Evaluation of the host specificity of Eimeria uekii and Eimeria raichoi for Japanese rock ptarmigans by oocyst transfer to taxonomically related birds.

Eimeria spp. are protozoan parasites that are commonly found in a broad range of vertebrate hosts. These parasites generally exhibit strict host specificity, but some Eimeria spp. can infect groups of closely related species such as species within a genus or family. Compared with Eimeria spp. that infect livestock, limited information is available about such infections in wild animals including data on host specificity, virulence, and prevalence. The Japanese rock ptarmigan, Lagopus muta japonica, is an endangered bird belonging to the family Phasianidae, order Galliformes, and inhabits only alpine areas of Japan. In conservation efforts for these birds, two Eimeria spp., E. uekii and E. raichoi, were frequently detected. Here, we examined cross-transmission of the parasites to other bird species to characterize their infectivity as well as the development of experimental bird models to contribute to conservation programs by the oocyst transfer. Consequently, among the examined eight bird species (chickens, Japanese pheasants, turkeys, chukar partridges, quails, helmeted guineafowls and ducks), only turkeys (family Phasianidae, order Galliformes) could be infected with E. raichoi. However, the number of oocysts per feces was relatively low, and few parasites in the intestinal mucosa could be found by histopathological analyses. These results might indicate that E. uekii and E. raichoi are highly adapted to Japanese rock ptarmigans that inhabit the alpine zone although further studies are anticipated.

Temperature increase and frost decrease driving upslope elevational range shifts in Alpine grouse and hares.

Global climate change has led to range shifts in plants and animals, thus threatening biodiversity. Latitudinal shifts have been shown to be more pronounced than elevational shifts, implying that northern range edge margins may be more capable to keeping pace with warming than upper elevational limits. Additionally, global climate change is expected to disadvantage habitat specialists. In the Alps, climatic variation along the elevation gradient allows the coexistence of habitat specialists and generalists. Alpine species are anticipated to adapt their elevational ranges to the change of various climate variables caused by global climate change. Regional differences might buffer elevational shifts. Furthermore, distinct climate variables might differently affect the shifts of habitat specialists and generalists. To study the effect of climate change on Alpine species, we analysed hunting bag, climate and biogeographical data of two grouse species (Tetrao tetrix and Lagopus muta) and two hare species (Lepus timidus varronis and L. europaeus) in Grisons, Switzerland, over a period of 30 years. Our results based on 84,630 harvested specimens were as follows: (1) only three out of seven climate variables changed significantly within the study period. (2) The grouse species significantly shifted towards higher elevations, whereas the hare species only shifted in their minimum/maximum elevations. (3) Hunting elevation of habitat generalists increased more than in habitat specialists. (4) The elevational shifts were mostly related to the number of frost days. (5) Hunting elevation increased especially in the southern biogeographical region. To conclude, all four taxa respond to climate change but habitat generalists more rapidly than habitat specialists. The range shift to higher elevations due to global climate change will lead to a reduction in habitat availability for snow-adapted species. Climate change is thus a serious threat to alpine biodiversity. Regions rich in alpine habitats will have an increased responsibility to conserve these species.

Gastrointestinal parasitic infestation in the Rock ptarmigan Lagopus muta in the French Alps and French Pyrenees based on long-term sampling (1987-2018).

Data presented in this work represents the first record of parasites from the Alpine and Pyrenean Lagopus muta subspecies, providing valuable information to consider for conservation management. From 1987 to 2018, 207 Rock ptarmigans were collected in the framework of a long-term sanitary monitoring in France. Eight parasites were found in the Alpine Rock ptarmigan, and one in the Pyrenean subspecies. Only two parasites occurred with high prevalence in the Alpine Rock ptarmigan: Capillaria caudinflata (38.9%) and Eimeria sp. (34.7%). Prevalence of the other parasites (Ascaridia compar, Cestodes, Amphimerus sp. and Trichostrongylus tenuis) was lower than 20%. Dispharynx nasuta was found with a prevalence of 52.9% in the Pyrenean Rock ptarmigan. Overall, we found a spatially aggregated distribution of parasites in the northern French Alps, probably due to both favourable climatic conditions for parasite cycle and high host density. Statistical analyses indicated a positive effect of altitude and latitude on C. caudinflata occurrence whereas risk factors for Eimeria sp. were the distance from urban areas and land cover. In addition, the majority of the infested birds came from areas close to ski-pistes, where human disturbance increases the susceptibility to diseases, causing stress to wildlife.

