Skip to main content
SpringerLink
Log in

Endoparasite survey of free-swimming baleen whales (Balaenoptera musculus, B. physalus, B. borealis) and sperm whales (Physeter macrocephalus) using non/minimally invasive methods

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A number of parasitic diseases have gained importance as neozoan opportunistic infections in the marine environment. Here, we report on the gastrointestinal endoparasite fauna of three baleen whale species and one toothed whale: blue (Balaenoptera musculus), fin (Balaenoptera physalus), and sei whales (Balaenoptera borealis) and sperm whales (Physeter macrocephalus) from the Azores Islands, Portugal. In total, 17 individual whale fecal samples [n = 10 (B. physalus); n = 4 (P. macrocephalus); n = 2 (B. musculus); n = 1 (B. borealis)] were collected from free-swimming animals as part of ongoing studies on behavioral ecology. Furthermore, skin biopsies were collected from sperm whales (n = 5) using minimally invasive biopsy darting and tested for the presence of Toxoplasma gondii, Neospora caninum, and Besnoitia besnoiti DNA via PCR. Overall, more than ten taxa were detected in whale fecal samples. Within protozoan parasites, Entamoeba spp. occurred most frequently (64.7 %), followed by Giardia spp. (17.6 %) and Balantidium spp. (5.9 %). The most prevalent metazoan parasites were Ascaridida indet. spp. (41.2 %), followed by trematodes (17.7 %), acanthocephalan spp., strongyles (11.8 %), Diphyllobotrium spp. (5.9 %), and spirurids (5.9 %). Helminths were mainly found in sperm whales, while enteric protozoan parasites were exclusively detected in baleen whales, which might be related to dietary differences. No T. gondii, N. caninum, or B. besnoiti DNA was detected in any skin sample. This is the first record on Giardia and Balantidium infections in large baleen whales.

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

References

  • 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. doi:10.1007/BF00017666

    Article  Google Scholar 

  • Akao S (1970) A new species of sarcocystis parasitic in the whale balaenoptera borealis. J Protozool 17:290–294. doi:10.1111/j.1550-7408.1970.tb02372.x

    Article  Google Scholar 

  • Anderson RC (1992) Nematode parasites of vertebrates: their development and transmission. CABI Pub, Cambridge

    Google Scholar 

  • Andrade AL, Pinedo MC, Barreto AS (2001) Gastrointestinal parasites and prey items from a mass stranding of false killer whales, Pseudorca crassidens, in Rio Grande do Sul, Southern Brazil. Braz J Biol 61:55–61

    CAS  PubMed  Google Scholar 

  • Arundel JH (1978) Parasites and parasitic diseases of Australian marina mammals. In: House L (ed) The University of Sidney, Post-Graduate Committee in Veterinary Science, Proceedings No. 36 of Course for Veterinarians, Sidney, Australia, pp 323-333

  • Baylis HA (1932) A list of worms parasitic in Cetacea. Discovery Reports 6:26

    Google Scholar 

  • Bogomolni AL et al (2008) Victims or vectors: a survey of marine vertebrate zoonoses from coastal waters of the Northwest Atlantic. Dis Aquat Organ 81(1):13–38. doi:10.3354/dao01936

    Article  PubMed  Google Scholar 

  • Cabezón O, Hall AJ, Vincent C, Pabon M, Garcia-Bocanegra I, Dubey JP, Almeria S (2011) Seroprevalence of toxoplasma gondii in north-eastern atlantic harbor seal (Phoca vitulina vitulina) and grey seal (Halichoerus grypus). Vet Parasitol 179:253–256. doi:10.1016/j.vetpar.2011.01.046

    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. doi:10.1007/s00436-010-2226-y

    Article  PubMed  Google Scholar 

  • Colon-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. doi:10.1007/s00436-009-1544-4

    Article  PubMed  Google Scholar 

  • Conrad PA et al (2005) Transmission of toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int J Parasitol 35:1155–1168. doi:10.1016/j.ijpara.2005.07.002

