Advertisement

Parasitology Research

, Volume 113, Issue 4, pp 1405–1415 | Cite as

Gastrointestinal parasites of free-living Indo-Pacific bottlenose dolphins (Tursiops aduncus) in the Northern Red Sea, Egypt

  • S. KleinertzEmail author
  • C. Hermosilla
  • A. Ziltener
  • S. Kreicker
  • J. Hirzmann
  • F. Abdel-Ghaffar
  • A. Taubert
Article
First Online:

Abstract

The present study represents the first report on the gastrointestinal parasite fauna infecting the free-living and alive Indo-Pacific bottlenose dolphins (Tursiops aduncus) inhabiting waters of the Red Sea at Hurghada, Egypt. A total of 94 individual faecal samples of the examined bottlenose dolphins were collected during several diving expeditions within their natural habitats. Using classical parasitological techniques, such as sodium acetate acetic acid formalin method, carbol fuchsin-stained faecal smears, coproantigen ELISA, PCR and macroscopical analyses, the study revealed infections with 21 different parasite species belonging to protozoans and metazoans with some of them bearing zoonotic and/or pathogenic potential. Four identified parasite species are potential zoonotic species (Giardia spp., Cryptosporidium spp., Diphyllobothrium spp., Ascaridida indet.); three of them are known to have high pathogenic potential for the examined dolphin species (Nasitrema attenuata, Zalophotrema spp. and Pholeter gastrophilus) and some appear to be directly associated with stranding events. In detail, the study indicates stages of ten protozoan species (Giardia spp., Sarcocystis spp., Isospora (like) spp., Cystoisospora (like) spp., Ciliata indet. I and II, Holotricha indet., Dinoflagellata indet., Hexamita (like) spp., Cryptosporidium spp.), seven trematode species (N. attenuata, Nasitrema spp. I and II, Zalophotrema curilensis, Zalophotrema spp., Pholeter gastrophilus, Trematoda indet.), one cestode species (Diphyllobothrium spp.), two nematode species (Ascaridida indet, Capillaria spp.) and one crustacean parasite (Cymothoidae indet.). Additionally, we molecularly identified adult worms of Anisakis typica in individual dolphin vomitus samples by molecular analyses. A. typica is a common parasite of various dolphin species of warmer temperate and tropical waters and has not been attributed as food-borne parasitic zoonoses so far. Overall, these parasitological findings include ten new host records for T. aduncus (i.e. in case of Giardia spp., Sarcocystis spp., Cryptosporidium spp., Nasitrema spp., Zalophotrema spp., Pholeter gastrophilus, A. typica, Capillaria spp., Diphyllobothrium spp. and Cymothoidae indet.). The present results may be used as a baseline for future monitoring studies targeting the impact of climate or other environmental changes on dolphin’s health conditions and therefore contribute to the protection of these fascinating marine mammals.

Keywords

Marine Mammal Bottlenose Dolphin Common Dolphin Metazoan Parasite Cetacean Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We greatly acknowledge Michael Stadermann and his team at the SWDF Diving Center (Hurghada, Egypt), the Dolphin Watch Alliance (Gossau, Switzerland) for providing study samples, boat equipment and field support and Marquardt Media Production on behalf of the television company ZDF/Arte. We also thank Natalia Pryanishnikova for providing underwater photographs and Dr. Kernt Köhler (Institute for Veterinary Pathology, Giessen, Germany) for his support in taking pictures of adult A. typica and Cymothoidae indet. specimens.

