Hostname: page-component-7479d7b7d-jwnkl Total loading time: 0 Render date: 2024-07-12T02:47:17.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of ultraviolet radiation on the transmission process of an intertidal trematode parasite

Published online by Cambridge University Press:  05 January 2012

A. STUDER ,
M. D. LAMARE  and
R. POULIN
A. STUDER*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
M. D. LAMARE
Affiliation:
Department of Marine Sciences, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. Tel: +64 3 479 7964 Fax: +64 3 479 7584. E-mail: studeranja@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The transmission of parasites takes place under exposure to a range of fluctuating environmental factors, one being the changing levels of solar ultraviolet radiation (UVR). Here, we investigated the effects of ecologically relevant levels of UVR on the transmission of the intertidal trematode Maritrema novaezealandensis from its first intermediate snail host (Zeacumantus subcarinatus) to its second intermediate amphipod host (Paracalliope novizealandiae). We assessed the output of parasite transmission stages (cercariae) from infected snail hosts, the survival and infectivity of cercariae, the susceptibility of amphipod hosts to infection (laboratory experiments) and the survival of infected and uninfected amphipod hosts (outdoor experiment) when exposed to photo-synthetically active radiation only (PAR, 400–700 nm; no UV), PAR+UVA (320–700 nm) or PAR+UVA+UVB (280–700 nm). Survival of cercariae and susceptibility of amphipods to infection were the only two steps significantly affected by UVR. Survival of cercariae decreased strongly in a dose-dependent manner, while susceptibility of amphipods increased after exposure to UVR for a prolonged period. Exposure to UVR thus negatively affects both the parasite and its amphipod host, and should therefore be considered an influential component in parasite transmission and host-parasite interactions in intertidal ecosystems.

Keywords

transmissionhost-parasite interactionsMaritrema novaezealandensisParacalliope novizealandiaeZeacumantus subcarinatusintertidal soft-sediment ecosystem
Type
Research Article
Information
Parasitology , Volume 139 , Issue 4 , April 2012 , pp. 537 - 546
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ariyo, A. A. and Oyerinde, J. P. O. (1990). Effect of ultraviolet radiation on survival, infectivity and maturation of Schistosoma mansoni cercariae. International Journal for Parasitology 20, 893–897.CrossRefGoogle ScholarPubMed
Bancroft, B. A., Baker, N. J. and Blaustein, A. R. (2007). Effects of UVB radiation on marine and freshwater organisms: a synthesis through meta-analysis. Ecology Letters 10, 332–345. doi: 10.1111/j.1461-0248.2007.01022.x.CrossRefGoogle ScholarPubMed
Bothwell, M. L., Sherbot, D. M. J. and Pollock, C. M. (1994). Ecosystem response to solar ultraviolet-B radiation: Influence of trophic-level interactions. Science 265, 97–100.CrossRefGoogle ScholarPubMed
Bryan-Walker, K., Leung, T. L. F. and Poulin, R. (2007). Local adaptation of immunity against a trematode parasite in marine amphipod populations. Marine Biology 152, 687–695. doi: 10.1007/s00227-007-0725-x.CrossRefGoogle Scholar
Chalker-Scott, L. (1995). Survival and sex ratios of the intertidal copepod, Tigriopus californicus, following ultraviolet-B (290–320 nm) radiation exposure. Marine Biology 123, 799–804.CrossRefGoogle Scholar
Connelly, S. J., Wolyniak, E. A., Williamson, C. E. and Jellison, K. L. (2007). Artificial UV-B and solar radiation reduce in vitro infectivity of the human pathogen Cryptosporidium parvum. Environmental Science & Technology 41, 7101–7106. doi: 10.1021/es071324r.CrossRefGoogle ScholarPubMed