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

    Article  CAS  PubMed  Google Scholar 

  • Davidson AD et al (2012) Drivers and hotspots of extinction risk in marine mammals. Proc Natl Acad Sci U S A 109:3395–3400. doi:10.1073/pnas.1121469109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Cadiz AE, Jeelani G, Nakada-Tsukui K, Caler E, Nozaki T (2013) Transcriptome analysis of encystation in Entamoeba invadens. PLoS One 8:e74840. doi:10.1371/journal.pone.0074840

    Article  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Doney SC et al (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37. doi:10.1146/annurev-marine-041911-111611

    Article  PubMed  Google Scholar 

  • Dubey JP et al (2008) Isolation of Toxoplasma gondii from bottlenose dolphins (Tursiops truncatus). J Parasitol 94:821–823. doi:10.1645/ge-1444.1

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

  • Eichinger D (1997) Encystation of entamoeba parasites. Bioessays 19:633–639. doi:10.1002/bies.950190714

    Article  CAS  PubMed  Google Scholar 

  • Fiscus CH, Baines GA, Wilke F (1962) Pelagic fur seal investigations, Alaska waters. U.S. Fish and Wildlife Services, Special Scientific Report on Fish 475: 1-59

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

    Article  CAS  PubMed  Google Scholar 

  • Fujii K et al (2007) Seroepidemiology of Toxoplasma gondii and Neospora caninum in seals around Hokkaido, Japan. J Vet Med Sci 69:393–398

    Article  PubMed  Google Scholar 

  • Gannon WL, Sikes RS, Comm ACU (2007) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 88:809–823. doi:10.1644/06-mamm-f-185r1.1

    Article  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 

  • Golvan YJ (1959) A canthocephala of the genus Corynosoma Luhe 1904, mammalian parasites from Alaska & Midway. Ann Parasit Hum Comp 34:288–321

    CAS  Google Scholar 

  • Gubanov NM (1951) Giant nematoda from the placenta of Cetacea; Placentonema gigantissima nov. gen., nov. sp. Dokl Akad Nauk SSSR+ 77:1123-1125

  • Hassell JM et al (2013) Occurrence and molecular analysis of Balantidium coli in mountain gorilla (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. J Wildlife Dis 49:1063–1065. doi:10.7589/2013-02-041

    Article  Google Scholar 

  • Hermosilla C, Navarro M, Taubert A (2013) Gastrointestinal endoparasite fauna of ‘urban’ sea lions (Otaria flavenscens) in Valdivia, Chile (in German). In: DVG (ed) Tagung der DVG-Fachgruppe “Parasitologie und Parasitäre Krankheiten”, Giessen, Germany. p 134

  • 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. doi:10.1645/ge-545r.1

    Article  CAS  PubMed  Google Scholar 

  • Hunt KE et al. (2013) Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conserv Physiol 1. doi:10.1093/conphys/cot006

  • Kleinertz S, Klimpel S, Palm HW (2012) Parasite communities and feeding ecology of the European sprat (Sprattus sprattus L.) over its range of distribution. Parasitol Res 110:1147–1157. doi:10.1007/s00436-011-2605-z

    Article  PubMed  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. doi:10.1007/s00436-014-4085-4

    Article  CAS  PubMed  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. doi:10.1007/s00436-014-3781-4

    Article  CAS  PubMed  Google Scholar 

  • Klimpel S, Palm HW, Ruckert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9. doi:10.1007/s00436-004-1154-0

    Article  PubMed  Google Scholar 

  • 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 

  • Lambertsen RH (1985) Taxonomy and distribution of a Crassicauda species (Nematoda: Spirurida) infecting the kidney of the common fin whale (Balaenoptera physalus Linne, 1758). J Parasitol 71:485–488

