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Genetic identification and insights into the ecology of Contracaecum rudolphii A and C. rudolphii B (Nematoda: Anisakidae) from cormorants and fish of aquatic ecosystems of Central Italy

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Abstract

Contracaecum rudolphii (s. l.) is a complex of sibling species of anisakid nematodes having the fish-eating birds belonging to the Family Phalacrocoracidae as final hosts. The great cormorant Phalacrocorax carbo sinensis is parasitized by C. rudolphii A and C. rudolphii B. Adults and L4 specimens of C. rudolphii (s. l.) (N = 3282) were collected in cormorants from brackish and freshwater ecosystems of Central Italy. Third-stage larvae of Contracaecum (N = 882) were obtained from the fish species Dicentrarchus labrax, Anguilla anguilla, Aphanius fasciatus, Atherina boyeri, Leuciscus cephalus, Barbus barbus, and Carassius carassius captured in the same geographical areas of cormorants’ standings. Contracaecum rudolphii A and C. rudolphii B were identified by a multilocus genetic approach: allozymes, sequences analysis of the mtDNA cox2, and ITS region of rDNA gene loci. Differential distribution of the two parasite species was observed in different aquatic environments. Contracaecum rudolphii B outnumbered C. rudolphii A in wintering cormorants from freshwater ecosystems; the opposite trend was found in cormorants from brackish water. Analogously, C. rudolphii A larvae were more prevalent in brackish water fish, while C. rudolphii B larvae were found infecting only freshwater fish. The findings seem to confirm that C. rudolphii A and C. rudolphii B would have a life-cycle adapted to brackish and freshwater environments, respectively. A differential feeding behavior of wintering cormorants, the ecology of the infected fish species, and abiotic factors related to early stages of the parasites are supposed to maintain the distinctiveness of the two parasite species’ life cycles in the two different aquatic ecosystems.

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References

  • Barak NA, Mason CF (1992) Population density, growth and diet of eels, Anguilla anguilla L., in two rivers in eastern England. Aquac Res 23:59–70

    Article  Google Scholar 

  • Baruš V, Sergeeva TP, Sonin MD, Ryzhikov KM (1978) Helminths of fish-eating birds of the Palaearctic Region I: Nematoda. In: Rysavy, B, Ryzhikov, K, M (Eds) Helminths of fish eating birds. Springer, Praha, p 318

    Book  Google Scholar 

  • Bullini L, Nascetti G, Paggi L, Orecchia P, Mattiucci S, Berland B (1986) Genetic variation of ascaridoid worms with different life cycles. Evolution 40:437–440

    Article  CAS  PubMed  Google Scholar 

  • Culurgioni J, Sabatini A, De Murtas R, Mattiucci S, Figus V (2014) Helminth parasites of fish and shellfish from the Santa Gilla Lagoon in southern Sardinia, Italy. J Helminthol 88:489–498

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

  • D’Amelio S, Nascetti G, Mattiucci S, Cianchi R, Orecchia P, Paggi L, Berland B, Bullini L (1990) Ricerche elettroforetiche su alcune specie del genere Contracaecum, parassiti di uccelli ittiofagi (Ascaridida: Anisakidae). Parassitologia 32:77

    Google Scholar 

  • D’Amelio S, Barros NB, Ingrosso S, Fauquier DA, Russo R, Paggi L (2007) Genetic characterization of members of the genus Contracaecum (Nematoda: Anisakidae) from fish-eating birds from west-central Florida, USA, with evidence of new species. Parasitology 134:1041–1051

    Article  PubMed  CAS  Google Scholar 

  • D’Amelio S, Cavallero S, Dronen NO, Barros NB, Paggi L (2012) Two new species of Contracaecum Railliet & Henry, 1912 (Nematoda: Anisakidae), C. fagerholmi n. sp. and C. rudolphii F from the brown pelican Pelecanus occidentalis in the northern Gulf of Mexico. Syst Parasitol 81:1–16

    Article  PubMed  Google Scholar 

  • Dezfuli BS, Manera M, Bosi G, DePasquale JA, D'Amelio S, Castaldelli G, Giari L (2016) Anguilla anguilla intestinal immune response to natural infection with Contracaecum rudolphii A larvae. J Fish Dis 39:1187–1200

