Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Acta Parasitologica

IMPACT FACTOR 2017: 1.039
5-year IMPACT FACTOR: 1.121

CiteScore 2017: 1.17

SCImago Journal Rank (SJR) 2017: 0.641
Source Normalized Impact per Paper (SNIP) 2017: 0.738

More options …
Volume 60, Issue 2


Parasitic fauna of a yellow-legged gull colony in the island of Escombreras (South-eastern Mediterranean) in close proximity to a landfill site: potential effects on cohabiting species

Sandra Hervías Parejo
  • Corresponding author
  • Animal Health Department, Veterinary Faculty, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30100-Espinardo, Murcia, Spain
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Carlos Martínez-Carrasco
  • Animal Health Department, Veterinary Faculty, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30100-Espinardo, Murcia, Spain
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Julia I. Diaz
  • Centro de Estudios Parasitologicos y de Vectores (CCT La Plata, CONICET-UNLP), 1900, La Plata, Argentina
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Lidia Chitimia
  • Animal Health Department, Veterinary Faculty, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30100-Espinardo, Murcia, Spain
  • Institute for Diagnosis and Animal Health, Bucharest, 63 Dr. Staicovici, sector 5, 050557 Bucharest, Romania
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Juana Ortiz
  • Animal Health Department, Veterinary Faculty, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30100-Espinardo, Murcia, Spain
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Elvira Mayo
  • Animal Health Department, Veterinary Faculty, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30100-Espinardo, Murcia, Spain
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Rocío Ruiz de Ybáñez
  • Animal Health Department, Veterinary Faculty, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30100-Espinardo, Murcia, Spain
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-03-25 | DOI: https://doi.org/10.1515/ap-2015-0041


We identified the ectoparasites and helminth fauna of yellow-legged gulls (Larus michahellis michahellis), breeding near to a solid waste landfill, and compared infection levels with those of other yellow-legged gull colonies. Moreover, we analysed correlations between parasites and sex and body condition of yellow-legged gulls, co-infections and the helminth community structure in order to propose the role of this species as reservoir of certain parasites. We also discuss the potential transmission of parasites between the yellow-legged gull and the endangered Audouin’s gull, because interactions between these two species, such as kleptoparasitism and predation, occur frequently around colonies. The following species were recorded: Ornithodorus capensis (Arthropoda); Cosmocephalus obvelatus, Paracuaria adunca, Eucoleus contortus, Tetrameres skrjabini and Contracaecum sp. (Nematoda); Tetrabothrius cylindraceus (Cestoda); Acanthotrema armata, Cardiocephaloides longicollis and Ornithobilharzia intermedia (Digenea). Tetrabothrius cylindraceus, A. armata and O. capensis are new parasite records for this host. The dependence of yellow-legged-gulls on fishery discards is supported by the dominance of parasites transmitted through marine intermediate hosts with interest to fisheries in the study area. However, the shift in diet from natural resources to food derived from human activities seems not to affect the parasitic fauna of yellow-legged gull. Besides of direct physical contact between individuals in nesting and resting habitats, the high availability of fishery discards could increase the risk of Audouin’s gulls to be infected by common parasites of yellow-legged gull.

Keywords: Fishery discards; helminths; Larus audouinii; Larus michahellis; parasite transmission; reservoir; rubbish dump; ticks


  • Abeyeba O.A, Akinbo J.A. 2002. Pathogenic intestinal parasite and bacterial agents on solid wastes. East African Medical Journal, 79, 158-163. DOI: 10.4314/eamj.v79i11.8807CrossrefGoogle Scholar

  • Alvarez M.F., Cordeiro-Paredes J.A., Leiro J.M., Sanmartin M.L. 2006. Influence of host age and sex on the helminth fauna of the yellow-legged gull (Larus michahellis) in Galicia (northwestern Spain). Journal of Parasitology, 92, 454-458. DOI: 10.1645/GE-3546.1CrossrefGoogle Scholar

  • Anderson R.C. 1992. Nematode parasites of vertebrates: their development and transmission. CAB International, Wallingford, UK, 578 pp.Google Scholar

  • Anderson R.C., Chabaud A.G., Willmott S. 1974. CIH Keys to the nematode parasites of vertebrates. Common Wealth Agricultural Bureaux, Farnham Royal, UK Google Scholar

