Decline and Local Extinction of Caribbean Eusocial Shrimp

J Emmett Duffy,Kristin M Hultgren,Tin Chi Solomon Chak,Dustin R Rubenstein,Kenneth S Macdonald Iii

doi:10.1371/journal.pone.0054637

J Emmett Duffy, Kristin M Hultgren + Show 3 more

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https://doi.org/10.1371/journal.pone.0054637

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Abstract

The tropical shrimp genus Synalpheus includes the only eusocial marine animals. In much of the Caribbean, eusocial species have dominated the diverse fauna of sponge-dwelling shrimp in coral rubble for at least the past two decades. Here we document a recent, dramatic decline and apparent local extinction of eusocial shrimp species on the Belize Barrier Reef. Our collections from shallow reefs in central Belize in 2012 failed to locate three of the four eusocial species formerly abundant in the area, and showed steep declines in colony size and increases in frequency of queenless colonies prior to their disappearance. Concordant with these declines, several nonsocial, pair-forming Synalpheus species increased in frequency. The decline in eusocial shrimp is explained in part by disappearance of two sponge species on which they specialize. Eusocial shrimp collections from Jamaica in 2012 showed similar patterns of decline in colony size and increased queenlessness compared with prior Jamaican collections. The decline and local extinction of eusocial shrimp happened against a backdrop of changes in coral assemblages during recent decades, and may reflect changes in abundance and quality of dead coral substratum and succession of the diverse cryptic organisms living within it. These changes document potentially worrisome declines in a unique taxon of eusocial marine animals.

Highlights

Tropical reefs are widely recognized as centers of marine biodiversity [1]
SIMPER revealed that the strongest contributors to changing shrimp assemblages through time were the eusocial species S. filidigitus, S. chacei, and S. regalis, as well as the nonsocial pair-forming species S. bousfeldi, which together accounted for 45% of the dissimilarity between collections in 2012 and in prior years
Most notable was the eusocial shrimp S. filidigitus, a dominant species on shallow reefs in the Sand Bores, which occurred in roughly half of the samples and comprised 54% of all shrimp collected prior to 2012, but was completely absent in 2012

Summary

Introduction

Tropical reefs are widely recognized as centers of marine biodiversity [1]. The corals that build them have been well studied, as have the charismatic and ecologically important fishes they support. Within the porous reef structure of dead corals, algae, mollusks, and other organisms lives a rich variety of largely invisible organisms of every phylum Most of these species are poorly known they comprise the bulk of marine biodiversity. Comparative studies in Belize showed that eusocial Synalpheus species were more abundant, used a wider range of host species, and were less likely to share the host with congeners, than were their less social relatives [6]. This dominance by eusocial species may be facilitated by the benefits of cooperative nest defense [9]. Eusocial species have dominated the diverse faunas of cryptic sponge assemblages in several Caribbean areas since our collections began nearly a quarter century ago [5,10,11]

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