Modeling future wildlife habitat suitability: serious climate change impacts on the potential distribution of the Rock Ptarmigan Lagopus muta japonica in Japan's northern Alps.

BACKGROUND: The Rock Ptarmigan Lagopus muta japonica lives in the alpine zones of central Japan, which is the southern limit of the global distribution for this species. This species is highly dependent on alpine habitats, which are considered vulnerable to rapid climate change. This study aimed to assess the impact of climate change on potential L. muta japonica habitat based on predicted changes to alpine vegetation, to identify population vulnerability under future climatic conditions for conservation planning. We developed species distribution models, which considered the structure of the alpine ecosystem by incorporating spatial hierarchy on specific environmental factors to assess the potential habitats for L. muta japonica under current and future climates. We used 24 general circulation models (GCMs) for 2081-2100 as future climate conditions. RESULTS: The predicted potential habitat for L. muta japonica was similar to the actual distribution of the territories in the study area of Japan's northern Alps (36.25-36.5°N, 137.5-137.7°E). Future potential habitat for L. muta japonica was projected to decrease to 0.4% of the current potential habitat in the median of occurrence probabilities under 24 GCMs, due to a decrease in alpine vegetation communities. Some potential habitats in the central and northwestern part of the study area were predicted to be sustained in the future, depending on the GCMs. CONCLUSIONS: Our model results predicted that the potential habitats for L. muta japonica in Japan's northern Alps, which provides core habitat for this subspecies, would be vulnerable by 2081-2100. Small sustainable habitats may serve as refugia, facilitating the survival of L. muta japonica populations under future climatic conditions. Impact assessment studies of the effect of climate change on L. muta japonica habitats at a nationwide scale are urgently required to establish effective conservation planning for this species, which includes identifying candidate areas for assisted migration as an adaptive strategy.

Population limitation in a non-cyclic arctic fox population in a changing climate.

Arctic foxes Vulpes lagopus (L.) display a sharp 3- to 5-year fluctuation in population size where lemmings are their main prey. In areas devoid of lemmings, such as Iceland, they do not experience short-term fluctuations. This study focusses on the population dynamics of the arctic fox in Iceland and how it is shaped by its main prey populations. Hunting statistics from 1958-2003 show that the population size of the arctic fox was at a maximum in the 1950s, declined to a minimum in the 1970s, and increased steadily until 2003. Analysis of the arctic fox population size and their prey populations suggests that fox numbers were limited by rock ptarmigan numbers during the decline period. The recovery of the arctic fox population was traced mostly to an increase in goose populations, and favourable climatic conditions as reflected by the Subpolar Gyre. These results underscore the flexibility of a generalist predator and its responses to shifting food resources and climate changes.

Experimental evaluation of pathogenicity and acquired immunity of Eimeria species, E. uekii and E. raichoi, infecting Japanese rock ptarmigans in a subspecies of the birds.

