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

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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.

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References

  • 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 18:133–138

    Article  Google Scholar 

  • 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 63:429–437

    Article  Google Scholar 

  • 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 39:607–616

    PubMed  Google Scholar 

  • Arizono N, Yamada M, Nakamura-Uchiyama F, Ohnishi K (2009) Diphyllobothriasis associated with eating raw Pacific salmon. Emerg Infect Dis 15:866–870

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 323–333

    Google Scholar 

  • 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 18:238–245

    Google Scholar 

  • Aznar FJ, Raga JA, Balbuena JA (1994) Are epizoites biological indicators of a western Mediterranean striped dolphin die-off? Dis Aquat Organ 18:159–163

    Article  Google Scholar 

  • 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. 385–423

    Google Scholar 

  • 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 133:369–380

    Article  CAS  PubMed  Google Scholar 

  • Bauer C (2006) Untersuchungsmethoden. In: Schnieder T (ed) Veterinärmedizinische Parasitologie, 6th edn. Parey, Berlin, pp 84–104

    Google Scholar 

  • Bejder L, Samuels A, Whitehead H, Gales N (2006) Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Anim Behav 72:1149–1158

    Article  Google Scholar 

  • Bunkley-Williams L, Williams EH Jr (1998) Isopods associated with fishes: a synopsis and corrections. J Parasitol 84:893–896

    Article  CAS  PubMed  Google Scholar 

  • 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 173:116–122

    Article  PubMed  Google Scholar 

  • 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 108:781–792

    Article  PubMed  Google Scholar 

  • Cerioni S, Mariniello L (1996) Parasitic metazoans of Stenella coeruleoalba (Cetacea: Delphinidae) stranded along the coast of Latium, 1985–1991. Parassitologia 38:505–510

    CAS  PubMed  Google Scholar 

  • Chai JY, Darwin Murrell K, Lymbery AJ (2005) Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35:1233–1254

    Article  PubMed  Google Scholar 

  • 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 11:91–99

    Article  Google Scholar 

  • 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 150:297–305

    Article  CAS  PubMed  Google Scholar 

  • 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 105:1239–1252

    Article  PubMed  Google Scholar 

  • Cordes DO, O’Hara PJ (1979) Diseases of captive marine mammals. N Z Vet J 27:147–150

    Article  CAS  PubMed  Google Scholar 

  • Curtis MA, Bylund G (1991) Diphyllobothriasis: fish tapeworm disease in the circumpolar north. Arctic Med Res 50:18–24

    CAS  PubMed  Google Scholar 

  • 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 805–847

    Google Scholar 

  • Dailey MD (2001) Parasites diseases. In: Dierauf LA, Gulland FMD (eds) CRC handbook of marine mammal medicine. CRC Press, Boca Raton, pp 767–778

    Google Scholar 

  • 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 74:229–232

    Article  Google Scholar 

  • Dailey MD, Stroud R (1978) Parasites and associated pathology observed in cetaceans stranded along the Oregon coast. J Wildl Dis 14:503–511

    Article  CAS  PubMed  Google Scholar 

  • Dailey MD, Walker WA (1978) Parasitism as a factor (?) in single strandings of southern California cetaceans. J Parasitol 64:593–596

    Article  CAS  PubMed  Google Scholar 

  • 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 1:519–612

    Article  Google Scholar 

  • 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, Nairobi

    Google Scholar 

  • 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 522

  • Deng MQ, Peterson RP, Cliver DO (2000) First findings of Cryptosporidium and Giardia in California sea lions (Zalophus californianus). J Parasitol 86:490–494

    CAS  PubMed  Google Scholar 

  • Eckert J, Friedhoff KT, Zahner H, Deplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin. Enke Verlag, Stuttgart, p 632

    Google Scholar 

  • 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 102:371–379

    Article  PubMed  Google Scholar 

  • 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 28:767–775

    Article  PubMed  Google Scholar 

  • Fernández M, Littlewood DTJ, Latorre A, Raga JA, Rollinson D (1998b) Phylogenetic relationships of the family Campulidae (Trematoda) based on 18S rRNA sequences. Parasitology 117:383–391

    Article  PubMed  Google Scholar 

  • 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 90:418–420

    Article  PubMed  Google Scholar 

  • Fertl D (2002) Barnacles. In: Perrin WF, Würsig B, Thewissen HGM (eds) Encyclopedia of marine mammals. Academic, San Diego, pp 75–78

    Google Scholar 

  • Fleischman RW, Squire RA (1970) Verminous pneumonia in the California sea lion (Zalophus californianus). Pathol Vet 7: 89-101

    Google Scholar 

  • Gasser RB, Chilton NB, Hoste H, Beveridge I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res 21:2525–2526

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gasser RB, Stewart LE, Speare R (1996) Genetic markers in ribosomal DNA for hookworm identification. Acta Trop 62:15–21

    Article  CAS  PubMed  Google Scholar 

  • Geraci JR, St. Aubin DJ (1987) Effects of parasites on marine mammals. Int J Parasitol 17:407–414

    Article  CAS  PubMed  Google Scholar 

  • 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 641–652

    Google Scholar 

  • 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 244:563–574

    Article  Google Scholar 

  • 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 120

    Google Scholar 

  • Heine J (1982) Eine einfache Nachweismethode für Kryptosporidien im Kot. Zbl Vet Med B 29:324–327

    Article  CAS  Google Scholar 

  • 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 92:50–52

    Article  PubMed  Google Scholar 

  • 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 159:410–414

    Article  CAS  PubMed  Google Scholar 

  • Jardine JE, Dubey JP (2002) Congenital toxoplasmosis in a Indo-Pacific bottlenose dolphin (Tursiops aduncus). J Parasitol 88:197–199

