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New insights on the role of the holoplanktonic mollusk Firoloida desmarestia (Gastropoda: Pterotracheidae) as host for digenetic trematodes

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Abstract

Interactions of holoplanktonic mollusks with symbionts and parasites are poorly known. We investigated the ecology of infection (prevalence, intensity, and abundance) in Firoloida desmarestia, caught during two sampling campaign sessions in 2012, off the Baja California Peninsula, Mexico (IMECOCAL, 83 stations) and a coastal research center near La Sorpresa Beach, Baja California Sur, in the Gulf of California (14 stations). Only females of F. desmarestia were parasitized. Hemiuroidea parthenita rediae infected 1% of F. desmarestia population at IMECOCAL, whereas young unencysted metacercariae stages of Opechona pyriformis (Lepocreadiidae) parasitized 6.6% of the same host species at La Sorpresa. Overall, finding of rediae and metacercariae represent new geographical and host records and shows that F. desmarestia has a dual host function in the life cycle of trematodes. As first intermediate host, F. desmarestia harbors hemiuroid rediae, functioning as the source of infection to other zooplanktonic groups by dispersing successive cercariae. As second intermediate hosts, it harbors infective unencysted metacercariae stages of O. pyriformis, which parasitize nektonic predators (fish), most likely through trophic interaction. Our results suggest that some trematodes are able to spend their entire life cycle infecting only pelagic hosts. Parasite–F. desmarestia interaction is shown in a conceptual model, where we propose that transmission of trematodes may occur between individuals of F. desmarestia within the same swarm. Relevance of F. desmarestia as a potential host in which life cycle abbreviation of trematodes may take place is discussed. This is the first quantitative study of helminth interaction on F. desmarestia in the Eastern Pacific.

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References

  • Angulo-Campillo OJ (2010) Taxocenosis de moluscos holoplanctonicos (Mollusca, Gastropoda) y su relación biogeográfica en el Golfo de California. Dissertation, Centro Interdisciplinario de Ciencias Marinas, La Paz

  • Averbuj A, Cremonte F (2010) Parasitic castration of Buccinanops cochlidium (Gastropoda: Nassariidae) caused by a lepocreadiid digenean in San José gulf, Argentina. J Helminthol 84:381–389

    Article  PubMed  CAS  Google Scholar 

  • Barnett LJ, Miller TL, Cribb TH (2014) A review of the currently recognised opecoelid cercariae, including the identification and emergence ecology of Cercaria capricornia XII (Digenea: Opecoelidae) from Nassarius olivaceus (Gastropoda: Nassariidae) in Central Queensland, Australia. Parasitol Int 63:670–682

    Article  PubMed  Google Scholar 

  • Batistić M, Kršinić F, Jasprica N, Carić M, Viličić D, Lučić D (2004) Gelatinous invertebrate zooplankton of the south Adriatic: species composition and vertical distribution. J Plankton Res 26:459–474

    Article  Google Scholar 

  • Blackburn M (1956) Sonic scattering layers of heteropods. Nature 177:374–375

    Article  Google Scholar 

  • Bonnevie K (1916) Mitteilung über Pteropoden. L. Beobachtungen über den Geschlechtsapparat von Cuvierina columnella Rang. Jena Zeits Med Nat Jenaische Zeitschr Naturwiss 54:245–276

    Google Scholar 

  • Briz LMD, Martorelli SR, Genzano GN, Mianzan HW (2012) Parasitism (Trematoda, Digenea) in medusae from the southwestern Atlantic Ocean: medusa hosts, parasite prevalences, and ecological implications. Hydrobiologia 690:215–226

    Article  Google Scholar 

  • Bullard SA, Overstreet RM (2008) Digeneans as enemies of fishes. J Fish Dis 2:817–976

    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  PubMed  CAS  Google Scholar 

  • Daponte MC, de Pertierra AAG, Palmieri MA, de Núñez MO (2006) Parasite infections (Trematoda, Digenea) of Sagitta friderici (Chaetognatha) from the southwestern Atlantic Ocean: prevalence and distribution. Dis Aquat Org 71:225–232

    Article  PubMed  Google Scholar 

  • Daponte MC, de Pertierra AG, Palmieri MA, de Nuñez MO (2008) Monthly occurrence of parasites of the chaetognath Sagitta friderici off mar del Plata, Argentina. J Plankton Res 30:567–576

    Article  Google Scholar 

  • Dawes B (1958) Sagitta as a host of larval trematodes, including a new and unique type of cercaria. Nature 182:960–961. https://doi.org/10.1038/182960a0

    Article  PubMed  CAS  Google Scholar 

  • Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci 105:11482–11489

    Article  PubMed  PubMed Central  Google Scholar 

  • Esch GW, Barger MA, Fellis KJ (2002) The transmission of digenetic trematodes: style, elegance, complexity. Integr Comp Biol 42:304–312