  • Aponte V, Locke S.A., Gentes M.-L., Giroux J.-F., Marcogliese D.J., McLaughlin D., Verreault J. 2014. Effect of habitat use and diet on the gastrointestinal parasite community of an avian omnivore from an urbanized environment. Canadian Journal of Zoology, 92, 629-636. DOI: 10.1139/cjz-2013-0268CrossrefGoogle Scholar

  • Atkinson C.T., Van Riper C. 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: (J.E. Loye and M. Zuk) Bird-parasite interactions: ecology, evolution, and behaviour, Oxford, UK.Google Scholar

  • Austin F. 1984. Ticks as arbovirus vectors in New Zealand. New Zealand Entomologist, 8, 105-106. DOI: 10.1080/00779962. 1984.9722481CrossrefGoogle Scholar

  • Baer J.G. 1954. Revision taxinomique et etude biologique des Cestodes de la famille des Tetrabothriidae: parasites d’oiseaux de haute mer et de mammiferes marins. Mémoires de L’Université de Neuchâtel, Serie Inquarto, 1, 4-122Google Scholar

  • BirdLife International. 2014. Species factsheet: Larus audouinii. Downloaded from http://www.birdlife.org on 30/11/2014.Google Scholar

  • Bosch M. 1996. Sexual Size Dimorphism and Determination of Sex in Yellow-Legged Gulls. Journal of Field Ornithology, 67, 534-541Google Scholar

  • Bosch M., Figuerola J. 1999. Detrimental effects of ticks Ornithodoros maritimus on the growth of yellow-legged gull Larus michahellis chicks. Ardea, 87, 83-89Google Scholar

  • Bosch M., Figuerola J., Cantos F., Velarde R. 1997. Intracolonial differences in the infestation by Haemoproteus lari on yellowlegged gulls Larus cachinnans. Ornis Fennica, 74, 105-112Google Scholar

  • Bosch M., Oro D., Ruiz X. 1994. Dependence of yellow-legged gulls (Larus cachinnans) on food from human activity in two western Mediterranean colonies. Avocetta, 18, 135-139Google Scholar

  • Bosch M., Torres J., Figuerola J. 2000. A helminth community in breeding Yellow-legged Gulls (Larus cachinnans): pattern of association and its effect on host fitness. Canadian Journal of Zoology, 78, 777-786. DOI: 10.1139/z99-252CrossrefGoogle Scholar

  • Bot A.N.M., Currie C.R., Hart A.G., Boomsma J.J. 2001.Waste management in leaf-cutting ants. Ethology Ecology & Evolution, 13, 225-237. DOI: 10.1080/08927014.2001.9522772CrossrefGoogle Scholar

  • Bush A.O., Holmes J.C. 1986. Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology, 64, 132-141. DOI: 10.1139/z86-022CrossrefGoogle Scholar

  • Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575-583Google Scholar

  • Castilla A.M. 1995. Intensive predation of artificial Audouin’s Gull nests by the Yellow-legged Gull in the Columbretes Islands, Spain. Colonial Waterbirds, 18, 226-230Google Scholar

  • Cordeiro-Paredes J.A. 2004. Helmintofauna de la gaviota patiamarilla (Larus cachinnans) en Galicia: Aspectos descriptivos y ecologicos. PhD Thesis, University of Santiago de Compostela, Spain Google Scholar

  • Cramp S., Simmons K. 1983. Handbook of the birds of the western Palearctic. Vol. III. Gulls to waders. Oxford University Press, Oxford, UK Delgado-V. C.A., French K. 2012. Parasite-bird interactions in urban areas: current evidence and emerging questions. Landscape and Urban Planning, 105, 5-14. DOI: 10.1016/j.landurbplan.2011.12.019CrossrefGoogle Scholar

  • Duhem C., Vidal E. Legrand J., Tatoni T. 2003. Opportunistic feeding responses of the Yellow-legged Gull Larus michahellis to accessibility of refuse dumps: The gulls adjust their diet composition and diversity according to refuse dump accessibility. Bird Study, 50, 61-67. DOI: 10.1080/00063650309461291CrossrefGoogle Scholar

