Obvious Invaders and Overlooked Infauna: Unexpected Constituents of the Decapod Crustacean Fauna at Twin Cays, Belize Darryl L. Felder, Peter C. Dworschak, Rafael Robles, Heather D. Bracken, Amanda M. Windsor, Jennifer M. Felder, and Rafael Lemaitre ABSTRACT. Decapod crustaceans in the vicinity of Carrie Bow Cay and Twin Cays, Belize, have been under study for more than 25 years. Large collections have been as- sembled, and new species have been discovered. The effort has included photographic documentation of coloration, yielding characters of value in identifi cation of problematic tropical taxa. Measurements of diversity have been markedly enhanced by extraction corer (yabby pump) sampling in shallow subtidal sediments, especially at Twin Cays. This technique revealed species, genera, and families of thalassinidean decapods not pre- viously known from the region. Studies continue on the ecological roles of these burrow- ers, dominant bioturbators in seagrass beds where they produce conspicuous mounds of sediment and constitute a major infaunal biomass at Twin Cays. By contrast, famil- iar large reptant decapods typically dominate shallow rocky substrates. Within the past four years, however, the nonindigenous portunid crab Charybdis hellerii has extensively invaded large portions of hard substrates at Twin Cays. In 2007, it was found to domi- nate cavities under coral heads in survey areas along the northeastern and southwestern shorelines, possibly displacing populations of large Mithrax, Menippe, Callinectes, and Panulirus previously found there in abundance. INTRODUCTION Fieldwork centered on Carrie Bow Cay and surrounding habitats, including Darryl L. Felder, Rafael Robles, Heather D. a variety of settings at Twin Cays. The effort continues work by the fi rst author Bracken, Amanda M. Windsor, and Jennifer M. in collaboration with the late Ray Manning in 1983, as well as work by the late Felder, Department of Biology and Laboratory Brian Kensley during the 1980s and early 1990s (Kensley, 1981, 1996). Early for Crustacean Research, University of Louisiana efforts produced abundant grass-bed and reef-crest species generally identifi able at Lafayette, Lafayette, Louisiana 70504-2451, with known Caribbean taxa, along with small cryptic forms obtained by cutting USA. Peter C. Dworschak, Naturhistorisches open sponges, breaking rubble, poisoning in situ, or using several narcotants to Museum in Wien, Burgring 7, A-1014 Wien, Aus- drive out small decapods from rubble isolated in containers. Rich collections tria. Rafael Lemaitre, Department of Invertebrate Zoology, National Museum of Natural History, that have accumulated in the the Smithsonian Institution’s National Museum of MRC 163, Smithsonian Institution, Washington, Natural History were fi xed in formalin, limiting their value in genetic analyses. D.C. 20013-7012, USA. Corresponding author: Efforts in 2002 and 2007 shifted emphasis to varied intertidal and subtidal habi- D. Felder ([email protected]). Manuscript tats of Twin Cays and to resampling the regional fauna to obtain alcohol-fi xed received 13 May 2008; accepted 20 April 2009. materials for molecular genetic analyses. 111_Felder_181-188_Lang.indd1_Felder_181-188_Lang.indd 118181 99/24/09/24/09 99:49:00:49:00 AAMM 182 • SMITHSONIAN CONTRIBUTIONS TO THE MARINE SCIENCES Concerted effort has been made to photographically and its macrocrustacean associates was a targeted effort. document coloration of fresh specimens, given the value These decapods were captured from under pieces of dead of color in the identifi cations of tropical species and the subtidal coral and debris that were lifted while snorkeling long-term goal of producing a guidebook for the regional over and adjacent to seagrass (Thalassia) beds in water 1– 2 decapod fauna (DLF and RL, in progress). More than 260 m deep. Sampling of most thalassinideans and related deca- decapod species have been enumerated in our collections pod burrowers was accomplished with a suction extrac- from the Carrie Bow Cay region, some yet to be named. tor (yabby pump) and bag-sieve while wading, snorkeling, Under U.S. National Science Foundation AToL “Deca- or SCUBA diving in water 0.5– 4 m deep. In addition to pod Tree of Life” support, molecular and morphological collections of Glypturus acanthochirus (Callianassidae) systematic studies are under way concerning alpheid and by suction extractor, some specimens of this species were other caridean shrimps, paguroid hermit crabs, thalassini- obtained with “weighted line” traps (de Vaugelas, 1985). dean shrimps, and panopeid, portunid, grapsoid, pinnoth- Specimens of Axiopsis serratifrons (Axiidae) were ob- erid, and majoid crabs, as well as family-level relationships tained by baiting animals to the apertures of their burrows, among all major decapod groups. Work incorporating where they were captured by cutting off the burrow or by porcelain crab collections from the region has been pub- spearing the specimens. Casts of burrows were made as lished (Rodríguez et al., 2005, 2006) as has work by other described by Dworschak and Ott (1993). Specimens