Distribution of Pholeter gastrophilus (Digenea) within the stomach of four odontocete species: the role of the diet and digestive physiology of hosts | Parasitology | Cambridge Core (original) (raw)

Abstract

We compared the distribution of the digenean Pholeter gastrophilus in the stomach of 27 harbour porpoises, Phocoena phocoena, 27 striped dolphins, Stenella coeruleoalba, 18 bottlenose dolphins, Tursiops truncatus, and 100 long-finned pilot whales, Globicephala melas. The stomach of these species is composed of 4 chambers of different size, structure and function. In all species, P. gastrophilus was largely restricted to the glandular region of the stomach, but the parasite tended to favour the fundic chamber in bottlenose dolphins and harbour porpoises, the pyloric chamber in pilot whales, and none in striped dolphins. However, predictability at infrapopulation level was generally low, suggesting a weak preference of P. gastrophilus for any of the chambers. Three hypotheses were tested to investigate a common cause for the distribution of P. gastrophilus in all host species, namely, colonization of chambers was (1) sequential, (2) dependent on chamber size, or (3) dependent on the passage time of food through the whole stomach. The latter hypothesis was indirectly tested by assuming, based on previous evidence from other vertebrates, that the greater the size of the stomach and/or the energy content of prey, the greater the delay of food passage. We found no compelling evidence that chamber colonization was sequential, or related to chamber size in any species. However, the distribution of P. gastrophilus was significantly more anteriad when the host species had larger stomachs and, particularly, when hosts fed on prey with higher caloric content. Accordingly, the stomach distribution of P. gastrophilus at this scale seems to be passively driven by features of the diet and digestive physiology of each host species. This study provides a general framework to formulate null hypotheses in future studies on microhabitat choice by parasites.

References

Akritas, M. G.,Kuha, J. andOsgood, D. W. (2002).A nonparametric approach to matched pairs with missing Data.Sociological Methods and Research 30,425–454.CrossRefGoogle Scholar

Andersen, N. G. (1999).The effects of predator size, temperature, and prey characteristics on gastric evacuation in whiting.Journal of Fish Biology 54,287–301.CrossRefGoogle Scholar

Anthony, J. A.,Roby, D. D. andTurco, K. R. (2000).Lipid content and energy density of forage fishes from the northern Gulf of Alaska.Journal of Experimental Marine Biology and Ecology 248,53–78.CrossRefGoogle Scholar

Aznar, F. J.,Fernández, M.,Balbuena, J. A. andRaga, J. A. (1992).Patterns of colonization of Pholeter gastrophilus in Stenella coeruleoalba and Phocoena phocoena.European Research on Cetaceans 6,214–217.Google Scholar

Aznar, F. J.,Balbuena, J. A. andRaga, J. A. (1994).Helminth communities of Pontoporia blainvillei (Cetacea: Pontoporiidae) in Argentinian waters.Canadian Journal of Zoology 72,702–706.CrossRefGoogle Scholar

Aznar, F. J.,Herreras, M. V.,Balbuena, J. A. andRaga, J. A. (2003).Population structure and habitat selection by Anisakis simplex in 4 odontocete species from Northern Argentina.Comparative Parasitology 70,66–71.CrossRefGoogle Scholar

Blanco, C.,Aznar, F. J. andRaga, J. A. (1995).Cephalopods in the diet of the striped dolphin Stenella coeruleoalba from the western Mediterranean during an epizootic in 1990.Journal of Zoology (London) 237,151–158.CrossRefGoogle Scholar

Blanco, C.,Salomón, O. andRaga, J. A. (2001).Diet of the bottlenose dolphin (Tursiops truncatus) in the western Mediterranean sea.Journal of the Marine Biological Association of the United Kingdom 81,1053–1058.CrossRefGoogle Scholar

Berón-Vera, B.,Pedraza, S. N.,Raga, J. A.,Gil de Pertierra, A.,Crespo, E. A.,Koen Alonso, M. andGoodall, R. N. P. (2001).Gastrointestinal helminths of Commerson's dolphins Cephalorhynchus commersonii from central Patagonia and Tierra del Fuego.Diseases of Aquatic Organisms 47,201–208.CrossRefGoogle Scholar

Beverley-Burton, M. (1978).Helminths of the alimentary tract from a stranded herd of the Atlantic white-sided dolphin, Lagenorhynchus acutus.Journal of the Fisheries Research Board of Canada 35,1356–1359.CrossRefGoogle Scholar

