Advertisement

Polar Biology

, Volume 42, Issue 6, pp 1175–1182 | Cite as

Identification assisted by molecular markers of larval parasites in two limpet species (Patellogastropoda: Nacella) inhabiting Antarctic and Magellan coastal systems

  • K. Flores
  • Z. López
  • D. Levicoy
  • C. P. Muñoz-Ramírez
  • C. González-Wevar
  • M. E. Oliva
  • L. CárdenasEmail author
Original Paper
  • 65 Downloads

Abstract

In the Southern Ocean, many parasites of vertebrates (mainly helminth groups) have been recognized as endemic species, but parasites of marine invertebrates remain almost unknown. It is reasonable to assume that digenean larvae will parasitize gastropods, bivalves, amphipods, and annelids, the usual first and second intermediate hosts for those parasites. Here, using an identification assisted by molecular markers, we report the Digenea species parasitizing the most abundant limpet species inhabiting ice-free rocky intertidal and subtidal zones of the Southern Ocean, viz. Nacella concinna from the Antarctic and Nacella deaurata from the Magellan region. The limpets harbored larval Digenea (two metacercariae and one sporocyst). Phylogenetic analysis based on the multilocus tree supported the hypothesis that N. concinna is parasitized by a species of Gymnophallidae, whereas the limpet N. deaurata is parasitized by Gymnophalloides nacellae and a species of Renicolidae. In addition, differences in prevalence and intensity were also recorded between the two compared host species and also from other congeneric species. This new knowledge in parasite species in marine invertebrates from the Southern Ocean reveals the presence of a particular parasite fauna and confirms the utility of molecular tools to identify biodiversity still scarcely known.

Keywords

Nacella concinna Nacella deaurata Digenean parasites Molecular markers Southern Ocean 

Notes

Acknowledgements

This work was supported and funded by the Instituto Antártico Chileno through the Inach RT 02–15 Grant, the National Commission of Scientific and Technological Investigation of Chile through the Fondo de Financiamiento de Centros de Investigación en Áreas Prioritarias (FONDAP) programme research center: Dynamics of High Latitude Marine Ecosystems (grant no. 15150003), and FONDECYT (postdoctoral grant no. 3180331 to C.P.M.-R.).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Supplementary material

300_2019_2511_MOESM1_ESM.docx (17 kb)
Supplementary file 1 (DOCX 17 kb)
300_2019_2511_MOESM2_ESM.r (6 kb)
Supplementary file 2 (R 6 kb)
300_2019_2511_MOESM3_ESM.csv (39 kb)
Supplementary file 3 (CSV 38 kb)
300_2019_2511_MOESM4_ESM.pptx (61 kb)
Supplementary file 4 (PPTX 60 kb)

