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Gastroenteric parasite of wild Galliformes in the Italian Alps: implication for conservation management

Published online by Cambridge University Press:  19 December 2019

A. Fanelli Open the ORCID record for A. Fanelli [Opens in a new window] ,
G. Menardi ,
M. Chiodo ,
O. Giordano ,
G. Ficetto ,
M. Bessone Open the ORCID record for M. Bessone [Opens in a new window] ,
A. Lasagna ,
M.G. Carpignano ,
A. Molinar Min  and
A. Gugiatti
...Show all authors
A. Fanelli
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
G. Menardi
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
M. Chiodo
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
O. Giordano
Affiliation:
Comprensorio Alpino CN2 “Valle Varaita”, Valle Varaita, Italy
G. Ficetto
Affiliation:
Comprensorio Alpino CN2 “Valle Varaita”, Valle Varaita, Italy
M. Bessone
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
A. Lasagna
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
M.G. Carpignano
Affiliation:
Comprensorio Alpino CN3 “Valli Maira e Grana”, Valli Maira e Grana, Italy
A. Molinar Min
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
A. Gugiatti
Affiliation:
Comprensorio Alpino “Sondrio”, Sondrio, Italy
P.G. Meneguz
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
P. Tizzani*
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, 10090 – Grugliasco (Turin), Italy
*
Author for correspondence: Paolo Tizzani, E-mail: [email protected]
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Abstract

This study provides insights about the diversity, prevalence and distribution of alpine wild galliformes gastrointestinal parasite community, trying to fill a gap in the scientific information currently available in scientific literature. The analysis included three host species: 77 rock partridge (Alectoris graeca saxatilis), 83 black grouse (Tetrao tetrix tetrix) and 26 rock ptarmigan (Lagopus muta helveticus) shot during the hunting seasons 2008–2015. Parasites isolated were Ascaridia compar, Capillaria caudinflata and cestodes. The rock ptarmigan was free from gastrointestinal parasites, whereas the most prevalent helminth (37%) was A. compar in both black grouse and rock partridge. C. caudinflata occurrence was significantly higher in black grouse (prevalence = 10%, mean abundance = 0.6 parasites/sampled animal) than in rock partridge (prevalence = 1.20%, mean abundance = 0.01 parasites/sampled animal). Significant differences were detected among hunting districts. A. compar was found with a significant higher degree of infestation in the hunting districts in the northern part of the study area whereas cestodes abundance was higher in Lanzo Valley. Quantitative analysis of risk factors was carried out using a generalized linear model (GLM) only on the most common parasite (A. compar). Latitude was the only factors associated with infestation risk (OR = 52.4). This study provides information on the composition and variability of the parasite community in the alpine Galliformes species.

Keywords

AlpsAscaridiaconservationGalliformesparasites
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 471 - 477
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Copyright
Copyright © Cambridge University Press 2019

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Footnotes

*

These authors equally contribute to the paper.