  • Ebert D. 1998. Experimental evolution of parasites. Science, 282, 1432-1436. DOI: 10.1126/science.282.5393.1432CrossrefGoogle Scholar

  • Feare C. 1976. Desertation and abnormal development in a colony of Sooty terns Sterna fuscata infested by virus-infected ticks. Ibis, 118, 112-115. DOI: 10.1111/j.1474-919X.1976.tb02015.x CrossrefGoogle Scholar

  • Fedynich A.M., Pence D.B. 1994. Helminth community structure and pattern in a migratory host (Anas platyrhynchos). Canadian Journal of Zoology, 72, 496-505. DOI: 10.1139/z94-067CrossrefGoogle Scholar

  • Furness R.W., Ensor K. Hudson A.V. 1992. The use of fishery waste by gull populations around the British Isles. Ardea, 80, 105-113Google Scholar

  • Gamble H., Bessonov A.S., Cuperlovic K., Gajadhar A.A, van Knapen F., Noeckler K., Schenone H., Zhu X. 2000. Recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Veterinary Parasitology, 93, 393-408PubMedCrossrefGoogle Scholar

  • Gewin V. 2004. Troubled waters, the future of global fisheries. PLoS Biology 2, 422-427. DOI: 10.1371/journal.pbio.0020113.CrossrefGoogle Scholar

  • Grant P. J. 1982. Gulls: a guide to identification. London, T & AD Poyser, Calton, UK, 352 pp.Google Scholar

  • Hanski I. 1982. Dynamics of regional distribution: the core and satellite species hypothesis. Oikos, 38, 210-221Google Scholar

  • Hatch J.J. 1996. Threats to public health from gulls (Laridae). International Journal of Environmental Health Research, 6, 5-16. DOI: 10.1080/09603129609356867CrossrefGoogle Scholar

  • Hernandez-Matias A. Ruiz X. 2003. Predation on common tern eggs by the yellow-legged gull at the Ebro Delta. Scientia Marina, 67, 95-101. DOI: 10.3989/scimar.2003.67s295CrossrefGoogle Scholar

  • Holmes J.C., Price P.W. 1986. Communities of Parasites. In: (J. Kikkawa and D.J. Anderson) Community ecology: pattern and process. Oxford, Blackwell, 187-213Google Scholar

  • Hoogstraal H., Clifford C.M., Keirans J.E. 1979. The Ornithodoros (Alectorobius) capensis group (Acarina: Ixodoidea: Argasidae) of the Palearctic and Oriental regions. O. (A.) coniceps: identity, bird and mammal hosts, virus infections and distribution in Europe, Africa and Asia. Journal of Parasitology, 65, 395-407CrossrefGoogle Scholar

  • Ishikura H., Kikuchi K., Nagasawa K., Ooiwa T., Takamiya H., Sato N., Sugane K. 1992. Anisakidae and anisakidosis. In: (T. Sun) Progress in clinical parasitology. Vol. III, Springer-Verlag, New York, 43-102Google Scholar

  • Jones E.K, Clifford C.M., Keirans J.E., Kohls G.M. 1972. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the Western Hemisphere. Brigham Young Univ. Sciencie Bulletin, Biological Series, 17, 1-40Google Scholar

  • Keirans J.E., Hutcheson H., Oliver J.H. 1992. Ornithodoros (Alectorobius) capensis Neumann (Acari: Ixodoidea: Argasidae), a parasite of seabirds, established along the southeastern seacoast of the United States. Journal of Medical Entomology, 29, 371-373Google Scholar

  • Khalil L.F., Jones A., Bray R.A. 1994. Keys to the cestode parasites of vertebrates. Cab International, Wallingford, UK Kohls G.M. 1957. Insects of Micronesia. Acarina: Ixodoidea. Insects of Micronesia, 3, 85-104Google Scholar

  • Kolařova L., Skirnisson K., Rudolfova J., Jouet D., Leger N., Ferte H. 2005. Avian schistosomes of the genus Trichobilharzia in final hosts in Europe. Bulletin-Scandinavian Society for Parasitology, 14, 85-86Google Scholar