Japanese rock ptarmigans (Lagopus muta japonica) are birds that inhabit only alpine regions of central Honshu Island, Japan, known as the Japanese Alps. The number of these birds has recently declined, and in situ and ex situ national conservation programs for Japanese rock ptarmigans have been initiated. The infections of Eimeria spp. as protozoan parasites of the phylum Apicomplexa, E. uekii and E. raichoi, were frequently reported in the birds. However, the virulence of these Eimeria parasites has not been determined. Here, we analyzed the pathogenicity of these Eimeria parasites using experimental infections of a subspecies model of Japanese rock ptarmigans, Svalbard rock ptarmigans (Lagopus mutus hyperboreus), and evaluated acquired protective immunity against challenge in birds tolerant of low-dose inoculation with Eimeria parasites. Following inoculation with two Eimeria parasites derived from Japanese rock ptarmigans (dose range of 4 × 104 to 4 × 102 for E. uekii and 1.7 × 104 to 4 × 101 for E. raichoi), oocysts were detected at 6-8 days post-inoculation (PI), and the maximum number of oocysts per gram of feces was observed 7-10 days PI and then gradually decreased. The mortality rate and reduction in weight gain of chicks increased following high-dose inoculation of oocysts with abnormal feces (soft and diarrhea). Developmental zoites were detected histopathologically in epithelial tissues and sometimes the lamina propria from the duodenum to the colon. Chicks that survived low-dose inoculation did not show clear clinical symptoms after challenge inoculation. Our results suggest that the pathological characteristics of Eimeria parasites infecting Japanese rock ptarmigans include abnormal feces and reduction in weight gain, resulting in mortality in cases of heavy infection due to high-dose inoculation. These findings provide helpful data for Japanese rock ptarmigan conservation efforts.

A chromosome-level genome assembly for the Rock Ptarmigan (Lagopus muta).

The Rock Ptarmigan (Lagopus muta) is a cold-adapted, largely sedentary, game bird with a Holarctic distribution. The species represents an important example of an organism likely to be affected by ongoing climatic shifts across a disparate range. We provide here a high-quality reference genome and mitogenome for the Rock Ptarmigan assembled from PacBio HiFi and Hi-C sequencing of a female bird from Iceland. The total size of the genome is 1.03 Gb with a scaffold N50 of 71.23 Mb and a contig N50 of 17.91 Mb. The final scaffolds represent all 40 predicted chromosomes, and the mitochondria with a BUSCO score of 98.6%. Gene annotation resulted in 16,078 protein-coding genes out of a total 19,831 predicted (81.08% excluding pseudogenes). The genome included 21.07% repeat sequences, and the average length of genes, exons, and introns were 33605, 394, and 4265 bp, respectively. The availability of a new reference-quality genome will contribute to understanding the Rock Ptarmigan's unique evolutionary history, vulnerability to climate change, and demographic trajectories around the globe while serving as a benchmark for species in the family Phasianidae (order Galliformes).

Identifying sources of variation in parasite aggregation.

Aggregation of macroparasites among hosts is a near-universal pattern, and has important consequences for the stability of host-parasite associations and the impacts of disease. Identifying which potential drivers are contributing to levels of aggregation observed in parasite-host associations is challenging, particularly for observational studies. We apply beta regressions in a Bayesian framework to determine predictors of aggregation, quantified using Poulin's index of discrepancy (D), for 13 species of parasites infecting Icelandic Rock Ptarmigan (Lagopus muta) collected over 12 years. 1,140 ptarmigan were collected using sampling protocols maximizing consistency of sample sizes and of composition of host ages and sexes represented across years from 2006-2017. Parasite species, taxonomic group (insect, mite, coccidian, or nematode), and whether the parasite was an ecto- or endoparasite were tested as predictors of aggregation, either alone or by modulating an effect of parasite mean abundance on D. Parasite species was an important predictor of aggregation in models. Despite variation in D across samples and years, relatively consistent aggregation was demonstrated for each specific host-parasite association, but not for broader taxonomic groups, after taking sample mean abundance into account. Furthermore, sample mean abundance was consistently and inversely related to aggregation among the nine ectoparasites, however no relationship between mean abundance and aggregation was observed among the four endoparasites. We discuss sources of variation in observed aggregation, sources both statistical and biological in nature, and show that aggregation is predictable, and distinguishable, among infecting species. We propose explanations for observed patterns and call for the review and re-analysis of parasite and other symbiont distributions using beta regression to identify important drivers of aggregation-both broad and association-specific.

Japanese rock ptarmigan displays high levels of polyunsaturated fatty acid in egg yolk compared to chicken and quail.

