Skip to main content

Advertisement

SpringerLink
Log in

Occurrence of anthropozoonotic parasitic infections and faecal microbes in free-ranging sperm whales (Physeter macrocephalus) from the Mediterranean Sea

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Sperm whales (Physeter macrocephalus) are the largest toothed whales and only living member of family Physeteridae. Present survey represents first report on cultivable faecal microbes and gastrointestinal helminths and protozoans infecting free-ranging sperm whales inhabiting Mediterranean Sea waters surrounding Balearic Archipelago, Spain. Twenty-five individual sperm whale scat samples, including one calf, were collected without disturbance of animals during the summer of 2016. Parasitological diagnostic methods, such as sodium acetate acetic formalin (SAF) method, carbol fuchsin-stained faecal smears, Giardia/Cryptosporidium coproantigen ELISAs and an Anisakis-specific PCR were applied for further identification. Five bacterial genera, i.e. Acinetobacter, Clostridium, Enterococcus, Staphylococcus and Streptococcus, and one fungus namely Cladosporium were identified. Parasitological infections included seven different parasite species with some of them bearing anthropozoonotic potential. Thus, four of these parasites were zoonotic, i.e. Anisakis, Balantidium, Diphyllobothriidae gen. sp. and Giardia. Additionally, Zalophotrema curilensis eggs, spirurid-like eggs and Cystoisospora-like oocysts were identified. Molecular characterization identified Anisakis physeteris as the species infecting these whales. This survey provides first records on occurrence of two zoonotic enteropathogenic protozoan parasites (Giardia and Balantidium) and of facultative pathogenic bacteria (Clostridium and Enterococcus) in sperm whales. Presented data should be considered as a baseline study for future monitoring surveys on anthropozoonotic pathogens affecting free-living sperm whale populations and enhance investigations on possible impact on public health as well as on isolated Mediterranean sperm whale subpopulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abat C, Raoult D, Rolain JM (2016) Low level of resistance in enterococci isolated in four hospitals, Marseille, France. Microb Drug Resist 22:218–222

    Article  PubMed  CAS  Google Scholar 

  • Abeywardena H, Jex AR, Gasser RB (2015) A perspective on cryptosporidium and giardia, with an emphasis on bovines and recent epidemiological findings. Adv Parasitol 88:243–301

    Article  PubMed  Google Scholar 

  • Abril E, Balbuena JA, 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 

  • Aldape MJ, Bryant AE, Stevens DL (2006) Clostridium sordellii infection: epidemiology, clinical findings, and current perspectives on diagnosis and treatment. Clin Infect Dis 43:1436–1446

    Article  PubMed  CAS  Google Scholar 

  • Bauer C (2006) Untersuchungsmethoden. In: Schnieder T (ed) Veterinärmedizinische parasitologie. 6th edn. Parey MVS Medizinverlage Stuttgart, Stuttgart, pp 84–104

    Google Scholar 

  • Beineke A, Siebert U, Wohlsein P, Baumgartner W (2010) Immunology of whales and dolphins. Vet Immunol Immunopathol 133:81–94

    Article  PubMed  CAS  Google Scholar 

  • Bejder L et al (2006) Decline in relative abundance of bottlenose dolphins exposed to long-term disturbance. Conserv Biol 20:1791–1798

    Article  PubMed  Google Scholar 

  • Berón-Vera B, Crespo EA, Raga JA (2008) Parasites in stranded cetaceans of Patagonia. J Parasitol 94:946–948

    Article  PubMed  Google Scholar 

  • Bik EM, Costello EK, Switzer AD, Callahan BJ, Holmes SP, Wells RS, Carlin KP, Jensen ED, Venn-Watson S, Relman DA (2016) Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat Commun 7:10516

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bisping W, Amtsberg G (1988) Colour atlas for the diagnosis of bacterial pathogens in animals. John Wiley & Sons, Limited

    Google Scholar 

  • Bohm KH (1971) New selective culture media for erysipelothrix. Zentralbl Bakteriol Orig A 218:330–334

    PubMed  CAS  Google Scholar 

  • Bouzid M, Halai K, Jeffreys D, Hunter PR (2015) The prevalence of giardia infection in dogs and cats, a systematic review and meta-analysis of prevalence studies from stool samples. Vet Parasitol 207:181–202

    Article  PubMed  Google Scholar 

  • Brotons J (2015) Catxalots a balears: Una cultura amenaçada Monografia de la SHNB , 20 (LLibre verd de protecció d'Espècies a les Balears):326

