Bopyrid Parasite Infestation Affects Activity Levels and Morphology of the Eusocial Snapping Shrimp Synalpheus Elizabethae
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Vol. 431: 195–204, 2011 MARINE ECOLOGY PROGRESS SERIES Published June 9 doi: 10.3354/meps09123 Mar Ecol Prog Ser Bopyrid parasite infestation affects activity levels and morphology of the eusocial snapping shrimp Synalpheus elizabethae M. McGrew1, 2, K. M. Hultgren1, 3,* 1Department of Biology, Vassar College, Poughkeepsie, New York 12604, USA 2School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA 3Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, MRC 163, Washington, DC 20013, USA ABSTRACT: Sponge-dwelling snapping shrimps are often more heavily parasitized by bopyrid isopods than their free-living relatives, but little is known about how parasitism influences the be - havior and morphology of these shrimps. In this study, we measured parasitism rates in the eusocial snapping shrimp Synalpheus elizabethae and tested whether parasitism by bopyrid isopods (Bopyri- one sp.) affects shrimp activity levels and morphology. Using field surveys, we found that S. eliza- bethae suffer higher parasitism rates when inhabiting the sponge Lissodendoryx colombiensis than do co-occurring pair-forming congeners (S. yano and S. dardeaui) in the same host. In laboratory behavioral assays, parasitized S. elizabethae showed 50% lower activity levels than unparasitized colony members, suggesting that infection by bopyrids decreases shrimp activity. Finally, parasitism influenced shrimp morphology; parasitized S. elizabethae individuals were larger, but had relatively smaller major chelae (25% reduction) than unparasitized individuals. Parasites comprised ~5% of the entire body weight of an individual shrimp. Together these data suggest that parasitism by bopyrid isopods may incur significant energetic costs for commensal sponge-dwelling shrimps such as Synalpheus, and may be especially severe for social species such as S. elizabethae. KEY WORDS: Parasitism . Synalpheus elizabethae . Eusociality . Bopyridae . Morphology . Behavior Resale or republication not permitted without written consent of the publisher INTRODUCTION nutrition from their host sponge (Duffy 1996b, Mac- donald et al. 2006, Rios & Duffy 2007). Body size in Coral reefs are some of the most diverse marine these shrimps is closely correlated with the size of the ecosystems, and much of that diversity consists of spe- interior canals of the sponges they inhabit (Duffy 1992, cies involved in specialized relationships, e.g. smaller Hultgren & Duffy 2010). Appropriate sponge hosts are associate species living in larger ‘host’ species (Banner a limiting resource in the field (Macdonald et al. 2006), & Banner 1975, Bruce 1976). Such close physical asso- and living in sponges likely affords shrimps protection ciations can have strong morphological and population from generalist predators (Duffy 1996b, 2007). consequences for both partners in the relationship, Inhabiting a long-lived, valuable resource (the with important ecological and evolutionary implica- sponge host) is thought to be one of many factors facil- tions. Snapping shrimps in the genus Synalpheus itating the evolution of different types of reproductive (Decapoda: Caridea: Alpheidae) are a prime example; strategies in sponge-dwelling Synalpheus — specifi- in the Caribbean, most species belong to the S. gam- cally, the evolution of eusocial breeding strategies. barelloides species group, a monophyletic group of Members of the S. gambarelloides species group are >40 species that dwell exclusively in the internal unique in that they include the first described case of canals of sponges, and are thought to gain most of their eusociality in marine invertebrates (Duffy 1996a). *Corresponding author. Email: [email protected] © Inter-Research 2011 · www.int-res.com 196 Mar Ecol Prog Ser 431: 195–204, 2011 Eusocial Synalpheus live in colonies of 10s to 1000s of Here we examine effects of parasitism by branchial individuals, typically with reproduction limited to 1 (or bopyrid isopods on Synalpheus elizabethae, a eusocial a few) female ‘queen(s);’ non-breeding colony mem- species in the S. gambarelloides species group. S. eliz- bers serve an important, albeit indirect, role of enhanc- abethae often co-occur in individual sponges with 2 ing colony fitness by using their enlarged snapping congeneric species, S. yano and S. dardeaui, that typi- claw to aggressively fend off intruders and defend cally live in heterosexual pairs or in larger groups with their host sponge (Duffy et al. 2002, Toth & Duffy 2005, equal sex ratios (Macdonald et al. 2006). All 3 can be Duffy 2007). In S. regalis, there is evidence for further infected by branchial and abdominal bopyrid isopods. morphological differentiation