    Article  PubMed  Google Scholar 

  • Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmissions, and evolution of digenetic trematodes, 1st edn. Springer Science and Business Media, Boston

    Book  Google Scholar 

  • Gómez del Prado-Rosas MDC, Segura-Puertas L, Álvarez-Cadena JN, Lamothe-Argumedo R (2000) Opechona pyriforme metacercaria (Trematoda: Lepocreadiidae) in Eirene lactaea (Cnidaria: Hydroidomedusae) from a reef lagoon in the Mexican Caribbean Sea. An Inst Biol Ser Zool 71:1–6

    Google Scholar 

  • Hochberg FG, Seapy RR (1985) Parasites of holopelagic molluscs. Int Symp Mar Plankton July 1984Tokai University, Shimizu Japan. Bull mar Sci 37:767 (Abstract)

  • Jamieson BGM (1966) Larval stages of the progenetic trematode Parahemiurus bennettae Jamieson, 1966 (Digenea, Hemiuridae) and the evolutionary origin of cercariae. Proc R Soc Queensland 77:81–91

    Google Scholar 

  • Jarling C, Kapp H (1985) Infestation of Atlantic chaetognaths with helminths and ciliates. Dis Aquat Org 1:23–28

    Article  Google Scholar 

  • Júnior MN, Diaz-Briz L, Haddad MA (2013) New records of Opechona sp metacercariae (Digenea: Trematoda) on hydromedusae from south Brazil. Mar Biodivers Rec 6:1–4

    Article  Google Scholar 

  • Køie M (1975) On the morphology and life-history of Opechona bacillaris (Molin, 1859) Looss, 1907 (Trematoda, Lepocreadiidae). Ophelia 13:63–86

    Article  Google Scholar 

  • Køie M (1982) The redia, cercaria and early stages of Aporocotyle simplex Odhner, 1900 (Sanguinicolidae) a digenetic trematode which has a polychaete annelid as the only intermediate host. Ophelia 21:115–145

    Article  Google Scholar 

  • Køie M (1995) The life-cycle and biology of Hemiurus communis Odhner, 1905 (Digenea, Hemiuridae). Parasite 2:195–202

    Article  Google Scholar 

  • Køie M, Karlsbakk E, Nylund A (2002) A cystophorous cercaria and metacercaria in Analis entails (L.) (Mollusca, Scaphopoda) in Norwegian waters, the larval stage of Lecithophyllum botryophorum (Olsson, 1868) (Digenea, Lecithasteridae). Sarsia 87:302–311

    Article  Google Scholar 

  • Kondo Y, Ohtsuka S, Hirabayashi T, Okada S, Ogawa NO, Ohkouchi N, Shimazu T, Nishikawa J (2016) Seasonal changes in infection with trematode species utilizing jellyfish as hosts: evidence of transmission to definitive host fish via medusivory. Parasite 23:1–16

    Article  Google Scholar 

  • Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513

    Article  Google Scholar 

  • Lalli CM, Gilmer RW (1989) Pelagic snails: the biology of holoplanktonic gastropod mollusks. Stanford University Press, Stanford

    Google Scholar 

  • Land MF (1982) Scanning eye movements in a heteropod mollusk. J Exp Biol 96:427–430

  • Lebour MV (1917) Some parasites of Sagitta bipunctata. J Mar Biol Assoc UK 11:201–206

    Article  Google Scholar 

  • Lemus-Santana E, Sanvicente-Anorve L, Hermoso-Salazar M, Flores-Coto C (2014) The holoplanktonic Mollusca from the southern Gulf of Mexico. Part 1: heteropods. Cah Biol Mar 55:229–239

    Google Scholar 

  • Lemus-Santana E, Sanvicente-Añorve L, Alatorre-Mendieta M, Flores-Coto C (2015) Population structure and mating encounter rates in a marine pelagic invertebrate, Firoloida desmarestia (Mollusca). Sex Early Dev Aquat Org 1:163–173

  • Lester RJ, Newman LJ (1986) First rediae and cercariae to be described from heteropods. J Parasitol 72:95–197

    Article  Google Scholar 

  • Leuckart R (1854) Bericht über die Leistungen in der Naturgeschichte der niederen Thiere während der Jahre 1848-1853. Archiv für Naturgeschichte 20:289–473

    Google Scholar 

  • Lozano-Cobo H, Gómez del Prado-Rosas MDC, Sánchez-Velasco L, Gómez-Gutiérrez J (2017) Seasonal variation in chaetognath and parasite species assemblages along the northeastern coast of the Yucatan peninsula. Dis Aquat Org 124:55–75