References

  1. Bagnato E, Gilardoni C, Di Giorgio G, Cremonte F (2015) A checklist of marine larval trematodes (Digenea) in molluscs from Argentina, Southwestern Atlantic coast. Check List 11(4):1706CrossRefGoogle Scholar
  2. Barbosa A, Palacios MJ (2009) Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biol 32:1095–1115CrossRefGoogle Scholar
  3. Bartoli P (1974) Recherches sur les Gymnophallidae F. N. Morozov, (1955) (Digenea) Parasites d’oiseaux des côtes de Camargue: Systématique, biologie et ecologie. Thèse. Universite d’Aix-Marseille, Marseille, FranceGoogle Scholar
  4. Blakeslee AM, Altman I, Miller AW, Byers JE, Hamer CE, Ruiz GM (2012) Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges. J Biogeogr 39:609–622CrossRefGoogle Scholar
  5. Blasco-Costa I, Cutmore SC, Miller TL, Nolan MJ (2016) Molecular approaches to trematode systematics: ‘best practice’and implications for future study. Syst Parasitol 93:295–306CrossRefGoogle Scholar
  6. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput Biol 10:e1003537CrossRefGoogle Scholar
  7. Bray RA, Gibson D, Jones A (2008) Keys to the Trematoda. CAB International and Natural History Museum, LondonCrossRefGoogle Scholar
  8. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefGoogle Scholar
  9. Byers JE, Malek AJ, Quevillon LE, Altman I, Keogh CL (2015) Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale. Oikos 124:1511–1519CrossRefGoogle Scholar
  10. Cremonte F, 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 99:85–92CrossRefGoogle Scholar
  11. Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58:198–202CrossRefGoogle Scholar
  12. Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257CrossRefGoogle Scholar
  13. Diaz JI, Fusaro B, Vidal V, González-Acuña D, Costa ES, Dewar M, et al. (2017) Macroparasites in Antarctic penguins. In: Biodiversity and Evolution of Parasitic Life in the Southern Ocean, Springer, Switzerland, pp 183–204Google Scholar
  14. Falk BG, Perkins SL (2013) Host specificity shapes population structure of pinworm parasites in Caribbean reptiles. Mol Ecol 22:4576–4590CrossRefGoogle Scholar
  15. Froeschke G, von der Heyden S (2014) A review of molecular approaches for investigating patterns of coevolution in marine host–parasite relationships. Adv Parasit 84:209–252CrossRefGoogle Scholar
  16. Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda (Vol. 2). CAB International and Natural History Museum, LondonGoogle Scholar
  17. Gilardoni C, Di Giorgio G, Bagnato E, Cremonte F (2018) Survey of trematodes in intertidal snails from Patagonia, Argentina: new larval forms and diversity assessment. J Helminthol 93:342–351Google Scholar
  18. González-Wevar CA, Nakano T, Cañete JI, Poulin E (2011) Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province. Mol Ecol 20:1936–1951CrossRefGoogle Scholar
  19. Hall KA, Cribb TH, Barker SC (1999) V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data. Syst Parasitol 43:81–92CrossRefGoogle Scholar
  20. Hassouna N, Mithot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583CrossRefGoogle Scholar
  21. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192CrossRefGoogle Scholar
  22. Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–385CrossRefGoogle Scholar
  23. Hudson P, Greenman J (1998) Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol 13:387–390CrossRefGoogle Scholar
  24. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
  25. Klimpel S, Kuhn T, Mehlhorn H (eds) (2017) Biodiversity and evolution of parasitic life in the Southern Ocean. Springer, SwitzerlandGoogle Scholar
  26. Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15:111–115CrossRefGoogle Scholar
  27. Loos-Frank B (1969) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes. I. Die Alternativzyklen von Gymnophallus choledochus Odhner, 1900. Z. Parasitenkd 32:135–156Google Scholar
  28. Loos-Frank B (1971) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes. IV. Übersicht über die gymnophalliden Larven aus Mollusken der Gezeitenzone. Z. Parasitenkd 36:206–232Google Scholar
  29. López Z, Cardenas L, Runil F, González MT (2015) Contrasting definitive hosts as determinants of the genetic structure in a parasite with complex life cycle along the south-eastern Pacific. Mol Ecol 24:1060–1073CrossRefGoogle Scholar
  30. MacKenzie K (2017) The History of Antarctic Parasitological Research. Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Springer, Switzerland, pp 13–31CrossRefGoogle Scholar
