Abstract
Lungworms of the genera Parafilaroides and Otostrongylus are responsible for parasitic bronchopneumonia, the foremost disease of eastern Atlantic common seals (EACS, Phoca vitulina vitulina) in the Dutch North Sea. Recently, there have been increased reports of lungworm cases and observations of unusually long Parafilaroides sp. adults in this location. The initial aim of this study was to confirm the identity of the Parafilaroides species infecting this population. Parafilaroides are usually small and delicate, making them difficult to extract from host tissue, and there is often difficulty accessing fresh specimens for morphological study. The large size of the Dutch worms and the accessibility of specimens from numerous animals enabled the description and measurement of many intact specimens (N = 64) from multiple host animals (N = 20). Species identity was confirmed by targeted sequencing of ribosomal and mitochondrial DNA amplicons from a subset of worms. Worm morphology was consistent with descriptions for P. gymnurus, but the mature females were 1.9-fold and 3.4-fold longer than those recovered from French EACS (P ≤ 0.001) and Canadian western Atlantic common seals (Phoca vitulina concolor; P ≤ 0.0001). They were also significantly longer than mature female P. gymnurus described from other seal species, with the exception of those from harp seals of Les Escoumins, Quebec. We suggest that intraspecific genetic differences in P. gymnurus and the environment within the host could contribute to the variation reported here. This study is the first to describe P. gymnurus using morphological and molecular methods and should serve as a reference for identification of the species.
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References
Al-Banna L, Williamson V, Gardner SL (1997) Phylogenetic analysis of nematodes of the genus Pratylenchus using nuclear 26S rDNA. Mol Phylogenet Evol 7:94–102. https://doi.org/10.1006/mpev.1996.0381
Anderson RC (1978) Keys to genera of the superfamily Metastrongyloidea. In: Anderson RC, Chabaud AG, Wilmott S (eds) CIH keys to the nematode parasites of vertebrates, no. 5. Commonwealth Agricultural Bureaux, Farnham Royal, pp 1–40
Blaxter ML (2004) The promise of a DNA taxonomy. Philos Trans R Soc Lond Ser B Biol Sci 1444:669–679. https://doi.org/10.1098/rstb.2003.1447
Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531. https://doi.org/10.1016/S0020-7519(01)00357-5
Borgsteede FHM, Bus HGJ, Verplanke JAW, Vanderburg WPJ (1991) Endoparasitic helminths of the harbor seal, Phoca vitulina, in the Netherlands. Neth J Sea Res 28:247–250
Brasseur SMJM, Reijinders PJH, Cremer J, Meesters E, Kirkwood R, Jensen LF, Jeβ A, Galatius A, Teilmann J, Aarts G (2018) Echoes from the past: regional variations in recovery within a harbour seal population. PLoS One 13:e0189674. https://doi.org/10.1371/journal.pone.0189674
Cable RM (1977) An illustrated laboratory manual of parasitology, 5th edn. Burgess, Minneapolis
Cable J, Barber I, Boag B, Ellison AR, Morgan ER, Murray K, Pascoe EL, Sait SM, Wilson AJ, Booth M (2017) Global change, parasite transmission and disease control: lessons from ecology. Phil Trans R Soc B 372:20160088. https://doi.org/10.1098/rstb.2016.0088
Carreno RA, Nadler SA (2003) Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. J Parasitol 89:965–973. https://doi.org/10.1645/GE-76R
CBS, PBL, RIVM, WUR (2017) Gewone en grijze zeehond in Waddenzee en Deltagebied, 1960–2016 (indicator 1231, versie 14, 23 November 2017). www.clo.nl. Centraal Bureau voor de Statistiek (CBS), Den Haag; PBL Planbureau voor de Leefomgeving, Den Haag; RIVM Rijksinstituut voor Volksgezondheid en Milieu, Bilthoven; en Wageningen University and Research, Wageningen. https://www.clo.nl/indicatoren/nl123114
