Vol. 100: 149–158, 2012 DISEASES OF AQUATIC ORGANISMS Published August 27 doi: 10.3354/dao02507 Dis Aquat Org Contribution to DAO Special 6 ‘Disease effects on lobster fisheries, ecology, and culture’ OPENPEN ACCESSCCESS Epizootic shell disease in American lobsters Homarus americanus in southern New England: past, present and future Kathleen M. Castro1,*, J. Stanley Cobb1, Marta Gomez-Chiarri1, Michael Tlusty2 1University of Rhode Island, Department of Fisheries, Animal and Veterinary Sciences, Kingston, Rhode Island 02881, USA 2New England Aquarium, Boston, Massachusetts 02110, USA ABSTRACT: The emergence of epizootic shell disease in American lobsters Homarus americanus in the southern New England area, USA, has presented many new challenges to understanding the interface between disease and fisheries management. This paper examines past knowledge of shell disease, supplements this with the new knowledge generated through a special New Eng- land Lobster Shell Disease Initiative completed in 2011, and suggests how epidemiological tools can be used to elucidate the interactions between fisheries management and disease. KEY WORDS: Epizootic shell disease · Lobster · Epidemiology Resale or republication not permitted without written consent of the publisher INTRODUCTION 1992, Murray 2004). Changes in fishing policy may impact host biomass and disease dynamics. Knowl- The American lobster Homarus americanus (Milne edge about the epizootiology of ESD should be incor- Edwards) is an important component of the ecosys- porated into management strategies. The need to tem in southern New England (SNE) and supports a understand the impact of disease in this new era of valuable commercial fishery. Near the end of 1996, a emergent marine diseases is of utmost importance. new lobster disease, epizootic shell disease (ESD), This paper reviews existing and new knowledge emerged, affecting lobster in SNE. The disease pre- about ESD and suggests that a new emphasis be sented as deep shell lesions along the anterior dorsal placed on the interactions between disease and fish- carapace, rapidly spreading to all parts of the dorsal eries management. surface (Smolowitz et al. 2005). ESD subsequently spread spatially and temporally along the northeast coast of the United States (Castro & Somers 2012). SHELL DISEASE Errant American lobsters with shell disease were also captured in Norwegian waters (van der Meeren Past 2008). The American lobster stock in SNE is now classi- The term ‘shell disease’ is a general one, used to fied as overfished and in larval recruitment failure describe a wide range of erosive lesions, pits and/or (ASMFC 2010), and severe management options are discolorations in the cuticle of the exoskeleton of being considered that will affect the fishery. While crustaceans (Smolowitz et al. 2005, Cawthorn 2011). these management strategies are designed to ad - Shell disease is common in crustaceans. Generally dress the problems in the lobster stock, they may also thought to be caused by chitinoclastic or lipolytic affect the host−pathogen dynamics (Kuris & Lafferty bacteria, it is identified by discolored or eroded exo- *Email: [email protected] © Inter-Research 2012 · www.int-res.com 150 Dis Aquat Org 100: 149–158, 2012 skeleton re sulting in rust disease in red king crabs al. 2005) with irregularly shaped lesions attributed to Paralithodes camtschaticus and Tanner crabs Chio- several different fungi (Stewart 1980) and/or bacteria noecetes bairdi, burnt spot disease in the European (Rosen 1970, Sindermann 1991). crab Carcinus maenas, brown spot disease in shrimp Enzootic or endemic shell disease (EnSD) has been Neohelice granulata and just plain ‘shell disease’ in observed in fished lobsters for many years, but was blue crabs Callinectes sapidus and lobsters Homarus only recently recognized formally and named. It is americanus (Sindermann 1990). Typically, the bacte- characterized by light to moderate ‘pitting’ of lobster ria as sociated with the lesions are rod-shaped, chiti- shell (Cobb & Castro 2006), and in this respect may nolytic and gram-negative (Porter et al. 2001). Sin- be an analog of ISD. The number of affected individ- dermann (1991) emphasized that shell disease uals in any wild population has been relatively small, should be more accurately called a ‘syndrome’ char- and the relative impact on the affected population acterized by progressive exoskeletal erosion result- assumed to be insignificant. Typically, lobsters in ing from activity of chitinoclastic microorganisms, Rhode Island, USA, exhibited minor EnSD signs often affecting stressed crustaceans. Syndrome is a (monitored during a Rhode Island Department of general term defined as a collection of signs and Environmental Management trawl survey). EnSD