GASTRO-INTESTINAL HELMINTH COMMUNITY OF LEPUS EUROPAEUS IN BOLOGNA PROVINCE (EMILIA ROMAGNA REGION): BIODIVERSITY DROP IN DECLINING POPULATIONS?

Since the Seventies, a continual reduction of the European brown hare population (Lepus europaeus) has been observed in most European Countries, including Italy. In the Bologna Province, Emilia Romagna Region, after a recovery phase a sudden acceleration of the hare population decline was noticeable from 2008: the hare captured in protected areas for restocking dropped from about 7,000 in 2007-‘08 to 1,891 in 2014-’15. In 2013, from September 15th to October 5th, 53 hares haunted in agro-ecosystems of the Po Plain (Province of Bologna, ATC BO2) were collected for parasitological analysis. All the helminthes were collected from the stomach and the intestine using standard parasitological techniques, preserved in 70% ethyl alcohol and 5% glycerin and therefore microscopically identified following clarification with 20% lactophenol. The sex of each hare and the weight of 52 of them were recordered by hunters; age class was assigned to 51 hare out of 53 by observing Stroh’s tubercle. The animals examined were 40% adults and 60% juveniles, 57% females and 43% males. Mean weight was 3.4 Kg (range: 2.1-4.5 Kg). Only one helminth species was collected, i.e. the nematode Trichostrongylus retortaeformis. Thirty-eight out of 53 hare hosted T. retortaeformis (prevalence 72%); the mean parasite abundance was 22 helminth/examined-hare. Parasite prevalence was significantly higher in adults (95%) than in juveniles (54.8%) (Fisher exact test, p<0.01). Parasite abundance was significantly higher in adults and in heavier animals (multiple negative binomial regression with sex, age and weight as independent variables, p<0.05); parasites were significantly aggregated, with overall estimated k=0.29. None of the other gastro-intestinal helminth species commonly reported in hare (both nematodes and cestodes) were observed. T. retortaeformis is the most common helminth of European brown hare. Several authors reported high prevalence of this parasite in Europe (50-91.7%). A prevalence of 92% had been reported about 20 years ago in the Bologna Province, but the helminth community, although dominated by T. retortaeformis, was characterized by a certain grade of biodiversity with an overall richness of 4 helminth species (3 nematoda and 1 cestoda). Some authors report that severely T. retortaeformis infected animals can undertake chronic enteritis, mortality or body weight loss. In our case, the abundance of the infection is relatively low and it positively correlates to both the animal weight and age, suggesting no evident effect on parasitized individuals. In addition, the aggregation of parasites suggests that only a minimal part of host population would, if ever, be influenced by this infection. T. retortaeformis infection has been also proposed as a possible causal agent of the cyclic population dynamics of L. timidus possibly mediated by the reduction in the body condition and fertility of the infected hosts. Although parasites can cause cyclical fluctuations in host populations (mediated by sub-lethal effects), they did not appear involved in long-lasting decline in hare populations. A positive relationship between host density and parasite abundance is consistent with both theoretical and some empirical studies. The situation observed in our study area, and in particular low parasite abundance, is consistent with the low host density, that probably makes parasite transmission more difficult; in addition, the intense hare population turn-over, due also to seasonal hunt, make it difficult for parasites to gain high abundance due to the lack of older and heavy hosts. The absence of other usually observed parasite species is probably due to their lowest ability to infect hosts if compared with the “well-adapted” T. retortaeformis, usually dominant in hare parasite biocoenosis. In conclusion, the critical situation of host population parallels with the critical loss of biodiversity observed in parasite community. This could eventually induce a harmful loop, since biodiversity is considered a stabilizing factor in ecological webs and the lack of specific brown hare parasites in biocoenosis may be a predisposing factor for the occurrence of exogenous and potentially dangerous parasite taxa in the hare population. The present study suggests that nor T. retortaeformis or other gastro-intestinal helminths were involved in the recent hare population decline (although it is not possible to ascertain that they are, or were, not involved in natural cyclic population dinamic); however, parasite community has probably suffered, direcltly (environmental mechanisms acting on both host and parasites) or indirecltly (mechanisms acting on host density and therefore on parasite transmission), the same until now unknown cause of brown hare decline.