Bagaza virus and Plasmodium spp. coinfection in red-legged partridges ( Alectoris rufa ), in southern Spain 2019

Flaviviruses West Nile (WNV), Usutu (USUV) and Bagaza (BAGV) virus and avian malaria parasites are vector borne pathogens that circulate naturally between avian and mosquito hosts. WNV and USUV and potentially also BAGV constitute zoonoses. Temporal and spatial co-circulation and co-infection with Plasmodium spp., and West Nile virus has been documented in birds and mosquito vectors, and fatally USUV infected passerines coinfected with Plasmodium spp. had more severe lesions. Also, WNV, USUV and BAGV have been found to co-circulate. Yet little is known about the interaction of BAGV and malaria parasites during consecutive or co-infections of avian hosts. Here we report mortality of free-living red-legged partridges in a hunting estate in Southern Spain due to coinfection with BAGV and Plasmodium spp. The outbreak occurred in the area where BAGV first emerged in Europe in 2010 and where co-circulation of BAGV, USUV and WNV was confirmed in 2011 and 2013. Partridges were found dead in early October 2019. Birds had mottled locally pale pectoral muscles, enlarged, congestive greenish-black tinged livers and enlarged kidneys. Microscopically congestion and predominantly mononuclear inflammatory infiltrates were evident and Plasmodium phanerozoites were present in the liver, spleen, kidneys, muscle and skin. Molecular testing and sequencing detected Plasmodium spp. and BAGV in different tissues of the partridges, and immunohistochemistry confirmed the presence and co-localization of both pathogens in the liver and spleen. Although Plasmodium spp. are known to be highly prevalent in red-legged partridges, this is the first account of mortality caused by co-infection with BAGV and Plasmodium sp. Due to the importance of the red-legged partridge in the ecosystem of the Iberian Peninsula and as driver of regional economy such mortalities are of concern. Also, they may reflect climate change related changes in host, vector and pathogen ecology and interactions that could emerge similarly in other pathogens.

Risk of Infection, Local Prevalence and Seasonal Changes in an Avian Malaria Community Associated with Game Bird Releases

Anthropogenic activities, such as the translocation or introduction of animals, may cause a parallel movement of exotic parasites harboured by displaced animals. Although introduction and/or relocation of animals for hunting purposes is an increasingly common management technique, the effects of gamebird release as a major vehicle for the introduction of parasites into new geographic regions have rarely been reported. We examined the prevalence and distribution of avian malaria parasites infecting resident avian hosts (red-legged partridge Alectoris rufa) at a local scale, with a particular emphasis on the effects of releasing farm-reared birds for hunting on the spatial and temporal structure of the parasite community. We collected blood samples from adult partridges from two game estates with partridge releases and two sites without releases over two periods (spring and autumn). We tested the probability of infection and differences in the parasite community in relation to the management model (releases vs. non releases) and sampling period, comparing autumn (when farm-reared birds are released) and spring (after hunting season, when mostly wild birds can be found in the population). We found a high prevalence (54%) of Plasmodium spp., and substantial differences in the spatial and temporal distribution of parasite lineages among the populations studied. Some parasite lineages occurred at high frequencies in game estates without introduction of farm-reared partridges, while other lineages were more abundant in game estates with releases than in those without releases. Overall, the prevalence of avian malaria was similar between spring and autumn at non-release sites, whereas in sites with releases, it was higher in autumn than in spring—probably due to artificial restocking with infected farm-reared birds at the onset of the hunting season. In short, humans may be an important agent driving the alteration of the spatial structure of local parasite fauna via the introduction of exotic parasites by gamebird release, which could cause avian malaria outbreaks with severe repercussions for native avifauna.

How many gamebirds are released in the UK each year?

Large numbers of gamebirds (pheasants Phasianus colchicus, red-legged partridges Alectoris rufa and mallard Anus platyrhynchos) are released annually in the UK to support recreational shooting. It is important to know how many of these birds are being released because their release and management has ecological effects on the wildlife and habitats of the UK. There is little regulation governing their release, and consequently, an accurate figure for the numbers being released is unknown. I took 12 different approaches, totalling 4329 estimates of the numbers of birds being released annually, based on a series of datasets that described numbers of birds being held for breeding, rearing or release, being released, managed or shot on game shoots, being shot by individual guns or being recorded during breeding bird surveys. These 12 approaches produced estimates ranging from 14.7 to 106.1 million with a mean of 43.2 million (95% CI 29.0–57.3 million). This suggests that 31.5 million pheasants (range 29.8–33.7 million), 9.1 million red-legged partridges (range 5.6–12.5 million) and 2.6 million mallard (range 0.9–6.0 million) are released annually in the UK. These figures differ substantially from both official records of gamebirds and previous published estimates, and I discuss why such differences may occur. I set these figures in the context of the number and behaviour of shoots operating in the UK. Improved estimates of numbers of gamebird being released are critical if we are to better understand the ecological effects occurring in areas where they are released and managed.