symptoms known to frequently appear together but gave way, in the 1990s, to a much more aggressive without a known cause. The term ‘disease’ is more form characterized by extensive, melanized and specific and is defined as a disorder in a system or deep lesions of the carapace. The lesions appeared to organ that affects the body’s function and usually start in the dorsal area of the carapace just behind meets at least 2 of these criteria: recognized etiologic the rostrum and along the midline. This new and agent (cause); iden tifiable group of signs and symp- aggressive disease was first documented in Rhode toms; or consistent anatomic alterations. Island waters in 1997 (Castro & Angell 2000), and by Shell disease in Homarus americanus was first 2000 it was classified as an epizootic as it was widely described 75 yr ago in lobsters held for extended time distributed both temporally and spatially (Smolowitz periods at high densities in tidal impoundments et al. 2005). The appearance of this disease corre- (Hess 1937). This type of shell disease in lobster is sponded with record abundance levels for the SNE called ‘classical’ shell disease. Two types of classical lobster stock (ASMFC 2009) (Fig. 1). shell disease have been described: impoundment Fine-scale monitoring data records on ESD in disease (ISD) and burn/rust spot disease (BSSD). The Rhode Island coastal waters from 1994 to present early lesions of ISD are bilaterally symmetrical and show trends in prevalence, size, and sex (Castro & are centered around setal cores on the dorsum of Somers 2012). Larger males and females (> 80 mm the animal (Bullis et al. 1988). The disease is seen carapace length) were the first to show signs of the as melanized brown to black-colored erosions that disease, specifically ovigerous females that retain commence with the removal of epicuticle, extend their shells for longer periods of time. The inshore through the exocuticle and then the calcified endo- areas of Narragansett Bay showed the highest pre - cuticle, and in extreme cases, penetrate the non- valence, which was closely aligned with molting calcified endocuticle to the internal tissues (Smolo - periods that occurred in the late spring and early fall witz et al. 1992). The blackening or melanization (Castro & Angell 2000, Castro et al. 2006). There occurs as an inflammatory response and causes cross- were many reports of females with shell disease linking in the proteins in the layers of the carapace, molting with eggs still attached to the disfigured cast forming a wall that inhibits invasion by pathogens shell (Castro & Angell 2000). (Unestam & Ajaxon 1976, Lightner & Redman 1977). Initial studies by Chistoserdov et al. (2005) de - A common histological characteristic of ISD is a scribed ESD as a cuticular disease with no obvious scooped out appearance of the eroded cuticle (Smolo- implications of immune system failure or systemic witz et al. 2005). Damage to the exoskeleton is not problems. Some bacterial communities were identi- a prerequisite to shell damage, although it can be a fied, but the bacteria present in the lesions were not precursor (Stewart 1984). Malloy (1978) was able to primarily chitinoclastic. Other organisms apart from experimentally transmit ISD in H. americanus after bacteria found in the lesions were thought to be sec- abrasion under laboratory conditions (Getchell 1989). ondary invaders. Smolowitz et al. (2005) confirmed BSSD was first described from lobsters found in pol- that the pathology of the lesions differed from other luted areas (Ziskowski et al. 1996). The appearance shell disease types in that pillars of chitin remained of the spots both histologically and grossly is consis- while degradation occurred in the other polymers in tent with focal trauma to the carapace (Smolowitz et the carapace. Lobsters with ESD were found to have Castro et al.: Epizootic shell disease 151 40 40 Stevens (2009) also found evidence for increased Abundance 35 Shell disease prevalence 35 mortality in the laboratory during molting due to ) 6 complications of ESD. 30 30 ESD appeared to be spatially restricted to the SNE 25 25 area with occasional reports of low prevalence in the areas south of the Long Island Sound (LIS), deeper 20 20 offshore areas, the Gulf of Maine and Canadian 15 15 waters. Temperature was implicated as a factor in Prevalence (%) Prevalence ESD, lower temperatures limiting the spread of the 10 10 Total abundance (x 10 Total bacteria and increasing water temperature, causing 5 5 physiological stress leading to a more susceptible 0 0 host (Tlusty et al. 2007). Glenn & Pugh (2006) showed 1960 1970 1980 1990 2000 2010 a significant correlation between disease in Buzzards Year Bay and a series of warmer than average water tem- Fig. 1. Homarus