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Muscular Microsporidian Infection in Arctic Char Salvelinus Alpinus from Two Lakes in Nunavik, Quebec, Canada

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Muscular Microsporidian Infection in Arctic Char Salvelinus Alpinus from Two Lakes in Nunavik, Quebec, Canada Vol. 144: 209–220, 2021 DISEASES OF AQUATIC ORGANISMS Published online May 27 https://doi.org/10.3354/dao03593 Dis Aquat Org OPEN ACCESS Muscular microsporidian infection in Arctic char Salvelinus alpinus from two lakes in Nunavik, Quebec, Canada Marion Jalenques1, Justin Sanders2, Lilian Tran3, Laurie Beaupré4, Michael Kent2, Stéphane Lair1,* 1Centre québécois sur la santé des animaux sauvages / Canadian Wildlife Health Cooperative, Faculté de médecine vétérinaire, Université de Montréal, St. Hyacinthe, Quebec J2S 2M2, Canada 2Carlson College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, USA 3Makivik Corporation, Kuujjuaq, Quebec J0M 1C0, Canada 4Direction de la gestion de la faune du Nord-du-Québec Ministère des Forêts, de la Faune et des Parcs, Chibougamau, Quebec G8P 2Z3, Canada ABSTRACT: Arctic char Salvelinus alpinus is an important cultural and subsistence resource for Inuit communities. Muscular infections by microsporidia were diagnosed for the first time in Arctic char originating from 2 different lakes in Nunavik (Quebec, Canada). The consumption of these infected fish was associated with digestive tract disorders in people. To better characterize microsporidiosis in these char populations, a cross-sectional study was conducted on 91 fish. The microsporidium was classified as a member of the Microsporidium collective genus by morpholog- ical evaluation and phylogenetic analysis using small subunit ribosomal DNA sequence data. The presence and severity of infection were determined histologically. Microsporidian infection occurred in 61% of the fish (56/91) and was significantly associated with an increase in their age, length and weight. The severity of infection (percentage of muscle area affected by microsporidia) was mild in most cases (<1% of the total muscle area). Based on multiple linear regression mod- eling, the severity of infection was significantly greater in females and negatively correlated with the body condition. Despite a high prevalence, the low pathogenicity of the infection suggests that microsporidiosis has little impact on these char populations. Moreover, since digestive-tract dis - orders following ingestion of fish infected by microsporidia have never been reported in humans, it seems unlikely that it was responsible for the reported clinical signs. Anisakid larvae are occasionally observed in these char populations. Digestive-tract infection associated with inges- tion of these larvae should thus be considered as a potential differential diagnosis in these Inuit communities. KEY WORDS: Microsporidia · Salvelinus alpinus · Arctic char · Myositis · Nunavik · Anisakis · Zoonosis 1. INTRODUCTION where they occur as both anadromous and resident freshwater (landlocked) populations (Fisheries and Arctic char Salvelinus alpinus, teleosts from the Oceans Canada 2014, Kuhnlein & Humphries 2017, family Salmonidae, are found in lakes, rivers and Martyniuk et al. 2020). This fish species is an impor- coas tal saltwater across northern North America, tant part of the traditional Inuit diet and is consumed © The authors 2021. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 210 Dis Aquat Org 144: 209–220, 2021 raw, boiled, dried or fermented in local communities study were to (1) determine the prevalence of mi- (Kuhnlein & Humphries 2017). Muscular infections crosporidiosis in Arctic char populations from Lakes by microsporidia (microsporidiosis) have been oppor- Duquet and Françoys-Malherbe, (2) characterize the tunistically documented in Arctic char from Lake lesions caused by this organism, (3) evaluate the as- Duquet located near Salluit, Nunavik, Quebec, Can- sociation between the infection and fish characteris- ada (Wildlife Health Intelligence Platform, Canadian tics such as body condition and (4) elucidate the taxo- Wildlife Health Cooperative). These fish, which were nomic status of this novel infection. Potential causes harvested by fishermen from local communities, of the symptoms reported by Inuit following the con- were submitted in response to the occurrence of var- sumption of raw fish will also be discussed. ious symptoms including vomiting and oral-tingling sensations, following consumption of raw char flesh. Similar symptoms have also been reported in people 2. MATERIALS AND METHODS fishing in the nearby Lake Françoys-Malherbe. These occurrences took place in spring (April) or summer 2.1. Study area and sampling (September). The prevalence of the parasite, its sig- nificance for the health of this population of fish and This project was realized from 1−7 May 2018, in its zoonotic potential are unknown. collaboration with regional stakeholders including Microsporidia are obligate sporulating intracellular the Makivik Corporation, the Ministère des Forêts, parasites related to Fungi. This group includes over de la Faune et des Parc (MFFP) and Raglan Mine. 1000 