  • Buck JD, Shepard LL, Spotte S (1987) Clostridium perfringens as the cause of death of a captive Atlantic bottlenosed dolphin (tursiops truncatus). J Wildl Dis 23:488–491

    Article  PubMed  CAS  Google Scholar 

  • Burkhardt F (1992) Mikrobiologische thieme verlag. Stuttgart New York,

  • Carter GR, Roberts AW, Chengappa MM (1995) Essentials of veterinary microbiology. vol viii, 394 p., [4] p. of plates. Williams & Wilkins, Baltimore

  • 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 

  • Clark GC, Briggs DC, Karasawa T, Wang X, Cole AR, Maegawa T, Jayasekera PN, Naylor CE, Miller J, Moss DS, Nakamura S, Basak AK, Titball RW (2003) Clostridium absonum alpha-toxin: new insights into clostridial phospholipase c substrate binding and specificity. J Mol Biol 333:759–769

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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

  • Danil K, St Leger JA, Dennison S, Bernaldo de Quiros Y, Scadeng M, Nilson E, Beaulieu N (2014) Clostridium perfringens septicemia in a long-beaked common dolphin delphinus capensis: an etiology of gas bubble accumulation in cetaceans. Dis Aquat Org 111:183–190

    Article  PubMed  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science 287:443–449

    Article  PubMed  CAS  Google Scholar 

  • Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Izdatel'stvo Akiademii Nauk SSSR, Moscow

  • Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16s rdna bacterial tag-encoded flx amplicon pyrosequencing (btefap). BMC Microbiol 8:125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eckert J, Friedhof KT, Zahner H, Desplazes P (2008) Lehrbuch der parasitologie für die tiermedizin. Enke Verlag, Stuttgart

  • Esteban JG, Aguirre C, Angles R, Ash LR, Mas-Coma S (1998) Balantidiasis in aymara children from the northern bolivian altiplano. Am J Trop Med Hyg 59:922–927

    Article  PubMed  CAS  Google Scholar 

  • Fernández M, Aznar FJ, Latorre A, Raga J (1998) Molecular phylogeny of the families campulidae and nasitrematidae (trematoda) based on mtdna sequence comparisonfn1fn1note: nucleotide sequence data reported in this paper are available in the embl, genbanktm and ddjb data bases under the accession numbers af034551, af034552, af034553, af034554, af034555, af034556 and af034557. Int J Parasitol 28:767–775

    Article  PubMed  Google Scholar 

  • Fernandez M, Littlewood DTJ, Latorre A, Raga JA, Rollinson D (1998) Phylogenetic relationships of the family campulidae (trematoda) based on 18s rrna sequences. Parasitology 117:383–391

    Article  PubMed  CAS  Google Scholar 

  • Fleischman RW, Squire RA (1970) Verminous pneumonia in the California Sea lion (zalophus californianus). Pathol Vet 7:89–101

    PubMed  CAS  Google Scholar 

  • Garcia Alonso M, Caballero ML, Umpierrez A, Lluch-Bernal M, Knaute T, Rodriguez-Perez R (2015) Relationships between t cell and ige/igg4 epitopes of the anisakis simplex major allergen ani s 1. Clin Exp Allergy 45:994–1005

    Article  PubMed  CAS  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  PubMed  PubMed Central  CAS  Google Scholar 

  • Gasser RB, Hoste H (1995) Genetic markers for closely-related parasitic nematodes. Mol Cell Probes 9:315–320

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 

  • Gibson DI, Jones A, Bray RA, Gibson DI (2005) Family brachycladiidae odhner:1905

  • Greenwood AG, Taylor DC (1978) Clostridial myositis in marine mammals. Vet Rec 103:54–55

    Article  PubMed  CAS  Google Scholar 

  • Guass O, Haapanen LM, Dowd SE, Sirovic A, McLaughlin RW (2016) Analysis of the microbial diversity in faecal material of the endangered blue whale, balaenoptera musculus. Antonie Van Leeuwenhoek 109:1063–1069

    Article  PubMed  Google Scholar 

  • Hale A, Kirby JE, Albrecht M (2016) Fatal spontaneous clostridium bifermentans necrotizing endometritis: a case report and literature review of the pathogen. Open Forum Infect Dis 3:ofw095

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammerum AM (2012) Enterococci of animal origin and their significance for public health. Clin Microbiol Infect 18:619–625