  • Krants G. 1978. A Manual of Acarology. 2nd Edition, Oregon State University Book Stores, Corvallis, Oregon Kuklin V.V. 2013. The peculiarities of helminthofauna of seabirds on offshore water of the Barents Sea. Rossi_iski_i Parazitologicheski _i Zhurnal, 3, 16-21Google Scholar

  • Martinez-Abrain A., Gonzalez-Solis J., Pedrocchi V., Genovart M., Abella J.C., Ruiz X., Jimenez J., Oro D. 2003. Predation, kleptoparasitism and disturbances of yellow-legged gull on Audouin’s gull in three western Mediterranean colonies. In: (E. Minguez, D. Oro, E. De Juana and A. Martinez-Abrain) Mediterranean seabirds and their conservation. Scientia Marina, 67, 89-94Google Scholar

  • Mollhagen T.R. 1976. A study of the systematics and hosts of the parasitic nematode genus Tetrameres (Habronematoidea: Tetrameridae). PhD Thesis, Texas Tech University, Lubbock Moravec F. 1994. Parasitic nematodes of freshwater fishes of Europe. Academy of Sciences of the Czech Republic, Academia, 473 pp.Google Scholar

  • Muzaffar S., Jones I.L. 2004. Parasites and diseases of the auks (Alcidae) of the world and their ecology - A review. Marine Ornithology, 32, 121-146Google Scholar

  • Olsen K.M., Larsson H. 2004. Gulls of North America, Europe, and Asia. Princeton University Press Princeton, New Jersey Oppliger A., Christe P., Richner H. 1996. Clutch size and malaria resistance. Nature, 381, 565. DOI: 10.1038/381565a0CrossrefGoogle Scholar

  • Oro D., Bertolero A., Vilalta A.M., Lopez M.A. 2004. The biology of the Little Tern in the Ebro Delta (northwestern Mediterranean). Waterbirds, 27, 434-440. DOI: 10.1675/1524-4695CrossrefGoogle Scholar

  • Oro D., Leon A., Minguez E., Furness R.W. 2005. Estimating predation on breeding European storm-petrels (Hydrobates pelagicus) by yellow-legged gulls (Larus michahellis). Journal of Zoology, 265, 421-429. DOI: 10.1017/S0952836905006515CrossrefGoogle Scholar

  • Oro D.,Martinez-Vilalta A. 1994. Factors affecting kleptoparasitism and predation rates upon a colony of Audouin’s Gull (Larus audouinii) by Yellow-legged Gulls (Larus cachinnans) in Spain. Colonial Waterbirds, 17, 35-41 Google Scholar

  • Pearson J., Bray R., Gibson D., Jones A. 2008. Family Heterophyidae Leiper, 1909. In: (R.A. Bray, D.I. Gibson and A. Jones). Keys to the Trematoda, Vol 3, CAB International, 113-141Google Scholar

  • Pons J.M., Crochet P.A., Thery M., Bermejo A. 2004. Geographical variation in the yellow-legged gull: introgression or convergence from the herring gull? Journal of Zoological Systematics and Evolutionary Research, 42, 245-256. DOI: 10.1111/j.1439-0469.2004.00255.x CrossrefGoogle Scholar

  • Poulin R. 2001. Interactions between species and the structure of helminth communities. Parasitology, 122, S3-S11. DOI: 10.1017/S0031182000016991CrossrefPubMedGoogle Scholar

  • Pozio E., La Rosa G. 2003. PCR-derived methods for the identification of Trichinella parasites from animal and human samples. Methods in Molecular Biology, 216, 299-309. DOI: 10. 1385/1-59259-344-5:299CrossrefGoogle Scholar

  • Prevot G., Bartoli P. 1980. Demonstration de l’existence d’un cycle marin chez les Strigeides: Cardiocephalus longicollis Szidat, 1928 (Trematoda: Strigeidae). Annales de Parasitologie Humaine et Comparee, 55, 407-25Google Scholar

  • Pritchard M.H., Kruse G.O.W. 1982. The collection and preservation of animal parasites. University of Nebraska Press, Lincoln, NE Ramos R., Ramirez F., Sanpera C., Jover L., Ruiz X. 2009. Diet of Yellow- legged Gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: the relevance of refuse dumps. Journal of Ornithology, 150, 265-272. DOI: 10.1007/s10336-008-0346-2CrossrefGoogle Scholar

