Abstract
This is an integrative study of a potential zoonotic digenean from the Magellanic Southwestern Atlantic coast. The life cycle of the gymnophallid Gymnophalloides nacellae Cremonte, Pina, Gilardoni, Rodrigues, Chai and Ituarte, 2013 (Digenea) at the type locality, Puerto Deseado (47° 45′ S, 65° 51′ W), Santa Cruz province, was elucidated. This digenean uses the upper subtidal clam Gaimardia trapesina (Lamarck) (Gaimardiidae), which lives on the fronds of the giant kelp, as first intermediate host. A very short-stem furcocercous cercaria emerges and enters the limpets, Nacella magellanica (Gmelin) and N. deaurata (Gmelin) (Nacellidae), which live in the lower rocky intertidal zone. The unencysted metacercariae inhabit the extrapallial space of the limpet at high prevalences and intensities of infection. When the black oystercatcher Haematopus ater Vieillot and Oudart (Charadriidae) preys upon it, it becomes infected, acting as the definitive host. This parasite seems to exhibit a high specificity for their first and second intermediate hosts. Its geographical distribution is from 47 to 55° S in Patagonia, and it is restricted to those sites where the giant kelp reaches to lower intertidal and upper subtidal zones where the limpets are present. Gymnophalloides seoi Lee, Chai and Hong, 1993, a parasite of the Pacific oyster Magallana gigas (Thunberg) (Ostreidae), causes a zoonotic disease in Korea; thus, G. nacellae represent a risk of being a zoonotic parasite if infected limpets are consumed.
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References
Aranzamendi MC, Bastida R, Gardenal C (2011) Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the South-western Atlantic coast. Mar Biol 158:2405–2418. https://doi.org/10.1007/s00227-011-1742-3
Bagnato E, Gilardoni C, Di Giorgio G, Cremonte C (2015) A checklist of marine larval trematodes (Digenea) in molluscs from Argentina. Southwestern Atlantic coast Check List 11:1706. https://doi.org/10.15560/11.4.1706
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al revisited. J Parasitol 83:575–583. https://doi.org/10.7939/R3J38KV04
Chai JY, Lee GC, Park YK, Han ET, Seo M, Kim J, Guk SM, Shin EH, Choi MH, Lee SH (2000) Persistent endemicity of Gymnophalloides seoi infection in a southwestern coastal village of Korea with special reference to its egg laying capacity in the human host. Korean J Parasitol 38:51–57. https://doi.org/10.3347/kjp.2000.38.2.51
Chai JY, Park JH, Han ET, Shin EH, Kim JL, Hong KS, Rim HJ, Lee SH (2001) A nationwide survey of the prevalence of human Gymnophalloides seoi infection on western and southern coastal islands in the Republic of Korea. Korean J Parasitol 39:23–30. https://doi.org/10.3347/kjp.2001.39.1.23
Ching HL (1995) Four new gymnophallid digeneans from rice rats, willets, and molluscs in Florida. J Parasitol 81:924–928
Cremonte F (2004) Life cycle and geographic distribution of the gymnophallid Bartolius pierrei (Digenea) on the Patagonian coast, Argentina. J Nat Hist 38:1591–1604. https://doi.org/10.1080/0022293031000156187
Cremonte C, Pina S, Gilardoni C, Rodrigues P, Chai JY, Ituarte C (2013) A new species of gymnophallid (Digenea) and an amended diagnosis of the genus Gymnophalloides Fujita, 1925. J Parasitol 99:85–92. https://doi.org/10.1645/GE-2909.1
Cremonte F, Gilardoni C, Pina S, Rodrigues P, Ituarte C (2015) Revision of the family Gymnophallidae Odhner, 1905 (Digenea) based on morphological and molecular data. Parasitol Int 64:202–210. https://doi.org/10.1016/j.parint.2014.12.003
Cribb TH, Bray R (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Syst Parasitol 76:1–7. https://doi.org/10.1007/s11230-010-9229-z
de Castellanos Ageitos ZJ, Landoni NA (1988) Catálogo descriptivo de la malacofauna marina Magallánica 2. Comisión de Investigaciones Científicas 2:1–40
Elías I, Carozza C, Di Giácomo EE, Isla MS, Orensanz JML, Parma AM, Pereiro RC, Perier MR, Perrotta RG, Ré ME, Ruarte CO (2011) Coastal fisheries of Argentina. In: Salas S, Chuenpagdee R, Charles A, Seijo JC (eds) Coastal fisheries of Latin America and the Caribbean. FAO Fisheries and Aquaculture Technical Paper, Rome, pp 13–48
Flores K, López Z, Levicoy D, Muñoz-Ramírez CP, González-Wevar C, Oliva ME, Cárdenas L (2019) Identifcation assisted by molecular markers of larval parasites in two limpet species (Patellogastropoda: Nacella) inhabiting Antarctic and Magellan coastal systems. Pol Biol 42:1175–1182. https://doi.org/10.1007/s00300-019-02511-6
Fujita T (1925) Etudes sur les parasites de l′huitre comestible du Japon Ostrea gigas Thunberg. Ann Parasitol Hum Comp 3:37–59. https://doi.org/10.1051/parasite/1925031037
Galaktionov K, Irwin SWB, Saville DH (2006) One of the most complex life-cycles among trematodes: a description of Parvatrema margaritense (Ching, 1982) n. comb. (Gymnophallidae) possessing parthenogenetic metacercariae. Parasitology 132:733–746. https://doi.org/10.1017/S0031182005009765