    Article  CAS  PubMed  Google Scholar 

  • Marietto-Goncalves GA, Fernandes TM, Silva RJ, Lopes RS, Andreatti Filho RL (2008) Intestinal protozoan parasites with zoonotic potential in birds. Parasitol Res 103:1237–1240. doi:10.1007/s00436-008-1125-y

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Matsubayashi M, Kanamori K, Sadahiro M, Tokoro M, Abe N, Haritani M, Shibahara T (2015) First molecular identification of Entamoeba polecki in a piglet in Japan and implications for aggravation of ileitis by coinfection with Lawsonia intracellularis. Parasitol Res 114:3069–3073. doi:10.1007/s00436-015-4509-9

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Mazzariol S et al (2012) Dolphin morbillivirus and Toxoplasma gondii coinfection in a mediterranean fin whale (Balaenoptera physalus). BMC Vet Res 8:20. doi:10.1186/1746-6148-8-20

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mehlhorn H, Peter W (1983) Diagnose der Parasiten des Menschen einschießlich der Therapie einheimischer und tropisch Parasitosen. Gustav Fisher Verlag, Stuttgart

    Google Scholar 

  • Mehlhorn H, Piekarski G (1998) Grundiß der Parasitenkunden. Parasiten des Menschen und der Nutztiere. Gustav FIsher Verlag, Stuttgart

    Google Scholar 

  • Miller MA et al (2008) Type x Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal california: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. Int J Parasitol 38:1319–1328. doi:10.1016/j.ijpara.2008.02.005

    Article  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. doi:10.1645/ge-522r.1

    Article  CAS  PubMed  Google Scholar 

  • Ojha S, Ahamad J, Bhattacharya A, Bhattacharya S (2014) Ribosomal RNA and protein transcripts persist in the cysts of Entamoeba invadens. Mol Biochem Parasit 195:6–9. doi:10.1016/j.molbiopara.2014.05.003

    Article  CAS  Google Scholar 

  • Pompa S, Ehrlich PR, Ceballos G (2011) Global distribution and conservation of marine mammals. PNAS 108:13600–13605. doi:10.1073/pnas.1101525108

    Article  PubMed Central  CAS  PubMed  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. doi:10.1016/j.protis.2011.06.008

    Article  CAS  PubMed  Google Scholar 

  • Prester L (2015) Seafood allergy, toxicity, and intolerance: a review. J Am Coll Nutr:1-13. doi:10.1080/07315724.2015.1014120

  • Raga JA, Balbuena JA, Aznar J, Fernandez M (1997) The impact of parasites on marine mammals: a review. Parassitologia 39:293–296

    CAS  PubMed  Google Scholar 

  • Raga JA, Fernandez M, Balbuena JA, Aznar FJ (2008) Parasites. In: Perrin WF, Thewissen HGM, Würsing B (eds) Encyclopedia of Marine Mammals, 2nd edn. Academic Press Elsevier Inc., San Diego, pp 821–830

    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. doi:10.1016/j.vetpar.2014.03.018

    Article  CAS  PubMed  Google Scholar 

  • Reichel M et al (2015) Harbour seal (Phoca vitulina) PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gondii. Dev Comp Immunol 50:106–115. doi:10.1016/j.dci.2015.02.002

    Article  CAS  PubMed  Google Scholar 

  • Ridgway SH (1972) Cerebral and cerebellar involvement of trematode parasites in dolphins and their possible role in stranding. J Wildlife Dis 8:33–43

    Article  CAS  Google Scholar 

  • Salles JM, Salles MJ, Moraes LA, Silva MC (2007) Invasive amebiasis: an update on diagnosis and management. Expert Rev Anti-infe 5:893–901. doi:10.1586/14787210.5.5.893

    Article  CAS  Google Scholar 

  • Schuster FL, Ramirez-Avila L (2008) Current world status of Balantidium coli. Clin Microbiology Rev 21:626–638. doi:10.1128/cmr.00021-08

    Article  Google Scholar 

  • Skappak C et al (2014) Invasive amoebiasis: a review of Entamoeba infections highlighted with case reports. Can J Gastroenterol Hepatol 28:355–359