among non-breeders; Despite relatively high incidences of parasitism in larger, more aggressive individuals with proportion- sponge-dwelling Synalpheus (up to 30% of a popula- ally larger fighting chelae spend more time near the tion parasitized; Duffy 1992), few studies have exam- periphery of the sponge (Duffy 2007, Toth & Duffy ined the effects of parasitism on Synalpheus. Hernáez 2008). et al. (2010) found that abdominal parasite infestation Although most work on Synalpheus has focused on decreased fecundity in S. yano (but did not inhibit the relative benefits of the sponge-dwelling and reproduction completely), and ovigerous female indi- group-living lifestyles, early work on Synalpheus doc- viduals of Synalpheus with abdominal or branchial umented one potential disadvantage to commensal liv- parasites are occasionally found in the field (K. M. ing in sponges. Duffy (1992) showed that sponge- Hultgren pers. obs.). Together these data suggest that dwelling Synalpheus had higher rates of parasitism by these parasites do not completely castrate their hosts. bopyrid isopods (Isopoda: Bopyridae) than did non- However, little is known about how abdominal bopy- sponge-dwelling species, possibly due to the high pop- rids affect eusocial species of Synalpheus, where ulation densities in sponge-dwelling populations. reproduction is limited to a few individuals (queen Bopyrid isopods have a complex life cycle. Larvae first shrimps are rarely parasitized; K. M. Hultgren unpubl. attach to an intermediate host (typically a calanoid data), or how branchial bopyrids affect shrimp activity copepod) and metamorphose into microniscus larvae levels or morphology. In this study, we focused on (O’Brien & Van Wyk 1985, Cash & Bauer 1993); micro- 3 questions: (1) do S. elizabethae experience different niscus larvae molt into free-swimming cryptoniscus parasitism rates compared to cohabiting non-social larvae (detached from the copepod) that seek out and species in the sponge Lissodendoryx colombiensis; (2) infect the definitive hosts, i.e. decapod crustaceans do branchial bopyrids (Bopyrione sp.) affect S. eliza- (Mark ham 1985, 2003). As adults, bopyrids feed on the bethae activity levels; and (3) do branchial bopyrids hemolymph of their hosts (O’Brien & Van Wyk 1985), affect S. elizabethae morphology? decreasing host growth (Anderson 1977, Jay 1989, Somers & Kirkwood 1991) and negatively affecting host metabolism (Anderson 1975). In caridean shrimps, MATERIALS AND METHODS bopyrids typically occur either in the abdominal region (hereafter ‘abdominal bopyrids’), or on the right or left Field surveys. We measured parasitism rates of side of the branchial cavity (‘branchial bopyrids’). Synalpheus elizabethae, S. yano, and S. dardeaui in Abdominal bopyrids often have strong effects on their the Bocas del Toro region of Caribbean Panama (2007 host’s reproductive system, reducing fecundity (Pike & to 2009). S. elizabethae typically occurs in 2 different Manton 1960, Hernáez et al. 2010) or causing partial to sponge host species in Bocas del Toro (Hymeniacidon full castration of their hosts (Allen 1966, O’Brien & Van caerulea and Lissodendoryx colombiensis), while S. Wyk 1985, Nakashima 1995, Calado et al. 2005). yano and S. dardeaui occur in L. columbiensis. H. Branchial bopyrids are thought to affect metabolism caerulea was collected at Boca del Drago (9° 25.28’ N, and activity levels through their effects on respiration 82° 20.56’ W), Isla San Cristobal (9° 18.03’ N, 82° (Anderson 1975, Bass & Weis 1999, Chaplin-Ebanks & 16.48’ W), Isla Pastores (9° 13.104’ N, 82° 19.485’ W), Curran 2005), but have also been shown to inhibit and Swan Cay (9° 27.08’ N, 82° 18.00’ W); L. colombien- reproduction (Pike & Manton 1960, Choi et al. 2004) sis was collected at Crawl Cay (9° 14.71’ N, 82° 8.60’ W) and to reduce the size of secondary sex characters in and in seagrass shallows north and south of STRI point their shrimp hosts (Beck 1980). Mature branchial bo - (9° 20.91’ N, 82° 15.74’ W). These collections were part pyrids are easily identified because they cause a char- of a set of standardized regional taxonomic surveys of acteristic bulge in the branchial region of the carapace sponge-dwelling Synalpheus (Macdonald et al. 2006, of the host. As such, branchial bopyrids may impede 2009, Hultgren et al. 2010). Sponges were collected at movement of sponge-dwelling Synalpheus, whose 2 to 19 m depth via snorkeling or SCUBA, kept in streamlined bodies closely match the canal dimensions running seawater for 1 to 4 h until processed, and of their sponge hosts (Hultgren & Duffy 2010). individually dissected until all macrofauna had been McGrew & Hultgren: Effects of parasitism on eusocial shrimps 197 removed. Live Synalpheus were identified and listed colonies) using laboratory behavioral assays (June as