Dahms, H. U. and Lee, J. S. (2010). UV radiation in marine ectotherms: molecular effects and responses. Aquatic Toxicology 97, 3–14. doi: 10.1016/j.aquatox.2009.12.002.CrossRefGoogle ScholarPubMed
Day, T. A. and Neale, P. J. (2002). Effects of UV-B radiation on terrestrial and aquatic primary producers. Annual Review of Ecology and Systematics 33, 371–396. doi: 10.1146/annurev.ecolysis.33.010802.150434.CrossRefGoogle Scholar
de Mora, S., Demers, S. and Vernet, M. (2000). The Effects of UV Radiation in the Marine Environment. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Ewing, M. S., Blazer, V. S., Fabacher, D. L., Little, E. E. and Kocan, K. M. (1999). Channel catfish response to ultraviolet-B radiation. Journal of Aquatic Animal Health 11, 192–197.2.0.CO;2>CrossRefGoogle Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265. doi: 10.1016/j.jembe.2004.05.011.CrossRefGoogle Scholar
Ghandour, A. M. and Webbe, G. (1975). Effect of ultraviolet radiation on cercariae of Schistosoma mansoni and Schistosoma haematobium. Journal of Helminthology 49, 153–159.CrossRefGoogle ScholarPubMed
Gleason, D. F. and Wellington, G. M. (1995). Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Marine Biology 123, 693–703.CrossRefGoogle Scholar
Haeder, D. P., Kumar, H. D., Smith, R. C. and Worrest, R. C. (1998). Effects on aquatic ecosystems. Journal of Photochemistry and Photobiology B Biology 46, 53–68.CrossRefGoogle Scholar
Haeder, D. P., Helbling, E. W., Williamson, C. E. and Worrest, R. C. (2011). Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochemical & Photobiological Sciences 10, 242–260. doi:10.1039/C0PP90036B.CrossRefGoogle Scholar
Hansson, L. A. and Hylander, S. (2009). Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton. Photochemical & Photobiological Sciences 8, 1266–1275. doi: 10.1039/b908825c.CrossRefGoogle ScholarPubMed
Helbling, E. W., Menchi, C. F. and Villafane, V. E. (2002 a). Bioaccumulation and role of UV-absorbing compounds in two marine crustacean species from Patagonia, Argentina. Photochemical & Photobiological Sciences 1, 820–825. doi: 10.1039/b206584c.CrossRefGoogle ScholarPubMed
Helbling, E. W. and Zagarese, H. (2003). UV Effects in Aquatic Organisms and Ecosystems. The Royal Society of Chemistry, Cambridge, UK.Google Scholar
Helbling, E. W., Zaratti, F., Sala, L. O., Palenque, E. R., Menchi, C. F. and Villafane, V. E. (2002 b). Mycosporine-like amino acids protect the copepod Boeckella titicacae (Harding) against high levels of solar UVR. Journal of Plankton Research 24, 225–234.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Karentz, D. (2001). Chemical defences of marine organisms against solar radiation exposure: UV absorbing mycosporine-like amino acids and scytonemin. In Marine Chemical Ecology (ed. McClintock, J. and Baker, B.), pp. 481–520. CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
Koehler, A. V. and Poulin, R. (2010). Host partitioning by parasites in an intertidal crustacean community. Journal of Parasitology 96, 862–868. doi: 10.1645/ge-2460.1.CrossRefGoogle Scholar
Kramer, K. J. M. (1990). Effects of increased solar UVB radiation on coastal marine ecosystems – an overview. In Expected Effects of Climatic Change on Marine Coastal Ecosystems (ed. Beukema, J. J., Wolff, W. J. and Brouns, J. J. M. W.), pp. 195–210. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences, USA 103, 11211–11216. doi: 10.1073/pnas.0604755103.CrossRefGoogle ScholarPubMed
Lamare, M. D., Barker, M. F. and Lesser, M. P. (2007). In situ rates of DNA damage and abnormal development in Antarctic and non-Antarctic sea urchin embryos. Aquatic Biology 1, 21–32.CrossRefGoogle Scholar