Claussen D, Strauss V, Ising S, Jager M, Schnieder T, Stoye M (1991) The helminth fauna from the common seal (Phoca vitulina vitulina, Linné, 1758) of the Wadden Sea in Lower Saxony. Part 2. Nematodes. Zentralbl Veterinarmed B 38:649–656
Dailey MD (2006) Restoration of Parafilaroides (Dougherty, 1946) (Nematoda: Metastrongyloidea) with description of two new species from pinnipeds of eastern Central Pacific. J Parasitol 92:589–594. https://doi.org/10.1645/GE-3525.1
Dailey MD (2009) A new species of Parafilaroides (Nematoda: Filaroididae) in three species of fur seals (Carnivora: Otariidae) from the southern hemisphere. J Parasitol 95:156–159. https://doi.org/10.1645/GE-1521.1
Dankers N, Dijkema KS, Reijnders PJH, Smit CJ (1990) De waddenzee in de toekomst - waarom en hoe te bereiken? pp. 112. RIN-report 90/19. Rijksinsituut voor Natuurbeheer, Texel. http://edepot.wur.nl/388960. Accessed 10 Oct 2018
Desforges J-PW, Sonne C, Levin M, Siebert U, De Guise S, Dietz R (2016) Immunotoxic effects of environmental pollutants in marine mammals. Environ Int 86:126–139. https://doi.org/10.1016/j.envint.2015.10.007
Dougherty EC (1946) The genus Aelurostrongylus Cameron, 1927 (Nematoda, Metastrongylidae), and its relatives; with descriptions of Parafilaroides, gen. Nov., and Angiostrongylus gubernaculatus, sp. nov. Proc Helminthol Soc Wash 13:16–25
Elson-Riggins JG (2002) Characterization of Otostrongylus circumlitus, a lungworm from seals, and host–parasite interaction in harbor and northern elephant seals. Dissertation, University of California Riverside
Frouin H, Lebeuf M, Hammill M, Sjare B, Fournier M (2011) PBDEs in serum and blubber of harbour, grey and harp seal pups from eastern Canada. Chemosphere 82:663–669. https://doi.org/10.1016/j.chemosphere.2010.11.007
Gasser RB, Chilton NB, Hoste H, Beveridge I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res 21:2525–2526
Gosselin JF, Measures LN (1997) Redescription of Filaroides (Parafilaroides) gymnurus (Railliet, 1899) (Nematoda:Metastrongyloidea), with comments on other species in pinnipeds. Can J Zool 75:359–370. https://doi.org/10.1139/z97-045
Gosselin JF, Measures LN, Huot J (1998) Lungworm (Nematoda: Metastrongyloidea) infections in Canadian phocids. Can J Fish Aquat Sci 55:825–834. https://doi.org/10.1139/f97-306
Greig DJ, Ylitalo GM, Wheeler EA, Boyd D, Gulland FMD, Yanagida GK, Harvey JT, Hall AJ (2011) Geography and stage of development affect persistent organic pollutants in stranded and wild-caught harbor seals pups from Central California. Sci Total Environ 409:3537–3547. https://doi.org/10.1016/j.scitotenv.2011.05.047
Henderson NG, Stear MJ (2006) Eosinophil and IgA responses in sheep infected with Teladorsagia circumcincta. Vet Immunol Immunopathol 112:62–66. https://doi.org/10.1016/j.vetimm.2006.03.012
Hernández JN, Hernández A, Stear MJ, Conde-Felipe M, Rodríguez E, Piedrafita D, González JF (2016) Potential role for mucosal IgA in modulating Haemonchus contortus adult worm infection in sheep. Vet Parasitol 223:153–158. https://doi.org/10.1016/j.vetpar.2016.04.022
Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MAS, Lacy RC, Dasmahapatra KK (2014) High-throughput sequencing reveals inbreeding depression in a natural population. Proc Natl Acad Sci U S A 111:3775–3780. https://doi.org/10.1073/pnas.1318945111
Hong C, Timms BJ (1986) Variation in size of Ostertagia circumcincta, a nematode parasite of sheep, induced experimentally and during preparation and preservation. Syst Parasitol 9:39–42
Jacobs DE, Rose CH (1990) Studies on Ostertagia spp. from Greenlandic sheep: arrested development and worm length. Acta Vet Scand 31:333–337