    Article  PubMed  CAS  Google Scholar 

  • Hassell JM, Blake DP, Cranfield MR, Ramer J, Hogan JN, Noheli JB, Waters M, Hermosilla C (2013) Occurrence and molecular analysis of balantidium coli in mountain gorilla (gorilla beringei beringei) in the volcanoes national park, Rwanda. J Wildl Dis 49:1063–1065

    Article  PubMed  Google Scholar 

  • Heine J (1982) An easy technique for the demonstration of cryptosporidia in feces. Zentralblatt fur Veterinarmedizin Reihe B-journal of veterinary medicine series B-infectious diseases immunology food hygiene veterinary. Public Health 29:324–327

    CAS  Google Scholar 

  • Hermosilla C, Silva LM, Kleinertz S, Prieto R, Silva MA, Taubert A (2016a) Endoparasite survey of free-swimming baleen whales (balaenoptera musculus, b. Physalus, b. Borealis) and sperm whales (physeter macrocephalus) using non/minimally invasive methods. Parasitol Res 115:889–896

    Article  PubMed  Google Scholar 

  • Hermosilla C, Silva LM, Navarro M, Taubert A (2016b) Anthropozoonotic endoparasites in free-ranging "urban" south american sea lions (otaria flavescens). J Vet Med 2016:7507145

    Article  PubMed  PubMed Central  Google Scholar 

  • Hermosilla C, Silva LM, Prieto R, Kleinertz S, Taubert A, Silva MA (2015) Endo- and ectoparasites of large whales (cetartiodactyla: Balaenopteridae, physeteridae): overcoming difficulties in obtaining appropriate samples by non- and minimally-invasive methods. Int J Parasitol Parasites Wildl 4:414–420

    Article  PubMed  PubMed Central  Google Scholar 

  • Hernandez F, Arguello AP, Rivera P, Jimenez E (1993) Balantidium coli (vestibuliferida: Balantidiidae): the persistence of an old problem. Rev Biol Trop 41:149–151

    PubMed  CAS  Google Scholar 

  • Hudson PJ, Cattadori M, Boag B, Dobson AP (2006) Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. J Helminthol 80:175–182

    Article  PubMed  CAS  Google Scholar 

  • Hughes-Hanks JM, Rickard LG, Panuska C, Saucier JR, O'Hara TM, Dehn L, Rolland RM (2005) Prevalence of cryptosporidium spp. and giardia spp. in five marine mammal species. J Parasitol 91:1225–1228

    Article  PubMed  CAS  Google Scholar 

  • Hunt KE, Moore MJ, Rolland RM, Kellar NM, Hall AJ, Kershaw J, Raverty SA, Davis CE, Yeates LC, Fauquier DA, Rowles TK, Kraus SD (2013) Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conservation Physiology 1

  • 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 

  • Jones JL, Dubey JP (2010) Waterborne toxoplasmosis--recent developments. Exp Parasitol 124:10–25

    Article  PubMed  CAS  Google Scholar 

  • Kleinertz S, Christmann S, Silva LM, Hirzmann J, Hermosilla C, Taubert A (2014a) Gastrointestinal parasite fauna of emperor penguins (aptenodytes forsteri) at the Atka bay, Antarctica. Parasitol Res 113:4133–4139

    Article  PubMed  CAS  Google Scholar 

  • Kleinertz S, Hermosilla C, Ziltener A, Kreicker S, Hirzmann J, Abdel-Ghaffar F, Taubert A (2014b) Gastrointestinal parasites of free-living indo-pacific bottlenose dolphins (tursiops aduncus) in the northern red sea, Egypt. Parasitol Res 113:1405–1415

    Article  PubMed  CAS  Google Scholar 

  • Kolkhir P, Balakirski G, Merk HF, Olisova O, Maurer M (2016) Chronic spontaneous urticaria and internal parasites--a systematic review. Allergy 71:308–322

    Article  PubMed  CAS  Google Scholar 

  • Kuhn T, Cunze S, Kochmann J, Klimpel S (2016) Environmental variables and definitive host distribution: a habitat suitability modelling for endohelminth parasites in the marine realm. Sci Rep 6:30246

  • 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  PubMed  CAS  Google Scholar 

  • Ladas SD, Savva S, Frydas A, Kaloviduris A, Hatzioannou J, Raptis S (1989) Invasive balantidiasis presented as chronic colitis and lung involvement. Dig Dis Sci 34:1621–1623

    Article  PubMed  CAS  Google Scholar 

  • Lambertsen RH (1997) Natural disease problems of the sperm whale. Bulletin de l'Institut Royal des Sciences Naturelles de Belgique Biologie 67:105–112

