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Scaphanocephalus-Associated Dermatitis As the Basis for Black Spot Disease in Acanthuridae of St

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Scaphanocephalus-Associated Dermatitis As the Basis for Black Spot Disease in Acanthuridae of St Vol. 137: 53–63, 2019 DISEASES OF AQUATIC ORGANISMS Published online November 28 https://doi.org/10.3354/dao03419 Dis Aquat Org OPENPEN ACCESSCCESS Scaphanocephalus-associated dermatitis as the basis for black spot disease in Acanthuridae of St. Kitts, West Indies Michelle M. Dennis1,*, Adrien Izquierdo1, Anne Conan1, Kelsey Johnson1, Solenne Giardi1,2, Paul Frye1, Mark A. Freeman1 1Center for Conservation Medicine and Ecosystem Health, Ross University School of Veterinary Medicine, St. Kitts, West Indies 2Department of Sciences and Technology, University of Bordeaux, Bordeaux, France ABSTRACT: Acanthurus spp. of St. Kitts and other Caribbean islands, including ocean surgeon- fish A. bahianus, doctorfish A. chirurgus, and blue tang A. coeruleus, frequently show multifocal cutaneous pigmentation. Initial reports from the Leeward Antilles raised suspicion of a parasitic etiology. The aim of this study was to quantify the prevalence of the disease in St. Kitts’ Acanthuri- dae and describe its pathology and etiology. Visual surveys demonstrated consistently high adjusted mean prevalence at 3 shallow reefs in St. Kitts in 2017 (38.9%, 95% CI: 33.8−43.9) and 2018 (51.5%; 95% CI: 46.2−56.9). There were no differences in prevalence across species or reefs, but juvenile fish were less commonly affected than adults. A total of 29 dermatopathy-affected acanthurids were sampled by spearfishing for comprehensive postmortem examination. Digenean metacercariae were dissected from <1 mm cysts within pigmented lesions. Using partial 28S rDNA sequence data they were classified as Family Heterophyidae, members of which are com- monly implicated in black spot disease of other fishes. Morphological features of the parasite were most typical of Scaphanocephalus spp. (Creplin, 1842), and 2 genetic profiles were obtained sug- gesting more than 1 digenean species. Histologically, pigmented lesions had mild chronic perivas- cular dermatitis and increased melanophores and melanin density, often centered on encysted digenean metacercariae. In 1 affected A. chirurgus, similar metacercariae were histologically identified in skeletal and cardiac muscle. Further research is needed to clarify impact on host fitness, establish the number of heterophyid digenean species that cause black spots on Carib- bean fishes and to determine the intermediate and definitive host species. KEY WORDS: Scaphanocephalus · Black spot disease · Heterophyidae · Dermatitis · Dermatopathy · Digenean · Pigment 1. INTRODUCTION Diplostomatidae and Heterophyidae in temperate and tropical freshwater fishes (Gratzek 2010, Poyn- Pigmented dermatopathies of fishes, presenting as ton & Hoffman 2010). In contrast, most reports of focal black circular spots or papules, are often associ- black spot disease in marine tropical fish implicate ated with cutaneous endoparasites. Metacercariae of turbellarians rather than digenean metacercariae digenean trematodes that encyst in the dermis are (Cannon & Lester 1988, Justine et al. 2009). Further- particularly common etiologies of so-called ‘black more, pigmented skin lesions may also be noninfec- spot disease’, including Cryptocotyle lingua (Family tious, resulting, for example, from previous skin Heterophyidae) in costal cold-water marine fishes injury or from neoplasia of chromatophores (Work & (Poynton 2010), and several parasites of the Families Aeby 2014). © Ross University School of Veterinary Medicine, Adtalem *Corresponding author: [email protected] Global Education 2019. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 54 Dis Aquat Org 137: 53–63, 2019 Members of the Family Acanthuridae, including selected because of known prevalence of Acanthuri- ocean surgeonfish Acanthurus bahianus (also re - dae, previous observation of the black spot disease, ferred to as A. tractus, Bernal & Rocha 2011), doctor- and accessibility from the shoreline. fish A. chirurgus, and blue tang A. coeruleus, are A 1 h timed swim, covering approximately 0.7 to herbivores prevalent on Caribbean reefs. They play a 1.0 km, was conducted at each survey site, once in key role in structuring benthic communities through July 2017 and again in July 2018. The surveys were macro algae grazing (Burkepile & Hay 2010, Marshell completed by 2 observers, one in 2017 and the other & Mumby 2015). Their depletion can have detrimen- in 2018. Each were similarly trained and used the tal impacts on coral reefs by favoring the competitive same methods in order to reduce intra-operator vari- growth of macroalgae over coral (Edwards et al. ability. Surveys were undertaken