtella myrmecophila, Hirtella physophora, Remejia physophora, and Tococa spp. (Wheeler 1942;Fonseca 1999;Izzo and Vasconcelos 2002;Fernández 2007). Although further work is needed to determine whether these collections represent a single species or a complex of closely related species (Fernández 2007), genetic data indicate that throughout the Peruvian Amazon the Allomerus ants found in C. nodosa are all from one species (Debout et al 2009).…”

“…Interacting with a mutualist can result in physical damage, such as the destruction of host reproductive structures by phytoecious ants (Yu and Pierce 1998;Stanton et al 1999;Izzo and Vasconcelos 2002;). This cost of mutualism is also thought to result in selection for defense (e.g., tolerance; Edwards and Yu 2008) more often than in selection for cheating (but see Izzo and Vasconcelos 2002).…”

“…Interacting with a mutualist can result in physical damage, such as the destruction of host reproductive structures by phytoecious ants (Yu and Pierce 1998;Stanton et al 1999;Izzo and Vasconcelos 2002;). This cost of mutualism is also thought to result in selection for defense (e.g., tolerance; Edwards and Yu 2008) more often than in selection for cheating (but see Izzo and Vasconcelos 2002). The evolution of specialization can be considered to be another cost of mutualism (e.g., Bronstein 2001) because the participants lose evolutionary flexibility, such as the ability to live independently or associate with a more beneficial partner.…”