Jensen LF, Ejbye-Ernst R, Michaelsen TY, Jensen A, Hansen DM, Nielsen ME, Pertoldi C (2017) Assessing the genetic effects of rehabilitating harbor seals (Phoca vitulina) in the Wadden Sea using stochastic simulations. Mamm Res 62:363–372. https://doi.org/10.1007/s13364-017-0323-3
Kappe AL, Bijlsma R, Osterhaus ADME, van Delden W, van de Zande L (1997) Structure and amount of genetic variation at minisatellite loci within the subspecies complex of Phoca vitulina (the harbour seal). Heredity 78:457–463
Laane RWPM, Vethaak AD, Gandrass J, Vorkamp K, Köhler A, Larsen MM, Strand J (2013) Chemical contaminants in the Wadden Sea: sources, transport, rate and effects. J Sea Res 82:10–53. https://doi.org/10.1016/j.seares.2013.03.004
Lagrue C, Kelly DW, Hicks A, Poulin R (2011) Factors influencing infection patterns of trophically transmitted parasites among a fish community: host diet, host-parasite compatibility or both? J Fish Biol 79:466–485. https://doi.org/10.1111/j.1095-8649.2011.03041.x
Lehnert K, von Samson-Himmelstjerna G, Schaudien D, Bleidorn C, Wohlsein P, Siebert U (2010) Transmission of lungworms of harbour porpoises and harbour seals: molecular tools determine potential vertebrate intermediate hosts. Int J Parasitol 40:845–853. https://doi.org/10.1016/j.ijpara.2009.12.008
Lehnert K, Ronnenberg K, Weijs L, Covaci A, Das K, Hellwig V, Siebert U (2016) Xenobiotic and immune-relevant molecular biomarkers in harbor seals as proxies for pollutant burden and effects. Arch Environ Contam Toxicol 70:106–120. https://doi.org/10.1007/s00244-015-0202-3
Leignel V, Cabaret J (2001) Massive use of chemotherapy influences life traits of parasitic nematodes in domestic ruminants. Funct Ecol 15:569–574. https://doi.org/10.1046/j.0269-8463.2001.00567.x
Mair C, Matthews L, De Cisneros JP, Stefan T, Stear MJ (2015) Multitrait indices to predict worm length and number in sheep with natural, mixed predominantly Teladorsagia circumcincta infection. Parasitology 142:773–782. https://doi.org/10.1017/S0031182014001905
Mattig FR (2017) Contaminants in bird eggs. In: Kloepper S. et al. (eds) Wadden Sea Quality Status Report 2017. Common Wadden Sea secretariat, Wilhelmshaven, Germany. Last updated 21.12.2017. https://qsr.waddensea-worldheritage.org/reports/contaminants-bird-eggs. Accessed 11 June 2018
Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasitol 66:47–148. https://doi.org/10.1016/S0065-308X(08)00202-9
Measures LN (2001) Lungworms of marine mammals. In: Samuel WM, Pybus MJ, Kocan AA (eds) Parasitic diseases of wild mammals, 2nd edn. Iowa State University Press, Ames, pp 279–300
Morand S (1996) Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Funct Ecol 10:210–218
Morissette L, Castonguay M, Savenkoff C, Swain D, Chabot D, Bourdages H, Hammill MO, Hanson JM (2009) Contrasting changes between the northern and southern gulf of St. Lawrence ecosystems associated with the collapse of groundfish stocks. Deep Sea Res Pt II Top Stud Oceanogr 56:2117–2131. https://doi.org/10.1016/j.dsr2.2008.11.023
Nyström J, Shen Z, Aili M, Flemming A, Leroi A, Tuck S (2002) Increased or decreased levels of Caenorhabditis elegans lon-3, a gene encoding a collagen, cause reciprocal changes in body length. Genetics 161:83–97
Osinga N, ‘t Hart P (2010) Harbour seals (Phoca vitulina) and rehabilitation. NAMMCO Sci Publ 8:355–372. https://doi.org/10.7557/3.2699
Philippart C, Gerkema T, van der Veer HW (2017) North Sea coastal ecology: future challenges. J Sea Res 127:227–230. https://doi.org/10.1016/j.seares.2017.07.004
Railliet MA (1899) Sur quelques parasites rencontrés à l'autopsie d’un phoque (Phoca vitulina L.). Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 51:128–130