    Google Scholar 

  • Lambertsen RH, Kohn BA (1987) Unusual multisystemic pathology in a sperm whale bull. J Wildl Dis 23:510–514

    Article  PubMed  CAS  Google Scholar 

  • Lang B, Eskens U, Hartmann A, Braun V, Schmidt MJ, von Hegel G (2014) Focal meningitis in a California Sea lion (zalophus californianus)--diagnostic procedure and pathology. Tierarztl Prax Ausg G Grosstiere Nutztiere 42:368–372

    Article  PubMed  CAS  Google Scholar 

  • Lewis T, Gillespie D, Lacey C, Matthews J, Danbolt M, Leaper R, McLanaghan R, Moscrop A (2007) Sperm whale abundance estimates from acoustic surveys of the ionian sea and straits of sicily in 2003. J Mar Biol Assoc U K 87:353–357

    Article  Google Scholar 

  • Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: Evolution of the vertebrate gut microbiota. 6:776

  • Litvaitis MK, Nunn G, Thomas WK, Kocher TD (1994) A molecular approach for the identification of meiofaunal turbellarians (platyhelminthes, turbellaria). Mar Biol 120:437–442

    Article  CAS  Google Scholar 

  • Maclennan JD (1962) The histotoxic clostridial infections of man. Bacteriol Rev 26:177–276

    PubMed  PubMed Central  CAS  Google Scholar 

  • Margolis L (1954) List of the parasites recorded from sea mammals caught off the west coast of north america. J Fish Res Board Can 11:267–283

    Article  Google Scholar 

  • Margolis L, Pike GC (1955) Some helminth parasites of Canadian pacific whales. J Fish Res Board Can 12:97–120

    Article  Google Scholar 

  • Marti H, Escher E (1990) Saf--an alternative fixation solution for parasitological stool specimens. Schweiz Med Wochenschr 120:1473–1476

    PubMed  CAS  Google Scholar 

  • Martinez-Aranguren RM, Gamboa PM, Garcia-Lirio E, Asturias J, Goikoetxea MJ, Sanz ML (2014) In vivo and in vitro testing with rani s 1 can facilitate diagnosis of anisakis simplex allergy. J Investig Allergol Clin Immunol 24:431–438

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 

  • 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  PubMed  CAS  Google Scholar 

  • McClane BA, Robertson SL, Li J (2013) Food microbiology: Fundamentals and frontiers

  • McClelland G (1980) Phocanema decipiens: pathology in seals. Exp Parasitol 49:405–419

    Article  PubMed  CAS  Google Scholar 

  • McDowall RM, Peregrine AS, Leonard EK, Lacombe C, Lake 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Medeiros AW, Giongo A, Valdez FP, Blaese de Amorin D, Tavares M, d’Azevedo PA, Franco AC, Frazzon J, Frazzon APG (2016) Characterization of the faecal bacterial community of wild young south american (arctocephalus australis) and subantarctic fur seals (arctocephalus tropicalis). FEMS Microbiol Ecol 92

  • Medema GJ, Bahar M, Schets FM (1997) Survival of cryptosporidium parvum, escherichia coli, faecal enterococci and clostridium perfringens in river water: influence of temperature and autochthonous microorganisms. Water Sci Technol 35:249–252

    Article  CAS  Google Scholar 

  • Mehlhorn H, Peter W (1983) Diagnose der parasiten des menschen einschießlich der therapie einheimischer und tropisch parasitosen. Gustav Fisher Verlag. In: Stuttgart

    Google Scholar 

  • Mehlhorn H, Piekarski G (1998) Grundiß der parasitenkunden. Parasiten des menschen und der nutztiere. Gustav FIsher Verlag, Stuttgart

  • Morris PJ, Johnson WR, Pisani J, Bossart GD, Adams J, Reif JS, Fair PA (2011) Isolation of culturable microorganisms from free-ranging bottlenose dolphins (tursiops truncatus) from the southeastern United States. Vet Microbiol 148:440–447

    Article  PubMed  Google Scholar 

  • Nachman S, Kaul A, Li KI, Slim MS, San Filippo JA, Van Horn K (1989) Liver abscess caused by clostridium bifermentans following blunt abdominal trauma. J Clin Microbiol 27:1137–1138

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nakauchi K (1999) The prevalence of balantidium coli infection in fifty-six mammalian species. J Vet Med Sci 61:63–65