species able to infect a broad spectrum of hosts, Fish were obtained from Lake Duquet (Tasialujjuaq) from unicellular organisms to vertebrates, including (62° 03’ 18’’ N, 74° 31’ 51’’ W) and Lake Françoys- humans (Lom 2002, Stentiford et al. 2016). Although Malherbe (Pangaligiak) (62° 00’ 06’’ N, 74° 15’ 25’’ W). infections by these organisms are relatively common These lakes, which are 7.7 × 1 km and 25 × 1−1.5 km in fish, most species are poorly described and new in size, respectively, are located in proximity to the species are regularly discovered. Species in the gen- community of Salluit, Nunavik (Quebec, Canada) era Heterosporis, Pleistophora, Kabatana, Tetrami- and used by the local fishermen. Both freshwater cra, Myosporidium and in the collective group Micro - lakes outflow into Deception Bay (Hudson Strait) via sporidium are known to infect the skeletal muscles of the Deception River. Even if anadromous and land- susceptible teleost fish hosts (Kent et al. 1999, 2014, locked char populations inhabit these lakes, the Lom 2002, Ahonen 2017). It is believed that most fish present study involves char from the anadromous microsporidia complete their life cycle within a sin- population only. Anadromous Arctic char at Decep- gle host, through horizontal transmission by inges- tion Bay only feed out at sea, where they prey oppor- tion of infected tissues or spores in the water. In addi- tunistically on zooplankton and pelagic and benthic tion, some species of microsporidia include vertical fishes (Martyniuk et al. 2020). (intraovum) transmission in their life cycles (e.g. For this study, sampling took place in the spring Pseu doloma neurophilia: Sanders & Kent 2013; Ovi - when anadromous Arctic char are fasting (Martyniuk pleistophora ovariae: Kent et al. 2014). With horizon- et al. 2020). A total of 91 Arctic char, 61 from Lake tal transmission, microsporidia that infect muscle Duquet and 30 from Lake Françoys-Malherbe, were enter the intestinal wall and reach the muscles where captured respectively by gill nets and fishing lines they multiply (merogony) and produce new spores set under the ice cover as part of planned subsistence (sporogony) that will be released into the tissues or fishing by local elders. Once captured, the fish were the external environment (Lom 2002, Miller 2009, stunned, pithed and stored in an isolated cooler to Kent et al. 2014). The infection may cause significant prevent them from freezing. Morphological meas- muscle damage and contribute to indirect fish mor- urements and macroscopic examination were per- tality due to debilitation or increased susceptibility to formed on the day of capture. Sex, age (otolith analy- predation (Sprengel & Lüchtenberg 1991, Figueras et sis; Campana & Thorrold 2001), fork length, weight, al. 1992, Miller 2009, Kent et al. 2014, Phelps et al. and Fulton’s condition factor K were determined for 2015). In addition, heavy infections of the muscle each fish. Fulton’s condition factor was defined by often cause macroscopic changes that diminish the K = 100 × total weight / (fork length)3 with the weight value of the fish for human consumption (Toma - in grams and the fork length in centimeters (Ricker michel et al. 2018). 1975). Characteristics of the sampled fish are pre- Here we describe a microsporidian infection in Arc- sented in Table 1. A complete post-mortem examina- tic char in 2 lakes in Nunavik. The objectives of this tion, including thorough inspections of filleted mus- Jalenques et al.: Muscular microsporidian infection in Arctic char 211 Table 1. Characteristics of the Arctic char Salvelinus alpinus sampled in this study. Arctic char were captured respectively by gill nets and jig fishing lines set under the ice cover from Lake Duquet and Lake Françoys-Malherbe, located near the com- munity of Salluit, Nunavik, Canada. Fulton’s condition factor defined as: K = 100 × total weight / (fork length)3, with total weight in grams and fork length in centimeters Duquet (n = 61) Françoys-Malherbe (n = 30) Total (n = 91) Sex Female 36 22 58 (64%) Male 25 8 33 (36%) Age (yr)a 10 ± 1 (7−15) 9 ± 2 (5−14) 10 ± 2 (5−15) Fork length (cm)a 46.1 ± 12.9 (42.9−66.3) 51.6 ± 6.3 (19.5−70.4) 49.8 ± 9.3 (19.5−70.4) Total weight (g)a 1449 ± 583 (786−3108) 1125 ± 763 (63−2522) 1341 ± 662 (63−3108) Fulton’s K a 1.01 ± 0.10 (0.67−1.22) 0.93 ± 0.13 (0.61−1.10) 0.98 ± 0.12 (0.61−1.22) Presence of internal helminths 32 (52%) 16 (53%) 48 (53%) Coelomic helminthsb 32 (52%) 13 (43%) 45 (49%) Intestinal cestodes 2 (3%) 4 (13%) 6 (7%) Presence of copepods 14 (23%) 6 (20%) 20 (22%) aMean ± SD (minimum−maximum) bPresence of Anisakidae larvae, adult Philonema sp. or plerocercoids of cestodes encysted in the coelomic cavity, visceral serosa or muscles cles to detect areas of discoloration or texture varia- trast between affected and non-affected areas was tion, was done on each fish. To measure the micro - enhanced using Adobe Photoshop on nu merized im- sporidia spore, wet mount preparations were made ages of each histological slide (Aperio ImageScope from frozen muscular tissue of 1 specimen with gross software, version 12.4.0, Leica Biosystems Imaging).
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