    Article  PubMed  Google Scholar 

  • Macfarlane WV (1951) The life cycle of Stegodexamene anguillae n.G., n.Sp., an allocreadiid trematode from New Zealand. Parasitology 41:1–10

    Article  PubMed  CAS  Google Scholar 

  • MacLean SA, Farley CA, Newman MW, Rosenfield A (1981) Gross and microscopic observations on some biota from deep water dumpsite 106. In: Ketchum BH, Kester DR, Park PK (eds) Ocean dumping of industrial wastes, 1st edn. Plenum Press, New York, pp 421–437

    Chapter  Google Scholar 

  • Marcogliese DJ (1995) The role of zooplankton in the transmission of helminth parasites to fish. Rev Fish Biol Fish 5:336–371

    Article  Google Scholar 

  • Martell-Hernández LF, Ocaña-Luna A, Sánchez-Ramírez M (2011) Seasonal occurrence of Opechona pyriforme metacercariae (Digenea: Lepocreadiidae) in Eirene tenuis medusae (hydrozoa: Leptothecata) from a hypersaline lagoon in western Gulf of Mexico. J Parasitol 97:68–71

    Article  PubMed  Google Scholar 

  • Martorelli SR (1994) Una nueva cercaria de tipo cystophorous (Digenea, Hemiuriformes) en Potamolithus agapetus (Mollusca, Hydrobiidae): comportamiento de atracción del hospedador. Iheringia Ser Zool 76:15–19

    Google Scholar 

  • Martorelli SR (1996) First record of encysted metacercaria in hydrozoan jellyfishes and ctenophores of the southern Atlantic. J Parasitol 82:352–353

    Article  PubMed  CAS  Google Scholar 

  • Martorelli SR (2001) Digenean parasites of jellyfish and ctenophores of the southern Atlantic. Hydrobiologia 451:305–310

    Article  Google Scholar 

  • Morales-Ávila JR, Gómez-Gutiérrez J, Gómez del Prado-Rosas MDC, Robinson CJ (2015) Larval trematodes Paronatrema mantae and Copiatestes sp. parasitize gulf of California krill (Nyctiphanes simplex, Nematoscelis difficilis). Dis Aquat Org 116:23–35

    Article  PubMed  CAS  Google Scholar 

  • Morandini AC, Martorelli SR, Marques AC, Silveira FLD (2005) Digenean metacercaria (Trematoda, Digenea, Lepocreadiidae) parasitizing "coelenterates" (Cnidaria, Scyphozoa and Ctenophora) from southeastern Brazil. Braz J Oceanogr 53:39–45

    Article  Google Scholar 

  • Moreno-Alcántara M, Aceves-Medina G, Angulo-Campillo O, Murad-Serrano JP (2014) Holoplanktonic molluscs (Gastropoda: Pterotracheoidea, Thecosomata and Gymnosomata) from the southern Mexican Pacific. J Molluscan Stud 80:131–138

    Article  Google Scholar 

  • Newman LJ (1990) Holoplanktonic molluscs (Gastropoda; Thecosomata, Gymnosomata and Heteropoda) from the waters of Australia and Papua New Guinea: their taxonomy, distribution and biology. Dissertation, University of Queensland, Australia p 191

  • Niewiadomska K, Pojmanska T (2011) Multiple strategies of digenean trematodes to complete their life cycles. Wiad Parazytol 57:233–241

    Google Scholar 

  • Nogueira-Júnior MN, Diaz-Briz L, Haddad MA (2013) New records of Opechona sp. metacercariae (Digenea: Trematoda) on hydromedusae from South Brazil. Mar Biodivers Rec 6:1–4

    Article  Google Scholar 

  • Nogueira-Júnior MN, Briz LMD, Haddad MA (2015) Monthly and inter-annual variations of Opechona sp. (Digenea: Lepocreadiidae) parasitizing scyphomedusae off southern Brazil. Mar Biol 162:391–400

    Article  Google Scholar 

  • Øresland V, Bray RA (2005) Parasites and headless chaetognaths in the Indian Ocean. Mar Biol 147:725–734

    Article  Google Scholar 

  • Parker GA, Chubb JC, Ball MA, Roberts GN (2003) Evolution of complex life cycles in helminth parasites. Nature 425:480–484

    Article  PubMed  CAS  Google Scholar 

  • Pearson JC (1992) On the position of the digenean family Heronimidae: an inquiry into a cladistics classification of the Digenea. Syst Parasitol 21:81−166

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Reimer LW, Berger C, Heuer B, Lainka H, Rosenthal I, Scharnweber I (1971) On the distribution of larvae of helminths in plankton animals of the North Sea. Parazitilogiya 5:542–550 (in Russian with English summary)

    Google Scholar 

  • Richter G, Seapy RR (1999) Heteropoda. In: Boltovskoy D (ed) South Atlantic zooplankton. Backhuys, Leiden, pp 621–647