    Article  CAS  PubMed  Google Scholar 

  • Farjallah S, Merella P, Ingrosso S, Rotta A, Slimane BB, Garippa G, Said K, Busi M (2008) Molecular evidence for the occurrence of Contracaecum rudolphii A (Nematoda: Anisakidae) in shag Phalacrocorax aristotelis (Linnaeus) (Aves: Phalacrocoracidae) from Sardinia (western Mediterranean Sea). Parasitol Int 57:437–440

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Frederiksen M, Korner-Nievergelt F, Marion L, Bregnballe T (2018) Where do wintering cormorants come from? Long-term changes in the geographical origin of a migratory bird on a continental scale. J Appl Ecol 55:1–14

    Article  Google Scholar 

  • Garbin L, Mattiucci S, Paoletti M, González-Acuña D, Nascetti G (2011) Genetic and morphological evidences for the existence of a new species of Contracaecum (Nematoda: Anisakidae) parasite of Phalacrocorax brasilianus (Gmelin) from Chile and its genetic relationships with congeners from fish-eating birds. J Parasitol 97:476–492

    Article  CAS  PubMed  Google Scholar 

  • Hartwich G (1964) Revision der Vogelparasitischen Nematoden Mitteleuropas II. Die Gattung Contracaecum Railliet and Henry, 1912 (Ascaridoidea). Mitt Zool Mus Berl 40:15–53

    Google Scholar 

  • Hillis DM, Bull JJ, White ME, Badgett MR, Molineux IJ (1993) Experimental approaches to phylogenetic analysis. Syst Biol 42:90–92

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2005) Bayesian analysis of molecular evolution using MrBayes. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, New York, pp 183–226

    Chapter  Google Scholar 

  • Huizinga HW (1966) Studies on the life cycle and development of Contracaecum spiculigerum (Rudolphi, 1809) (Ascaridoidea: Heterocheilidae) from marine piscivorous birds. J. Elisa Mitchell. Sci Soc 82:180–195

    Google Scholar 

  • Karvonen A, Jokela J, Laine AL (2018) Importance of sequence and timing in parasite coinfections. Trends Parasitol 35:109–118

    Article  PubMed  Google Scholar 

  • Laffaille P, Lefeuvre JC, Schricke MT, Feunteun E (2001) Feeding ecology of 0- group sea bass, Dicentrarchus labrax, in salt marshes of Mont Saint Michel Bay (France). Estuaries 24:116–125

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2647–2648

    Article  CAS  Google Scholar 

  • Li A, D’Amelio S, Paggi L, He F, Gasser RB, Lun Z, Abollo E, Turchetto M, Zhu X (2005) Genetic evidence for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) and the validity of Contracaecum septentrionale (Kreis, 1955) (Nematoda: Anisakidae). Parasitol Res 96:361–366

    Article  PubMed  Google Scholar 

  • Ludovisi A, Minozzo M, Pandolfi P, Taticchi MI (2005) Modelling the horizontal spatial structure of planktonic community in Lake Trasimeno (Umbria, Italy) using multivariate geostatistical methods. Ecol Model 181:247–262

    Article  Google Scholar 

  • Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematics of anisakids nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasitol 66:47–148

    Article  PubMed  Google Scholar 

  • Mattiucci S, Turchetto M, Brigantini F, Nascetti G (2002) On the occurrence of the sibling species of Contracaecum rudolphii complex (Nematoda: Anisakidae) in cormorants (Phalacrocorax carbo sinensis) from Venice and Caorle lagoons: Genetic markers and ecological studies. Parassitologia 44:105

    Google Scholar 

  • Mattiucci S, Paoletti M, Oliverio-Verbel J, Baldiris R, Arroyo-Salgado B, Garbin L, Navone G, Nascetti G (2008a) Contracaecum bioccai n. sp. from the brown pelican Pelecanus occidentalis (L.) in Colombia (Nematoda: Anisakidae): morphology, molecular evidence and its genetic relationship with congeners from fish-eating birds. Syst Parasitol 69:101–121