References

  1. Abril E, Balbuena JA, Fernández M, Raga JA (1991) A new species of the genus Zalophotrema (Digenea: Campulidae), Zalophotrema atlanticum n. sp., from the liver of the striped dolphin Stenella coeruleoalba (Meyen, 1833) (Cetacea: Delphinidae) in Atlantic waters. Syst Parasitol 18:133–138CrossRefGoogle Scholar
  2. Amir OA, Berggren P, Ndaro SGM, Jiddawi N (2005) Feeding ecology of the Indo-Pacific bottlenose dolphin (Tursiops aduncus) incidentally caught in the gillnet fisheries off Zanzibar, Tanzania. Estuar Coast Shelf Sci 63:429–437CrossRefGoogle Scholar
  3. Arafa SZA, Al-Hoot AA, Hussein HS (2009) Pathological and ultrastructural studies on Anisakis simplex Rudolphi-1809 infecting Carangoides bajad with special reference to intestinal maturation in puppies. J Egypt Soc Parasitol 39:607–616PubMedGoogle Scholar
  4. Arizono N, Yamada M, Nakamura-Uchiyama F, Ohnishi K (2009) Diphyllobothriasis associated with eating raw Pacific salmon. Emerg Infect Dis 15:866–870PubMedCentralPubMedCrossRefGoogle Scholar
  5. Arundel JH (1978) Parasites and parasitic diseases of Australian marine mammals. In: The University of Sydney, Post-Graduate Committee in Veterinary Science, Proceedings No. 36 of Course of Veterinareans. Lincoln House, Sydney, Australia, pp 323–333Google Scholar
  6. Aytemiz I, Dede A, Danyer E, Tonay AM (2012) Morphological identification of parasites found in the stomach contents of bycaught striped dolphins (Stenella coeruleoalba) from Turkish Eastern Mediterranean Sea coast. J Black Sea Mediterr Environ 18:238–245Google Scholar
  7. Aznar FJ, Raga JA, Balbuena JA (1994) Are epizoites biological indicators of a western Mediterranean striped dolphin die-off? Dis Aquat Organ 18:159–163CrossRefGoogle Scholar
  8. Aznar FJ, Balbuena JA, Fernández M, Raga JA (2001) Living together: the parasites of marine mammals. In: Evans PGH, Raga JA (eds) Marine mammals. Biology and conservation. Kluwer Academic Plenum, London, pp 385–421, pp. 385–423Google Scholar
  9. Aznar FJ, Fognani FJ, Balbuena JA, Pietrobelli M, Raga JA (2006) Distribution of Pholeter gastrophilus (Digenea) within the stomach of four odontocete species: the role of the diet and digestive physiology of hosts. Parasitology 133:369–380PubMedCrossRefGoogle Scholar
  10. Bauer C (2006) Untersuchungsmethoden. In: Schnieder T (ed) Veterinärmedizinische Parasitologie, 6th edn. Parey, Berlin, pp 84–104Google Scholar
  11. Bejder L, Samuels A, Whitehead H, Gales N (2006) Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Anim Behav 72:1149–1158CrossRefGoogle Scholar
  12. Bunkley-Williams L, Williams EH Jr (1998) Isopods associated with fishes: a synopsis and corrections. J Parasitol 84:893–896PubMedCrossRefGoogle Scholar
  13. Carvalho VL, Bevilaqua CML, Myo Iñiguez A, Mathews-Cascon H, Bezerra Ribeiro F, Bezerra Pessoa LM, Oliveira de Meirelles AC, Gomes Borges JC, Marigo J, Soares L, de Lima Silva FJ (2010) Metazoan parasites of cetaceans off the northeastern coast of Brazil. Vet Parasitol 173:116–122PubMedCrossRefGoogle Scholar
  14. Cavallero S, Nadler SA, Paggi L, Barros NB, D’Amelio S (2011) Molecular characterization and phylogeny of anisakid nematodes from cetaceans from southeastern Atlantic coasts of USA, Gulf of Mexico, and Caribbean Sea. Parasitol Res 108:781–792PubMedCrossRefGoogle Scholar
  15. Cerioni S, Mariniello L (1996) Parasitic metazoans of Stenella coeruleoalba (Cetacea: Delphinidae) stranded along the coast of Latium, 1985–1991. Parassitologia 38:505–510PubMedGoogle Scholar
  16. Chai JY, Darwin Murrell K, Lymbery AJ (2005) Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35:1233–1254PubMedCrossRefGoogle Scholar
  17. Christiansen F, Lusseau D, Stensland E, Berggren P (2010) Effects of tourist boats on the behaviour of Indo-Pacific bottlenose dolphins off the south coast of Zanzibar. Endanger Species Res 11:91–99CrossRefGoogle Scholar