    PubMed Central  PubMed  Google Scholar 

  • Skriabin 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

  • Stanley SL Jr (2003) Amoebiasis. Lancet 361:1025–1034. doi:10.1016/s0140-6736(03)12830-9

    Article  CAS  PubMed  Google Scholar 

  • Stensvold CR et al (2011) Increased sampling reveals novel lineages of Entamoeba: consequences of genetic diversity and host specificity for taxonomy and molecular detection. Protist 162:525–541. doi:10.1016/j.protis.2010.11.002

    Article  PubMed  Google Scholar 

  • Tada I, Otsuji Y, Kamiya H, Mimori T, Sakaguchi Y, Makizumi S (1983) The first case of a human infected with an acanthocephalan parasite, Bolbosoma sp. J Parasitol 69:205–208

    Article  CAS  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. doi:10.1016/j.tvjl.2007.09.022

    Article  PubMed  Google Scholar 

  • Van Bressem MF et al (2009) Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Organ 86:143–157. doi:10.3354/dao02101

    Article  PubMed  Google Scholar 

  • Vazquezdelara-Cisneros LG, Arroyo-Begovich A (1984) Induction of encystation of Entamoeba invadens by removal of glucose from the culture medium. J Parasitol 70:629–633

    Article  CAS  PubMed  Google Scholar 

  • Walton MJ, Silva MA, Magalhaes SM, Prieto R, Santos RS (2008) Fatty acid characterization of lipid fractions from blubber biopsies of sperm whales Physeter macrocephalus located around the Azores. J Mar Biol Assoc UK 88:1109–1115. doi:10.1017/s0025315408000775

    Article  Google Scholar 

  • Woodard JC, Zam SG, Caldwell DK, Caldwell MC (1969) Some parasitic diseases 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 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  CAS  PubMed  Google Scholar 

  • Young KH, Bullock SL, Melvin DM, Spruill CL (1979) Ethyl acetate as a substitute for diethyl ether in the formalin-ether sedimentation technique. J Clin Microbiol 10:852–853

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are deeply thankful to those who contributed to the whale images included in this work: Claudia Oliveira (Fig. 1a) and N. Liebsich (Fig. 1b, c), and Christine Henrich for her molecular work. We further acknowledge funds and support from the Portuguese Fundação para a Ciência e a Tecnologia (FCT), Fundo Regional da Ciência e Tecnologia (FRCT), through research projects TRACE-PTDC/MAR/74071/2006 and MAPCET-M2.1.2/F/012/2011 [FEDER, the Competitiveness Factors Operational (COMPETE), QREN European Social Fund, and Proconvergencia Açores/EU Program]. We furthermore acknowledge funds provided by FCT to MARE and by the FRCT—Government of the Azores pluri-annual funding. RP is supported by a research grant from the Azores Regional Fund for Science and Technology (M3.1.5/F/115/2012). MAS is supported by FCT through a Program Investigator FCT fellowship (IF/00943/2013).

Author information

Authors and Affiliations

  1. Institute of Parasitology, Biomedical Research Center Seltersberg, Justus Liebig University Giessen, Schubertstr. 81, 35392, Giessen, Germany

    Carlos Hermosilla, Liliana M. R. Silva & Anja Taubert

  2. Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, 18059, Rostock, Germany

    Sonja Kleinertz

  3. MARE—Marine and Environmental Sciences Centre and IMAR—Institute of Marine Research, University of the Azores, 9901-862, Horta, Portugal

    Rui Prieto & Monica A. Silva

  4. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA

    Monica A. Silva

Authors
  1. Carlos Hermosilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liliana M. R. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonja Kleinertz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rui Prieto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Monica A. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anja Taubert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carlos Hermosilla.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hermosilla, C., Silva, L.M.R., Kleinertz, S. et al. 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 (2016). https://doi.org/10.1007/s00436-015-4835-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4835-y

Keywords

Search

Navigation