Callinectes Sapidus) Populations Across Louisiana, USA
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This authors' personal copy may not be publicly or systematically copied or distributed, or posted on the Open Web, except with written permission of the copyright holder(s). It may be distributed to interested individuals on request. Vol. 114: 1–10, 2015 DISEASES OF AQUATIC ORGANISMS Published May 11 doi: 10.3354/dao02854 Dis Aquat Org Prevalence and distribution of three protozoan symbionts in blue crab (Callinectes sapidus) populations across Louisiana, USA Holly A. Rogers1, Sabrina S. Taylor1, John P. Hawke2, Julie A. Anderson Lively1,* 1School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana 70803, USA 2School of Veterinary Medicine, Louisiana State University, Baton Rouge, Louisiana 70803, USA ABSTRACT: Louisiana has one of the largest blue crab (Callinectes sapidus) fisheries in the USA, but little is known about blue crab diseases, parasites, and symbionts in this area. In 2013–2014, large juvenile and adult blue crabs were collected at 4 diverse sites to determine the prevalence of the protozoan symbionts associated with black gill disease (Lagenophrys callinectes), buckshot crabs (Urosporidium crescens), and bitter crab disease (Hematodinium perezi). A high aggregate prevalence of L. callinectes (93.2%) was identified across all seasons at all 4 collection sites regardless of salinity. A moderately low aggregate prevalence of U. crescens (22.4%) was identi- fied across all seasons and sites. Prevalence of U. crescens depended on site salinity, with only 10% of infections detected at sites with <6.3 ppt salinity, and no infections detected at the low salinity site. While L. callinectes and U. crescens are commensal parasites of blue crabs, infections can result in unmarketable and unappealing meat. In the Louisiana fishery, H. perezi has been blamed circumstantially for adult mortalities in the low salinity nearshore fishing grounds. Despite this, H. perezi was not detected in any of the large crabs sampled, even from the low salinity sites. The prevalence data reported here for these 3 protozoans are the first to include blue crabs sampled seasonally at multiple locations along the Louisiana coast over the period of a year. KEY WORDS: Crab symbionts · Callinectes sapidus · Protozoans · Hematodinium · Urosporidium · Lagenophrys Resale or republication not permitted without written consent of the publisher INTRODUCTION ing to consumers. L. callinectes is a commensal, lori- cated ciliate that infests blue crab gills and is shed The prevalence of diseases, parasites, and sym- during ecdysis (Couch 1967, Couch & Martin 1982, bionts of the blue crab Callinectes sapidus Rathbun, Shields & Overstreet 2007, Mayen-Estrada & Agui- 1896, has not been determined in many regions of lar-Aguilar 2012). It has been hypothesized that its natural distribution range including the Gulf of heavy L. callinectes infestations can impair respira- Me xi co. While protozoan symbionts such as Lage - tory ability and in some circumstances can asphyxi- no phrys callinectes (Peritrichida: Lagenophryidae), ate crabs (Couch 1966, 1967, Couch & Martin 1982, Uro sporidium crescens (Haplosporida: Anurosporidi - Shields & Overstreet 2007). Infestations with L. call- idae), and Hematodinium perezi (Peridiniales: Syn- inectes can cause brown or black discoloration of the diniaceae) are known to occur in Gulf blue crabs, gills (Couch 1967) and result in a syndrome colloqui- their prevalence has not been examined. ally called black gill disease. L. callinectes and U. crescens are usually innocu- U. crescens hyperparasitizes blue crabs by infect- ous to the blue crab, but can have a negative eco- ing the trematode Microphallus basodactylophallus nomic effect when infected crabs appear unappetiz- (Perkins 1971, Couch 1974, Messick & Sindermann *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 2 Dis Aquat Org 114: 1–10, 2015 1992). Uninfected trematodes are lightly colored, waters (Messick & Sindermann 1992, Messick 1998), approximately one-third of the size of infected trema- but its prevalence in crabs inhabiting low salinity copy todes, and more resistant to rupture than infected estuaries such as Lake Pontchartrain, Louisiana (LA), trematodes (Perkins 1971, Couch 1974, Shields & USA, have not been investigated. While H. perezi Overstreet 2007). Infected trematodes are easily rec- has not been recorded in wild crabs inhabiting sites ognized as large black spots in the muscle, hepa - with water salinities <11 ppt, it has been shown Author topancreas, and ventral ganglia of affected crabs that experimentally that infections established in higher are described colloquially as pepper spot or buckshot salinity water where the hypothesized