    CAS  PubMed  Google Scholar 

  • 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 182:54–69

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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, Düsseldorf

    Google Scholar 

  • Klimpel S, Palm HW, Rückert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9

    Article  PubMed  Google Scholar 

  • 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 193:126–133

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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 49:289–292

    Article  CAS  PubMed  Google Scholar 

  • Lehnert K, Raga JA, Siebert U (2005) Macroparasites in stranded and bycaught harbour porpoises from German and Norwegian waters. Dis Aquat Organ 64:265–269

    Article  CAS  PubMed  Google Scholar 

  • Lewis RJ, Berry K (1988) Brain lesions in a Pacific white-sided dolphin (Lagenorhynchus obliquidens). J Wildl Dis 24:577–581

    Article  CAS  PubMed  Google Scholar 

  • 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 76:521–524

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardine, 1845: an update. Parasite 13:99–113

    Article  CAS  PubMed  Google Scholar 

  • 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 51:159–170

    Article  CAS  PubMed  Google Scholar 

  • 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 61:157–171

    Article  PubMed  Google Scholar 

  • 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 52:1329–1333

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mehlhorn H, Peters W (1983) Diagnose der Parasiten des Menschen einschließlich der Therapie einheimischer und tropischer Parasitosen. Gustav Fischer Verlag, Stuttgart, p 275

    Google Scholar 

  • Mehlhorn H, Piekarski G (1998) Grundriß der Parasitenkunde. Parasiten des Menschen und der Nutztiere. 5, überarbeitete und erweiterte Auflage. Gustav Fischer Verlag, Stuttgart, p 516

    Google Scholar 

  • Mignucci-Giannoni AA, Hoberg EP, Siegel-Causey D, Williams EH Jr (1998) Metazoan parasites and other symbionts of cetaceans in the Caribbean. J Parasitol 84:939–946

    Article  CAS  PubMed  Google Scholar 

  • 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 86:380–393

    CAS  PubMed  Google Scholar 

  • 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 91:1413–1429

    Article  CAS  PubMed  Google Scholar 

  • 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 37:1055–1064

    Google Scholar 

  • 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, 23–25

  • 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 27:706–709

    Article  PubMed  Google Scholar 

  • 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 182:1–10

    Article  Google Scholar 

  • 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 91:965–967

    Article  PubMed  Google Scholar 

  • 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 45:3–12

    Article  CAS  Google Scholar 

  • Parker GA, Migaki G, Walker WA (1977) Cerebral trematodiasis in a dolphin. Mil Med 142:861–871

    CAS  PubMed  Google Scholar 

  • 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 99:576–579

    Article  PubMed  Google Scholar 

  • Raga JA, Balbuena JA, Aznar J, Fernández M (1997) The impact of parasites on marine mammals: a review. Parassitologia 394:293–296

    Google Scholar 

  • Ridgway SH, Dailey MD (1972) Cerebral and cerebellar involvement of trematode parasites in dolphins and their possible role in stranding. J Wildl Dis 8:33-43

    Google Scholar 

  • Riegl B, Velimirov B (1994) The structure of coral communities at Hurghada in the Northern Red Sea. Mar Ecol 15:213–231

    Article  Google Scholar 

  • 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):e1597

    Article  PubMed Central  PubMed  Google Scholar 

  • Scholz T, Garcia HH, Kuchta R, Wicht B (2009) Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clin Microbiol Rev 22:146–160

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 298:24–28

    Article  Google Scholar 

  • 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 35–40

  • Thompson RC, Palmer CS, O’Handley R (2008) The public health and clinical significance of Giardia and Cryptosporidium in domestic animals. Vet J 177:18–25

    Article  PubMed  Google Scholar 

  • 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 46:488–498

    Article  PubMed  Google Scholar 

  • Trilles JP (1991) Present researches and perspectives on Isopoda (Cymothoidae and Gnathiidae) parasites of fishes (systematics, faunistics, ecology, biology, and physiology). Wiad Parazytol 37:141–143

    CAS  PubMed  Google Scholar 

  • Tzipori S, Widmer G (2008) A hundred-year retrospective on cryptosporidiosis. Trends Parasitol 24:184–189

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 92:484–489

    Article  PubMed  Google Scholar 

  • 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 92:156–166

    Article  CAS  PubMed  Google Scholar 

  • 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 36:217–231

    Article  Google Scholar 

  • Wells RS (1998) Prey and feeding patterns of resident bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. J Mamm 79(3):1045–1059

    Article  Google Scholar 

  • Woodard JC, Zam SG, Caldwell DK, Caldwell MC (1969) Some parasitic disease of dolphins. Pathol Vet 6:257–272

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Scholten T (1977) A fixative for intestinal parasites permitting the use of concentration and permanent staining procedures. Am J Clin Pathol 67:300–304

    CAS  PubMed  Google Scholar 

  • 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 10:852–853

    CAS  PubMed Central  PubMed  Google Scholar 

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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.

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  1. Institute of Parasitology, Justus Liebig University Giessen, Rudolf-Buchheim-Str. 2, 35392, Giessen, Germany

    S. Kleinertz, C. Hermosilla, J. Hirzmann & A. Taubert

  2. Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland

    A. Ziltener & S. Kreicker

  3. Dolphin Watch Alliance (DWA), Gossau, Switzerland

    A. Ziltener & S. Kreicker

  4. Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt

    F. Abdel-Ghaffar

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  1. S. Kleinertz
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Correspondence to S. Kleinertz.

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Kleinertz, S., Hermosilla, C., Ziltener, A. et al. Gastrointestinal parasites of free-living Indo-Pacific bottlenose dolphins (Tursiops aduncus) in the Northern Red Sea, Egypt. Parasitol Res 113, 1405–1415 (2014). https://doi.org/10.1007/s00436-014-3781-4

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