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Parasitology Research

, Volume 115, Issue 2, pp 889–896 | Cite as

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

  • Carlos Hermosilla
  • Liliana M. R. Silva
  • Sonja Kleinertz
  • Rui Prieto
  • Monica A. Silva
  • Anja Taubert
Short Communication

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.

Keywords

Balaenoptera musculus B. borealis B. physalus Physeter macrocephalus Parasites Giardia Balantidium 

Notes

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).

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. Anderson RC (1992) Nematode parasites of vertebrates: their development and transmission. CABI Pub, CambridgeGoogle Scholar
  4. 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 61:55–61PubMedGoogle Scholar
  5. 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 323-333Google Scholar
  6. Baylis HA (1932) A list of worms parasitic in Cetacea. Discovery Reports 6:26Google Scholar
  7. 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 CrossRefPubMedGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 CrossRefPubMedGoogle Scholar
  10. 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 CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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
  13. Dailey MD, Walker WA (1978) Parasitism as a factor (?) in single strandings of southern California cetaceans. J Parasitol 64:593–596CrossRefPubMedGoogle Scholar
  14. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  15. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  16. Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Izdatel’stvo Akiademii Nauk SSSR, MoscowGoogle Scholar
  17. 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 CrossRefPubMedGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. Eckert J, Friedhof KT, Zahner H, Desplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin. Enke Verlag, StuttgartCrossRefGoogle Scholar
  20. Eichinger D (1997) Encystation of entamoeba parasites. Bioessays 19:633–639. doi: 10.1002/bies.950190714 CrossRefPubMedGoogle Scholar
  21. 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: 1-59Google Scholar
  22. Fleischman RW, Squire RA (1970) Verminous pneumonia in the California sea lion (Zalophus californianus). Pathol Vet 7:89–101CrossRefPubMedGoogle Scholar
  23. Fujii K et al (2007) Seroepidemiology of Toxoplasma gondii and Neospora caninum in seals around Hokkaido, Japan. J Vet Med Sci 69:393–398CrossRefPubMedGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. Geraci JR, St Aubin DJ (1987) Effects of parasites on marine mammals. Int J Parasitol 17:407–414CrossRefPubMedGoogle Scholar
  26. Golvan YJ (1959) A canthocephala of the genus Corynosoma Luhe 1904, mammalian parasites from Alaska & Midway. Ann Parasit Hum Comp 34:288–321Google Scholar
  27. Gubanov NM (1951) Giant nematoda from the placenta of Cetacea; Placentonema gigantissima nov. gen., nov. sp. Dokl Akad Nauk SSSR+ 77:1123-1125Google Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 134Google Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. 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 CrossRefPubMedGoogle Scholar
  35. 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 CrossRefPubMedGoogle Scholar
  36. 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 49:289–292CrossRefPubMedGoogle Scholar
  37. 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 71:485–488CrossRefPubMedGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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 24:431–438PubMedGoogle Scholar
  40. 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 CrossRefPubMedGoogle Scholar
  41. Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13:99–113CrossRefPubMedGoogle Scholar
  42. 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 PubMedCentralCrossRefPubMedGoogle Scholar
  43. McClelland G (1980) Phocanema decipiens: pathology in seals. Exp Parasitol 49:405–419CrossRefPubMedGoogle Scholar
  44. Mehlhorn H, Peter W (1983) Diagnose der Parasiten des Menschen einschießlich der Therapie einheimischer und tropisch Parasitosen. Gustav Fisher Verlag, StuttgartGoogle Scholar
  45. Mehlhorn H, Piekarski G (1998) Grundiß der Parasitenkunden. Parasiten des Menschen und der Nutztiere. Gustav FIsher Verlag, StuttgartGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. 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 CrossRefPubMedGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. Pompa S, Ehrlich PR, Ceballos G (2011) Global distribution and conservation of marine mammals. PNAS 108:13600–13605. doi: 10.1073/pnas.1101525108 PubMedCentralCrossRefPubMedGoogle Scholar
  50. 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 CrossRefPubMedGoogle Scholar
  51. Prester L (2015) Seafood allergy, toxicity, and intolerance: a review. J Am Coll Nutr:1-13. doi: 10.1080/07315724.2015.1014120
  52. Raga JA, Balbuena JA, Aznar J, Fernandez M (1997) The impact of parasites on marine mammals: a review. Parassitologia 39:293–296PubMedGoogle Scholar
  53. 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 821–830Google Scholar
  54. 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 CrossRefPubMedGoogle Scholar
  55. 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 CrossRefPubMedGoogle Scholar
  56. Ridgway SH (1972) Cerebral and cerebellar involvement of trematode parasites in dolphins and their possible role in stranding. J Wildlife Dis 8:33–43CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. Schuster FL, Ramirez-Avila L (2008) Current world status of Balantidium coli. Clin Microbiology Rev 21:626–638. doi: 10.1128/cmr.00021-08 CrossRefGoogle Scholar
  59. Skappak C et al (2014) Invasive amoebiasis: a review of Entamoeba infections highlighted with case reports. Can J Gastroenterol Hepatol 28:355–359PubMedCentralPubMedGoogle Scholar
  60. 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, KievGoogle Scholar
  61. Stanley SL Jr (2003) Amoebiasis. Lancet 361:1025–1034. doi: 10.1016/s0140-6736(03)12830-9 CrossRefPubMedGoogle Scholar
  62. 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 CrossRefPubMedGoogle Scholar
  63. 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 69:205–208CrossRefPubMedGoogle Scholar
  64. 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 CrossRefPubMedGoogle Scholar
  65. 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 CrossRefPubMedGoogle Scholar
  66. Vazquezdelara-Cisneros LG, Arroyo-Begovich A (1984) Induction of encystation of Entamoeba invadens by removal of glucose from the culture medium. J Parasitol 70:629–633CrossRefPubMedGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. Woodard JC, Zam SG, Caldwell DK, Caldwell MC (1969) Some parasitic diseases of dolphins. Pathol Vet 6:257–272CrossRefPubMedGoogle Scholar
  69. 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
  70. Young PC, Lowe D (1969) Larval nematodes from fish of the subfamily Anisakinae and gastro-intestinal lesions in mammals. J Comp Pathol 79:301–313CrossRefPubMedGoogle Scholar
  71. 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 10:852–853PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Carlos Hermosilla
    • 1
  • Liliana M. R. Silva
    • 1
  • Sonja Kleinertz
    • 2
  • Rui Prieto
    • 3
  • Monica A. Silva
    • 3
    • 4
  • Anja Taubert
    • 1
  1. 1.Institute of Parasitology, Biomedical Research Center SeltersbergJustus Liebig University GiessenGiessenGermany
  2. 2.Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental SciencesUniversity of RostockRostockGermany
  3. 3.MARE—Marine and Environmental Sciences Centre and IMAR—Institute of Marine ResearchUniversity of the AzoresHortaPortugal
  4. 4.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA

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