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Effects of salinity on multiplication and transmission of an intertidal trematode parasite

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Abstract

Salinity levels vary spatially in coastal areas, depending on proximity to freshwater sources, and may also be slowly decreasing as a result of anthropogenic climatic changes. The impact of salinity on host–parasite interactions is potentially a key regulator of transmission processes in intertidal areas, where trematodes are extremely common parasites of invertebrates and vertebrates. We investigated experimentally the effects of long-term exposure to decreased salinity levels on output of infective stages (cercariae) and their transmission success in the trematode Philophthalmus sp. This parasite uses the snail Zeacumantus subcarinatus as intermediate host, in which it asexually produces cercariae. After leaving the snail, cercariae encyst externally on hard substrates to await accidental ingestion by shorebirds, which serve as definitive hosts. We found that at reduced salinities (25 or 30 psu), the cercarial output of the parasite was lower, the time taken by cercariae to encyst was longer, fewer cercariae successfully encysted and encysted parasites had lower long-term survival than at normal seawater salinity (35 psu). The strong effect of salinity on the replication and transmission of this parasite suggests that there may be sources and sinks of transmission to birds along coastal areas, depending on local salinity conditions. Also, unless it evolves to adapt to changing conditions, the predicted reduction in salinity as a consequence of climate change may have negative impact on the parasite’s abundance.

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References

  • Adam P (1993) Saltmarsh ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Anderson P, Nowosielski J, Croll N (1976) The emergence of cercariae of Trichobilharzia ocellata and its relationship to the activity of its snail host Lymnaea stagnalis. Can J Zool 54:1481–1487

    Article  CAS  Google Scholar 

  • Berger V, Kharazova A (1997) Mechanisms of salinity adaptations in marine molluscs. Hydrobiologia 355:115–126

    Article  CAS  Google Scholar 

  • Cheng R, Casulli V, Gartner J (1993) Tidal, residual, intertidal mudflat (TRIM) model and its applications to San Francisco Bay, California. Estuar Coast Shelf Sci 36:235–280

    Article  Google Scholar 

  • Cheung S, Lam S (1995) Effect of salinity, temperature and acclimation on oxygen consumption of Nassarius festivus (Powys, 1835)(Gastropoda: Nassariidae). Comp Biochem Physiol A 111:625–631

    Article  Google Scholar 

  • Crain C, Silliman B, Bertness S, Bertness M (2004) Physical and biotic drivers of plant distribution across estuarine salinity gradients. Ecology 85:2539–2549

    Article  Google Scholar 

  • Deschaseaux E, Taylor A, Maher W, Davis A (2010) Cellular responses of encapsulated gastropod embryos to multiple stressors associated with climate change. J Exp Mar Biol Ecol 383:130–136

    Article  CAS  Google Scholar 

  • Dixon K (1975) The structure and composition of the cyst wall of the metacercaria of Cloacitrema narrabeenensis (Howell & Bearup, 1967) (Digenea: Philophthalmidae). Int J Parasitol 5:113–118

    Article  CAS  Google Scholar 

  • Evans N (1982) Effects of copper and zinc on the life cycle of Notocotylus attenuatus (Digenea: Notocotylidae). Int J Parasitol 12:363–369

    Article  CAS  Google Scholar 

  • Fredensborg BL, Mouritsen KN, Poulin R (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Mar Ecol Prog Ser 290:109–117

    Article  Google Scholar 

  • Graczyk T, Shiff C (1994) Viability of Notocotylus attenuatus (Trematoda: Notocotylidae) metacercariae under adverse conditions. J Wildl Dis 30:46–50

    CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  CAS  Google Scholar 

  • Hylleberg J (1975) The effect of salinity and temperature on egestion in mud snails (Gastropoda: Hydrobiidae). Oecologia 21:279–289

    Article  Google Scholar 

  • Ingole B, Parulekar A (1998) Role of salinity in structuring the intertidal meiofauna of a tropical estuarine beach: Field evidence. Indian J Mar Sci 27:356–361

    CAS  Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

  • Kalantan A, Arfin M, Al-Arefi H, Bobshait H, Hamadah S, Al-Thawab F, Al-Shamrani A (1997) Occurrence of larval Philophthalmus gralli (Mathis and Leger, 1910) in freshwater snail Melanoides tuberculatus (Muller) from Al-Hafuf, Saudi Arabia and its development into adult in various experimental hosts. Parasitol Int 46:127–136