First Data on Gastrointestinal Parasitic Infection in the Red-Legged Partridge (Alectoris rufa) in Italy

The Red-legged partridge (Alectoris rufa) is a Mediterranean Galliformes, recently classified as Near Threatened by the International Union for the Conservation of Nature, due to the constant and significant decline of its global population. While the gastrointestinal parasites of the species are well studied in some part of its range (Iberian peninsula), limited information is available for the Italian populations, that represent the eastern limit of the species range. This study was conducted to fill this gap of knowledge, determining the composition, richness, prevalence, intensity and abundance of A. rufa gastrointestinal parasite community in two populations in Italy. During the autumn seasons 2008–2009 and 2009–2010, necropsies were conducted on 18 Red-legged partridge from the southern part of Alessandria province (Piedmont, northwestern Italy) and 34 from the Parma province (Emilia Romagna, northern Italy). All the animals were examined for the presence of gastrointestinal parasites. Additionally, 229 fecal samples were collected from live animals in Alessandria province. Prevalence, abundance and intensity of infection were calculated for each parasite species, except for coccidia for which only the prevalence was determined. The following parasites were observed: Heterakis gallinarum, Ascaridia spp., Ascaridia columbae, Raillietina spp., Eimeria spp. The highest parasite prevalence was found in Alessandria province for Eimeria sp., infecting almost half of the sampled animals (P: 45%, CI95%: 39–51). Eimeria sp. was also the most prevalent parasite in Parma province but with much lower prevalence (P: 19%, CI95%: 5–32). Intestinal helminths prevalence ranged from 3% (CI95%: 0–9) for A. columbae and Raillietina spp. (Parma Province) to 9% for H. gallinarum in both Parma (CI95%: 0–19), and Alessandria province (CI95%: 0–22). To our knowledge, this is the first study providing information on the gastrointestinal parasites of the Red-legged partridge in Italy. Ascaridia columbae, a parasite typical of the domestic pigeon, was reported for the first time in A. rufa. The epidemiological descriptors reported herein could serve as a basis for future studies, allowing for epidemiological comparison across countries, locations, and time periods.

Pathogenesis of Two Western Mediterranean West Nile Virus Lineage 1 Isolates in Experimentally Infected Red-Legged Partridges (Alectoris rufa)

West Nile virus (WNV) is the most widespread flavivirus in the world with a wide vertebrate host range. Its geographic expansion and activity continue to increase with important human and equine outbreaks and local bird mortality. In a previous experiment, we demonstrated the susceptibility of 7-week-old red-legged partridges (Alectoris rufa) to Mediterranean WNV isolates Morocco/2003 and Spain/2007, which varied in virulence for this gallinaceous species. Here we study the pathogenesis of the infection with these two strains to explain the different course of infection and mortality. Day six post-inoculation was critical in the course of infection, with the highest viral load in tissues, the most widespread virus antigen, and more severe lesions. The most affected organs were the heart, liver, and spleen. Comparing infections with Morocco/2003 and Spain/2007, differences were observed in the viral load, virus antigen distribution, and lesion nature and severity. A more acute and marked inflammatory reaction (characterized by participation of microglia and CD3+ T cells) as well as neuronal necrosis in the brain were observed in partridges infected with Morocco/2003 as compared to those infected with Spain/2007. This suggests a higher neurovirulence of Morocco/2003, probably related to one or more specific molecular determinants of virulence different from Spain/2007.

Genome-wide markers redeem the lost identity of a heavily managed gamebird

Heavily managed wildlife may suffer from genetic homogenization and reshuffling of locally adapted genotypes with non-native ones. This phenomenon often affects natural populations by reducing their evolutionary potential and speeding up the ongoing biodiversity crisis. For decades, the red-legged partridge ( Alectoris rufa ), an intensively managed gamebird of conservation concern and considerable socio-economic importance, has been subjected to extensive releases of farm-reared hybrids with the chukar partridge ( Alectoris chukar ) and translocations irrespective of subspecific affinity. These practices have led to serious concerns that the genetic integrity and biogeographic structure of most red-legged partridge populations are irreversibly affected, as suggested by previous studies based on few genetic markers. Using over 168 000 genome-wide loci and a sampling across the entire A. rufa range, we detected unexpectedly limited and spatially uneven chukar introgression as well as significant intraspecific structure. We demonstrate that species widely feared to have irretrievably lost their genetic identity are likely to be much less affected by unsuitable management practices than previously assumed. Our results spell the need for a radical re-think on animal conservation, possibly restoring native status to populations long treated as compromised. Our study exemplifies how the application of innovative conservation-genomic methods is key to solving wildlife management problems dealing with introgressive hybridization worldwide.

Contribution of non-native galliforms to annual variation in biomass of British birds

Millions of individuals of two species of non-native galliform birds, the Common Pheasant (Phasianus colchicus) and Red-legged Partridge (Alectoris rufa) are released into the British countryside annually in late summer, supplementing established breeding populations of these two species. The biomass of birds involved in these releases has been compared to the British breeding bird biomass. However, the validity of this comparison is compromised because the biomass of wild birds varies across the year due to reproduction, mortality and migration. How the biomass of Common Pheasants and Red-legged Partridges compares to that of other British bird species in late summer, or across the whole year, is currently unknown. Here, we produce estimates of how British bird biomass varies across the year, to assess the contribution of the two non-native galliforms to this variation. We show that overall British bird biomass is probably lowest around the start of the breeding season in April, and peaks in late summer and autumn. We estimate that around a quarter of British bird biomass annually is contributed by Common Pheasants and Red-legged Partridges, and that at their peak in August these two species represent about half of all wild bird biomass in Britain.