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.
Host biological factors and habitat influence the faunal assemblages and biodiversity worldwide, including parasite communities of vertebrate and invertebrate hosts. The ecological relationship between hosts and parasites can be mediated by interaction of host's biological factors, as their physiological condition, diet and size, with the environmental components, somehow influencing the features of parasite infection in host populations. Here, we used boosted regression tree models to study the parasite communities of two sympatric sparid fishes, the salema Sarpa salpa and the white seabream Diplodus sargus, to investigate the role of specific host's traits in two contiguous coastal areas along the southern-western Tyrrhenian coast of Italy characterized by different degree of deterioration. Results showed that overall and across all parasite groups (ecto-, endo- and ecto- plus endo-parasites), sampling localities were the most important predictors of abundance, species richness, and diversity for salema. Moreover, seasonality was the main predictor of endo-parasite abundance, while size-related factors explained most of the variation in species richness and diversity. In the white seabream, size-related factors and reproductive cycle-related factors were the most important predictors for the overall parasite abundance and parasite richness, respectively. Our findings suggest that the parasite community of salema and white seabream responded differently to specific biological factors, highlighting how the environmental conditions under which they live may exert a strong influence on the parasite communities of each host fish.
In the context of wildlife conservation, there is a great interest to assess the role of pathogens in influencing population dynamics (Smith et al., 2006; Delogu et al., 2013). This is partially due to the fact that the number of pathogens to which wildlife is exposed has recently increased, for several reasons. In particular for wild Galliformes there is an increased risk of disease transmission as a consequence of the restocking of games species (Gortazar et al., 2014). Every year the red partridge, the ring neck pheasant and other wild species are introduced for hunting purposes in the Italian Alps (Regione Piemonte, 2018). These game animals, not always raised with adequate hygienic and sanitary conditions, can potentially shed pathogens in the environment, which might be hazardous for wildlife population. Based on scientific literature in fact, different factors make captive-born animals particularly susceptible to infectious diseases (Lafferty and Gerber, 2002). For this reason, they can potentially have heavy parasite loads that can be transmitted to wild populations (Power and Mitchell, 2004).
Taking into account that pathogens might have a negative impact on welfare and population dynamics (Hudson, 1986; Holmstad et al., 2005; Citterio et al., 2006), the studies on the parasite fauna hosted by endangered species can provide a better understanding of such interactions (Formenti et al., 2013). However, the health status of wild Galliformes populations is poorly known. This is in partly due to the complexity of sampling animals in the alpine environments, to the low density of targeted species and to the few ongoing projects focusing on health issues of Galliformes.
The low parasite richness recorded in this work is in accordance with previous studies carried out in Eastern Italian Alps (Viganò et al., 2012a, 2012b; Formenti et al., 2013). It is particularly worthy to highlight the complete absence of parasite in the rock partridge, living at high altitude, in areas with more extreme climatic conditions that probably do not allow the development of parasite cycles. On the contrary, some parasites extensively detected in previous studies like Heterakis gallinarum (in the rock patridge) (Florio and Gamba, 1993; Milani, 2010; Viganò et al., 2012b; Viganò and Giacomelli, 2014), were not detected in our survey. The absence of this parasite might be due to either a reduction of the host population density, which is no longer able to maintain the parasite cycle, or to a host-parasite equilibrium reached in the ecosystem. In a context of low host density, the parasite fitness can in fact declines with a lower ability to infest next generations and a potential local extinction in a long-term perspective.
Compared with similar surveys carried out in northern European countries, the parasite richness found in our study is significantly lower. Several parasite species found in northern Europe have never been recorded on the Alpine Galliformes. These include Heterakis bonasae (Kalla et al., 1997), Trycostrongilus tenuis (Holmstad et al., 2005) and Syngamus trachea (Wissler and Halvorsen, 1977). A possible explanation to these findings may be provided by the work of Altzier et al. (2007). These authors in fact have demonstrated how an isolated and low-density host population might have fewer parasites. Hence Alpine Galliformes may harbour fewer parasite species, as a consequence of restricted and isolated geographical ranges. This is particularly true for species like the rock ptarmigan that is a glacial relict, whose population remained isolated at the end of the last glaciation.
Additionally, Capillaria shows a clear host preference: 9 over 83 black grouse were found parasitized vs 1 over 77 rock partridge. This difference might be due to the fact that the parasite host-specificity increases with higher host densities (Forbes et al., 2017). In the Italian Alps in fact, the black grouse is the wild Galliformes with the highest population density (Giordano et al., 2017). Moreover, considering that Capillaria have an indirect cycle, with earthworms as an intermediate host, the different risk of infestation can also be due to different feeding behaviour and diet of the two host species. The black grouse in fact feed more on earthworms while the rock partridge on insects. Yet data on C. caudinflata infestation in wild Galliformes are relatively limited, this worm has been recorded in a wide range of bird species causing severe enteritis and anaemia leading to poor general conditions and weight loss even in the case of mild infestation (Villanúa et al., 2007, Pinto et al., 2008, McCain, 2015). The impact of this parasite on black grouse population dynamics should be then further evaluated.
In addition to density and diet preferences, other specific variables related to behaviour, phenology and nest structure can influence the predisposition to parasitism. Indeed, the quality of being a competent host for parasites depends on host-specific variation in parasite reproductive success (Stokke et al., 2018). However, more studies about parasites of Galliformes on the Alps are needed to better evaluate the factors explaining this variation in host selection.
As regards A. compar infestation, the prevalence, abundance and intensity values found in the hunting districts in the northern part of the study area (Lanzo and Biella Valleys) were significantly higher than in the southern part. This different degree of parasitism is probably due to different climatic conditions influencing the development and survival of both eggs, larvae and intermediate hosts of the parasites.
The spatial variation of parasitism degree might also reflect the sanitary management and sanitary status of game birds released in the different hunting districts. Restocking with farmed game birds, above all for red-legged partridge and ring-necked pheasant, is a practice still quite common in Italy. Specific articles of the Regional laws (Regione Piemonte, 2018) do not allow to release animals in the areas where alpine Galliformes lives; however, these interdictions are not always fully respected. Game birds are kept in aviaries were proper hygienic conditions cannot be maintained, thus infestation by parasites are likely (Stadler and Carpenter, 1996). Moreover, sanitary check before releasing the animals is always lacking. Once released, these animals can shed their parasites in the environment which becomes a potential source of infestation for free-ranging wild birds. This might be an additional problem for wild Galliformes conservation (Tompkins et al., 2015). A study carried out in Spain have clearly demonstrated that areas where restocking is a common practice, the sanitary status of the wild Galliformes can significantly deteriorate (Villanúa et al., 2008). Under this perspective, the sanitary status of the different areas could be considered an indirect index of the quality of the wildlife management activity carried out in the different hunting districts.
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