Lauckner, G. (1984). Impact of trematode parasitism on the fauna of a North Sea tidal flat. Helgoländer Meeresuntersuchungen 37, 185–199.CrossRefGoogle Scholar
Leech, D. M. and Williamson, C. E. (2000). Is tolerance to UV radiation in zooplankton related to body size, taxon, or lake transparency? Ecological Applications 10, 1530–1540.CrossRefGoogle Scholar
Lesser, M. P. and Barry, T. M. (2003). Survivorship, development, and DNA damage in echinoderm embryos and larvae exposed to ultraviolet radiation (290–400 nm). Journal of Experimental Marine Biology and Ecology 292, 75–91. doi: 10.1016/s0022-0981(03)00141-2.CrossRefGoogle Scholar
Lister, K. N., Lamare, M. D. and Burritt, D. J. (2010). Sea ice protects the embryos of the Antarctic sea urchin Sterechinus neumayeri from oxidative damage due to naturally enhanced levels of UV-B radiation. Journal of Experimental Biology 213, 1967–1975. doi: 10.1242/jeb.039990.CrossRefGoogle ScholarPubMed
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Siddall, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85–144.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology – Revue Canadienne de Zoologie 79, 1331–1352.CrossRefGoogle Scholar
Martorelli, S. R., Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Description and proposed life cycle of Maritrema novaezealandensis N. sp (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. Journal of Parasitology 90, 272–277.CrossRefGoogle Scholar
McArdle, J. and Bullock, A. M. (1987). Solar ultraviolet radiation as a causal factor of summer syndrome in cage-reared Atlantic salmon, Salmo salar L – a clinical and histopathological study. Journal of Fish Diseases 10, 255–264.CrossRefGoogle Scholar
McFadzen, I., Baynes, S., Hallam, J., Beesley, A. and Lowe, D. (2000). Histopathology of the skin of UV-B irradiated sole (Solea solea) and turbot (Scophthalmus maximus) larvae. Marine Environmental Research 50, 273–277.CrossRefGoogle ScholarPubMed
McKenzie, R., Conner, B. and Bodeker, G. (1999). Increased summertime UV radiation in New Zealand in response to ozone loss. Science 285, 1709–1711.CrossRefGoogle ScholarPubMed
McKenzie, R. L., Aucamp, P. J., Bais, A. F., Bjorn, L. O. and Ilyas, M. (2007). Changes in biologically active ultraviolet radiation reaching the Earth's surface. Photochemical & Photobiological Sciences 6, 218–231. doi: 10.1039/b700017k.CrossRefGoogle ScholarPubMed
McKenzie, R. L., Bjorn, L. O., Bais, A. and Ilyasd, M. (2003). Changes in biologically active ultraviolet radiation reaching the Earth's surface. Photochemical & Photobiological Sciences 2, 5–15. doi: 10.1039/b211155c.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117. doi: 10.1017/s0031182002001476.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2010). Parasitism as a determinant of community structure on intertidal flats. Marine Biology 157, 201–213. doi: 10.1007/s00227-009-1310-2.CrossRefGoogle Scholar
Obermueller, B., Karsten, U. and Abele, D. (2005). Response of oxidative stress parameters and sunscreening compounds in Arctic amphipods during experimental exposure to maximal natural UVB radiation. Journal of Experimental Marine Biology and Ecology 323, 100–117. doi: 10.1016/j.jembe.2005.03.005.CrossRefGoogle Scholar
Patz, J. A., Epstein, P. R., Burke, T. A. and Balbus, J. M. (1996). Global climate change and emerging infectious diseases. Jama-Journal of the American Medical Association 275, 217–223.CrossRefGoogle ScholarPubMed
Paul, N. D. and Gwynn-Jones, D. (2003). Ecological roles of solar UV radiation: towards an integrated approach. Trends in Ecology & Evolution 18, 48–55.CrossRefGoogle Scholar
Prah, S. K. and James, C. (1977). Influence of physical factors on survival and infectivity of miracidia of Schistosoma mansoni and Schistosoma haematobium. 1. Effect of temperature and UV light. Journal of Helminthology 51, 73–85.CrossRefGoogle Scholar