    Article  PubMed  Google Scholar 

  • Mattiucci S, Paoletti M, Webb SC, Sardella N, Timi JT, Berland B, Nascetti G (2008b) Genetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda: Anisakidae) from pinnipeds based on mitochondrial cox2 sequences, and congruence with allozyme data. Parasite 15:408–419

    Article  CAS  PubMed  Google Scholar 

  • Mattiucci S, Paoletti M, Consuegra Solorzano A, Nascetti G (2010) Contracaecum gibsoni n. sp. and C. overstreeti n. sp. (Nematoda: Anisakidae) from the Dalmatian pelican Pelecanus crispus (L.) in Greek waters: genetic and morphological evidence. Syst Parasitol 75:207–224

    Article  PubMed  Google Scholar 

  • Merella P, Garippa G (2001) Metazoan parasites of grey mullets (Teleostea: Mugilidae) from the Mistras Lagoon (Sardinia-western Mediterranean). Sci Mar 65:201–206

    Article  Google Scholar 

  • Molnár K, Székely C, Baska F, Müller T, Zuo S, Kania PW, Nowak B, Buchmann K (2019) Differential survival of 3rd stage larvae of Contracaecum rudolphii type B infecting common bream (Abramis brama) and common carp (Cyprinus carpio). Parasitol Res 7:1–7

    Google Scholar 

  • Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Academia, Prague

    Google Scholar 

  • Moravec F (2009) Experimental studies on the development of Contracaecum rudolphii (nematode: Anisakidae) in copepod and fish paratenic hosts. Folia Parasitol 56:185–193

    Article  Google Scholar 

  • Moravec F, Kaiser H (1995) Helminth parasites from West Indian frogs, with descriptions of two new species. Carib J Sci 31:252–268

    Google Scholar 

  • Morrison DA (2006) Phylogenetic analyses of parasites in the new millennium. Adv Parasitol 63:2–97

    Google Scholar 

  • Mozgovoy AA (1953) [principles of nematodology. In: Skrjabin KI (ed) Ascaridata of animals and man and the diseases caused by them.] pp 8–42 (In Russian)

  • Mozgovoy AA, Shakhmatova VI, Semenova MK (1965) The life-cycle of Contracaecum spasskii (Ascaridata: Anisakidae) - a parasite of fish-eating birds Izdat Akad Nauk SSSR 96-103

  • Mozgovoy AA, Shakhmatova VI, Semenova MK (1968) [Life cycle of Contracaecum spiculigerum (Ascaridata: Anisakidae), a parasite of domestic and game birds.] Trudi GELAN 19: 129–136 (In Russian)

  • Nadler SA, Hudspeth DS (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J Parasitol 86:380–393

    Article  CAS  PubMed  Google Scholar 

  • Nascetti G, Cianchi R, Mattiucci S, D'amelio S, Orecchia P, Paggi L, Brattey J, Berland B, Smith JW, Bullini L (1993) Three sibling species within Contracaecum osculatum (Nematoda, Ascaridida, Ascaridoidea) from the Atlantic arctic-boreal region: reproductive isolation and host preferences. Int J Parasitol 23:105–120

    Article  CAS  PubMed  Google Scholar 

  • Penttinen OP, Holopainen IJ (1992) Seasonal feeding activity and ontogenetic dietary shifts in crucian carp, Carassius carassius. Environ Biol Fish 33:215–221

    Article  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Parasitol 53:793–808

    Google Scholar 

  • Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Raida MK, Buchmann K (2007) Temperature-dependent expression of immune-relevant genes in rainbow trout following Yersinia ruckeri vaccination. Dis Aquat Org 77:41–52

    Article  CAS  Google Scholar 

  • Reeder TW (2003) A phylogeny of the Australian Sphenomorphus group (Scincidae: Squamata) and the phylogenetic placement of the crocodile skinks (Tribolonotus): Bayesian approaches to assessing congruence and obtaining confidence in maximum likelihood inferred relationships. Mol Phylogenet Evol 27:384–397

    Article  CAS  PubMed  Google Scholar 

  • Reiczigel J, Rózsa L (2005) Quantitative parasitology 3.0. Budapest. Distributed by the authors

  • Reiczigel J, Marozzi M, Fábián I, Rózsa L (2019) Biostatistics for parasitologists–a primer to quantitative parasitology. Trends Parasitol 35:277–281

