Skip to main content

Advertisement

SpringerLink
Log in

Austrodiplostomum sp., Bolbophorus sp. (Digenea: Diplostomidae), and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae in inland silverside Menidia beryllina from catfish aquaculture ponds, with notes on the infectivity of Austrodiplostomum sp. cercariae in channel catfish Ictalurus punctatus

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In the southeastern USA, catfish aquaculture is burdened by predation from piscivorous birds and the digenetic trematodes they carry. In addition to cultured ictalurid fish, other forage or incidental fish species inhabit catfish production ponds. Of these, the inland silverside Menidia beryllina was recently found to harbor larval metacercariae of several trematode species. Three species of metacercariae were reported, two of which represent the first morphological descriptions of an Austrodiplostomum sp. and Bolbophorus sp. metacercaria, respectively. A total of 15 silversides were collected from a commercial catfish pond and examined for trematode infection. These fish were parasitized by metacercariae of an Austrodiplostomum sp. (100 % prevalence) in the eyes and brain, a Bolbophorus sp. (86.7 % prevalence) in the musculature, and Clinostomum marginatum (33.3 % prevalence) in the musculature and fins. All three trematode species were characterized morphologically and molecularly by sequencing of the cytochrome c oxidase subunit 1 gene (CO1). In addition, the internal transcribed spacer 1 region (ITS1), 5.8S rRNA gene, and ITS2 region were determined for the Bolbophorus sp., which linked this metacercaria to a Bolbophorus sp. cercaria from a planorbid snail Planorbella trivolvis and an unnamed Bolbophorus sp. adult from the American white pelican Pelecanus erythrorhynchos. Furthermore, Biomphalaria havanensis snails were collected from the same pond and found actively shedding cercariae morphologically and molecularly consistent with a diplostomid cercaria reported from Bi . havanensis in catfish ponds in Mississippi, USA. Sequence comparisons deemed these cercariae conspecific to the Austrodiplostomum sp. from inland silverside described here. Channel catfish fingerlings were exposed to these cercariae at doses of 50 and 100 cercariae per fish. The infectivity of this Austrodiplostomum sp. in channel catfish was assessed at 10 and 20 days post exposure (dpe). Metacercariae were observed in both the eyes and brain of infected channel catfish, supporting molecular data that suggests the cercaria and metacercaria are both stages of a previously unidentified Austrodiplostomum sp. life cycle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Blasco-Costa I, Poulin R, Presswell B (2016) Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules. Parasitol Res 115:271–289

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Caffara M, Locke SA, Gustinelli A, Marcogliese DJ, Fioravanti ML (2011) Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. J Parasitol 97:884–891

    Article  PubMed  Google Scholar 

  • Doffitt CM, Pote LM, King DT (2009) Experimental Bolbophorus damnificus (Digenea: Bolbophoridae) infections in piscivorous birds. J Wildl Dis 45:684–691

    Article  PubMed  Google Scholar 

  • Dorr B, King DT, Tobin ME, Harrel JB, Smith PL (2004) Double-crested cormorant movements in relation to aquaculture in eastern Mississippi and western Alabama. Waterbirds 27:147–154

    Article  Google Scholar 

  • Drago FB, Lunaschi LI, Schenone M (2011) Digenean parasites of the Neotropic cormorant Phalacrocorax brasilianus (Gmelin, 1789) (Aves: Phalacrocoracidae) from Argentina: Distribution extension and new host records. Check List 6:871–875

  • Dronen NO (2009) Austrodiplostomum ostrowskiae n. sp. (Digenea: Diplostomidae: Diplostominae) from the double-crested cormorant, Phalacrocorax auritus (Phalacrocoracidae) from the Galveston, Texas area of the Gulf of Mexico, U.S.A. Comp Parasitol 76:34–39

    Article  Google Scholar 

  • Flowers JR, Poore MF, Mullen JE, Levy MG (2004) Digeneans collected from piscivorous birds in North Carolina, U.S.A. Comp Parasitol 71:243–244

    Article  Google Scholar 

  • Flowers JR, Poore MF, Pote LM, Litaker RW, Levy MG (2005) Cercariae of Bolbophorus damnificus and Bolbophorus sp. with notes on North American Bolbophorids. Comp Parasitol 72:220–226

    Article  Google Scholar 

  • García-Varela M, Sereno-Uribe AL, Pinacho-Pinacho CD, Domínguez-Domínguez O, Pérez-Ponce de León G (2015) Molecular and morphological characterization of Austrodiplostomum ostrowskiae Dronen, 2009 (Digenea: Diplostomatidae), a parasite of cormorants in the Americas. J Helminthol 90:174–185