transmissive crabs (Couch 1974, Messick & Sindermann 1992). dino spore is active can be maintained when crabs U. crescens is not pathogenic to the crab, but has the are moved to low salinity water (Newman & Johnson ability to reduce but not eliminate mobility of the 1975, Messick & Shields 2000, Coffey et al. 2012). infected trematode, with spores released upon their Regardless of the abiotic factors dictating H. perezi rupture (Perkins 1971, Couch 1974). prevalence, H. perezi has been blamed for adult H. perezi is a parasitic dinoflagellate found in crab mortalities in the low salinity, nearshore LA fishing hemolymph and tissues. Infection reduces hemocyte grounds. numbers as well as hemocyanin density in hemo - Little is known about protozoan symbionts of blue lymph, thus reducing its oxygen transport ability, and crabs inhabiting LA despite it often having the high- lyses cells in hepatopancreas and muscle tissues (Tay- est commercial catches in the USA, with a dockside lor et al. 1996, Shields & Squyars 2000, Shields et al. value in 2012 of $43.1 million (National Marine Fish- 2003). Infected crabs are typically lethargic and pos- eries Service 2013). Research on parasites of blue sess milky or chalky-white hemolymph with reduced crabs inhabiting the Gulf of Mexico has been spo- clotting ability (Newman & Johnson 1975, Shields et radic and geographically limited. Following the al. 2003). Lethargy and reduced feeding activities can Deepwater Horizon oil spill in 2010, this lack of lead to crab death due to starvation (Taylor et al. 1996, knowledge became evident when processors, fisher- Stentiford et al. 2000, Shields et al. 2003). H. perezi men, and shedding facilities reported higher than has been associated with mass mortality in several average die-offs and higher disease and parasite crab species as well as with decreased commercial prevalence (J. A. Anderson Lively & J. P. Hawke un - landings of blue crabs along the US East Coast (Mes- publ. data). Some of the mortalities were attributed sick & Shields 2000, Shields 2003). tentatively to H. perezi and L. callinectes even The prevalence of L. callinectes, U. crescens, and though salinities were too low for H. perezi. How- H. perezi varies based on water temperature. Be - ever, with no baseline data available for the region, cause L. callinectes is lost during molting, prevalence fisheries managers and researchers could not deter- of this ciliate should be highest in adult crabs that mine whether disease or parasite prevalence had molt infrequently and particularly at sites with low increased due to the environmental damage. To water temperatures (Guillory et al. 2001). However, determine the consequences of future natural and unlike the US East Coast, its prevalence in the Gulf of anthropogenic impacts on parasite prevalence and to Mexico has not been highly correlated with water more fully understand reasons for declines in com- temperature as they tend to stay high year-round mercial landings, our goal was to examine the preva- (Shields & Overstreet 2007). U. crescens hyperpara- lence of L. callinectes, U. crescens, and H. perezi in sitization has not been found to vary seasonally in blue crabs caught at 4 sites along the LA coast crabs sampled along the US East Coast in autumn through 2013 to the beginning of 2014. and winter (Messick 1998). H. perezi epizootics along the US East Coast vary seasonally, peaking in autumn and declining in winter when water temper- MATERIALS AND METHODS atures are <9°C (Messick et al. 1999, Lee & Frischer 2004). This seasonality has not been established in Sample collection crabs inhabiting the Gulf of Mexico. Parasite prevalence can also vary with salinity. As Four field sites in Louisiana (LA), USA, were se lec - L. callinectes is hypothesized to be the most common ted for crab collection: Lake Pontchartrain (30° 12’ commensal parasite of blue crabs (Shields & Over- 55’’ N, 89° 45’ 0’’ W), Grand Isle (29° 14’ 19’’ N, 90° 0’ street 2007), its prevalence might not vary based on 11’’ W), Cocodrie (29° 21’ 3’’ N, 90° 37’ 34’’ W), and salinity. U. crescens hyperparasitization has been Rockefeller Wildlife Refuge (29° 41’ 26’’ N, 92° 49’ documented in crabs inhabiting moderately saline 53’’ W) (Fig. 1). These sites vary from low salinity at Rogers et al.: Blue crab protozoan symbionts 3 Lake Pontchartrain to high salinity at Grand Isle YSI 63-10FT Handheld Salinity, Conductivity and (Table 1). Temperature System. To remove daily and diel varia- copy To assess parasite prevalence, crabs were collected tions in water temperatures within a season, data seasonally at each site (Table 1). Sampling occurred were averaged from water monitoring stations near in 2013 to 2014 with winter 1 referring to 2013 and each site (east to west): (1) Rigolets