only when visibility 2014, Adam et al. 2015). was >15 m. The snorkeler surveyed the reef unidi- A pigmented dermatopathy affecting Caribbean rectionally with attention focused towards oncoming reef fish, especially Acanthuridae, was recently re - fish to minimize resighting bias. Each observed indi- ported that involved several regions across the Car- vidual of Acanthurus spp. within around 2.5 to 3.0 m ibbean (Bernal et al. 2016, Eierman & Tanner 2019, of either side of the observer was recorded. A. bahi- Elmer et al. 2019). Prevalences in acanthurids have anus was distinguished by uniform body color, A. ranged from around 12% (Bernal et al. 2016) to 60% chirurgus by the presence of 10 to 12 vertical bars on (Eierman & Tanner 2019, Elmer et al. 2019). The the body, and A. coeruleus by its overall bright blue disease was initially assumed to be the result of color. Fish were classified as juveniles or adults cutaneous parasitism and turbellarians were first based on estimated size (<~7 cm or ≥~7 cm, respec - suspec ted (Bernal et al. 2016). More recently, the tive ly). A. coeruleus juveniles were further distin- der matopathy has been demonstrated to occur in as - guished by a yellow body or yellow tail. A size refer- sociation with encysted metacercariae of the hetero- ence previously applied to objects of known size at a phyid Scaphanocephalus expansus (Creplin, 1842) in variety of distances was used to help classify juvenile 10 species of reef fish in Bonaire (Kohl et al. 2019). fish. For each individual, designation of black spot The geographical extent of this infection is unknown disease was recorded. Designation of black spot dis- although one other report from the Caribbean exists, ease was based on the presence of 1 or more fairly involving a gray snapper Lutjanus griseus from the discrete dark brown to black circular cutaneous Florida Keys (Overstreet & Hawkins 2017). It is lesion(s). Lesion severity score was recorded for each unclear if the same etiology is the basis for the pig- fish, based on the number of lesions on 1 side: appar- mented dermatopathy at locations other than Bon - ently healthy (none, score 0); mild (1 to 5 lesions, aire. In addition, the histopathology of Scaphano - score 1); moderate (6 to 10 lesions, score 2); or severe cephalus infection has not yet been described and is (>10 lesions, score 3). important for understanding the extent to which the While conducting the surveys, or while sampling parasite impacts its host. fish for postmortem examination, any clinical signs The objective of this study was to gauge the preva- associated with the dermatopathy were recorded. lence of the pigmented dermatopathy in Acanthuridae of St. Kitts and to describe its pathology and etio logy. 2.2. Postmortem examination 2. MATERIALS AND METHODS Since surgeonfish showing the pigmented dermato - pathy were not for sale at the fish market, affected 2.1. Surveys fish were sampled by spearfishing. A total of 29 surgeonfish showing the pigmented dermatopathy The Federation of St. Kitts and Nevis is a 2 island (13 A. bahianus, 10 A. coeruleus, and 6 A. chirurgus) nation in the Leeward Islands of the Lesser Antilles. were sampled from White House Bay, the study site Surveys were conducted on 3 shallow coastal patch most conducive to spearfishing, over 6 fishing expe- reefs in St. Kitts: Timothy Beach (17.277° N, 62.685° W), ditions from November 2017 through June 2018. Reggae Beach (17.228° N, 62.631° W), and White Where death was not instantaneous, fish were House Bay (17.253° N, 62.659° W). These reefs reflect humanely euthanized by cervical transection with similar confluent habitats separated from one an - a sharp knife, followed by pithing, in accordance other by <10 km of shoreline, each at <10 m depth with Ross University Institutional Animal Care and with rocky and sandy substrata. These areas were Use Committee approval (protocol approval number Dennis et al.: Acanthurid black spot disease 55 17.07.34). Fish were transported to the laboratory on with LSU5, product 840 bp). All reactions had an - ice and a postmortem examination was conducted nealing temperatures of 55°C and extension times of within 3 h of sampling. For control fish, 4 A. bahi- 1 min, and were repeated for 40 cycles. PCR products anus, 5 A. coeruleus, and 3 A. chirurgus that lacked of the expected sizes were visualized on agarose gels skin lesions and were apparently healthy were pur- and recovered from the remaining PCR products chased from a fish market, part in September 2017 using a GeneMATRIX PCR products extraction kit and the remaining in November 2018. Information (EURx). Sequencing reactions were performed using about the location from which they were collected BigDyeTM Terminator cycle sequencing chemistry was not available. utilizing the same oligonucleotide
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