    Article  PubMed  CAS  Google Scholar 

  • Nolan B, Leers WD, Schatzker J (1972) Septic arthritis of the knee due to clostridium bifermentans. Report of a case J Bone Joint Surg Am 54:1275–1278

    Article  PubMed  CAS  Google Scholar 

  • Nonnenmann MW, Bextine B, Dowd SE, Gilmore K, Levin JL (2010) Culture-independent characterization of bacteria and fungi in a poultry bioaerosol using pyrosequencing: a new approach. J Occup Environ Hyg 7:693–699

    Article  PubMed  CAS  Google Scholar 

  • Numberger D, Herlemann DP, Jurgens K, Dehnhardt G, Schulz-Vogt H (2016) Comparative analysis of the fecal bacterial community of five harbor seals (phoca vitulina). Microbiologyopen 5:782–792

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nunn GB (1992) Nematode molecular evolution : An investigation of evolutionary patterns among nematodes based upon DNA sequences

  • Olsen MA, Blix AS, Utsi TH, Sormo W, Mathiesen SD (2000) Chitinolytic bacteria in the minke whale forestomach. Can J Microbiol 46:85–94

    Article  PubMed  CAS  Google Scholar 

  • Ortega J, Daft B, Assis RA, Kinde H, Anthenill L, Odani J, Uzal FA (2007) Infection of internal umbilical remnant in foals by clostridium sordellii. Vet Pathol 44:269–275

    Article  PubMed  CAS  Google Scholar 

  • Owen CG, Kakulas BA (1968) Sarcosporidiosis in the sperm whale. Aust J Sci 31:46–47

  • Pencek TL, Burchiel KJ (1986) Delayed brain abscess related to a retained foreign body with culture of clostridium bifermentans. Case report J Neurosurg 64:813–815

    PubMed  CAS  Google Scholar 

  • Ponce-Gordo F, Fonseca-Salamanca F, Martinez-Diaz RA (2011) Genetic heterogeneity in internal transcribed spacer genes of balantidium coli (litostomatea, ciliophora). Protist 162:774–794

    Article  PubMed  CAS  Google Scholar 

  • Reboredo-Fernandez A, Ares-Mazas E, Martinez-Cedeira JA, Romero-Suances R, Caccio SM, Gomez-Couso H (2015) Giardia and cryptosporidium in cetaceans on the european Atlantic coast. Parasitol Res 114:693–698

    Article  PubMed  Google Scholar 

  • Reboredo-Fernandez A, Gomez-Couso H, Martinez-Cedeira JA, Caccio SM, Ares-Mazas E (2014) Detection and molecular characterization of giardia and cryptosporidium in common dolphins (delphinus delphis) stranded along the galician coast (Northwest Spain). Vet Parasitol 202:132–137

    Article  PubMed  CAS  Google Scholar 

  • Rechtman DJ, Nadler JP (1991) Abdominal abscess due to cardiobacterium hominis and clostridium bifermentans. Rev Infect Dis 13:418–419

    Article  PubMed  CAS  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:e1597

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanders JG, Beichman AC, Roman J, Scott JJ, Emerson D, McCarthy JJ, Girguis PR (2015) Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat Commun 6:8285

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scanlan DR, Smith MA, Isenberg HD, Engrassia S, Hilton E (1994) Clostridium bifermentans bacteremia with metastatic osteomyelitis. J Clin Microbiol 32:2867–2868

    PubMed  PubMed Central  CAS  Google Scholar 

  • Scharff RL (2012) Economic burden from health losses due to foodborne illness in the United States. J Food Prot 75:123–131

    Article  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  PubMed  PubMed Central  CAS  Google Scholar 

  • Shimamura Y, Ishii N, Ego M, Nakano K, Ikeya T, Nakamura K, Takagi K, Fukuda K, Fujita Y (2016) Multiple acute infection by anisakis: a case series. Intern Med 55:907–910

    Article  PubMed  Google Scholar 

  • Silva MA, Prieto R, Jonsen I, Baumgartner MF, Santos RS (2013) North Atlantic blue and fin whales suspend their spring migration to forage in middle latitudes: building up energy reserves for the journey? PLoS One 8:e76507

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Skrjabin AS (1966) A new crassicauda (crassicauda delamureana n. Sp.) -parasite of the sea whale. [in russ.]. V. Sb. Krayevaya parasitologiya i prirodna ochagovosty transmissiica bolyexnyey. Naukova dumka, Kiev

  • Smith L, Williams BL (1984) The pathogenic anaerobic bacteria. Thomas Publisher, Limited, Charles C