References

Akaike, H (1973) Information theory and an extension of the maximum likelihood principle. In Petrov, BN and Csaki, F (eds), Proceedings of the 2nd International Symposium on Information Theory. Budapest: Akadémiai Kiadó, pp. 267–281.Google Scholar
Altizer, S, Nunn, CL and Lindenfors, P (2007) Do threatened hosts have fewer parasites? A comparative study in primates. Journal of Animal Ecology 76, 304–314.CrossRefGoogle ScholarPubMed
Anfodillo, T (2007) Cambiamenti climatici e dinamica di popolazione al limite superiore del bosco: importanza delle ricerche di lungo termine. Forest@ 4, 3–5.CrossRefGoogle Scholar
ARPA Piedmont (2019) Il clima in Piemonte: relazioni tecniche. Available at http://www.arpa.piemonte.it/, accessed August 2019.Google Scholar
Asters (2012) Fiches espèces d ’ intérêt communautaire – Site Natura 2000 du Massif du Bargy 2. In Aster (ed.), pp.18.Google Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B 57, 289–300.Google Scholar
Calcagno, V (2019) glmulti: Model Selection and Multimodel Inference Made Easy. R package version 1.0.7.1.Google Scholar
Citterio, CV, Caslini, C, Milani, F, Sala, M, Ferrari, N and Lanfranchi, P (2006) Abomasal nematode community in an Alpine chamois (Rupicapra R. Rupicapra) population before and after a die-off materials and methods study area and population. Journal of Parasitology 92, 918–927.CrossRefGoogle Scholar
Delogu, M, Ghetti, G, Gugiatti, A, Cotti, C, Piredda, I, Frasnelli, M and De Marco, MA (2013) Virological investigation of Avian influenza virus on postglacial species of phasianidae and tetraonidae in the Italian Alps. ISRN Veterinary Science 2013, 26–31.CrossRefGoogle ScholarPubMed
Doerken, S, Avalos, M, Lagarde, E and Schumacher, M (2019) Penalized logistic regression with low prevalence exposures beyond high dimensional settings, PLoS One 14, 1–14. https://doi.org/10.1371/journal.pone.0217057.CrossRefGoogle ScholarPubMed
European Parliament and European Council (2009) Directive 2009/147/EC of the European Parliament and of the Council of 30 November 2009 on the conservation of wild birds. Official Journal Language 20, p. 7–25.Google Scholar
Florio, F and Gamba, M (1993) Parassitofauna dei galliformi di montagna sull'arco alpino italiano. Università degli studi di Torino. These: pp. 120.Google Scholar
Forbes, MR, Morrill, A and Schellinck, J (2017) Host species exploitation and discrimination by animal parasites. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160090. https://doi.org/10.1098/rstb.2016.0090.CrossRefGoogle ScholarPubMed
Formenti, N, Viganò, R, Rotelli, L, Ferrari, N, Cerutti, MC and Lanfranchi, P (2013) Effect of suboptimal environment and host age on helminth community of black grouse (Tetrao Tetrix). European Journal of Wildlife Research 59, 351–358.CrossRefGoogle Scholar
Giordano, O, Ficetto, G and Tizzani, P (2017) Monitoraggio primaverile dei galliformi alpini: status e trend delle popolazioni in Valle Varaita (Piemonte, Cuneo). In XIX Convegno italiano di Ornitologia, Turin, Italy.Google Scholar
Gortazar, C, Diez-Delgado, I, Barasona, JA, Vicente, J, De La Fuente, J and Boadella, M (2014) The wild side of disease control at the wildlife-livestock-human interface: a review. Frontiers in Veterinary Science 1, 1–12. https://doi.org/10.3389/fvets.2014.00027.Google ScholarPubMed
Heiberger, RM (2018) HH: Statistical analysis and data display: Heiberger and Holland. R package version 3.1-35.Google Scholar
Holmstad, PR, Hudson, PJ and Skorping, A (2005) The influence of a parasite community on the dynamics of a host population: a longitudinal study on willow ptarmigan and their parasites, Oikos 111, 377–391. https://doi.org/10.1111/j.0030-1299.2005.13640.x.CrossRefGoogle Scholar
