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Ecological Effects of the Invasive Parasite <I>Loxothylacus Panopaei

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Ecological Effects of the Invasive Parasite <I>Loxothylacus Panopaei Bull Mar Sci. 90(2):611–621. 2014 research paper http://dx.doi.org/10.5343/bms.2013.1060 Ecological effects of the invasive parasite Loxothylacus panopaei on the flatback mud crabEurypanopeus depressus with implications for estuarine communities 1 School of Coastal and Marine Kathryn A O’Shaughnessy 1 * Systems Sciences, Coastal Juliana M Harding 2 Carolina University, PO Box 2 261954, Conway, South Carolina Erin J Burge 29528-6054. 2 Department of Marine Science, Coastal Carolina University, PO Box 261954, Conway, South ABSTRACT.—The rhizocephalan barnacle Loxothylacus Carolina 29528-6054. panopaei (Gissler, 1884) is a parasitic castrator that infects xanthid crabs and is invasive on the US Atlantic coast. It was * Corresponding author email: introduced with infected crabs to Chesapeake Bay in the mid- <[email protected]>. 1960s, and has since expanded north to Long Island Sound, New York, and south to Cape Canaveral, Florida. Results of an 8-mo field study (January–August 2012) indicate mean monthly L. panopaei prevalence of 18.2% ± 6.2 (mean ± 95% CI; n = 66/384; monthly range 9.4%–30.3%) in Eurypanopeus depressus (Smith, 1869) in Clambank Creek, North Inlet, South Carolina. Prey consumption was compared between parasitized (externa-bearing) and unparasitized (externa- lacking) E. depressus 8–13 mm carapace width. Parasitized crabs (n = 43) consumed significantly fewer (median = 2) mussels (5–9 mm shell height) than unparasitized crabs (n = 29, median = 4) over 72 hrs, suggesting the ecological role of E. depressus may be modified. The parasite was only found in Date Submitted: 25 July, 2013. E. depressus 5.8–14.0 mm carapace width. Unparasitized E. Date Accepted: 27 December, 2013. Available Online: 26 February, 2014. depressus ranged from 2.3 to 17.0 mm carapace width. The Rhizocephala includes parasitic barnacles that castrate decapod crustaceans, including xanthid crabs. Parasitic anecdysis of the crab host results from infection (O’Brien and Van Wyk 1985), while endocrine and central nervous systems sustain damage from the parasitic internal rootlet system (Høeg 1995). This internal system ramifies throughout the host hemolymph, absorbs nutrients, and emerges from the crab abdomen as a reproductive sac called the externa (O’Brien and Van Wyk 1985). The rhizocephalan barnacle, Loxothylacus panopaei (Gissler, 1884), infects mud crabs and is native to coastal estuarine habitats from Cape Canaveral, Florida, south into the Gulf of Mexico and Caribbean waters as far east as Venezuela (Hines et al. 1997, Kruse and Hare 2007, Kruse et al. 2012). Infection with L. panopaei halts the molt- ing process, thereby inhibiting host growth (O’Brien and Van Wyk 1985). Parasitic castration removes the infected individual from the genetic pool, reducing its eco- logical success, and potentially lowering the effective population size (Van Engel et al. 1966, Daugherty 1969). Additionally, host feeding behavior may be compromised Bulletin of Marine Science 611 © 2014 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 612 Bulletin of Marine Science. Vol 90, No 2. 2014 by internal damage to host organs from the parasitic rootlet system (Høeg 1995) and the presence of the parasitic externa (Bishop and Cannon 1979). Loxothylacus panopaei is invasive along the US Atlantic coast where prevalence reports have ranged from 10% to 93% in the flatback mud crab, Eurypanopeus de- pressus (Smith, 1869) (e.g., Daugherty 1969, Kruse and Hare 2007, Freeman et al. 2013). Crabs infected with L. panopaei were transplanted from the Gulf of Mexico to Chesapeake Bay with oysters during the mid-1960s (Van Engel et al. 1966). Since then, L. panopaei has invaded western Atlantic habitats from Long Island Sound, New York, to just north of Cape Canaveral, Florida (Kruse and Hare 2007, Kruse et al. 2012, Freeman et al. 2013). Mud crabs exert top-down control within temperate intertidal oyster reefs (Silliman et al. 2004) because they are voracious consumers of bivalves including the eastern oyster, Crassostrea virginica (Gmelin, 1791) (e.g., McDermott 1960, Bisker and Castagna 1987) and the Atlantic ribbed mussel, Geukensia demissa (Dillwyn, 1817) (e.g., Seed 1980). In intertidal US Atlantic oyster reef habitats, E. depressus feeds on small bivalves (McDermott 1960, Kulp et al. 2011) and macroalgae in oyster cultch interstices (Meyer 1994). Kulp et al. (2011) found that E. depressus of 15.8 mm mean carapace width consumed 22.7 (SD 2.9) C. virginica (5.9 mm shell length) 96 hrs−1 crab−1 at 25 °C. McDermott (1960) observed E. depressus (16.4–22.9 mm cara- pace width) consumption of C. virginica (3–30 mm) at a rate of 1.6 C. virginica hrs−1 crab−1 at 23 °C. Community-level changes in intertidal oyster reef trophic structure may occur when parasites are prevalent (Mouritsen and Poulin 2002). Because L. panopaei is an