Abstract
This study aimed to investigate the endoparasite fauna of wild European gray wolves, which are currently recolonizing Germany. In total, 69 fecal samples of wild wolves were collected in Lower Saxony, Germany, from 2013 to 2015, analyzed by the sedimentation-flotation and McMaster techniques and compared to previous results on captive European Gray wolves living in zoological gardens in Germany. In addition to coproscopy, taeniid-positive samples from wild as well as captive wolves were differentiated by amplification and sequencing of small subunit ribosomal RNA (SSU rRNA) and NADH dehydrogenase 1 (nad1) gene fragments. Missing Taenia krabbei SSU rRNA reference sequences were generated from two T. krabbei specimens. Overall, 60.87% (42/69) of wild wolve samples were microscopically positive for at least one of seven egg types. Capillaria/Eucoleus spp. showed the highest frequency (31.88% [22/69]), followed by Taeniidae (21.74% [15/69]), Ancylostomatidae (20.29% [14/69]), Alaria alata (15.94% [11/69]), Toxocara canis (13.04% [9/69]), and Toxascaris leonina and Trichuris vulpis (each 5.80% [4/69]). Amplification of SSU rRNA was successful for 7/15 Taeniidae-positive samples from wild and 20/39 samples from captive wolves, revealing T. hydatigena in two and 14 samples, respectively. Taenia krabbei was detected in two further samples of wild and three samples of captive wolves, while for the remaining samples, no differentiation between T. serialis/T. krabbei was possible. Echinococcus spp. were not detected. Sequence comparisons revealed that the SSU rRNA gene fragment was not suitable to differentiate between T. serialis and T. krabbei. Therefore, the use of this fragment alone cannot be recommended for species identification in future studies.
Abbreviations
- EpG :
-
Eggs per gram feces
- nad1 :
-
NADH dehydrogenase 1
- SSU rRNA :
-
Small subunit ribosomal RNA
- QC :
-
Query cover
References
Armua-Fernandez MT, Nonaka N, Sakurai T, Nakamura S, Gottstein B, Deplazes P, Phiri IGK, Katakura K, Oku Y (2011) Development of PCR/dot blot assay for specific detection and differentiation of taeniid cestode eggs in canids. Parasitol Int 60:84–89. https://doi.org/10.1016/j.parint.2010.11.005
Becker AC, Kraemer A, Epe C, Strube C (2016) Sensitivity and efficiency of selected coproscopical methods-sedimentation, combined zinc sulfate sedimentation-flotation, and McMaster method. Parasitol Res 115:2581–2587. https://doi.org/10.1007/s00436-016-5003-8
Bindke JD, Springer A, Böer M, Strube C (2017) Helminth fauna in captive European gray wolves (Canis lupus lupus) in Germany. Front Vet Sci 4(228). https://doi.org/10.3389/fvets.2017.00228
Bryan HM, Darimont CT, Hill JE, Paquet PC, Thompson RCA, Wagner B, Smits JEG (2012) Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology 139:781–790. https://doi.org/10.1017/S0031182011002319
Contact Office “Wolves in Saxony” [Kontaktbüro Wölfe in Sachsen] (2018) Distribution in Germany. https://dbb-wolf.de/wolfsvorkommen/territorien?Bundesland=&Jahr=2016. Accessed 14 August 2018.
Guerra D, Armua-Fernandez MT, Silva M, Bravo I, Santos N, Deplazes P, Carvalho LM (2013) Taeniid species of the Iberian wolf (Canis lupus signatus) in Portugal with special focus on Echinococcus spp. Int J Parasitol Parasites Wildl 2:50–53. https://doi.org/10.1016/j.ijppaw.2012.11.007
Federal Documentation and Advice Centre on the Wolf [Dokumentations- und Beratungsstelle des Bundes zum Thema Wolf] (2018) Wolfsterritorien in Niedersachsen. https://www.dbb-wolf.de/Wolfsvorkommen/territorien/karte-der-territorien. Accessed 14 August 2018.