  18. Coklin T, Farber J, Parrington L, Dixon B (2007) Prevalence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in dairy cattle in Ontario, Canada. Vet Parasitol 150:297–305PubMedCrossRefGoogle Scholar
  19. Colón-Llavina MM, Mignucci-Giannoni AA, Mattiucci S, Paoletti M, Nascetti G, Williams EH Jr (2009) Additional records of metazoan parasites from Caribbean marine mammals, including genetically identified anisakid nematodes. Parasitol Res 105:1239–1252PubMedCrossRefGoogle Scholar
  20. Cordes DO, O’Hara PJ (1979) Diseases of captive marine mammals. N Z Vet J 27:147–150PubMedCrossRefGoogle Scholar
  21. Curtis MA, Bylund G (1991) Diphyllobothriasis: fish tapeworm disease in the circumpolar north. Arctic Med Res 50:18–24PubMedGoogle Scholar
  22. Dailey MD (1985) Diseases of Mammalia: Cetacea. In: Kinne O (ed) Diseases of marine animals, vol. IV, part 2: Reptilia, Aves, Mammalia. Biologische Anstalt Helgoland, Hamburg, pp 805–847Google Scholar
  23. Dailey MD (2001) Parasites diseases. In: Dierauf LA, Gulland FMD (eds) CRC handbook of marine mammal medicine. CRC Press, Boca Raton, pp 767–778Google Scholar
  24. Dailey MD (2007) A new species of Digenea (Trematoda: Brachycladiidae) from the Gervais’ beaked whale, Mesoplodon europaeus, with comments on other cetacean liver flukes. Comp Parasitol 74:229–232CrossRefGoogle Scholar
  25. Dailey MD, Stroud R (1978) Parasites and associated pathology observed in cetaceans stranded along the Oregon coast. J Wildl Dis 14:503–511PubMedCrossRefGoogle Scholar
  26. Dailey MD, Walker WA (1978) Parasitism as a factor (?) in single strandings of southern California cetaceans. J Parasitol 64:593–596PubMedCrossRefGoogle Scholar
  27. De Ley P, Félix M-A, Frisse LM, Nadler SA, Sternberg PW, Thomas WK (1999) Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology 1:519–612CrossRefGoogle Scholar
  28. De Vantier LM, Turak E, Al-Shaikh KA, Cheung CPS, Abdul-Aziz M, De’ath G, Done TJ (2000) Ecological indicators of status of coral communities for marine protected areas planning: case studies from Arabia. In: Lloyd D, Done TJ, Diop S (eds) Information management and decision support for marine biodiversity protection and human welfare: coral reefs. UNEP, NairobiGoogle Scholar
  29. Delyamure SL (1955) Helminth fauna of marine mammals (ecology and phylogeny). Moscow: Akademiya Nauk SSSR, 517 pp (In Russian: translated by Israel Program for Scientific Translation, Jerusalem, 1968), p 522Google Scholar
  30. Deng MQ, Peterson RP, Cliver DO (2000) First findings of Cryptosporidium and Giardia in California sea lions (Zalophus californianus). J Parasitol 86:490–494PubMedGoogle Scholar
  31. Eckert J, Friedhoff KT, Zahner H, Deplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin. Enke Verlag, Stuttgart, p 632Google Scholar
  32. Farjallah S, Ben Slimane B, Busi M, Paggi L, Amor N, Bell H, Said K, D’Amelio S (2008) Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitol Res 102:371–379PubMedCrossRefGoogle Scholar
  33. Fernández M, Aznar FJ, Latorre A, Raga JA (1998a) Molecular phylogeny of the families Campulidae and Nasitrematidae (Trematoda) based on mtDNA sequence comparison. Int J Parasitol 28:767–775PubMedCrossRefGoogle Scholar
  34. Fernández M, Littlewood DTJ, Latorre A, Raga JA, Rollinson D (1998b) Phylogenetic relationships of the family Campulidae (Trematoda) based on 18S rRNA sequences. Parasitology 117:383–391PubMedCrossRefGoogle Scholar
  35. Fernández M, Aznar FJ, Montero FE, Georgiev BB, Raga JA (2004) Gastrointestinal helminths of Cuvier’s beaked whales, Ziphius cavirostris, from the western Mediterranean. J Parasitol 90:418–420PubMedCrossRefGoogle Scholar
  36. Fertl D (2002) Barnacles. In: Perrin WF, Würsig B, Thewissen HGM (eds) Encyclopedia of marine mammals. Academic, San Diego, pp 75–78Google Scholar
  37. Fleischman RW, Squire RA (1970) Verminous pneumonia in the California sea lion (Zalophus californianus). Pathol Vet 7: 89-101Google Scholar