    Article  PubMed  Google Scholar 

  • Georgieva S, Soldánova M, Pérez-del-Olmo A, Dangel DR, Sitko J, Sures B, Kostadinova A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. Intern J Parasitol 43:57–72

    Article  CAS  Google Scholar 

  • Glahn JF, King DT (2004) Bird depredation. In: Tucker CS, Hargreaves JA (eds) Biology and culture of channel catfish. Elsevier, Amsterdam, pp 503–529

    Chapter  Google Scholar 

  • Glahn JF, Harrel JB, Vyles C (1998) The diet of wintering double-crested cormorants feeding at lakes in the southeastern United States. Colonial Waterbirds 21:431–437

    Article  Google Scholar 

  • Griffin MJ, Khoo LH, Quiniou SM, O’Hear MM, Pote LM, Greenway TE, Wise DJ (2012) Genetic sequence data identifies the cercaria of Drepanocephalus spathans (Digenea: Echinostomatidae), a parasite of the double-crested cormorant (Phalacrocorax auritus), with notes on its pathology in juvenile channel catfish (Ictalurus punctatus). J Parasitol 98:967–972

    Article  CAS  PubMed  Google Scholar 

  • Griffin MJ, Khoo LH, Steadman JM, Ware C, Quiniou SM, Mischke CC, Greenway TE, Wise DJ (2014) Chronic pathology and longevity of Drepanocephalus spathans infections in juvenile channel catfish. J Aquat Anim Health 26:210–218

    Article  PubMed  Google Scholar 

  • Hawke JP, Khoo LH (2004) Infectious diseases. In: Tucker CS, Hargreaves JA (eds) Biology and culture of the channel catfish, 1st edn. Elsevier, Amsterdam, pp 387–443

    Chapter  Google Scholar 

  • King DT (1996) Movements of double-crested cormorants among winter roosts in the delta region of Mississippi. J Field Ornithol 67:205–211

    Google Scholar 

  • Karvonen A (2012) Diplostomum spathaceum and related species. Woo PTK and Buchmann K (eds) In Fish parasites: Pathobiology and protection. CAB International, Oxfordshire, U.K. pp 260–269

  • Kinsella JM, Spalding MG, Forrester DJ (2004) Parasitic helminthes of the American white pelican Pelecanus erythrorhynchos, from Florida, U.S.A. Comp Parasitol 71:29–36

    Article  Google Scholar 

  • Kohn A, Fernandes BMM, Baptista-Farias MFD (1995) Metacercariae of Diplostomum (Austrodiplostomum) compactum (Trematoda, Diplostomidae) in the eyes of Plagioscion squamosissimus (Teleostei, Sciaenidae) from the reservoir of the hydroelectric power station of Itaipu, Brazil. Mem Inst Oswaldo Cruz, Rio de Janeiro 90:341–344

    Article  Google Scholar 

  • Kudlai O, Kostadinova A, Pulis EE, Tkach VV (2015) A new species of Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae) from the double-crested cormorant Phalacrocorax auritus (Lesson) (Aves: Phalacrocoracidae) in North America. Syst Parasitol 90:221–230

    Article  PubMed  Google Scholar 

  • Levy MG, Flowers JR, Poore MF, Mullen JE, Khoo LH, Pote LM, Paperna L, Dzikowski R, Litaker RW (2002) Morphologic, pathologic, and genetic investigations of Bolbophorus species affecting cultured channel catfish in the Mississippi Delta. J Aquat Anim Health 14:235–246

    Article  Google Scholar 

  • Locke SA, McLaughlin JD, Dayanadan S, Marcogliese DJ (2010a) Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. Int J Parasitol 40:333–3432

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, McLaughlin JD, Marcogliese DJ (2010b) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Mol Ecol 19:2813–2827

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, Al-Nasiri FS, Caffara M, Drago F, Kalve M, Lapierre AR, McLaughlin JD, Nie P, Overstreet RM, Souza GTR, Takemoto RM, Marcogliese DJ (2015a) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. Int J Parasitol 45:841–855

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, Caffara M, Marcogliese DJ, Fioravanti ML (2015b) A large-scale molecular survey of Clinostomum (Digenea, Clinostomidae). Zool Scr 44:203–217

    Article  Google Scholar 

  • Matthews D, Cribb TH (1998) Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni n. sp. from Egretta intermedia. Syst Parasitol 39:199–208