invasive parasite, the effects on native host populations and related trophic structure are unknown but they potentially decrease native species abundance (Van Engel et al. 1966, Ruiz et al. 1997). The presence of L. panopaei on an oyster reef may impact predator (E. depressus) demographics, population size and, thus, the relative impor- tance of prey (bivalve) species. Investigations of L. panopaei in South Carolina waters are lacking. There has been only a single parasite prevalence study in South Carolina, which reported an ab- sence of L. panopaei in the 1980s (Hines et al. 1997). Recent parasite prevalence studies have been restricted mainly to Florida (Tolley et al. 2006, Kruse and Hare 2007, Kruse et al. 2012), North Carolina (Reisser and Forward 1991, Hines et al. 1997), Georgia (Hines et al. 1997, Kruse and Hare 2007, Kruse et al. 2012), Maryland, Virginia (Hines et al. 1997, Kruse and Hare 2007, Kruse et al. 2012), and New York (Freeman et al. 2013). While mud crab feeding rates have been studied (Seed 1980, Milke and Kennedy 2001, Kulp et al. 2011), feeding behavior in mud crabs parasitized by Loxothylacus species has not been examined, and little is known about the overall effects of the Rhizocephala on intertidal oyster reef food webs. The present study de- scribed parasite prevalence from E. depressus populations at Clambank Creek, North Inlet, South Carolina, and examined prey consumption in E. depressus infected with L. panopaei. Materials and Methods Parasite Prevalence.—Monthly (January–August 2012) xanthid crab (E. depressus and Panopeus herbstii H. Milne-Edwards, 1834) collections were made by hand (Hines et al. 1997, Kruse et al. 2012) from a natural fringing oyster reef in O’Shaughnessy et al.: L. panopaei reduces feeding in E. depressus 613 Clambank Creek (33°20.07´N, 79°11.52´W). Collection consisted of excavating all surface oyster cultch, buried shell, and aerobic sediment from a 0.25 m2 area. The excavated material was placed into a bin and the cultch was broken apart to ensure crabs of all sizes were captured. This process was repeated until approximately 100 crabs were collected, except between December and March when the target collection was set to 50 crabs because mud crabs have been found to be less dense intertidally (Dame and Vernburg 1982). All xanthid crabs present were collected (Hines et al. 1997) to avoid misidentification of E. depressus in the field and to confirm that L. panopaei infects only E. depressus in Clambank Creek. Crabs were returned to the laboratory where they were frozen for later examination. Water temperature (°C) and salinity were recorded monthly with a YSI 30 wa- ter temperature and salinity meter. Continuous water temperatures and salinities (January–August 2012) in Clambank Creek were also obtained from NOAA (http:// cdmo.baruch.sc.edu) to provide additional context for field temperature and salinity measurements. Crabs were identified to species and sexed based on external morphology in the laboratory (Williams 1984). Each crab abdomen was separated from the body and examined for an externa using a dissecting microscope. Crabs were classified as parasitized if an externa of any size (mature or virgin) was present. Maximum crab carapace width (CW) was measured to the nearest 0.1 mm using digital calipers. Feeding Experiments.—Laboratory feeding experiments were conducted in May and June 2012 in flow-through seawater tanks at the University of South Carolina Baruch Marine Field Laboratory, located in the North Inlet-Winyah Bay National Estuarine Research Reserve near Georgetown, South Carolina. Experimental E. de- pressus [range: 8–13 mm CW; median: 11.1 mm CW; mean: 11.0 (SD 1.5) mm CW] were collected by hand from oyster cultch in Clambank Creek, North Inlet. Mussels (G. demissa and Brachidontes exustus Linneaus, 1758, 5–9 mm shell length) were collected from pilings and among oyster cultch in Clambank Creek. Eurypanopeus depressus used in experiments were given at least 72 hrs to accli- mate to laboratory conditions and were maintained on natural, living oyster cultch in a flow-through seawater tank adjacent to and receiving the identical flow rate (19 L min−1) as the experimental tanks. Mussels were collected 1 wk before experimental runs, acclimated to laboratory conditions, and allowed to attach via byssal threads to matte ceramic tiles (95 × 95 mm) before placement in experimental containers. Source water was pumped from Oyster Landing in Crab Haul Creek, North Inlet (33°20.96´N, 79°11.35´W). Crab sex and species were assessed in the field and con- firmed with a dissecting microscope post experiments to minimize handling stress prior to experiments. Two treatments were used: unparasitized (externa-lacking) and parasitized (exter- na-bearing) E. depressus. The unparasitized treatment consisted of male E. depressus mud crabs (8–13 mm CW). Male E. depressus were used to avoid accidental inclusion of gravid females that feed at lower frequencies than nongravid crabs (Mantelatto and Christofoletti 2001).
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