  38. Gasser RB, Chilton NB, Hoste H, Beveridge I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res 21:2525–2526PubMedCentralPubMedCrossRefGoogle Scholar
  39. Gasser RB, Stewart LE, Speare R (1996) Genetic markers in ribosomal DNA for hookworm identification. Acta Trop 62:15–21PubMedCrossRefGoogle Scholar
  40. Geraci JR, St. Aubin DJ (1987) Effects of parasites on marine mammals. Int J Parasitol 17:407–414PubMedCrossRefGoogle Scholar
  41. Gibson DI (2005) Family Brachycladiidae (Odhner, 1905). In: Jones A, Gibson RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CAB International and The Natural History Museum, London, pp 641–652Google Scholar
  42. Gibson DI, Harris EA, Bray RA, Jepson PD, Kuiken T, Baker JR, Simpson VR (1998) A survey of the helminth parasites of cetaceans stranded on the coast of England and Wales during the period 1990–1994. J Zool 244:563–574CrossRefGoogle Scholar
  43. Goren M, Dor M (1994) An updated checklist of the fishes of the Red Sea (CLOFRES II). The Israel Academy of Sciences and Humanities, Jerusalem, Israel, p 120Google Scholar
  44. Heine J (1982) Eine einfache Nachweismethode für Kryptosporidien im Kot. Zbl Vet Med B 29:324–327CrossRefGoogle Scholar
  45. Ishiwata K, Shinohara A, Yagi K, Horri Y, Tsuchiya K, Nawa Y (2004) Identification of tissue-embedded ascarid larvae by ribosomal DNA sequencing. Parasitol Res 92:50–52PubMedCrossRefGoogle Scholar
  46. Jaber JR, Pérez J, Arbelo M, Zafra R, Fernández A (2006) Pathological and immunohistochemical study of gastrointestinal lesions in dolphins stranded in the Canary Islands. Vet Rec 159:410–414PubMedCrossRefGoogle Scholar
  47. Jardine JE, Dubey JP (2002) Congenital toxoplasmosis in a Indo-Pacific bottlenose dolphin (Tursiops aduncus). J Parasitol 88:197–199PubMedGoogle Scholar
  48. Jenkins EJ, Schurer JM, Gesy KM (2011) Old problems on a new playing field: helminth zoonoses transmitted among dogs, wildlife, and people in a changing northern climate. Vet Parasitol 182:54–69PubMedCrossRefGoogle Scholar
  49. Kleinertz S, Damriyasa M, Hagen W, Theisen S, Palm HW (2012) An environmental assessment of the parasite fauna of the reef-associated grouper Epinephelus areolatus from Indonesian waters. J Helminthol. doi: 10.1017/S0022149X12000715 PubMedGoogle Scholar
  50. Klimpel S, Palm HW (2011) Anisakid nematode (Ascaridoidea) life cycles and distribution: increasing zoonotic potential in the time of climate change? In: Mehlhorn H (ed) Progress in parasitology. Düsseldorf University Press, DüsseldorfGoogle Scholar
  51. Klimpel S, Palm HW, Rückert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9PubMedCrossRefGoogle Scholar
  52. Koinari M, Karl S, Elliot A, Ryan U, Lymbery AJ (2013) Identification of Anisakis species (Nematoda: Anisakidae) in marine fish hosts from Papua New Guinea. Vet Parasitol 193:126–133PubMedCrossRefGoogle Scholar
  53. Kuhn T, García-Màrquez J, Klimpel S (2011) Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PloS ONE 6(12):e28642. doi: 10.1371/journal.pone.0028642
  54. Kumar V, Vercruysse J, Kageruka P, Mortelmans J (1975) Nasitrema attenuata (Trematoda) infection of Tursiops truncatus and its potentialities as an aetiological agent of chronic pulmonary lesions. J Helminthol 49:289–292PubMedCrossRefGoogle Scholar
  55. Lehnert K, Raga JA, Siebert U (2005) Macroparasites in stranded and bycaught harbour porpoises from German and Norwegian waters. Dis Aquat Organ 64:265–269PubMedCrossRefGoogle Scholar
  56. Lewis RJ, Berry K (1988) Brain lesions in a Pacific white-sided dolphin (Lagenorhynchus obliquidens). J Wildl Dis 24:577–581PubMedCrossRefGoogle Scholar
  57. Loizaga de Casto RL, Leonardi MS, Grandi MF, García NA, Crespo EA (2011) Far from home: record of a vagrant striped dolphin in Patagonia with notes on diet, parasites and age determination. Mamm Biol 76:521–524Google Scholar