Bush, A. O.,Lafferty, K. D.,Lotz, J. M. andShostak, A. W. (1997).Parasitology meets ecology in its own terms: Margolis et al. revisited.Journal of Parasitology 83,575–583.CrossRefGoogle Scholar

Chase, B. C. (2002).Differences in diet of Atlantic bluefin tuna (Thunnus thynnus) at five seasonal feeding grounds on the New England continental shelf.Fisheries Bulletin 100,168–180.Google Scholar

Clarke, A.,Clarke, M. R.,Holmes, L. J. andWaters, T. D. (1985).Calorific values and elemental analysis of eleven species of oceanic squids (Mollusca: Cephalopoda).Journal of the Marine Biological Association of the United Kingdom 65,983–986.CrossRefGoogle Scholar

Conover, W. J. (1999).Practical Nonparametric Statistics, 3rd Edn.John Wiley and Sons,New York.

Conti, J. A. andFrohlich, R. K. (1984).Gastrointestinal Parasitism in Pygmy Killer Whales.Proceedings of the Helminthological Society of Washington 51,364–365.Google Scholar

Desportes, G. (1985).La nutrition des odontocètes en Atlantique Nord-Est (côtes Françaises- îles Feroë). Ph. D. thesis, University of Poitiers.

Desportes, G. andMouritsen, R. (1993).Preliminary results on the diet of long-finned pilot whales off the Faroe Islands.Reports of the International Whaling Commission Special Issue 14,305–324.Google Scholar

Dollfus, R. P. H. (1974).Pholeter gastrophilus (Trematoda, Digenea) from an intestinal cyst of Stenella coeruleoalba Meyen, 1833 (Odontoceti, Delphinidae). Comments on the Family Pholeteridae, Dollfus, 1939. List of helminths identified to date in S. coeruleoalba.Investigations on Cetacea 5,331–337.Google Scholar

Fernández, M.,Agustí, C.,Aznar, F. J. andRaga, J. A. (2003).Gastrointestinal helminths of Risso's dolphin Grampus griseus from the Western Mediterranean.Diseases of Aquatic Organisms 55,73–76.CrossRefGoogle Scholar

Forero, M. G.,Hobson, K. A.,Bortolotti, G. R.,Donázar, J. A.,Bertellotti, M. andBlanco, G. (2002).Food resource utilization by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality.Marine Ecology Progress Series 234,289–299.CrossRefGoogle Scholar

Fried, B. (1994).Metacercarial excystment of trematodes.Advances in Parasitology 33,91–144.CrossRefGoogle Scholar

Gaskin, D. E. (1978).Form and function in the digestive tract and associated organs in Cetacea, with a consideration of metabolic rates and specific energy budgets.Oceanography and Marine Biology Annual Review 16,313–345.Google Scholar

Geraci, J. R. andLounsbury, V. J. (1993).Marine Mammals Ashore. A Field Guide for Strandings.Texas A & M University Sea Grant College Program,Galveston, Texas.

Gibson, D. I.,Harris, E. A.,Bray, R. A.,Jepson, P. D.,Kuiken, T.,Baker, J. R. andSimpson, V. R. (1998).A survey of the helminth parasites of cetaceans stranded on the coast of England and Wales during the period 1990–1994.Journal of Zoology (London) 244,563–574.CrossRefGoogle Scholar

Gotelli, N. J. andRohde, K. (2002).Co-occurrence of ectoparasites of marine fishes: a null model analysis.Ecology Letters 5,86–94.CrossRefGoogle Scholar

Harrison, R. J.,Johnson, F. R. andYoung, B. A. (1970).The oesophagus and stomach of dolphins (Tursiops, Delphinus, Stenella).Journal of Zooogy (London) 160,377–390.CrossRefGoogle Scholar

Hilton, G. M.,Furness, R. W. andHouston, D. C. (2000 a).A comparative study of digestion in North Atlantic seabirds.Journal of Avian Biology 31,36–46.Google Scholar

Hilton, G. M.,Lilliendahl, K.,Solmundsson, J.,Houston, D. C. andFurness, R. W. (2000 b).Geographical variation in the size of body organs in seabirds.Functional Ecology 14,369–379.Google Scholar

Holmes, J. C. (1990).Competition, contacts, and other factors restricting niches of parasitic helminths.Annales de Parasitologie Humaine et Comparée 65,69–72.CrossRefGoogle Scholar

Howard, E. B.,Britt, J. O. JrandMatsumoto, G. (1983).Parasitic diseases. In_Pathobiology of Marine Mammal Diseases_, Vol. 1 ( ed. Howard, E. B.), pp.121–122.CRC Press,Boca Raton, USA.