    Article  Google Scholar 

  • Mitchell AJ, Goodwin AE, Levy MG (2006) Bolbophorus infections in cultured fathead minnow. J Aquat Anim Health 18:55–57

    Article  Google Scholar 

  • Morgan JAT, Blair D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: An aid to establishing relationships within the 37-collar-spine group. Parasitol 111:609–615

  • Morgan JAT, Blair D (1998) Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitol 116:289–297

    Article  CAS  Google Scholar 

  • Moszczynska A, Locke SA, McLaughlin D, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminthes. Mol Ecol Resour 9:75–82

    Article  CAS  PubMed  Google Scholar 

  • Niewiadomska K (2002) Family Diplostomidae Poirier, 1886. In Gibson DI, Jones A, and Bray RA (eds) Keys to the Trematoda. Vol. I. CAB International and the Natural History Museum, London U.K., pp 167–196

  • Novaes JLC, Ramos IP, Carvalho ED, Silva RJ (2006) Metacercariae of Diplostomum compactum Lutz, 1928 (Trematoda, Diplostomidae) in the eyes of acara Geophagus brasiliensis Quoy and Gaimard, 1824 (Teleostei, Cichlidae) from Barra Bonita Reservoir – São Paulo, Brazil. Arq Bras Med Vet Zootec 58:1229–1231

    Article  Google Scholar 

  • O’Hear M, Pote L, Yost M, Doffitt C, King T, Panuska C (2014) Morphologic and molecular identifications of digenetic trematodes in double-crested cormorants (Phalacrocorax auritus) from the Mississippi Delta, USA. J Wildl Dis 50:42–49

    Article  PubMed  Google Scholar 

  • Ostrowski de Núñez M (1968) Sobre el ciclo biologico de Austrodiplostomum mordax Szidat-Nani 1951. Neotrop 14:85–88

  • Ostroski de Núñez M (1977) El ciclo biolóogico de Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) Dubois 1970 (=Austrodiplostomum mordax Szidat y Nani 1951) (Trematoda, Diplostomatidae). Rev Mus Argent Cienc Nat Bernardino Rivadavia Parasitol 2:7–63

    Google Scholar 

  • Ostrowski de Núñez M (1982) Die entwicklungszyklen von Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) Dubois, 1970 und D. (A.) mordax (Szidat and Nani, 1951) n. comb. in Südamerika. Zool Anzeiger 208:393–404

    Google Scholar 

  • Overstreet RM, Curran SS (2004) Defeating diplostomoid dangers in USA catfish aquaculture. Folia Parasitol 51:153–165

    Article  PubMed  Google Scholar 

  • Overstreet RM, Curran SS, Pote LM, King DT, Blend CK, Grater WD (2002) Bolbophorus damnificus n. sp. (Digenea: Bolbophoridae) from the channel catfish Ictalurus punctatus and American white pelican Pelecanus erythrorhynchos in the USA based on life-cycle and molecular data. Syst Parasitol 52:81–96

    Article  PubMed  Google Scholar 

  • Paes JVK, Carvalho ED, Silva RJ (2010) Infection by Austrodiplostomum compactum metacercariae in fish from the Nova Avanhandava reservoir, Tietê river, São Paulo State, Brazil. Acta Sci Biol Sci 32:273–278

  • Pinto HA, Melo AL (2013) Biomphalaria straminea and Biomphalaria glabrata (Mollusca: Planorbidae) as new intermediate hosts of the fish eyefluke Austrodiplostomum compactum (Trematoda: Diplostomidae) in Brazil. J Parasitol 99:729–733

    Article  CAS  PubMed  Google Scholar 

  • Pinto HA, Caffara M, Fioravanti ML, Melo AL (2015) Experimental and molecular study of cercariae of Clinostomum sp. (Trematoda: Clinostomidae) from Biomphalaria spp. (Mollusca: Planorbidae) in Brazil. J Parasitol 101:108–113

    Article  CAS  PubMed  Google Scholar 

  • Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18:176–183

    Article  PubMed  Google Scholar 

  • Ramos IP, Franceschini L, Zago AC, Zica EOP, Wunderlich AC, Carvalho ED, Silva RJ (2013) New host records and a checklist of fishes infected with Austrodiplostomum compactum (Digenea: Diplostomidae) in Brazil. Rev Bras Parasitol Vet 22:511–518

    Article  PubMed  Google Scholar 

  • Ross ST (2001) Inland fishes of Mississippi. University Press of Mississippi, Jackson