    Google Scholar 

  • Sohn WM, Na BK, Kim TH, Park TJ (2015) Anisakiasis: report of 15 gastric cases caused by anisakis type i larvae and a brief review of korean anisakiasis cases. Korean J Parasitol 53:465–470

    Article  PubMed  PubMed Central  Google Scholar 

  • Soper DE (1986) Clostridial myonecrosis arising from an episiotomy. Obstet Gynecol 68:26S–28S

    PubMed  CAS  Google Scholar 

  • Stevens DL, Aldape MJ, Bryant AE (2012) Life-threatening clostridial infections. Anaerobe 18:254–259

    Article  PubMed  Google Scholar 

  • 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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Bonn WG (1995) Captive cetaceans. J Am Vet Med Assoc 206:155–156

    PubMed  Google Scholar 

  • Van der Auwera G, Chapelle S, De Wachter R (1994) Structure of the large ribosomal subunit rna of phytophthora megasperma, and phylogeny of the oomycetes. FEBS Lett 338:133–136

    Article  PubMed  Google Scholar 

  • VanWormer E, Fritz H, Shapiro K, Mazet JAK (2013) Molecules to modeling: Toxoplasma gondii oocysts at the human-animal-environment interface. Comp Immunol Microbiol Infect Dis 36:217–231

    Article  PubMed  Google Scholar 

  • Villagra-Blanco R, Silva LMR, Aguilella-Segura A, Arcenillas-Hernández I, Martínez-Carrasco C, Seipp A, Gärtner U, Ruiz de Ybañez R, Taubert A, Hermosilla C (2017) Bottlenose dolphins (tursiops truncatus) do also cast neutrophil extracellular traps against the apicomplexan parasite neospora caninum. Int J Parasitol Parasites Wildl 6:287–294

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waeschenbach A, Brabec J, Scholz T, Littlewood DTJ, Kuchta R (2017) The catholic taste of broad tapeworms - multiple routes to human infection. Int J Parasitol 47:831–843

    Article  PubMed  CAS  Google Scholar 

  • Waeschenbach A, Webster BL, Bray RA, Littlewood DT (2007) Added resolution among ordinal level relationships of tapeworms (platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal rna genes. Mol Phylogenet Evol 45:311–325

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

    PubMed  CAS  Google Scholar 

  • Young PC, Lowe D (1969) Larval nematodes from fish of the subfamily anisakinae and gastro-intestinal lesions in mammals. J Comp Pathol 79:301–313

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are deeply thankful to all international volunteers who participated in sperm whale scat collection during Tursiops Association summer expedition of 2016 in Spain. Furthermore, we would like to acknowledge Birgit Reinhardt, Agnes Mohr and Christine Henrich (Institute of Parasitology, Justus Liebig University Giessen, Germany) for their excellent technical support in parasitological-related investigations as well as molecular analyses of sperm whale samples.

Author information

Authors and Affiliations

  1. Institute of Parasitology, Biomedical Research Centre Seltersberg (BFS), Justus Liebig University Giessen, Schubertstr. 81, 35392, Giessen, Germany

    Carlos Hermosilla, J. Hirzmann, L. M. R. Silva & A. Taubert

  2. Tursiops Association, Palma de Mallorca, Spain

    J. M. Brotons & M. Cerdà

  3. Institute for Hygiene and Infectious Diseases of Animals, Justus Liebig University Giessen, Giessen, Germany

    E. Prenger-Berninghoff & C. Ewers

Authors
  1. Carlos Hermosilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Hirzmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. M. R. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. Brotons
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Cerdà
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. Prenger-Berninghoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. Ewers
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. Taubert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carlos Hermosilla.

Ethics declarations

All sperm whale sampling procedures were conducted in accordance with Institutional Ethic Commission of Tursiops Association (Spain) and to Justus Liebig University Giessen (Germany), and in accordance with current European Animal Welfare Legislation: ART13TFEU.

Conflict of interests

The authors declare that they have no conflicts of interest.

Additional information

Section Editor: Shokoofeh Shamsi

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hermosilla, C., Hirzmann, J., Silva, L.M.R. et al. Occurrence of anthropozoonotic parasitic infections and faecal microbes in free-ranging sperm whales (Physeter macrocephalus) from the Mediterranean Sea. Parasitol Res 117, 2531–2541 (2018). https://doi.org/10.1007/s00436-018-5942-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-5942-3

Keywords

Search

Navigation