N27 2018 Northeastern Naturalist Notes Vol. 25, No. 4 D.B. Carlon, et al. A First Report of Shell Disease Impacting Cancer borealis (Jonah Crab) in the Bay of Fundy David B. Carlon1,*, Patrick Warner1, Clay Starr1, David J Anderson1, Zakir Bulmer1, Hugh Cipparone1, Jesse Dunn1, Caroline Godfrey1, Claire Goffinet1, Miranda Miller1, and Charlotte Nash1 Abstract - Several shell diseases are impacting a variety of decapod crustaceans in southern New England, but have rarely been reported in the colder waters of the eastern Gulf of Maine. Here we document a possible outbreak of shell disease impacting Cancer borealis (Jonah Crab) on Kent Island, NB, Canada. On low tides of 31 August 31–3 September 2017 we found hundreds of Jonah Crabs stranded above the tide line and resting on top of the dense canopies of fucoid algae. Closer inspection of exoskeletons revealed the clinical signs of classical shell disease: dark circular patches and lesions that penetrated the cuticle. A sample of 30 stranded Jonah Crabs revealed that 28 (93%) were adult females. On the next low tide, we found the same pattern of exposed Jonah Crabs and observed numerous instances of Larus smithsonianus (Herring Gull) predation. Continuous monitoring of shallow-water temperatures over the last 3 years revealed that average daily summer temperatures have been regularly exceeding a shell-disease threshold of 12 °C on Kent Island. Between 13 September and 31 October 2015 there were 19 days with an average water temperature above 12 °C and 43 days during the same interval in 2016. Introduction. In the Northeast Atlantic, various forms of shell disease commonly infect Homarus americanus H. Milne-Edwards (American Lobster) from southern New England, with rates of epizootic shell disease as high as 40% (Castro et al. 2012). Shell-disease syndrome includes a number of diseases that break down the cuticle of crustaceans, including an older disease, termed classical shell disease, first described in the 1970s, and a newer disease that appeared in the 1990s in southern New England known as epizootic shell disease (reviewed by Vogan et al. 2008). In both diseases, chitinolytic bacteria colonize the epicuticle and eventually cause lesions that entirely penetrate all layers of the cuticle, leading to systematic bacterial infections, interference with molting, and death (Smolowitz et al. 1992). Demographic data suggest that slower-growing individuals, including reproductive females, are more susceptible to the negative effects of shell disease, due to the fact that molting frequency is too low to rid the organism of early infection (Glenn and Pugh 2006). In comparison to southern New England, cases of shell disease remain less frequent in the colder waters of the Gulf of Maine. The Maine Department of Marine Resources (MDMR) reported that the incidence of shell disease in American Lobster has been increasing since 2009. The prevalence of infection in 2016 was 1.25% in the Gulf of Maine west of the Penobscot River, and 0.5% in the colder waters east of the Penobscot River (MDMR 2016). It is noteworthy that nearly all of these infected American Lobsters were females or very large males. Although outbreaks of shell diseases are thought to be triggered by multiple environmental factors, temperature has been identified as a key physical driver, and epizootic shell disease becomes common when the maximum monthly mean bottom temperature ≥12 °C (Shields 2013). There is great concern that shell diseases could spread to the lucrative American Lobster fishery if the Gulf of Maine continues to warm over the next 50 y. Maynard et al. (2016) modeled a bottom-temperature threshold of 12 °C in 1Schiller Coastal Studies Center and Bowdoin College, 6500 College Station, Brunswick, ME 04032. *Corresponding author - dcarlon@bowdoin.edu. Manuscript Editor: Thomas Trott Notes of the Northeastern Naturalist, Issue 25/4, 2018 2018 Northeastern Naturalist Notes Vol. 25, No. 4 N28 D.B. Carlon, et al. southern New England and the Gulf of Maine, and predicted that some regions in the eastern Gulf of Maine including the Bay of Fundy and Nova Scotia would have a high probability of exceeding this threshold for ≥7 days during September 2015, and that the bottom waters of the entire eastern Gulf of Maine will regularly exceed 12 °C within the next 20 y. Perhaps due to smaller fisheries and less data, there is limited information on outbreaks of shell diseases in other crustaceans, but they have been reported in a wide variety of shrimp and decapod families (Wang 2011). Of particular relevance to the observations reported here is a well-studied outbreak of classical shell disease in a related species, Cancer pagurus L. (Brown Crab) in the UK (Vogan et al. 2002), where prevalence has exceeded 50% over the last few decades (Powell and Rowley 2005). Observations and temperature data. We report observations from Kent Island during low tides between 31 August and 3 September 2017. Kent Island is 1 of 3 small islands located south of Grand Manan, NB, Canada. On a student field trip, we surveyed sites on eastern and western shores, but found the highest numbers of Cancer borealis (Stimpson) Figure 1. The clinical signs of shell disease infecting Cancer borealis (Jonah Crab) on Kent Island, Bay of Fundy. (A) Stranded individual on the fucoid canopy at low tide. (B) Shell-disease lesions on a left chela indicated by yellow arrows. The lesion