  • Rind S. 1984. The blood fluke Ornithobilharzia canaliculata (Rudolphi, 1819) (Trematoda: Schistosomatidae) from the gull Larus dominicanus at Lyttleton, New Zealand. Mauri Ora, 11, 71-75Google Scholar

  • Roca V., Lafuente M., Carbonell E. 1999. Helminth communities in Audouin’s gulls, Larus audouinii from Chafarinas Islands (western Mediterranean). Journal of Parasitology, 85, 984-986Google Scholar

  • Ruiz X., Oro D., Gonzalez-Solis J. 1995. Incidence of a Haemoproteus lari parasitemia in a threatened gull: Larus audouinii. Ornis Fennica, 72, 159-164Google Scholar

  • Rusticali R., Scarton F., Valle R. 1999. Habitat selection and hatching success of Eurasian Oystercatchers in relation to nesting Yellow-legged Gulls and human presence. Waterbirds, 22, 367-375CrossrefGoogle Scholar

  • Sanmartin M., Cordeiro-Paredes J. A., Alvarez M., Leiro J.. 2005. Helminth fauna of the yellow-legged gull Larus cachinnans in Galicia, north-west Spain. Journal of Helminthology, 79, 361-371. DOI: 10.1079/JOH2005309 CrossrefGoogle Scholar

  • Schmidt G.D. 1986. CRC handbook of tapeworm identification. CRC press, Boca Raton, FL Skrjabin K.I., Shikhobalova N.P. 1951. Part I. Suborder Oxyurata Google Scholar

  • Skarjabin, 1923. In: (K. I. Skrjabin) Key to parasitic nematodes. Oxyurata and Ascaridata. Vol. 2. Akademiya Nauk SSSR Publishers, Moscow, 3-419Google Scholar

  • Temirova S.I., Skrjabin A.S. 1978. Tetrabotriaty i mezotsestoidaty lentochnye gel’minty ptits i mlekopitaiushchikh. OsnovyTsestodologii 9. Akademiia Nauk SSSR, Izdatel’stvo Nauka, Moskva Verdiell D.C. 2010. Ictiofauna de las zonas someras litorales del Mar Menor (SE Peninsula Iberica): parametros de su biologia y relaciones con el habitat. PhD Thesis. University of Murcia, Spain Vermeil C., Marguet S. 1967. Sur le diagnostic des larves d’ornithodores du complexe coniceps-capensis (Acarina: Argasidae) Ornithodoros coniceps (Canestrini 1890) maritimus n. ssp. prevaut dans les lles de basse Bretagne. Acarologia, 9, 557-565Google Scholar

  • Vidal E., Medail F., Tatoni T. 1998. Is the yellow-legged gull a superabundant bird species in the Mediterranean? Impact onfauna and flora, conservation measures and research priorities. Biodiversity & Conservation, 7, 1013-1026. DOI: 10.1023/ A:1008805030578CrossrefGoogle Scholar

  • Wilson P., Tidemann C., Meischke H. 1994. Are cats on rubbish dumps a problem? In: (D.W. Paxton) Urban animal management. Proceedings of the Third National Conference on Urban Animal Management in Australia, Sydney, 163-17Google Scholar

  • Wong P.L., Anderson R.C. 1982. The transmission and development of Cosmocephalus obvelatus (Nematoda: Acuaroidea) of gulls (Laridae). Canadian Journal of Zoology, 60, 1426-1440 Google Scholar

  • Yamaguti S. 1971. Synopsis of digenetic trematodes of vertebrates. Vol. 1, 2. Keigaku Publishing Co. Tokyo, 1074 pp. Google Scholar

About the article

Received: 2014-05-28

Revised: 2014-12-08

Accepted: 2015-01-12

Published Online: 2015-03-25

Published in Print: 2015-06-01

Citation Information: Acta Parasitologica, Volume 60, Issue 2, Pages 290–297, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2015-0041.

Export Citation

© 2015 W. Stefański Institute of Parasitology, PAS.Get Permission

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

André Tomás, Maria Teresa Rebelo, and Isabel Pereira da Fonseca
Veterinary Parasitology: Regional Studies and Reports, 2017, Volume 8, Page 13

Comments (0)

Please log in or register to comment.
Log in