Reijnders PJH, Brasseur SMJM, Ries EH (1996) The release of seals from captive breeding and rehabilitation programs: a useful conservation tool? In: St. Aubin DJ, Geraci JR, Lounsbury VJ (eds) Rescue, rehabilitation and release of marine mammals: an analysis of current views and practices. NOAA Technical Memorandum NMFS OPR 8:54–65
Rijks JM (2008) Phocine distemper revisited: multidisciplinary analysis of the 2002 phocine distemper virus epidemic in the Netherlands. Dissertation, Erasmus University Rotterdam, Rotterdam. http://hdl.handle.net/1765/14214
Siebert U, Joiris C, Holsbeek L, Benke H, Failing K, Frese K, Petzinger E (1999) Potential relation between mercury concentrations and necropsy findings in cetaceans from German waters of north and Baltic seas. Mar Pollut Bull 38:285–295. https://doi.org/10.1016/S0025-326X(98)00147-7
Skorping A (2007) Selecting for fast and slow maturing worms. Proc R Soc Lond B Biol Sci 274:1465–1466. https://doi.org/10.1098/rspb.2007.0313
Stear MJ, Strain S, Bishop SC (1999) Mechanisms underlying resistance to nematode infection. Int J Parasitol 29:51–56. https://doi.org/10.1016/S0020-7519(98)00179-9
Sures B, Nachev M, Selbach C, Marcogliese DJ (2017) Parasite responses to pollution: what we know and where we go in ‘environmental parasitology’. Parasit Vectors 10:65. https://doi.org/10.1186/s13071-017-2001-3
TSEG (2013) Harbour seal counts 2013. http://www.waddensea-secretariat.org/monitoring-tmap/topics/marine-mammals
Tuck S (2014) The control of cell growth and body size in Caenorhabditis elegans. Exp Cell Res 321:71–76. https://doi.org/10.1016/j.yexcr.2013.11.007
Tulp I, van der Veer HW, Walker P, van Walraven L, Bolle L (2017) Can guild- or site specific contrasts in trends or phenology explain the changed role of the Dutch Wadden Sea for fish? J Sea Res 127:150–163. https://doi.org/10.1016/j.seares.2016.10.001
van Aken HM (2008) Variability of the water temperature in the western Wadden Sea on tidal to centennial time scales. J Sea Res 60:227–234. https://doi.org/10.1016/j.seares.2008.09.001
van Walraven L, Dapper R, Nauw JJ, Tulp I, Witte JIJ, van der Veer HW (2017) Long-term patterns in fish phenology in the western Dutch Wadden Sea in relation to climate change. J Sea Res 127:173–181. https://doi.org/10.1016/j.seares.2017.04.001
Acknowledgements
We thank the staff and volunteers at the Seal Rehabilitation and Research Centre (currently: Seal Centre Pieterburen) and The Marine Mammal Center (TMMC) for their assistance with sample collection. Although the work on samples from eastern Atlantic common seals was conducted at Seal Centre Pieterburen, the conclusions and points of view elaborated in the Discussion section do not necessarily reflect the current views of the Seal Centre on this matter. We are grateful to the colleagues of the RVC and Gendika for their support with the laboratory work. We also thank Dr Lena Measures, Scientist Emeritus at Fisheries and Oceans Canada, Professor Dr Carlos Hermosilla of Justus Liebig University Giessen, and Dr Edward Platzer of University of California Riverside for discussions which helped improve the manuscript. The manuscript was also improved by the suggestions of an anonymous reviewer. The RVC has assigned this manuscript the reference PPS_01960.
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The study was funded by the Ministry of Economic Affairs, Government of the Netherlands and The Royal Veterinary College (RVC), UK.
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Elson-Riggins, J.G., Gibbons, L.M., Van Liere, D.W. et al. Surprisingly long body length of the lungworm Parafilaroides gymnurus from common seals of the Dutch North Sea. Parasitol Res 119, 1803–1817 (2020). https://doi.org/10.1007/s00436-020-06675-7
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DOI: https://doi.org/10.1007/s00436-020-06675-7