Jackson, S. andRyan, P. G. (1986).Differential digestion rates of prey by white-chinned petrels (Procellaria aequinoctialis).Auk 103,617–619.Google Scholar

Janse, M. (2003).Considerations on the diet composition and feeding rate of demersal sharks in 15 European public aquaria.Zoo Biology 22,203–226.CrossRefGoogle Scholar

Jobling, M. (1986).Mythical models of gastric emptying and implications for food consumption studies.Environmental Biology of Fishes 16,35–50.CrossRefGoogle Scholar

Kastelein, R. A.,Nieuwstraten, S. H. andVertegen, M. W. A. (1997).Passage time of carmine red dye through the digestive tract of harbour porpoises (Phocoena phocoena). In_The Biology of the Harbour Porpoise_ ( ed. Read, A. J., Wiepkema, P. R. and Nachtigall, P. E.), pp.265–275.De Spil Publishers,Woerden, The Netherlands.

Knowlton, N. (1993).Sibling species in the sea.Annual Reviews in Ecology and Systematics 24,189–216.CrossRefGoogle Scholar

Lymbery, A. J.,Hobbs, R. P. andThompson, R. C. A. (1989).The dispersion of Echinococcus granulosus in the intestine of dogs.Journal of Parasitology 75,562–570.CrossRefGoogle Scholar

Mattiucci, S.,Nascetti, G.,Cianchi, R.,Paggi, L.,Arduino, P.,Margolis, L.,Brattey, J.,Webb, S. C.,D'Amelio, S.,Orecchia, P. andBullini, L. (1997).Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae).Journal of Parasitology 83,401–416.CrossRefGoogle Scholar

Mattiucci, S.,Paggi, L.,Nascetti, G.,Abollo, E.,Webb, S. C.,Pascual, S.,Cianchi, R. andBullini, L. (2001).Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae).International Journal for Parasitology 31,9–14.CrossRefGoogle Scholar

Maerz, L. L.,Sankaran, H.,Scharpf, S. J. andDeveney, C. W. (1994).Effect of caloric content and composition of a liquid meal on gastric emptying in the rat.American Journal of Physiology 267 (Regulatory Integrative Comparative Physiology36):R1163–R1167.Google Scholar

Mead, J. G. (2002).Gastrointestinal tract. In_Encyclopedia of Marine Mammals_ ( ed. Perrin, W. F., Würsing, B. and Thewissen, H. G. M.), pp.488–495.Academic Press,San Diego, U.S.A.

Migaki, G.,van Dyke, D. andHubbard, R. C. (1971).Some histopathological lesions caused by helminths in marine mammals.Journal of Wildlife Diseases 7,281–289.CrossRefGoogle Scholar

Moore, J. andSimberloff, D. (1990).Gastrointestinal helminth communities of bobwhite quail.Ecology 71,344–359.CrossRefGoogle Scholar

Neuhäuser, M. andPoulin, R. (2004).Comparing parasite numbers between samples of hosts.Journal of Parasitology 90,689–691.CrossRefGoogle Scholar

Olson, R. J. andBoggs, C. H. (1986).Apex predation by yellowfin tuna (Thunnus albacares): independent estimates from gastric evacuation and stomach contents, bioenergetics, and cesium concentrations.Canadian Journal of Fisheries and Aquatic Sciences 43,1760–1775.CrossRefGoogle Scholar

Olson, R. J. andGalván-Magaña, F. (2002).Food habits and consumption rates of dolphinfish (Coryphaena hippurus) in the eastern Pacific Ocean.Fishery Bulletin 100,279–298.Google Scholar

Pedersen, J. andHislop, J. R. G. (2001).Seasonal variations in the energy density of fishes in the North Sea.Journal of Fish Biology 59,380–389.CrossRefGoogle Scholar

Peracchi, M.,Gebbia, C.,Ogliari, C.,Fraquelli, M.,Viganò, R.,Baldassarri, A.,Bianchi, P. A. andConte, D. (2000).Influence of caloric intake on gastric emptying of solids assessed by 13C-octanoid acid breath test.Scandinavian Journal of Gastroenterology 35,814–818.Google Scholar

Péres-Neto, P. R.,Olden, J. D. andJackson, D. A. (2001).Environmentally constrained null models: site suitability as occupancy criterion.Oikos 93,110–120.CrossRefGoogle Scholar

Piersma, T.,Koolhaas, A. andDekinga, A. (1993).Interactions between stomach structure and diet choice in shorebirds.Auk 110,552–564.CrossRefGoogle Scholar

Quéméner, L.,Suquet, M.,Mero, D. andGaignon, J. L. (2002).Selection method of new candidates for finfish aquaculture: the case of the French Atlantic, the Channel and the North Sea coasts.Aquatic Living Resources 15,293–302.CrossRefGoogle Scholar

Raga, J. A. (1994).Parasitismus bei Cetacea. In_Handbuch der Säugetiere Europas_ Bd. 6/1A ( ed. Robineau, D., Duguy, R. and Klima, M.), pp.132–179.Aula-Verlag,Wiesbaden, Germany.