Hudson, PJ (1986) The effect of a parasitic nematode on the breeding production of red grouse. Journal of Animal Ecology 55, 85–92. https://doi.org/10.2307/4694.CrossRefGoogle Scholar
Kalla, PI, Dimmick, RW and Patton, S (1997) Helminths in ruffed grouse at the host's southeastern range boundary. Journal of Wildlife Diseases 33, 503–510. https://doi.org/10.7589/0090-3558-33.3.503.CrossRefGoogle ScholarPubMed
Khalil, LF, Jones, A and Bray, RA (1994) Keys to the Cestode Parasite of Vertebrates, Wallingford, Oxon, UK: CAB International. pp. 768.Google Scholar
Lafferty, K and Gerber, L (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conservation Biology 16, 593–604.CrossRefGoogle Scholar
Lasagna, A (2009) La Pernice bianca Lagopus mutus helveticus (Thienemann 1829) in Valle d'Aosta. Indagine preliminare sullo status delle popolazioni. Assessorato Agricoltura e Risorse Naturali. Regione Valle d'Aosta (eds). Dipartimento Risorse Naturali e Corpo Forestale. Direzione Flora, Fauna, Caccia e Pesca.Google Scholar
Ludwig, T, Storch, I and Graf, RF (2009) Historic landscape change and habitat loss: the case of black grouse in Lower Saxony, Germany. Landscape Ecology 4, 533–546. https://doi.org/10.1007/s10980-357009-9330-3.CrossRefGoogle Scholar
McCain, S (2015) Charadriiformes. In Fowler's Zoo and Wild Animal Medicine, Vol. 8. WB Saunders, pp. 112–116.CrossRefGoogle Scholar
Milani, F (2010) Monitoraggio dei galliformi in provincia di Lecco 2010 (accessed on August 2019 https://diazilla.com/doc/59008/monitoraggio-galliformi-in-provincia-di-lecco-2010).Google Scholar
Nunn, CL, Altizer, SM, Sechrest, W and Cunningham, AA (2005) Latitudinal gradients of parasite species richness in primates. Diversity and Distributions 11, 249–256.CrossRefGoogle Scholar
Pearce-Higgins, JW, Grant, MC, Robinson, M and Haysom, SL (2007) The role of forest maturation in causing the decline of Black Grouse Tetrao tetrix. Ibis 149, 143–155.CrossRefGoogle Scholar
Pinto, RM, Brener, B, Tortelly, R, Caldas Menezes, R and Muniz-Pereira, LC (2008) Capillariid nematodes in Brazilian turkeys, Meleagris gallopavo (Galliformes, Phasianidae): pathology induced by Baruscapillaria obsignata and Eucoleus annulatus (Trichinelloidea, Capillariidae). Memórias do Instituto Oswaldo Cruz 103, 295–297. https://doi.org/10.1590/S0074-02762008005000017.CrossRefGoogle Scholar
Power, A and Mitchell, C (2004) Pathogen spillover in disease epidemics. The American Naturalist 164, S79–S89.CrossRefGoogle ScholarPubMed
QGIS Development Team (2017) QGIS Geographic Information System. Open Source Geospatial Foundation.Google Scholar
R Core Team (2018) A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.Google Scholar
Regione Piemonte (2018) Legge regionale 19 giugno 2018, n. 5. Tutela della fauna e gestione faunistico – venatoria. In Regione Piemonte (ed.), Torino: pp. 68.Google Scholar
Rondinini, C, Battistoni, A, Peronace, V and Teofili, R (2013) Lista Rossa IUCN dei Vertebrati Italiani. Comitato Italaliano IUCN e Ministero dell'Ambiente e della tutela del Territorio e del Mare.Google Scholar
Rozsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232. https://doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2.CrossRefGoogle ScholarPubMed
Sanchis-Monsonís, G, Fanelli, A, Tizzani, P and Martínez-Carrasco, C (2019) First epidemiological data on Spirocerca vulpis in the red fox: a parasite of clustered geographical distribution. Veterinary Parasitology: Regional Studies and Reports 18, 100338.Google ScholarPubMed
Signorell, N, Wirthner, S, Patthey, P, Schranz, R, Rotelli, L and Arlettaz, R (2010) Concealment from predators drives foraging habitat selection in brood-rearing Alpine black grouse Tetrao Tetrix Hens: habitat management implications. Journal of Wildlife Biology 16, 249–257. https://doi.org/409 10.2981/09-028.CrossRefGoogle Scholar
