Global patterns of the double mutualism phenomenon

Abstract

A double mutualism (DM) occurs when two interacting species benefit each other in two different functions, e.g. when an animal species acts both as pollinator and seed disperser of the same plant. Besides the double benefit, a DM also imposes a larger risk to both functions if the performance of one partner declines. We conducted the first global review of DMs involving pollinators and seed dispersers, aiming to: 1) assess their prevalence across ecosystems and biogeographical regions; 2) identify the main plant and animal taxa, and their traits, implicated in DMs; and 3) evaluate the conservation status of double mutualist species. We compiled published and unpublished DM records using specific search terms, noting the species involved, their conservation status and geographic location, as well as the type of study (species vs communitylevel) in which the DM was detected. We identified 302 DM cases involving 207 plant and 92 animal species from 16 mainland and 17 island areas. Most records come from tropical regions and islands. Animals included birds (62%), mammals (22%), and reptiles (16%), mostly opportunist species; only 18% were nectarivores. Plants were mainly fleshy-fruited shrub or tree species (59%) with actinomorphic flowers that were visited by several or many pollinator species (87%). Most (56%) DMs were detected in community-level studies. DMs are mostly prevalent in ecosystems with limited food resources and mutualist partners, and with high generalization levels. Nearly 30% of the species involved in DMs are threatened according to IUCN criteria, 68% of which are found on islands. The high prevalence of DM on islands paired with the threat status of island species suggest that the loss of a double mutualists and its cascading consequences may have a severe impact on community composition and functioning of fragile island ecosystems.

Evidence for a double mutualistic interaction between a lizard and a Mediterranean gymnosperm,Ephedra fragilis

“…Our study provides evidence that this plant–lizard relationship constitutes one of the five pollination/seed dispersal double mutualisms found around the World between an animal and a gymnosperm (Fuster et al 2018), besides representing the first double mutualism reported in the Mediterranean region. Although E. fragilis shows to be mainly pollinated by wind, we found that lizards, while obtaining energy resources from this gymnosperm, they are relevant for its reproduction as they (i) transport large amounts of pollen from male to female cones when feeding on pollination drops, (ii) increase the germination of light seeds and (iii) act as their main seed dispersers, at least on Dragonera Island (Rodríguez-Pérez et al 2012; Neghme et al 2017; this study).…”

“…Soriano and Ruiz 2002; Kelly et al 2004; Hansen and Müller 2009a; García et al 2012). Such phenomenon is known as ‘double mutualism’ (Hansen and Müller 2009a) and it appears to be especially frequent on island ecosystems, although a number of reports are also from mainland areas (Fuster et al 2018). One likely reason for the major prevalence of double mutualism on islands is the presence of species that compensate their densities, i.e.…”

“…Examples of trophic niche expansion have been observed in lizards, geckos, or even iguanas, which are most often carnivores or insectivores in the mainland, but consume floral and fruit resources in many islands, acting as potential pollinators and seed dispersers of a wide variety of plant species (Olesen and Valido 2003). Reptiles have indeed been found as important potential double mutualists worldwide, mainly in island ecosystems (Fuster et al 2018).…”

“…Vertebrates are the taxa most involved in double mutualism, although much remains to be investigated regarding how effective they are both as pollinators and seed dispersers of the same plant species (Fuster et al 2018). Studies in which both pollination and seed dispersal in the same species are simultaneously analysed are indeed rather scarce (Soriano and Ruiz 2002; Kelly et al 2004; Nyhagen et al 2005; Hansen and Müller 2009a; García et al 2012; Gomes et al 2014).…”

Ecological theory of mutualism: Models generalizing across different mechanisms

“…An interesting extension of our work would be to synthesize population dynamic behavior for "double mutualisms," in which there are two mechanisms of mutualistic benefit to a partner (Fuster et al 2019). Double mutualisms may play important ecological roles in ecosystems with limited resources, such as islands.…”