were investigators on some alpheid shrimp groups (Duffy, 1996; immobilized by immersion in chilled seawater or by nar- Duffy and Macdonald, 1999; Duffy et al., 2000, 2002; cotization with clove oil before photography. Photographs Macdonald et al., 2006; Ríos and Duffy, 2007). Previous of specimens immersed in a pan of seawater were made collections of upogebiid thalassinidean shrimp from Be- with a Fuji Fine Pix S1Pro digital camera equipped with a lize were included in Williams (1993). Several descriptions 60 mm macrolens while the subject was lighted by a com- of new species from our Belize collections have also ap- bination of direct and refl ected sunlight or high-intensity peared (Goy and Felder, 1988; Manning and Felder, 1996; 5000°K fl uorescent photographic lamps. All specimens Felder and Manning, 1997), but many species remain to were subsequently preserved in several exchanges of 95% be described. The second author has been involved in nondenatured ethanol and then stored in 75% nondena- several ecological studies of the infaunal decapods of the tured ethanol. Photographic voucher specimens were ar- region (Dworschak and Ott, 1993; Abed-Navandi and chived in the Zoological Collections of the University of Dworschak, 2005; Dworschak et al., 2006). Louisiana at Lafayette (ULLZ), and most other materials Our protracted fi eld sampling program has in some were deposited in the Smithsonian Institution–National cases allowed us to observe apparent changes in com- Museum of Natural History (USNM). Some collections munity composition. In a striking example, shallow sub- by the second author (especially thalassinideans) were de- tidal habitats at Twin Cays have been recently invaded posited in the Naturhistorisches Museum in Wien, Austria by the nonindigenous swimming crab Charybdis hellerii (NHMW) and the Muséum National d’Histoire Naturelle, (A. Milne-Edwards, 1867), previously unreported from Paris, France (MNHN). For fi gured specimens, size is indi- Belize. Recurrent trips have also provided opportunities cated as carapace width (cw) or carapace length (cl). for shallow subtidal sampling and burrow-casting of fos- sorial infauna in turtle grass (Thalassia) beds along shore- lines of Twin Cays, revealing unexpected thalassinidean RESULTS AND DISCUSSION diversity. A brief account of these latest efforts is our pres- INVASION BY CHARYBDIS HELLERII ent focus, preliminary to more comprehensive treatment of the full decapod assemblage. Large bottom debris (waterlogged wood, discarded building materials, dead coral heads) typically provides cover for large reptants such as spiny lobsters (Panulirus MATERIALS AND METHODS spp.), swimming crabs (Callinectes spp.), stone crabs (Me- nippe spp.), and large spider crabs (Mithrax spp.), espe- Sampling included the breaking of dead coral and cially in shallow well-lighted waters. Sampling of these conch shell rubble, netting, extraction of sediments, and environments at both Carrie Bow Cay and Twin Cays in sorting through hard-surface fouling organisms, but sam- October 2002 revealed no large decapods other than these pling of large crabs such as Charybdis hellerii (Brachyura) genera. That same year, however, a small specimen of the 111_Felder_181-188_Lang.indd1_Felder_181-188_Lang.indd 118282 99/24/09/24/09 99:49:01:49:01 AAMM NUMBER 38 • 183 nonindigenous portunid crab Charybdis hellerii was found Sampling was thereafter shifted to dead coral heads in an empty conch shell on the inshore side of Carrie Bow scattered among turtle grass beds on the northeast side of Cay, the fi rst such occurrence recorded in our sampling Twin Cays. A crude survey was there undertaken for coral program. heads in 1– 1.5 m depths, each head roughly 0.5– 0.7 m in In April 2007, sampling under large pieces of cover at diameter and separated from one another by roughly 6– 15 Twin Cays was undertaken to obtain fresh materials of the m. Of the 25 coral heads inspected, 13 were uninhabited aforementioned resident genera for genetic analyses. Initial by large reptant decapods, 8 harbored large specimens of sampling centered in the vicinity of the “Fisheries Camp” C. hellerii (Figure 1b), and four harbored only Menippe on the southeastern end of Twin Cays, where a storm had nodifrons Stimpson, 1859 (Figure 1a). Large single indi- scattered sheets of metal building siding from the shore- viduals of C. hellerii were found under 6 of the 25 heads line to depths of nearly 2 m. Inspections beneath 20 such that were lifted, a mating pair of C. hellerii was found sheets across this entire range of depths revealed none of under a single head, and a specimen of C. hellerii together the target species but at least seven variously sized indi- with a large specimen of M. nodifrons was found under an- viduals of the nonindigenous swimming crab C. hellerii. other head. No specimens of Mithrax spp., Callinectes spp., FIGURE 1. a, Stone crab Menippe nodifrons, male, 69.7 mm carapace width (cw), Twin Cays, Belize 10 April 2007, ULLZ 8991. b, Invasive Indo-Pacifi c swimming crab Charybdis hellerii, male, 75.3 mm cw, Twin Cays, Belize, 10 April 2007, ULLZ 8990.