Skrjabin, KI (1954) Trichostrongylids of Animals and Man. Essentials of Nematodology, Vol. III. Moscow: Academy of Sciences of the USSR.Google Scholar
Smith, KF, Sax, DF and Lafferty, KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20, 1349–1357. https://doi.org/10.1111/j.1523-1739.2006.00524.x.CrossRefGoogle ScholarPubMed
Stadler, CK and Carpenter, JW (1996) Parasites of backyard game birds. Seminars in Avian and Exotic Pet Medicine 5, 85–96.CrossRefGoogle Scholar
Stokke, BG, Ratikainen, II, Moksnes, A, Røskaft, E, Schulze-Hagen, K, Leech, DI, Møller, AP and Fossøy, F (2018) Characteristics determining host suitability for a generalist parasite. Scientific Reports 8, 6285. https://doi.org/10.1038/s41598-018-24627-1.CrossRefGoogle ScholarPubMed
Storch, I (1994) Habitat and survival of capercaillie Tetrao Urogallus nests and broods in the Bavarian Alps. Biological Conservation 70, 237–243. https://doi.org/10.1016/0006-3207(94)90168-6.CrossRefGoogle Scholar
Tinner, W and Vescovi, E (2007) Ecologia e oscillazioni del limite degli alberi nelle Alpi dal Pleniglaciale al presente. Studi Trentini di Scienze Naturali ACTA BIOLOGICA 82, 7–15.Google Scholar
Tompkins, DM, Carver, S, Jones, ME, Krkos, M and Skerratt, LF (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology 31, 149–159. https://doi.org/10.1016/j.pt.2015.01.007.CrossRefGoogle ScholarPubMed
Viganò, R and Giacomelli, S (2014) Relazione analisi parassitologiche stagioni venatorie 2012/2013 e 2013/2014. Monitoraggio delle popolazioni di galliformi alpini per la programmazione di interventi di miglioramento ambientale. Final report.Google Scholar
Viganò, R, Formenti, N, Ferrari, N, Cerruti, MC and Lafranchi, P (2012 a) Analisi parassitologiche sul Fagiano di monte (Tetrao tetrix). Progetto n. 88 ALCOTRA 2007–2013 GALLIFORMI ALPINI Monitoraggio delle popolazioni di galliformi alpini per la programmazione di interventi di miglioramento ambientale; relazione analisi parassitologiche stagioni venatorie 2012/2013 e 2013/2014. Final report.Google Scholar
Viganò, R, Formenti, N, Ferrari, N, Cerruti, MC and Lafranchi, P (2012 b) Analisi parassitologiche sulla Coturnice alpina (Alectoris graeca saxatilis). Progetto n. 88 ALCOTRA 2007–2013 GALLIFORMI ALPINI Monitoraggio delle popolazioni di galliformi alpini per la programmazione di interventi di miglioramento ambientale; relazione analisi parassitologiche stagioni venatorie 2012/2013 e 2013/2014. Final report.Google Scholar
Villanúa, D, Casas, F, Viñuela, J, Gortázar, C, García De La Morena, E and Morales, M (2007) First occurrence of Eucoleus contortus in a little bustard Tetrax Tetrax: Negative effect of Red-legged Partridge Alectoris rufa releases on steppe bird conservation? Ibis 149, 405–406. https://doi.org/10.1111/j.1474-919X.2006.00620.x.CrossRefGoogle Scholar
Villanúa, D, Pérez-Rodríguez, L, Casas, F, Alzaga, V, Acevedo, P, Viñuela, J and Gortázar, C (2008) Sanitary risks of red-legged partridge releases: introduction of parasites. European Journal of Wildlife Research 54, 199–204.CrossRefGoogle Scholar
Watson, A and Moss, R (2004) Impacts of ski-development on ptarmigan (Lagopus mutus) at Cairn Gorm, Scotland. Biological Conservation 116, 267–275. https://doi.org/10.1016/S0006-3207(03)00197-6.CrossRefGoogle Scholar
Wissler, K and Halvorsen, O (1977) Helminths from Willow grouse (Lagopus lagopus) in two localities in North Norway. Journal of Wildlife Diseases 13, 409–413. https://doi.org/10.7589/0090-3558-13.4.409.CrossRefGoogle ScholarPubMed
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