Species of Angiostrongylus (Nematoda: Metastrongyloidea) in Wildlife: a Review David M
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International Journal for Parasitology: Parasites and Wildlife 4 (2015) 178–189 Contents lists available at ScienceDirect International Journal for Parasitology: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Invited Review Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: A review David M. Spratt * Australian National Wildlife Collection, CSIRO National Research Collections, GPO Box 1700, Canberra, ACT 2601, Australia ARTICLE INFO ABSTRACT Article history: Twenty-one species of Angiostrongylus plus Angiostrongylus sp. (Nematoda: Metastrongyloidea) are known Received 15 January 2015 currently in wildlife. These occur naturally in rodents, tupaiids, mephitids, mustelids, procyonids, felids, Revised 16 February 2015 and canids, and aberrantly in a range of avian, marsupial and eutherian hosts including humans. Adults Accepted 20 February 2015 inhabit the pulmonary arteries and right atrium, ventricle and vena cava, bronchioles of the lung or ar- teries of the caecum and mesentery. All species pass first-stage larvae in the faeces of the host and all Keywords: utilise slugs and/or aquatic or terrestrial snails as intermediate hosts. Gastropods are infected by inges- Angiostrongylus spp tion or penetration of first-stage larvae; definitive hosts by ingestion of gastropods or gastropod slime. Wildlife Life cycles Transmission of at least one species may involve ingestion of paratenic hosts. Five developmental path- Geographical distribution ways are identified in these life cycles. Thirteen species, including Angiostrongylus sp., are known primarily Pathology from the original descriptions suggesting limited geographic distributions. The remaining species are wide- Zoonoses spread either globally or regionally, and are continuing to spread. Small experimental doses of infective larvae (ca. 20) given to normal or aberrant hosts are tolerated, although generally eliciting a granulo- matous histopathological response; large doses (100–500 larvae) often result in clinical signs and/or death. Two species, A. cantonensis and A. costaricensis, are established zoonoses causing neurological and ab- dominal angiostrongliasis respectively. The zoonotic potential of A. mackerrasae, A. malaysiensis and A. siamensis particularly warrant investigation. Angiostrongylus cantonensis occurs in domestic animals, mam- malian and avian wildlife and humans in the metropolitan areas of Brisbane and Sydney, Australia, where it has been suggested that tawny frogmouths and brushtail possums may serve as biosentinels. A major conservation issue is the devastating role A. cantonensis may play around zoos and fauna parks where captive rearing of endangered species programmes may exist and where Rattus spp. are invariably a problem. Crown Copyright © 2015 Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc- nd/4.0/). Contents 1. Introduction ........................................................................................................................................................................................................................................................ 179 2. Taxonomy ............................................................................................................................................................................................................................................................. 179 3. Host and geographic distribution of species occurring in wildlife .................................................................................................................................................. 180 4. Life cycles ............................................................................................................................................................................................................................................................. 181 4.1. Type I ....................................................................................................................................................................................................................................................... 182 4.2. Type II ..................................................................................................................................................................................................................................................... 182 4.3. Type III .................................................................................................................................................................................................................................................... 183 4.4. Type IV .................................................................................................................................................................................................................................................... 183 4.5. Type V ..................................................................................................................................................................................................................................................... 183 5. Geographic distribution and epidemiology ............................................................................................................................................................................................. 184 6. Impacts on hosts – pathology and pathogenesis ................................................................................................................................................................................... 184 7. Biodiversity and conservation issues ......................................................................................................................................................................................................... 185 8. Species in need of further investigation ................................................................................................................................................................................................... 185 9. Conclusions ......................................................................................................................................................................................................................................................... 186 * Australian National Wildlife Collection, CSIRO National Research Collections, GPO Box 1700, Canberra, ACT 2601, Australia. Tel.: +61 2 62421648; fax: +61 2 6242 1688. E-mail address: [email protected]. http://dx.doi.org/10.1016/j.ijppaw.2015.02.006 2213-2244/Crown Copyright © 2015 Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). D.M. Spratt/International Journal for Parasitology: Parasites and Wildlife 4 (2015) 178–189 179 Acknowledgements .......................................................................................................................................................................................................................................... 186 References ............................................................................................................................................................................................................................................................ 186 1. Introduction Ubelaker (1986) retained the genus Angiocaulus with type species A. gubernaculatus and placed Cardionema ten Yamaguti, 1941 from The parasitic nematode genus Angiostrongylus Kamensky, 1905 Martes malampus in Japan in Angiocaulus, while recognising its close belongs to the superfamily Metastrongyloidea, the so-called “lung- relationship with Parastrongylus. I follow Chabaud (1965), Dróz´dz´ worms” of vertebrates. Species occur naturally in cricetid, (1970) and Anderson (1978) in recognising Angiocaulus as a synonym heteromyid, soricid, glirid, sciurid and murid rodents, tupaiids, of Angiostrongylus and thus recognise Angiostrongylus gubernaculatus. mephitids, mustelids, procyonids, felids, canids and aberrantly in Given the importance of the male bursa in defining genera in the a range of avian, marsupial and eutherian hosts including humans. Angiostrongylidae, I follow Yamaguti (1961) and recognise the Some species inhabit the pulmonary arteries and right ventricle, species A. ten as incerta sedis, given it is based on female speci- some develop in the brain and then migrate via the venous system mens only. to the heart and pulmonary arteries, some occur in mesenteric veins Yanchev and Genov (1988) described Angiostrongylus daskalovi and others occur in the bronchioles of the lung. Regardless of site from three mustelid species in Bulgaria incorrectly placing it in the in the definitive host, all first-stage larvae pass through the gas- Filaroididae rather than Angiostrongylidae and distinguishing it from trointestinal tract and exit with the faeces. All species in which the A. chabaudi, A. gubernaculatus and A. vasorum. Subsequently, several life cycle is known utilise gastropods (slugs and terrestrial and aquatic new species of Angiostrongylus have been reported from members snails) as intermediate hosts and some species may also use paratenic of the genus Akodon (Cricetidae)