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck J (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Salati F, Meloni M, Cau M, Angelucci G (2013) Presence of Contracaecum spp. in teleosts cultured and fished in Sardinia. Vet Parasitol 196:382–387

    Article  PubMed  Google Scholar 

  • Shamsi S (2019) Parasite loss or parasite gain? Story of Contracaecum nematodes in antipodean waters. Paras epidemiol control 4:9

    Google Scholar 

  • Shamsi S, Suthar J (2016) A revised method of examining fish for infection with zoonotic nematode larvae. Int J Food Microbiol 227:13–16

    Article  PubMed  Google Scholar 

  • Shamsi S, Gasser R, Beveridge I, Shabani AA (2008) Contracaecum pyripapillatum n. sp. (Nematoda: Anisakidae) and a description of C. multipapillatum (von Drasche, 1882) from the Australian pelican, Pelecanus conspicillatus. Parasitol Res 103:1031–1039

    Article  PubMed  Google Scholar 

  • Shamsi S, Norman R, Gasser R, Beveridge I (2009a) Redescription and genetic characterization of selected Contracaecum spp. (nematoda: Anisakidae) from various hosts in Australia. Parasitol Res 104:1507–1525

    Article  PubMed  Google Scholar 

  • Shamsi S, Norman R, Gasser R, Beveridge I (2009b) Genetic and morphological evidences for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) (Nematoda: Anisakidae) in Australia. Parasitol Res 105:529–538

    Article  PubMed  Google Scholar 

  • Shamsi S, Turner A, Wassens S (2018a) Description and genetic characterization of a new Contracaecum larval type (Nematoda: Anisakidae) from Australia. J Helminthol 92:216–222

    Article  CAS  PubMed  Google Scholar 

  • Shamsi S, Stoddart A, Smales L, Wassens S (2018b) Occurrence of Contracaecum bancrofti larvae in fish in the Murray–Darling Basin. J Helminthol 93:574–579

    Article  PubMed  Google Scholar 

  • Szostakovka B, Fagerholm HP (2007) Molecular identification of two strains of third-stage larvae of Contracaecum rudolphii Sensu Lato (Nematoda: Anisakidae) from fish in Poland. J Parasitol 93:961–964

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Eerden MR, Gregersen J (1995) Long-term changes in the Northwest European population of cormorants Phalacrocorax carbo sinensis. Ardea 83:61–79

    Google Scholar 

  • Van Eerden MR, Munsterman MJ (1986) Importance of the Mediterranean for wintering Cormorants Phalacrocorax carbo sinensis. In: Monbailliu X (ed) Mediterranean Marine Avifauna. Springer Verlag, Berlin, pp 123–141

    Chapter  Google Scholar 

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Author notes

  1. Gian Luca Sbaraglia and Marialetizia Palomba contributed equally to this work.

Authors and Affiliations

  1. Department of Public Health and Infectious Diseases, Section of Parasitology, Sapienza -University of Rome, P.le Aldo Moro, 5, 00185, Rome, Italy

    Simonetta Mattiucci & Marialetizia Palomba

  2. Department of Ecological and Biological Sciences, Tuscia University, Viale dell’Università s/n, 01100, Viterbo, Italy

    Gian Luca Sbaraglia, Sara Filippi, Michela Paoletti & Giuseppe Nascetti

  3. Institute of Marine Research, Bergen, Norway

    Paolo Cipriani

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  1. Simonetta Mattiucci
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  2. Gian Luca Sbaraglia
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Correspondence to Simonetta Mattiucci.

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All applicable international, national, and/or institutional guidelines for the care and use of animals (cormorants and fish) were followed. The dead animals were examined under the permission of the Local Ethics Commission for Research Involving Animals at the Tuscia University (decision no. 050VT427). Fish were collected with the permission of the Lazio Region at the Tuscia University (decision G15884).

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Mattiucci, S., Sbaraglia, G.L., Palomba, M. et al. Genetic identification and insights into the ecology of Contracaecum rudolphii A and C. rudolphii B (Nematoda: Anisakidae) from cormorants and fish of aquatic ecosystems of Central Italy. Parasitol Res 119, 1243–1257 (2020). https://doi.org/10.1007/s00436-020-06658-8

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