    Google Scholar 

  • Seapy RR (1990) Patterns of vertical distribution in epipelagic heteropod molluscs off Hawaii. Mar Ecol Prog Ser 60:235–246

    Article  Google Scholar 

  • Seapy RR (2008) Offshore–inshore and vertical distributional patterns of heteropod mollusks off leeward Oahu, Hawaii. Mar Biol 154:985–995

    Article  Google Scholar 

  • Seapy R, Lalli CM, Wells FE (2003) Heteropoda from Western Australia waters. In: Wells FE, Walker DI, Jones DS (eds) The marine flora and fauna of Dampier, Western Australia. Western Australian Museum, Perth, pp 513–546

    Google Scholar 

  • Slankis AY, Shevchenko GG (1974) Data on the infestation of planktonic invertebrates with helminth larvae in the western part of the equatorial zone of the Pacific. Trans Pac Inst Fish Oceanogr (Vladivostok) 88:129–138

    Google Scholar 

  • Smith PE, Richardson S (1979) Técnicas modelo para la prospección de huevos y larvas de peces pelágicos. Documentos Técnicos de Pesca 175. FAO, Rome (in Spanish)

    Google Scholar 

  • Sousa WP (1992) Interspecific interactions among larval trematode parasites of freshwater and marine snails. Am Zool 32:583–592

    Article  Google Scholar 

  • Stunkard HW (1969) The morphology and life-history of Neopechona pyriforme (Linton, 1900) n. Gen., n. Comb. (Trematoda: Lepocreadiidae). Biol Bull 136:96–113

    Article  Google Scholar 

  • Stunkard HW (1980) Successive hosts and developmental stages in the life history of Neopechona cablei sp. n. (Trematoda: Lepocreadiidae). J Parasitol 66:636–641

    Article  Google Scholar 

  • Taylor D, Berner L (1970) The heteropoda (Mollusca: Gastropoda). In: Pequegnat JC, Chace FA (eds) Contributions on the biology of the Gulf of Mexico. Texas A&M University Oceanographic Studies 1, Gulf Publishing, Houston, pp 231–244

    Google Scholar 

  • Théodoridès J (1989) Parasitology of marine zooplankton. Adv Mar Biol 25:117–177

    Article  Google Scholar 

  • Thiriot-Quievreux C (1973) Heteropoda. Oceanogr Mar Biol Annu Rev 11:237–261

    Google Scholar 

  • van der Spoel S, Dadon JR (1999) Pteropoda. In: Boltovskoy D (ed) South Atlantic zooplankton. Backhuys, Leiden, pp 649–706

    Google Scholar 

  • Vande-Vusse FJ (1980) A pelagic gastropod first intermediate host for a hemiuroid trematode. J Parasitol 66:167–168

    Article  Google Scholar 

  • White AW (1977) Dinoflagellate toxins as probable cause of an Atlantic herring (Clupea harengus harengus) kill, and pteropods as apparent vector. J Fish Res Board Can 34:2421–2424

    Article  CAS  Google Scholar 

  • Yip SY (1984) Parasites of Pleurobrachia pileus Müller, 1776 (Ctenophora), from Galway Bay, western Ireland. J Plankton Res 6:107–121

    Article  Google Scholar 

  • Zimmermann MR, Luth KE, Esch GW (2016) Transmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites. Acta Parasitol 61:680–688

    Article  PubMed  Google Scholar 

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Acknowledgements

We deeply thank Sylvia P. Adelheid Jiménez Rosenberg for the samples used in this research (collected by the Investigaciones Mexicanas de la Corriente de California Program, IMECOCAL) and funded by the scientific initiatives “Variabilidad interanual de la producción primaria en frentes oceánicos de la Corriente de California frente a Baja California” (CONACYT 254745). We thank the scientific and technical staff of the R/V Francisco de Ulloa for assistance at sea. Laboratory work and data analysis was also supported by the Instituto Politécnico Nacional through scientific initiatives “Taxonomía y distribución vertical de larvas de peces al sur del Golfo de California y el Océano Pacífico adyacente” SIP20170376.

The Consejo Nacional de Ciencia y Tecnolgía supported this research through the scientific initiative “Variabilidad interanual de la producción primaria en frentes oceánicos de la Corriente de California frente a Baja California” (CONACYT 254745). R.J.S.M. was supported by a CICIMAR-IPN/COFAA grant.

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Morales-Ávila, J.R., Saldierna-Martínez, R.J., Moreno-Alcántara, M. et al. New insights on the role of the holoplanktonic mollusk Firoloida desmarestia (Gastropoda: Pterotracheidae) as host for digenetic trematodes. Parasitol Res 117, 2149–2158 (2018). https://doi.org/10.1007/s00436-018-5902-y

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