    Article  Google Scholar 

  • Kanev I, Radev V, Fried B (2005) Family Philophthalmidae Looss, 1899. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI Publishing, Wallingford, pp 87–97

    Google Scholar 

  • Knauss J (1978) Introduction to physical oceanography. Prentice Hall, New Jersey

    Google Scholar 

  • Koprivnikar J, Poulin R (2009) Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitol Res 105:957–965

    Article  Google Scholar 

  • Koprivnikar J, Lim D, Fu C, Brack S (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitol Res 106:1167–1177

    Article  Google Scholar 

  • Kuris A, Hechinger R, Shaw J et al (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518

    Article  CAS  Google Scholar 

  • Lafferty K (1993) Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Mar Ecol Prog Ser 96:229–237

    Article  Google Scholar 

  • Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90:888–900

    Article  Google Scholar 

  • Martorelli SR, Fredensborg BL, Leung TLF, Poulin R (2008) Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). N Z J Zool 35:73–84

    Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  • Mouritsen KN (2002) The Hydrobia ulvae–Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. J Helminthol 76:341–347

    Article  CAS  Google Scholar 

  • Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:S101–S117

    Google Scholar 

  • Mouritsen KN, Poulin R (2005) Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108:344–350

    Article  Google Scholar 

  • Mouritsen KN, Tompkins DM, Poulin R (2005) Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146:476–483

    Article  Google Scholar 

  • Nollen P, Kanev I (1995) The taxonomy and biology of philophthalmid eyeflukes. Adv Parasitol 36:205–269

    Article  Google Scholar 

  • Pequeux A (1995) Osmotic regulation in crustaceans. J Crustacean Biol 15:1–60

    Article  Google Scholar 

  • Pietrock M, Marcogliese D (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299

    Article  Google Scholar 

  • Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151

    Article  CAS  Google Scholar 

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Study Behav 41:151–186

    Article  Google Scholar 

  • Poulin R, Mouritsen KN (2006) Climate change, parasitism and the structure of intertidal ecosystems. J Helminthol 80:183–191

    Article  CAS  Google Scholar 

  • Shock B, Foran C, Stueckle T (2009) Effects of salinity stress on survival, metabolism, limb regeneration, and ecdysis in Uca pugnax. J Crustacean Biol 29:293–301

    Article  Google Scholar 

  • Shumway S (1979) The effects of fluctuating salinity on respiration in gastropod molluscs. Comp Biochem Physiol A 63:279–283

    Article  Google Scholar 

  • Sousa W (1991) Can models of soft-sediment community structure be complete without parasites? Am Zool 31:821–830

    Google Scholar 

  • Southgate V (1971) Observations on the fine structure of the cercaria of Notocotylus attenuatus and formation of the cyst wall of the metacercaria. Cell Tissue Res 120:420–449

    Google Scholar 

  • Studer A, Thieltges DW, Poulin R (2010) Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Mar Ecol Prog Ser 415:11–22

    Article  Google Scholar 

  • Stunkard H, Shaw C (1931) The effect of dilution of sea water on the activity and longevity of certain marine cercariae, with descriptions of two new species. Biol Bull 61:242–271

    Article  Google Scholar 

  • Thakur A, Cheng T (1968) The formation, structure, and histochemistry of the metacercarial cyst of Philophthalmus gralli Mathis and Leger. Parasitology 58:605–618

    Article  CAS  Google Scholar 

  • Thompson R, Mouritsen K, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85

    Article  Google Scholar 

  • Wood C, Byers J, Cottingham K, Altman I, Donahue M, Blakeslee A (2007) Parasites alter community structure. Proc Natl Acad Sci 104:9335–9339

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Anja Studer, Tommy Leung and Christoph Matthaei for assistance with logistical and statistical aspects of this study and Melanie Lloyd, Devon Latoa and Nathan Brown-Haysom for assistance during snail collection.

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Authors and Affiliations

  1. Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand

    Fengyang Lei & Robert Poulin

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  1. Fengyang Lei
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  2. Robert Poulin
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Correspondence to Robert Poulin.

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Communicated by S. D. Connell.

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Lei, F., Poulin, R. Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Mar Biol 158, 995–1003 (2011). https://doi.org/10.1007/s00227-011-1625-7

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  • DOI: https://doi.org/10.1007/s00227-011-1625-7

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