Egg yolk from captive and wild Japanese rock ptarmigan were analyzed for fatty acid composition. Compared to commercially reared poultry species, the ptarmigan yolk samples displayed higher level of polyunsaturated fatty acids as opposed to monounsaturated fatty acids. The difference between the commercial controls and ptarmigan were larger than the difference between groups of ptarmigan, indicating that the fatty acid profile of Japanese rock ptarmigan might be partly attributed to genetic factors rather than feed, despite wild and captive birds having vastly different diets, and captive birds having been artificially bred for several generations.

Herbivore species coexistence in changing rangeland ecosystems: First high resolution national open-source and open-access ensemble models for Iceland.

Rangeland ecosystems are changing worldwide with the abandonment of extensive pastoralism practices and greater interest for species coexistence. However, the lack of compiled data on current changes in the abundance and distribution of herbivores challenges rangeland management decisions. Here we gathered and made available for the first time the most extensive set of occurrence data for rangeland herbivores in Iceland in an Open Access framework for transparent and repeatable science-based decisions. We mapped fine scale species distribution overlap to identify areas at risk for wildlife-livestock conflict and overgrazing. Nationwide and long term (1861-2021) occurrence data from 8 independent datasets were used alongside 11 predictor raster layers ("Big Data") to data mine and map the distribution of the domestic sheep (Ovis aries), feral reindeer (Rangifer tarandus tarandus), pink-footed geese (Anser brachyrhynchus), and rock ptarmigan (Lagopus muta islandorum) over the country during the summer. Using algorithms of Maxent in R, RandomForest, TreeNet (stochastic gradient boosting) and MARS (Splines) in Minitab-SPM 8.3, we computed 1 km pixel predictions from machine learning-based ensemble models. Our high-resolution models were tested with alternative datasets, and Area Under the Curve (AUC) values that indicated good (reindeer: 0.8817 and rock ptarmigan: 0.8844) to high model accuracy (sheep: 0.9708 and pink-footed goose: 0.9143). Whenever possible, source data and models are made available online and described with ISO-compliant metadata. Our results illustrate that sheep and pink-footed geese have the greatest overlap in distribution with potential implication for wildlife-livestock conflicts and continued ecosystem degradation even under diminishing livestock abundance at higher elevation. These nationwide models and data are a global asset and a first step in making available the best data for science-based sustainable decision-making about national herbivores affecting species coexistence and environmental management.

Surveillance of Eimeria species in wild Japanese rock ptarmigans, Lagopus muta japonica, and insight into parasitic seasonal life cycle at timberline regions of the Japanese Alps.

The Japanese rock ptarmigan, Lagopus muta japonica, inhabits the alpine zone of mountainous areas at 3000 m above sea level. Since L. m. japonica is endangered due to a decline in the overall population, controlling infectious diseases such as those caused by protozoan parasites is a critical factor in the conservation of this species. Although Eimeria spp. are considered to have a negative impact on Japanese rock ptarmigan populations, the ecological interactions between the parasites and their hosts have not yet been fully clarified. We therefore conducted seasonal surveys of the prevalence of Eimeria spp. in Japanese rock ptarmigan populations. In addition, we recorded the ambient temperature in ptarmigan habitat and characterized the ability of eimerian isolates to acquire infectivity. Eimeria spp. were detected in 217 of 520 (41.7%) Japanese rock ptarmigan fecal samples in 2006 and in 177 of 308 (57.5%) fecal samples in 2007. Specifically, we observed two types of oocysts characteristic of E. uekii and type B. In adult birds and chicks, infection rates increased towards August (summer) and then decreased as the temperature decreased toward November (winter). Oocyst counts per gram (OPG) of feces peaked in August in adults and chicks, and OPG values were markedly higher in chicks than in adults. Isolated Eimeria spp. oocysts sporulated at temperatures as low as 8 °C and remained viable after being stored at 4 °C for 6 months. Our findings suggest that Eimeria spp. can complete their annual lifecycle in the cold timberline regions inhabited by the host, the Japanese rock ptarmigan, and that Eimeria spp. infection is widespread in the bird populations examined.