marked “P” has penetrated the cuticle. (C) A large, penetrating lesion on the ventral surface of a carapace margin. (D) Remains of a stranded crab eaten by Herring Gulls. N29 2018 Northeastern Naturalist Notes Vol. 25, No. 4 D.B. Carlon, et al. (Jonah Crab) at a site on the wave-exposed eastern shore (44°34'42.59''N, 66°45'12.00''W), a short walk from the Kent Island Scientific Station operated by Bowdoin College. Adult Jonah Crabs were conspicuous everywhere above the low-tide line, and easy to recognize by their bright pink shell color, which contrasted with the dark background of fucoid algae (Fig. 1A). We collected 30 adult individuals from an area of ~400 m2 for closer examination, and found they had dark plaques on the carapace, walking legs, and pleopods. Some crabs had developed shell-penetrating lesions on the ventral surface of the carapace and chela (Fig. 1B, C). Interestingly, of this sample of 30 randomly collected Jonah Crabs, 28 were female. We returned to this same site at low tide on 1 September, and again found many female Jonah Crabs above the tide line with the same clinical signs of shell disease. By the end of the tidal cycle, stranded Jonah Crabs were easy prey for Larus smithsonianus Coues (Herring Gull), resulting in an intertidal landscape of dead and dismembered Jonah Crabs (Fig. 1D). To determine how often shallow-water temperatures on Kent Island have been exceeding shell disease thresholds, we used continuous temperature data from a TidbiT® watertemperature data-logger (Onset Computer Corporation, Bourne, MA) installed on a low intertidal rock bench (5 m depth below mean high water) at the same site where we observed and sampled diseased crabs. This data logger has been recording temperature at 30-min intervals since 13 September 2015. After filtering low-tide aerial temperatures, we calculated the daily mean, maximum, and minimum for the entire data set. We determined the number of days between 13 September and 31 October where the mean temperature was >12 °C for the years 2015 and 2016. We found that there were 19 and 43 such days in 2015 and 2016, respectively. Further, the majority of days (79 d) during the months of August, September, and October of 2016 exceeded this threshold (Fig. 2). Discussion. The plaques and lesions we observed on Jonah Crabs from Kent Island are consistent with classical shell disease (Vogan et al. 2008), but accurate diagnosis will require further assays of the microbial communities that are breaking down the shell (Shields 2013). Occasional cases of shell-disease syndrome were reported by Malloy (1978) from lobster pounds in Nova Scotia, Canada. Currently, shell-disease syndrome appears to be Figure 2. Water temperature from an intertidal site on the eastern shore of Kent Island, recorded from a TidBit® data logger attached to a rock bench at 5 m below mean high water. Temperature was logged every 30 min, and daily watertemperature mean (solid line), maximum (dashed line), and minimum (dotted line) are presented. The heavy horizontal bar marks a 12 °C temperature threshold that was exceeded for 79 days during 2016. 2018 Northeastern Naturalist Notes Vol. 25, No. 4 N30 D.B. Carlon, et al. uncommon on decapods in the Bay of Fundy, including American Lobster (Russell Ingalls, fisherman, Grand Manan, NB, Canada, pers. comm.). Similarly, reports of shell disease infecting Jonah Crabs in the eastern Gulf of Maine are absent (Brian Beal, University of Maine, Machias, ME, pers. comm.). Our temperature data indicate that shallow-water temperatures on Kent Island are favorable for shell-disease outbreaks. We observed 79 days with shallow-water temperatures ≥12 °C during the summer of 2016, supporting the predictions of Maynard et al. (2016). While our intertidal temperatures are from shallow water, they may also represent deeper benthic habitats along Kent Island because of the strong effect of tidal mixing in the Bay of Fundy on bottom water temperature (Townsend et al. 1987). Working in southern New England, Glenn and Pugh (2006) hypothesized that increases in water temperature can increase infection rates of shell disease in female American Lobster because females reach maturity earlier, after which they grow slowly, resulting in longer molting intervals and fewer opportunities to rid themselves of disease. The fact that nearly all Jonah Crabs with clinical signs of shell disease from Kent Island were large females is consistent with their extended molting-interval hypothesis. However, a more recent experimental study showed that increases in temperature from 10 °C to 15 °C can increase the susceptibility to epizootic shell disease in juvenile American Lobsters, which have short molting intervals (Tlusty and Metzler 2012). More-intensive sampling of all life-history phases, combined with quantitative scores of lesion development (e.g., Stevens 2009) are required to confirm whether the clinical signs of shell disease are more common on large, female Jonah Crabs. Kent Island is one of the largest Herring Gull breeding sites in eastern Canada (Ronconi and Wong 2003) and aerially exposed Jonah Crabs were highly susceptible to Herring Gull predation. If disease is impacting the behavior of these crabs by making them more susceptible to predation, it could contribute to top-down control of community structure (Ellis et al. 2007, Lubchenco and Menge 1978). 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