Abstract
The acanthocephalan parasite Plagiorhynchus cylindraceus has a global distribution and utilizes isopods and birds as intermediate and definitive hosts, respectively. Occasionally, mammals of various orders can act as paratenic hosts. In hedgehogs, severe cases have been reported in juvenile specimens due to secondary infections, as a consequence of complete penetrations of the intestinal wall by cystacanths. In a 66-month study period, we found seven larvae of this parasite encysted in both, the peritoneal cavity and intestine of the Algerian hedgehog, Atelerix algirus in Majorca. Morphology alone was insufficient to identify the species, due to the lack of previous reports and taxonomy-informative characters. In the present report, we combined the use of morphology and the DNA-barcoding approach to confirm to identify cystacanths as P. cylindraceus. This is the first report of this parasite in this hedgehog species. The epidemiological implications will be discussed, including the risk of zoonosis and the importance of using modern approaches to identify immature acanthocephalan larvae in wildlife hosts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alcantar-Escalera FJ, Garcia-Varela M, Vazquez-Dominguez E, de Leon GPP (2013) Using DNA barcoding to link cystacanths and adults of the acanthocephalan Polymorphus brevis in central Mexico. Mol Ecol Resour 13:1116–1124
Alcover JA (2007) Atelerix algirus (Lereboullet, 1842). In: Palomo GJ, L.J, Blanco JC (eds) Atlas y libro rojo de los mamíferos terrestres de España. Dirección General de Conservación de la Naturaleza-SECEM-SECEMU, Madrid, pp 83–85
Amin OM, Canaris AG, Kinsella JM (1999) A taxonomic reconsideration of the genus Plagiorhynchus s. lat. (Acanthocephala : Plagiorhynchidae), with descriptions of South African Plagiorhynchus (Prosthorhynchus) cylindraceus from shore birds and P. (P.) malayensis, and a key to the species of the subgenus Prosthorhynchus. J Helminthol Soc Wash 66:123–132
Behr M (2005) Hedgehog zoonoses. Emerg Infect Dis 11:1146–1146
Ching HL, Leighton BJ, Stephen C (2000) Intestinal parasites of raccoons (Procyon lotor) from southwest British Columbia. Canadian Journal of Veterinary Research-Revue Canadienne De Recherche Veterinaire 64:107–111
Coady NR, Nickol BB (2000) Assessment of parenteral Plagiorhynchus cylindraceus (Acanthocephala) infections in shrews. Comp Parasitol 67:32–39
Cousquer G (2004) Analysis of tracheal sputum for diagnosing and monitoring verminous pneumonia in hedgehogs (Erinaceus europaeus). Vet Rec 154:332–333
Edmonds SJ (1989) A list of Australian Acanthocephala and their hosts. Records of the South Australian Museum 23:127–133
Falla AC, Brieva C, Bloor P (2015) Mitochondrial DNA diversity in the acanthocephalan Prosthenorchis elegans in Colombia based on cytochrome c oxidase I (COI) gene sequence. International Journal for Parasitology-Parasites and Wildlife 4:401–407
Ferrer D, Molina R, Castella J, Kinsella JM (2004) Parasitic helminths in the digestive tract of six species of owls (Strigiformes) in Spain. Vet J 167:181–185
Florescu BI (1984) Survey of Acanthocephala in Romania. Travaux du Muséum d’Histoire Naturelle Grigore Antipa 25:7–45
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial Cytochrome c Oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Garcia-Varela M, de Leon GPP (2008) Validating the systematic position of Profilicollis meyer, 1931 and Hexaglandula petrochenko, 1950 (Acanthocephala : Polymorphidae) using Cytochrome C oxidase (COX 1). J Parasitol 94:212–217
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hebert PDN, Ratnasingham S, deWaard JR (2003a) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc London Ser B-Biol Sci 270:S96–S99
Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003b) Biological identifications through DNA barcodes. Proc R Soc B-Biol Sci 270:313–321
Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci U S A 101:14812–14817
Khaldi M, Torres J, Samso B, Miquel J, Biche M, Benyettou M, Barech G, Benelkadi HA, Ribas A (2012) Endoparasites (helminths and coccidians) in the hedgehogs Atelerix algirus and Paraechinus aethiopicus from Algeria. Afr Zool 47:48–54
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948
Lisitsyna O (2010) Morphological variability of Plagiorhynchus (Prosthorhynchus) cylindraceus (Acanthocephala, Plagiorhynchidae) and its importance in assessment of taxonomy structure of the subgenus. Vestnik zoologii 44:e-35–e-44
Morales A, Rofes J (2008) Early evidence for the Algerian hedgehog in Europe. J Zool 274:9–12
Pfaffle M, Bolfikova BC, Hulva P, Petney T (2014) Different parasite faunas in sympatric populations of sister hedgehog species in a secondary contact zone. PLoS One 9:e114030
Salehabadi A, Mowlavi G, Sadjjadi SM (2008) Human infection with Moniliformis moniliformis (Bremser 1811) (Travassos 1915) in Iran: another case report after three decades. Vector-Borne and Zoonotic Diseases 8:101–103
Schmidt GD, Olsen OW (1964) Life cycle and development of Prosthorhynchus formosus (Van Cleave, 1918) Travassos, 1926, an acanthocephalan parasite of birds. J Parasitol 50:721–730
Skuballa J, Taraschewski H, Petney TN, Pfaffle M, Smales LR (2010) The avian acanthocephalan Plagiorhynchus cylindraceus (Palaeacanthocephala) parasitizing the European hedgehog (Erinaceus europaeus) in Europe and New Zealand. Parasitol Res 106:431–437
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Taraschewski H (2000) Host-parasite interactions in Acanthocephala: a morphological approach, pp. 1-179. In J. R. Baker, R. Muller and D. Rollinson (eds.), Adv Parasitol, Vol 46
Waindok P, Lehnert K, Siebert U, Pawliczka I, Strube C (2018) Prevalence and molecular characterisation of Acanthocephala in pinnipedia of the North and Baltic Seas. Int J Parasitol-Parasites Wildl 7:34–43
Wayland MT (2010) Proboscis profiler: a tool for detecting acanthocephalan morphotypes. Syst Parasitol 76:159–167
Acknowledgments
We thank to all members of the COFIB for their collaboration and enthusiasm in the development of this study. We truly appreciate the collaboration of the members of the Cell Biology and Botany laboratories from sharing their molecular laboratory facilities. We would also like to thank the SOIB JOVE program for funding the contract of SD. Finally, we thank Ursula Paredes and Richard Abel for their thoughtful criticism to the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interest.
Additional information
Handling Editor: Julia Walochnik
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Garcia-Salguero, A., Delgado-Serra, S., Sola, J. et al. Combined morphology and DNA-barcoding to identify Plagiorhynchus cylindraceus cystacanths in Atelerix algirus. Parasitol Res 118, 1473–1478 (2019). https://doi.org/10.1007/s00436-019-06299-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06299-6