Przeslawski, R., Davis, A. R. and Benkendorff, K. (2005). Synergistic effects associated with climate change and the development of rocky shore molluscs. Global Change Biology 11, 515–522. doi: 10.1111/j.1365-2486.2005.00918.x.CrossRefGoogle Scholar
Roy, S. (2000). Strategies for the minimisation of UV-induced damage. In The effects of UV radiation in the marine environment. (ed. de Mora, S., Demers, S. and Vernet, M.), pp. 177–205. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Ruelas, D. S., Karentz, D. and Sullivan, J. T. (2006). Lethal and sub-lethal effects of UVB on juvenile Biomphalaria glabrata (Mollusca: Pulmonata). Journal of Invertebrate Pathology 93, 192–200. doi: 10.1016/j.jip.2006.08.001.CrossRefGoogle ScholarPubMed
Ruelas, D. S., Karentz, D. and Sullivan, J. T. (2007). Sublethal effects of ultraviolet-B radiation on miracidia and sporocysts of Schistosoma mansoni: Intramolluscan development, infectivity, and photoreactivation. Journal of Parasitology 93, 1303–1310.CrossRefGoogle ScholarPubMed
Ruelas, D. S., Karentz, D. and Sullivan, J. T. (2009). Effects of UVB on interactions between Schistosoma mansoni and Biomphalaria glabrata. Journal of Invertebrate Pathology 101, 140–142. doi: 10.1016/j.jip.2009.04.001.CrossRefGoogle ScholarPubMed
Salo, H. M., Aaltonen, T. M., Markkula, S. E. and Jokinen, E. I. (1998). Ultraviolet-B irradiation modulates the immune system of fish (Rutilus rutilus, Cyprinidae). I. Phagocytes. Photochemistry and Photobiology 67, 433–437.CrossRefGoogle ScholarPubMed
Seckmeyer, G. and McKenzie, R. L. (1992). Increased ultraviolet radiation in New Zealand (45°S) relative to Germany (48°N). Nature 359, 135–137.CrossRefGoogle Scholar
Siebeck, O., Vail, T. L., Williamson, C. E., Vetter, R., Hessen, D., Zagarese, H., Little, E., Balseiro, E., Modenutti, B., Seva, J. and Shumate, A. (1994). Impact of UV-B radiation on zooplankton and fish in pelagic freshwater ecosystems. Advances in Limnology 43, 101–114.Google Scholar
Sinha, R. P. and Haeder, D. P. (2002). UV-induced DNA damage and repair: a review. Photochemical & Photobiological Sciences 1, 225–236. doi: 10.1039/b201230 h.CrossRefGoogle ScholarPubMed
Sommaruga, R. (2003). UVR and its effects on species interactions. In UV Effects in Aquatic Organisms and Ecosystems (ed. Helbling, E. W. and Zagarese, H.), pp. 485–508. The Royal Society of Chemistry, Cambridge, UK.Google Scholar
Sousa, W. P. (1991). Can models of soft-sediment community structure be complete without parasites? American Zoologist 31, 821–830.CrossRefGoogle Scholar
Standen, O. D. and Fuller, K. A. (1959). Ultraviolet irradiation of the cercariae of Schistosoma mansoni – inhibition of development to the adult stage. Transactions of the Royal Society of Tropical Medicine and Hygiene 53, 372–379.CrossRefGoogle Scholar
Studer, A., Thieltges, D. W. and Poulin, R. (2010). Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology-Progress Series 415, 11–22.CrossRefGoogle Scholar
Tedetti, M. and Sempere, R. (2006). Penetration of ultraviolet radiation in the marine environment. A review. Photochemistry and Photobiology 82, 389–397. doi: 10.1562/2005-11-09-ir-733.CrossRefGoogle ScholarPubMed
Vincent, W. F. and Neale, P. J. (2000). Mechanisms of UV damage to aquatic organisms. In The Effects of UV Radiation in the Marine Environment. (ed. de Mora, S., Demers, S. and Vernet, M.), pp. 149–176. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Williamson, C. E., Neale, P. J., Grad, G., De Lange, H. J. and Hargreaves, B. R. (2001). Beneficial and detrimental effects of UV on aquatic organisms: Implications of spectral variation. Ecological Applications 11, 1843–1857.CrossRefGoogle Scholar