Raga, J. A. andBalbuena, J. A. (1993).Parasites of the long-finned pilot whale, Globicephala melas (Traill, 1809), in European waters.Reports of the International Whaling Commission Special Issue 14,391–406.Google Scholar

Raga, J. A.,Carbonell, E.,Raduán, A. andBlanco, C. (1985).Sobre la presencia de Pholeter gastrophilus (Kossack, 1910) (Trematoda: Troglotrematidae), en quistes estomacales de Tursiops truncatus y Stenella coeruleoalba (Cetacea: Delphinidae), en las costas españolas del Mediterráneo.Revista Ibérica de Parasitología 45,123–128.Google Scholar

Reiczigel, J. (2003).Confidence intervals for the binomial parameter: some new considerations.Statistics in Medicine 22,611–621.CrossRefGoogle Scholar

Rohde, K. (2002).Niche restriction and mate finding in vertebrate hosts. In_The Behavioural Ecology of Parasites_ ( ed. Lewis, E. E., Campbell, J. F. and Sukhdeo, M. V. K.), pp.171–197.CAB International,Oxford.CrossRef

Rózsa, L.,Reiczigel, J. andMajoros, G. (2000).Quantifying parasites in samples of hosts.Journal of Parasitology 86,228–232.CrossRefGoogle Scholar

Santos, M. B.,Clarke, M. R. andPierce, G. J. (2001).Assessing the importance of cephalopods in the diets of marine mammals and other top predators: problems and solutions.Fisheries Research 52,121–139.CrossRefGoogle Scholar

Santos, M. B.,Pierce, G. J.,Learmonth, J. A.,Reid, R. J.,Ross, H. M.,Patterson, I. A. P.,Reid, D. G. andBeare, D. (2004).Variability in the diet of harbor porpoises (Phocoena phocoena) in Scottish waters 1992–2003.Marine Mammal Science 20,1–27.CrossRefGoogle Scholar

Smith, G. J. D. (1972).The stomach of the harbor porpoise Phocoena phocoena (L.).Canadian Journal of Zoology 50,1611–1616.CrossRefGoogle Scholar

Van Pelt, T. I.,Piatt, J. F.,Lance, B. K. andRoby, D. D. (1997).Proximate composition and energy density of some North Pacific forage fishes.Comparative Biochemistry and Physiology 118A,1393–1398.CrossRefGoogle Scholar

Van Waerebeek, K.,Reyes, J. C. andAlfaro, J. (1993).Helminth parasites and phoronts of dusky dolphins Lagenorhynchus obscurus (Gray, 1828) from Peru.Aquatic Mammals 19,159–169.Google Scholar

Varljen, J.,šulić, S.,Brmalj, J.,Batičić, L.,Osbernel, V. andKapović, M. (2003).Lipid classes and fatty acid composition of Diplodus vulgaris and Conger conger originating from the Adriatic Sea.Food Technology and Biotechnology 41,149–156.Google Scholar

Williams, T. M.,Haun, J.,Davis, R. W.,Fuiman, L. A. andKohin, S. (2001).A killer appetite: metabolic consequences of carnivory in marine mammals.Comparative Biochemistry and Physiology Part A 129,785–796.CrossRefGoogle Scholar

Wright, D. H.,Patterson, B. D.,Mikkelson, G. M.,Cutler, A. andAtmar, W. (1998).A comparative analysis of nested subset patterns of species composition.Oecologia 113,1–20.Google Scholar

Woodard, J. C.,Zam, S. G.,Caldwell, D. K. andCaldwell, M. C. (1969).Some parasitic diseases of dolphins.Pathologia Veterinaria 6,257–272.CrossRefGoogle Scholar

Zam, S. G.,Caldwell, D. K. andCaldwell, M. C. (1970).Some internal parasites from freshwater cetaceans from the upper Amazon river.Investigations on Cetacea 2,250–251.Google Scholar

Zam, S. G.,Caldwell, D. K. andCaldwell, M. C. (1971).Some endoparasites from small odontocete cetaceans collected in Florida and Georgia.Cetology 2,1–11.Google Scholar