Molecular identification of two Eimeria species, E. uekii and E. raichoi as type B, in wild Japanese rock ptarmigans, Lagopus muta japonica.

Thus far, two types of Eimeria parasites (E. uekii and type B) have been morphologically identified in wild Japanese rock ptarmigans, Lagopus muta japonica. Although high prevalences were reported for these parasites, genetic analyses have not been conducted. We first clarified the phylogenetic positions of two eimerian isolates using genetic analyses of 18S rRNA and mitochondrial cytochrome c oxidase subunit I gene regions. Consequently, of 61 samples examined, 21 and 11 samples were positive for E. uekii and type B, respectively. Additionally, the infection rate increased in the summer. Molecular analyses revealed both Eimeria isolates formed their own clusters; E. uekii was included in clades of chicken Eimeria and type B was include in clades of turkey Eimeria. Based on our findings in this study and previous data, we herein propose type B as E. raichoi. These genetic data will be helpful to conduct detailed classification and understand the impact of these parasites for conservation of endangered Japanese rock ptarmigans.

Cecal Microbiome Analyses on Wild Japanese Rock Ptarmigans (Lagopus muta japonica) Reveals High Level of Coexistence of Lactic Acid Bacteria and Lactate-Utilizing Bacteria.

Preservation of indigenous gastrointestinal microbiota is critical for successful captive breeding of endangered wild animals, yet its biology is poorly understood. Here, we compared the cecal microbial composition of wild living Japanese rock ptarmigans (Lagopus muta japonica) in different locations of Japanese mountains, and the dominant cecal microbial structure of wild Japanese rock ptarmigans is elucidated. Coriobacteraceae and Lachnospraceae were the two dominant bacterial families in all samples analyzed. At the genus level, 10 genera Olsenella, Actinomyces, Megasphaera, Slackia, Cloacibacillus, Bifidobacterium,Escherichia,Dialister, Megamonas, and Bilophila were dominant. These results reveal the high level of coexistence of lactic acid bacteria (Olsenella and Bifidobacterium) and lactate-utilizing bacteria (Megasphaera). This coexistence should be taken into account for the successful breeding of captive Japanese rock ptarmigans in the national conservation program.

A TEST OF THE GLACIAL REFUGIUM HYPOTHESIS USING PATTERNS OF MITOCHONDRIAL AND NUCLEAR DNA SEQUENCE VARIATION IN ROCK PTARMIGAN (LAGOPUS MUTUS).

The glacial refugium hypothesis (GRH) proposes that glaciers promoted differentiation and generation of intraspecific diversity by isolating populations in ice-free refugia. We tested three predictions of this hypothesis for the evolutionary divergence of rock ptarmigan (Lagopus mutus) during the Wisconsin glaciation of the late Pleistocene. To do this, we examined subspecies distributions, population genetic structure, and phylogenetic relationships in 26 populations across North America and the Bering Sea region. First, we analyzed sequence variation in the mitochondrial control region, in a nuclear intron (Gapdh), and in an internal transcribed spacer (ITS1). Control region sequences of 154 rock ptarmigan revealed strong population and phylogeographic structure. Variation in intron sequences of 114 rock ptarmigan also revealed significant population structure compatible with results for the control region. Rock ptarmigan were invariant for ITS1. Second, we show that five known Nearctic refugia and an Icelandic refugium are concordant with the current distribution of morphologically distinct subspecies; five of these six refugia are geographically concordant with the distribution of closely related control region haplotypes. Third, our estimates of the time since phylogenetic lineages diverged predated the last glacial maximum for all but two lineages. In addition, all lines of evidence suggest that two unknown refugia in the Bering Sea region supported rock ptarmigan during the Wisconsin glaciation. Overall, our results are most consistent with the hypothesis that isolated populations of rock ptarmigan diverged in multiple refugia during the Wisconsin and that geographic variation reflects patterns of recolonization of the Nearctic after the ice receded. The GRH may therefore offer the most plausible explanation for similar biogeographic patterns in a variety of Nearctic vertebrates.