  58. Mateu P, Raga JA, Aznar FJ (2011) Host specificity of Oschmarinella rochebruni and Brachycladium atlanticum (Digenea: Brachycladiidae) in five cetacean species from western Mediterranean waters. J Helminthol 85:12–19. doi: 10.1017/S0022149X10000180 PubMedCrossRefGoogle Scholar
  59. Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardine, 1845: an update. Parasite 13:99–113PubMedCrossRefGoogle Scholar
  60. Mattiucci S, Paggi L, Nascetti G, Portes Santos C, Costa G, Di Beneditto AP, Ramos R, Argyrou M, Cianchi R, Bullini L (2002) Genetic markers in the study of Anisakis typica (Diesing, 1860): larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Syst Parasitol 51:159–170PubMedCrossRefGoogle Scholar
  61. Mattiucci S, Nascetti G, Dailey M, Webb SC, Barros NB, Cianchi R, Bullini L (2005) Evidence for a new species of Anisakis (Dujardin, 1845): morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Syst Parasitol 61:157–171PubMedCrossRefGoogle Scholar
  62. McDowall RM, Peregrine AS, Leonard EK, Lacombe C, Leke M, Rebelo AR, Cai HY (2011) Evaluation of the zoonotic potential of Giardia duodenalis in fecal samples from dogs and cats in Ontario. Can Vet J 52:1329–1333PubMedCentralPubMedGoogle Scholar
  63. Mehlhorn H, Peters W (1983) Diagnose der Parasiten des Menschen einschließlich der Therapie einheimischer und tropischer Parasitosen. Gustav Fischer Verlag, Stuttgart, p 275Google Scholar
  64. Mehlhorn H, Piekarski G (1998) Grundriß der Parasitenkunde. Parasiten des Menschen und der Nutztiere. 5, überarbeitete und erweiterte Auflage. Gustav Fischer Verlag, Stuttgart, p 516Google Scholar
  65. Mignucci-Giannoni AA, Hoberg EP, Siegel-Causey D, Williams EH Jr (1998) Metazoan parasites and other symbionts of cetaceans in the Caribbean. J Parasitol 84:939–946PubMedCrossRefGoogle Scholar
  66. Nadler SA, Hudspeth DSS (2000) Phylogeny of the Ascaridoidea (nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J Parasitol 86:380–393PubMedGoogle Scholar
  67. Nadler SA, D’Amelio S, Dailey MD, Paggi L, Siu S, Sakanari JA (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. J Parasitol 91:1413–1429PubMedCrossRefGoogle Scholar
  68. Nel-S A, Dronen NO (2007) Studies on the juveniles of a species of Anisakis (Nematoda: Anisakidae) from the orange-spotted trevally Cangoides bajad (Carangidae), from the Red Sea, Egypt. J Egypt Soc Parasitol 37:1055–1064Google Scholar
  69. Notarbartolo-di-Sciara G, Addink M, Baldwin RH, Rudolph P, Smeenk C (2007) A review of cetaceans from the Red Sea. Abstracts, 21st Annual Conference of the European Cetacean Society, San Sebastian, Spain, 23–25Google Scholar
  70. O’Shea TJ, Homer BL, Greiner EC, Layton AW (1991) Nasitrema sp.-associated encephalitis in a striped dolphin (Stenella coeruleoalba) stranded in the Gulf of Mexico. J Wildl Dis 27:706–709PubMedCrossRefGoogle Scholar
  71. Oliveira JB, Morales JA, González-Barrientos RC, Hernández-Gamboa J, Hernández-Mora G (2011) Parasites of cetaceans stranded on the Pacific coast of Costa Rica. Vet Parasitol 182:1–10CrossRefGoogle Scholar
  72. Omata Y, Hammond T, Itoh K, Murata K (2005) Antibodies against Toxoplasma gondii in the Pacific bottlenose dolphin (Tursiops aduncus) from the Solomon Islands. J Parasitol 91:965–967PubMedCrossRefGoogle Scholar
  73. Palm HW, Damriyasa IM, Linda Oka IBM (2008) Molecular genotyping of Anisakis Dujardin, 1845 (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia. Helminthologia 45:3–12CrossRefGoogle Scholar
  74. Parker GA, Migaki G, Walker WA (1977) Cerebral trematodiasis in a dolphin. Mil Med 142:861–871PubMedGoogle Scholar
  75. Quiñones R, Giovannini A, Raga JA, Fernández M (2013) Intestinal helminth fauna of bottlenose dolphin Tursiops truncatus and common dolphin Delphinus delphis from the Western Mediterranean. J Parasitol 99:576–579PubMedCrossRefGoogle Scholar
  76. Raga JA, Balbuena JA, Aznar J, Fernández M (1997) The impact of parasites on marine mammals: a review. Parassitologia 394:293–296Google Scholar