    Google Scholar 

  • Rosser TG, Alberson NR, Khoo LH, Woodyard ET, Pote LM, Griffin MJ (2016) Characterization of the life cycle of a fish eye fluke, Austrodiplostomum ostrowskiae (Digenea: Diplostomidae), with notes on two other diplostomids infecting Biomphalaria havanensis (Mollusca: Planorbidae) from catfish aquaculture ponds in Mississippi, USA. J Parasitol 102:260–274

    Article  PubMed  Google Scholar 

  • Santos MD, Pimenta FDA, Martins ML, Takahashi HK, Marengoni NG (2002) Metacercariae of Diplostomum (Austrodiplostomum) compactum Lutz, 1928 (Digenea, Diplostomatidae) in fishes of Paraná River, Brazil. Prevalence, seasonality and intensity of infection. Acta Sci Biol Sci 24:475–480

    Google Scholar 

  • Siegmund I, Franjola R, Torres P (1997) Diplostomatid metacercariae in the brain of silversides from Lake Riñihue, Chile. J Wildl Dis 33:362–364

  • Terhune JS, Wise DJ, Khoo LH (2002) Bolbophorus confusus infections in channel catfish in northwestern Mississippi and effects of water temperature on emergence of cercariae from infected snails. N Am J Aquac 64:70–74

    Article  Google Scholar 

  • Van Steenkiste N, Locke SA, Castelin M, Marcogliese DJ, Abbott CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Mol Ecol Res 15:945–952

    Article  Google Scholar 

  • Wise DJ, Camus A, Schwedler T, Terhune J (2004) Health management. In: Tucker CS, Hargreaves JA (eds) Biology and culture of the channel catfish, 1st edn. Elsevier, Amsterdam, pp 482–488

    Google Scholar 

  • Wise DJ, Hanson TR, Tucker CS (2008) Farm-level economic impacts of Bolbophorus infections of channel catfish. N Am J Aquac 70:382–387

  • Yost MC (2008) The study of the life cycle of Bolbophorus damnificus and its pathology in the channel catfish (Ictalurus punctatus). PhD dissertation, Mississippi State University, Mississippi

    Google Scholar 

  • Zica EOP, Santos KR, Ramos IP, Zanatta AS, Carvalho ED, Silva RJ (2009) First case of an infection of the metacercariae of Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) in Hypostomus regani (Ihering, 1905) (Siluriformes: Loricariidae). Pan-Am J Aquat Sci 4:35–38

    Google Scholar 

  • Zica EOP, Brandão H, Zawadski CH, Nobile AB, Carvalho ED, Silva RJ (2011) The occurrence of Austrodiplostomum compactum (Lutz, 1928) (Digenea: Diplostomidae) metacercariae in the eyes of loricariid fish (Siluriformes: Osteichthyes: Loricariidae) from Brazil. J Helminthol 85:73–79

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge Mark Peterman and the catfish farmers for access to their farm. This was supported in part by the Mississippi State University College of Veterinary Medicine, the Mississippi Agricultural and Forestry Experiment Station, and the USDA-ARS Catfish Health Initiative (CRIS 6402-31320-002-02).

Author information

Authors and Affiliations

  1. Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39762, USA

    Thomas G. Rosser, Neely R. Alberson, Ethan T. Woodyard & Linda M. Pote

  2. Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, MS, 39762, USA

    Wes A. Baumgartner, Stephen R. Reichley & Matt J. Griffin

  3. Thad Cochran National Warmwater Aquaculture Center, Delta Research and Extension Center, Mississippi State University, Stoneville, MS, 38776, USA

    Stephen R. Reichley, David J. Wise & Matt J. Griffin

  4. Mississippi Agriculture and Forestry Experiment Station, Mississippi State University, Mississippi State, MS, 39762, USA

    David J. Wise

Authors
  1. Thomas G. Rosser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wes A. Baumgartner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Neely R. Alberson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ethan T. Woodyard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephen R. Reichley
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David J. Wise
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Linda M. Pote
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Matt J. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matt J. Griffin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosser, T.G., Baumgartner, W.A., Alberson, N.R. et al. Austrodiplostomum sp., Bolbophorus sp. (Digenea: Diplostomidae), and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae in inland silverside Menidia beryllina from catfish aquaculture ponds, with notes on the infectivity of Austrodiplostomum sp. cercariae in channel catfish Ictalurus punctatus . Parasitol Res 115, 4365–4378 (2016). https://doi.org/10.1007/s00436-016-5222-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-016-5222-z

Keywords

Search

Navigation