  31. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp 1–8Google Scholar
  32. Morriconi E (1999) Reproductive biology of the limpet Nacella (P.) deaurata (Gmelin, 1791) in bahía Lapataia (Beagle Channel). Scientia Marina 63:417–426CrossRefGoogle Scholar
  33. Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:101–117CrossRefGoogle Scholar
  34. Muñoz G, López Z, Cardenas L (2013) Morphological and molecular analyses of larval trematodes in the intertidal bivalve Perumytilus purpuratus from central Chile. J Helminthol 87:356–363CrossRefGoogle Scholar
  35. Oliva ME, Valdivia IM, Cardenas L, George-Nascimento M, González K, Guiñez R, Cuello D (2010) Molecular and experimental evidence refuse the life cycle of Proctoeces lintoni (Fellodistomidae) in Chile. Parasitol Res 106:737–740CrossRefGoogle Scholar
  36. Peribañez MA, Ordovás L, Benito J, Benejam L, Gracia MJ, Rodellar C (2011) Prevalence and sequence comparison of Phyllodistomum folium from zebra mussel and from freshwater fish in the Ebro River. Parasitol Int 60:59–63CrossRefGoogle Scholar
  37. Picken GB (1980) The distribution, growth, and reproduction of the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908). J Exp Mar Biol Ecol 42:71–85CrossRefGoogle Scholar
  38. Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18:176–183CrossRefGoogle Scholar
  39. Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution, Washington D.C., p 216Google Scholar
  40. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07–0, URL https://www.R-project.org/. R Found. Stat. Comput. Vienna, Austria.
  41. Rohde K (2005) Marine parasitology. CSIRO Publishing, AustraliaCrossRefGoogle Scholar
  42. Rosenfeld S, Marambio J, Ojeda J, Rodríguez JP, González-Wevar C, Gerard K et al (2018) Trophic ecology of two co-existing Sub-Antarctic limpets of the genus Nacella: spatio-temporal variation in food availability and diet composition of Nacella magellanica and N. deaurata. ZooKeys 738:1–25CrossRefGoogle Scholar
  43. Ríos C, Mutschke E (1999) Community structure of intertidal boulder-cobble fields in the Straits of Magellan, Chile. Sci Mar 63:193–201Google Scholar
  44. Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I (2018) GenBank. Nucleic Acids Res 47:D94–D99CrossRefGoogle Scholar
  45. Scholz T (2002) Family Gymnophallidae Odhner, 1905. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda. CAB International and Natural History Museum, London, pp 245–251CrossRefGoogle Scholar
  46. Silvestro D, Michalak I (2012) RaxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337CrossRefGoogle Scholar
  47. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefGoogle Scholar
  48. Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15CrossRefGoogle Scholar
  49. Valdovinos C, Ruth M (2005) Nacellidae limpets of the southern end of South America: taxonomy and distribution. Rev Chil Hist Nat 78:497–517CrossRefGoogle Scholar
  50. Wilcox TP, Zwickl DJ, Heath TA, Hillis DM (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Mol Phylogenet Evol 25:361–371CrossRefGoogle Scholar
  51. Zdzitowiecki K (1988) Occurrence of digenetic trematodes in fishes off South Shetlands (Antarctic). Acta Parasitol Pol 33:55–72Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • K. Flores
    • 1
  • Z. López
    • 2
    • 3
  • D. Levicoy
    • 1
  • C. P. Muñoz-Ramírez
    • 4
    • 5
  • C. González-Wevar
    • 6
  • M. E. Oliva
    • 7
    • 8
  • L. Cárdenas
    • 1
    Email author
  1. 1.Centro FONDAP-IDEAL, Inst. de Ciencias Ambientales & EvolutivasUniversidad Austral de ChileValdiviaChile
  2. 2.Instituto de Ecología Y Biodiversidad (IEB), Facultad de CienciasUniversidad de ChileSantiagoChile
  3. 3.Laboratorio de Ecosistemas Marinos Antárticos Y Sub-Antárticos (LEMAS)Universidad de MagallanesPunta ArenasChile
  4. 4.Centro de Investigación en Biodiversidad Y Ambientes Sustentables (CIBAS)Universidad Católica de La Santísima ConcepciónConcepciónChile
  5. 5.Facultad de CienciasUniversidad Católica de La Santísima ConcepciónConcepciónChile
  6. 6.Centro FONDAP-IDEAL, Instituto de Ciencias Marinas Y LimnológicasUniversidad Austral de ChileValdiviaChile
  7. 7.Instituto de Ciencias Naturales Alexander Von Humboldt, FACIMARUniversidad de AntofagastaAntofagastaChile
  8. 8.Instituto Milenio de Oceanografía, Universidad de ConcepciónConcepciónChile

Personalised recommendations