  77. Ridgway SH, Dailey MD (1972) Cerebral and cerebellar involvement of trematode parasites in dolphins and their possible role in stranding. J Wildl Dis 8:33-43Google Scholar
  78. Riegl B, Velimirov B (1994) The structure of coral communities at Hurghada in the Northern Red Sea. Mar Ecol 15:213–231CrossRefGoogle Scholar
  79. Salyer SJ, Gillespie TR, Rwego IB, Chapman CA, Goldberg TL (2012) Epidemiology and molecular relationships of Cryptosporidium spp. in people, primates, and livestock from Western Uganda. PLoS Negl Trop Dis 6(4):e1597PubMedCentralPubMedCrossRefGoogle Scholar
  80. Scholz T, Garcia HH, Kuchta R, Wicht B (2009) Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clin Microbiol Rev 22:146–160PubMedCentralPubMedCrossRefGoogle Scholar
  81. Skov J, Kania PW, Olsen MM, Lauridsen JH, Buchmann K (2009) Nematode infections of maricultured and wild fishes in Danish waters: a comparative study. Aquaculture 298:24–28CrossRefGoogle Scholar
  82. Slob CM, Hendrikx WML, Borgsteede FHM, Hartmann MG (1996) Lungworms in harbour porpoises (Phocoena phocoena) from Dutch waters. In: Hartmann MG (ed) Proceedings of the Third ECS Workshop on Cetacean Pathology. Lisabon, European Cetacean Society Newsletter no. 37, pp 35–40Google Scholar
  83. Thompson RC, Palmer CS, O’Handley R (2008) The public health and clinical significance of Giardia and Cryptosporidium in domestic animals. Vet J 177:18–25PubMedCrossRefGoogle Scholar
  84. Tomo I, Kemper CM, Lavery TJ (2010) Eighteen-year study of south Australian dolphins shows variation in lung nematodes by season, year, age, class, and location. J Wildl Dis 46:488–498PubMedCrossRefGoogle Scholar
  85. Trilles JP (1991) Present researches and perspectives on Isopoda (Cymothoidae and Gnathiidae) parasites of fishes (systematics, faunistics, ecology, biology, and physiology). Wiad Parazytol 37:141–143PubMedGoogle Scholar
  86. Tzipori S, Widmer G (2008) A hundred-year retrospective on cryptosporidiosis. Trends Parasitol 24:184–189PubMedCentralPubMedCrossRefGoogle Scholar
  87. Ugland KI, Strømnes E, Berland B, Aspholm PE (2004) Growth, fecundity and sex ratio of adult whaleworm (Anisakis simplex; Nematoda, Ascaridoidea, Anisakidae) in three whale species from the North-East Atlantic. Parasitol Res 92:484–489PubMedCrossRefGoogle Scholar
  88. Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone AA, Colom-Llavina MM, Nascetti G (2006) Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. J Parasitol 92:156–166PubMedCrossRefGoogle Scholar
  89. Van Wormer E, Fritz H, Shapiro K, Mazet JAK, Conrad PA (2013) Molecules to modeling: Toxoplasma gonii oocysts at the human-animal-environment interface. Comp Immunol Microbiol Infect Dis 36:217–231CrossRefGoogle Scholar
  90. Wells RS (1998) Prey and feeding patterns of resident bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. J Mamm 79(3):1045–1059CrossRefGoogle Scholar
  91. Woodard JC, Zam SG, Caldwell DK, Caldwell MC (1969) Some parasitic disease of dolphins. Pathol Vet 6:257–272PubMedCrossRefGoogle Scholar
  92. Yang J, Scholten T (1977) A fixative for intestinal parasites permitting the use of concentration and permanent staining procedures. Am J Clin Pathol 67:300–304PubMedGoogle Scholar
  93. Young KH, Bullock SL, Melvin DM, Sprull CL (1979) Ethyl acetate as a substitute for diethyl ether in the formalin-ether sedimentation technique. J Clin Microbiol 10:852–853PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • S. Kleinertz
    • 1
    Email author
  • C. Hermosilla
    • 1
  • A. Ziltener
    • 2
    • 3
  • S. Kreicker
    • 2
    • 3
  • J. Hirzmann
    • 1
  • F. Abdel-Ghaffar
    • 4
  • A. Taubert
    • 1
  1. 1.Institute of ParasitologyJustus Liebig University GiessenGiessenGermany
  2. 2.Anthropological Institute and MuseumUniversity of ZurichZurichSwitzerland
  3. 3.Dolphin Watch Alliance (DWA)GossauSwitzerland
  4. 4.Zoology Department, Faculty of ScienceCairo UniversityCairoEgypt

Personalised recommendations

Cite article

Buy options