Hermosilla C, Kleinertz S, Silva LMR, Hirzmann J, Huber D, Kusak J, Taubert A (2017) Protozoan and helminth parasite fauna of free-living Croatian wild wolves (Canis lupus) analyzed by scat collection. Vet Parasitol 233:14–19. https://doi.org/10.1016/j.vetpar.2016.11.011
Lesniak I, Heckmann I, Heitlinger E et al (2017) Population expansion and individual age affect endoparasite richness and diversity in a recolonising large carnivore population. Sci Rep 7:41730. https://doi.org/10.1038/srep41730
Lesniak I, Heckmann I, Franz M, Greenwood AD, Heitlinger E, Hofer H, Krone O (2018) Recolonizing gray wolves increase parasite infection risk in their prey. Ecol Evol 8:2160–2170. https://doi.org/10.1002/ece3.3839
Poglayen G, Gori F, Morandi B et al (2017) Italian wolves (Canis lupus italicus Altobello, 1921) and molecular detection of taeniids in the Foreste Casentinesi National Park. Northern Italian Apennines. Int J Parasitol Parasites Wildl 6:1–7. https://doi.org/10.1016/j.ijppaw.2017.01.001
Prelezov PN, Bauer C (2003) Comparative efficacy of flubendazole chewable tablets and a tablet combination of febantel, pyrantel embonate and praziquantel against Trichuris vulpis in experimentally infected dogs. Dtsch Tierarztl Wochenschr 110:419–421
Riehn K, Hamedy A, Große K, Wüste T, Lücker E (2012) Alaria alata in wild boars (Sus scrofa, Linnaeus, 1758) in the eastern parts of Germany. Parasitol Res 111:1857–1861. https://doi.org/10.1007/s00436-012-2936-4
Ripple WJ, Beschta RL (2012) Trophic cascades in Yellowstone: The first 15 years after wolf reintroduction. Biol Cons 145:205–213. https://doi.org/10.1016/j.biocon.2011.11.005
Segovia JM, Torres J, Miquel J, Llaneza L, Feliu C (2001) Helminths in the wolf, Canis lupus, from north-western Spain. J Helminthol 75:183–192. https://doi.org/10.1079/JOH200152
Szafrańska E, Wasielewski O, Bereszyński A (2010) A fecal analysis of helminth infections in wild and captive wolves, Canis lupus L., in Poland. J Helminthol 84:415–419. https://doi.org/10.1017/S0022149X10000106
Trachsel D, Deplazes P, Mathis A (2007) Identification of taeniid eggs in the feces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134:911–920. https://doi.org/10.1017/s0031182007002235
Wagner C, Holzapfel M, Kluth G, Reinhardt I, Ansorge H (2012) Wolf (Canis lupus) feeding habits during the first eight years of its occurrence in Germany. Mamm Biol 77:196–203. https://doi.org/10.1016/j.mambio.2011.12.004
Acknowledgements
The authors wish to thank Ines Lesniak and Heribert Hofer (Institute for Zoo and Wildlife Research, Berlin, Germany) for providing the DNA of Taenia krabbei as well as the Friedrich-Löffler-Institute, Federal Research Institute for Animal Health, Insel Riems, Germany, for providing the E. multilocularis DNA used as positive control in the multiplex DNA. The authors are grateful to Ursula Küttler for the excellent technical assistance.
Author information
Authors and Affiliations
Contributions
JDB collected parts of the fecal samples and carried out coproscopical analyses. EJ and AS performed the molecular analyses. JDB and AS performed the statistical analyses. CS and MB designed and coordinated the study. JDB, AS, and CS drafted the manuscript. All authors participated in the data interpretation. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Additional information
Section Editor: Domenico Otranto
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
Bindke, J.D., Springer, A., Janecek-Erfurth, E. et al. Helminth infections of wild European gray wolves (Canis lupus Linnaeus, 1758) in Lower Saxony, Germany, and comparison to captive wolves. Parasitol Res 118, 701–706 (2019). https://doi.org/10.1007/s00436-018-6181-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-6181-3