Guk SM, Park JH, Shin EH, Kim JL, Lin A, Chai JY (2006) Prevalence of Gymnophalloides seoi infection in coastal villages of Haenam-gun and Yeongam-gun, Republic of Korea. Korean J Parasitol 44:1–5. https://doi.org/10.3347/kjp.2006.44.1.1
Lauckner G (1983) Diseases of Mollusca: Bivalvia. Diseases of Marine Animals, 2. Biologische Anstalt Helgoland, Hamburg
Lee SH, Chai JY (2001) A review of Gymnophalloides seoi (Digenea: Gymnophallidae) and human infections in the Republic of Korea. Korean J Parasitol 39:85–118. https://doi.org/10.3347/kjp.2001.39.2.85
Lee SH, Chai JY, Hong ST (1993) Gymnophalloides seoi n. sp. (Digenea: Gymnophallidae), the first report of human infection by a gymnophallid. J Parasitol 79:677–680. https://doi.org/10.2307/3283602
Lee KD, Guk SM, Chai JY (2010) Toll-Like Receptor 2 and Muc2 Expression on Human Intestinal Epithelial Cells by Gymnophalloides seoi Adult Antigen. J Parasitol 96:58–66. https://doi.org/10.1645/GE-2195.1
Loos-Frank B (1969) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes. I. Die Alternativ-Zyklen von Gymnophallus choledochus Odhner, 1900. Z Parasitenk 32:135–156
Martorelli SR, Morriconi E (1998) A new gymnophallid metacercaria (Digenea) in Nacella (P.) magellanica and N. (P.) deaurata (Mollusca, Patellidae) from the Beagle Channel, Tierra del Fuego, Argentina. Acta Parasitol 43:20–25
Nawa Y, Hatz C, Blum J (2005) Sushi delights and parasites: the risk of fishborne and foodborne parasitic Zoonoses in Asia. Travel Med 4:1297–1303. https://doi.org/10.1086/496920
Pekkarinen M (1987) The cercaria and metacercaria of Gymnophallus gibberosus Loos-Frank, 1971 (Trematoda: Gymnophallidae) in Macoma balthica (L.) (Bivalvia) in the Baltic brackish water (southwestern Finland). Ann Zool Fennici 24:123–136
Praveen PK, Ganguly S, Para PA, Shekhar S, Wakchaure R, Sharma S, Dalai N, Pandey AK, Padhy A, Mahajan T, Qadri K (2015) Fish-borne parasitic zoonoses: a review. Int J Phar Biomed Res 2:20–22
Rios EC (1994) Seashells of Brazil, 2nd edn. Editora da Fundação Universidade do Rio Grande, Rio Grande
Seo M, Chun H, Ahn G, Jang KT, Guk SM, Chai JY (2006) A case of colonic lymphoid tissue invasion by Gymnophalloides seoi in a Korean man. Korean J Parasitol 44:87–89. https://doi.org/10.3347/kjp.2006.44.1.87
Skirnisson K, Galaktionov KV (2002) Life cycles and transmission patterns of seabird digeneans in SW Iceland. Sarsia 87:144–151. https://doi.org/10.1080/003648202320205229
Song H, Jung BK, Cho J, Chai JY (2018) Worm expulsion of Gymnophalloides seoi from C57BL/6 mice: role of metacercarial exosomes in upregulating TLR2 and MUC2 expression in intestinal tissues. Parasitol Res 117:3309–3314. https://doi.org/10.1007/s00436-018-6002-8
Valdovinos C, Rüth M (2005) Nacellidae limpets of the southern end of South America: taxonomy and distribution. Rev Chil Hist Nat 78:497–517. https://doi.org/10.4067/S0716-078X2005000300011
Woods RW (2014) Conservation assessment of the Blackish Oystercatcher Haematopus ater. Int Wader Stud 20:109–115
WoRMS Editorial Board (2019) World Register of Marine Species. https://www.marinespecies.org at VLIZ. Accessed 17 May 2019
Yanagida T, Shirakashi S, Iwaki T, Ikushima N, Ogawa K (2009) Gymnophallid digenean Parvatrema duboisi uses Manila clam as the first and second intermediate host. Parasitol Int 58:308–310. https://doi.org/10.1016/j.parint.2009.05.006
Yorio P, Bertellotti M (2002) Espectro trófico de la Gaviota Cocinera (Larus dominicanus) en tres áreas protegidas de Chubut, Argentina. El Hornero 17:91–95
Acknowledgements
Field works were conducted with permits provided by Wildlife Secretary of Santa Cruz province (Resolution Number 861/08). Authors thank to C. Ituarte, J. Diaz, E. Lorenti, M. Demetrio, A. Frizzera and M.E. Diez for the help in field and laboratory work, C. Medina for the help in molecular studies, A. Gatto and D. Zelaya for information about the host distributions, D. Podestá for the oystercatcher and limpet pictures, T. Zapata from Centro de Investigaciones, Universidad de la Patagonia Austral at Puerto Deseado, for kindly providing access to laboratory facilities, M. Luquet (Aluar S.A.) for the SEM photographs. Financial support was provided by ANPCyT (PICTs 2013-1702, 2016-0653, 2015-0841, Préstamo BID) y Conservation, Food and Health Foundation. FC, CG and EB are members of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).
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Gilardoni, C., Di Giorgio, G., Bagnato, E. et al. A potential zoonotic parasite, the digenean Gymnophalloides nacellae, on the Magellanic coast in the Southwestern Atlantic Ocean: its life cycle and geographical distribution. Polar Biol 43, 725–734 (2020). https://doi.org/10.1007/s00300-020-02674-7
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DOI: https://doi.org/10.1007/s00300-020-02674-7