Housekeeping mutualisms: do more symbionts facilitate host performance?

Adrian C Stier,Matthieu Leray,Michael A Gil,Suzanne C Mills,C Seabird Mckeon,Craig W Osenberg,Sarah Lemer

doi:10.1371/journal.pone.0032079

Abstract

Mutualisms often involve one host supporting multiple symbionts, whose identity, density and intraguild interactions can influence the nature of the mutualism and performance of the host. However, the implications of multiple co-occurring symbionts on services to a host have rarely been quantified. In this study, we quantified effects of decapod symbionts on removal of sediment from their coral host. Our field survey showed that all common symbionts typically occur as pairs and never at greater abundances. Two species, the crab Trapezia serenei and the shrimp Alpheus lottini, were most common and co-occurred more often than expected by chance. We conducted a mesocosm experiment to test for effects of decapod identity and density on sediment removal. Alone, corals removed 10% of sediment, but removal increased to 30% and 48% with the presence of two and four symbionts, respectively. Per-capita effects of symbionts were independent of density and identity. Our results suggest that symbiont density is restricted by intraspecific competition. Thus, increased sediment removal from a coral host can only be achieved by increasing the number of species of symbionts on that coral, even though these species are functionally equivalent. Symbiont diversity plays a key role, not through added functionality but by overcoming density limitation likely imposed by intraspecific mating systems.

Highlights

Mutualisms are widespread across taxa, contributing to the structure and function of ecosystems [1,2,3], especially when the mutualisms involve foundation species such as trees or stony corals
We developed an analytical approach similar to that used in ‘‘Multiple Predator Effect’’ (MPE) studies [11] to estimate the interactions between symbionts on sediment removal
The high frequency of corals occupied by just two species of symbionts was driven primarily by Trapezia serenei, which was positively associated with both species of alpheid shrimps (A. lottini and Synalpheus charon) (Fig. 1a)

Summary

Introduction

Mutualisms are widespread across taxa, contributing to the structure and function of ecosystems [1,2,3], especially when the mutualisms involve foundation species such as trees or stony corals. Experimental studies of predator-prey interactions have evaluated how the combined effects of two or more predator species compare to those predicted based upon pairwise effects of a single predator species [11]. These ‘‘multiple predator effect’’ studies evaluate if effects are independent (e.g., the predator species do not interact), synergistic (i.e., risk to prey is greater than expected), or inhibitory (e.g., predators incur intraguild predation or interference and risk to prey is reduced) [12]. Antagonism between pollinator species can reduce the pollination services provided to plants by subordinate pollinators [7]

Methods

Results

Conclusion