Comparative molecular analyses of Eimeria Schneider (Apicomplexa: Eimeriidae) species from rock ptarmigan in Iceland, Svalbard-Norway, and Japan.

The rock ptarmigan (Lagopus muta) has a Holarctic breeding distribution and is found in arctic and sub-arctic regions. Isolated populations and glacial relicts occur in alpine areas south of the main range, like the Pyrenees in Europe, the Pamir mountains in Central Asia, and the Japanese Alps. In recent decades considerable effort has been made to clarify parasite infections in the rock ptarmigan. Seven Eimeria spp. have been reported parasitizing rock ptarmigan. Two of those species, E. uekii and E. raichoi parasitizing rock ptarmigan (L. m. japonica) in Japan, have been identified genetically. Here we compare partial sequences of nuclear (18S rRNA) and mitochondrial (COI) genes and we detail the morphology of sporulated oocysts of E. uekii and E. raichoi from Japan, E. muta and E. rjupa, from the rock ptarmigan (L. m. islandorum) in Iceland, and two undescribed eimerian morphotypes, Eimeria sp. A, and Eimeria sp. B, from rock ptarmigan (L. m. hyperborea) in Norway (Svalbard in the Norwegian Archipelago). Two morphotypes, ellipsoidal and spheroidal, are recognized for each of the three host subspecies. Our phylogenetic analysis suggests that the ellipsoidal oocyst types, E. uekii, E. muta, and Eimeria sp. A (Svalbard-Norway) are identical and infects rock ptarmigan in Japan, Iceland, and Svalbard-Norway, respectively. Eimeria uekii was first described in Japan in 1981 so that E. muta, described in Iceland in 2007, and Eimeria sp. A in Svalbard-Norway are junior synonyms of E. uekii. Also, phylogenetic analysis shows that the spheroidal oocyst types, E. rjupa and Eimeria sp. B (Svalbard-Norway), are identical, indicating that rock ptarmigan in Iceland and Svalbard-Norway are infected by the same Eimeria species and differ from E. raichoi in Japan.

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.

Survival rates of adult and juvenile gyrfalcons in Iceland: estimates and drivers.

Knowledge of survival rates and their potential covariation with environmental drivers, for both adults and juveniles, is paramount to forecast the population dynamics of long-lived animals. Long-lived bird and mammal populations are indeed very sensitive to change in survival rates, especially that of adults. Here we report the first survival estimates for the Icelandic gyrfalcon (Falco rusticolus) obtained by capture-mark-recapture methods. We use a mark-recapture-recovery model combining live and dead encounters into a unified analysis, in a Bayesian framework. Annual survival was estimated at 0.83 for adults and 0.40 for juveniles. Positive effects of main prey density on juvenile survival (5% increase in survival from min to max density) were possible though not likely. Weather effects on juvenile survival were even less likely. The variability in observed lifespan suggests that adult birds could suffer from human-induced alteration of survival rates.

Primers to highly conserved elements optimized for qPCR-based telomere length measurement in vertebrates.

Telomere length dynamics are an established biomarker of health and ageing in animals. The study of telomeres in numerous species has been facilitated by methods to measure telomere length by real-time quantitative PCR (qPCR). In this method, telomere length is determined by quantifying the amount of telomeric DNA repeats in a sample and normalizing this to the total amount of genomic DNA. This normalization requires the development of genomic reference primers suitable for qPCR, which remains challenging in nonmodel organism with genomes that have not been sequenced. Here we report reference primers that can be used in qPCR to measure telomere lengths in any vertebrate species. We designed primer pairs to amplify genetic elements that are highly conserved between evolutionarily distant taxa and tested them in species that span the vertebrate tree of life. We report five primer pairs that meet the specificity and reproducibility standards of qPCR. In addition, we demonstrate an approach to choose the best primers for a given species by testing the primers on multiple individuals within a species and then applying an established computational tool. These reference primers can facilitate qPCR-based telomere length measurements in any vertebrate species of ecological or economic interest.

Correction to: Status and trends of circumpolar peregrine falcon and gyrfalcon populations.

While collating contributions and comments from 36 researchers, the coordinating authors accidentally omitted Dr. Suzanne Carrière from the list of contributing co-authors. Dr. Carrière's data are described in Tables 1 and 3, Figure 2 and several places in the narrative.The new author list is thus updated in this article.

Circumpolar status of Arctic ptarmigan: Population dynamics and trends.

Rock ptarmigan (Lagopus muta) and willow ptarmigan (L. lagopus) are Arctic birds with a circumpolar distribution but there is limited knowledge about their status and trends across their circumpolar distribution. Here, we compiled information from 90 ptarmigan study sites from 7 Arctic countries, where almost half of the sites are still monitored. Rock ptarmigan showed an overall negative trend on Iceland and Greenland, while Svalbard and Newfoundland had positive trends, and no significant trends in Alaska. For willow ptarmigan, there was a negative trend in mid-Sweden and eastern Russia, while northern Fennoscandia, North America and Newfoundland had no significant trends. Both species displayed some periods with population cycles (short 3-6 years and long 9-12 years), but cyclicity changed through time for both species. We propose that simple, cost-efficient systematic surveys that capture the main feature of ptarmigan population dynamics can form the basis for citizen science efforts in order to fill knowledge gaps for the many regions that lack systematic ptarmigan monitoring programs.

Status and trends of circumpolar peregrine falcon and gyrfalcon populations.

The peregrine falcon (Falco peregrinus) and the gyrfalcon (Falco rusticolus) are top avian predators of Arctic ecosystems. Although existing monitoring efforts are well established for both species, collaboration of activities among Arctic scientists actively involved in research of large falcons in the Nearctic and Palearctic has been poorly coordinated. Here we provide the first overview of Arctic falcon monitoring sites, present trends for long-term occupancy and productivity, and summarize information describing abundance, distribution, phenology, and health of the two species. We summarize data for 24 falcon monitoring sites across the Arctic, and identify gaps in coverage for eastern Russia, the Arctic Archipelago of Canada, and East Greenland. Our results indicate that peregrine falcon and gyrfalcon populations are generally stable, and assuming that these patterns hold beyond the temporal and spatial extents of the monitoring sites, it is reasonable to suggest that breeding populations at broader scales are similarly stable. We have highlighted several challenges that preclude direct comparisons of Focal Ecosystem Components (FEC) attributes among monitoring sites, and we acknowledge that methodological problems cannot be corrected retrospectively, but could be accounted for in future monitoring. Despite these drawbacks, ample opportunity exists to establish a coordinated monitoring program for Arctic-nesting raptor species that supports CBMP goals.

Quill mite infestation of rock ptarmigan Lagopus muta (Aves: Phasianidae) in relation to year and host age, sex, body condition, and density.

A total of 1209 ptarmigan were examined for Mironovia lagopus, including 721 juvenile birds (ca. 3 months old) and 488 adult birds (15 months or older). A total of 88 birds or 7.3% (n = 1209, 95% cl 5.9-8.9%) were infested with M. lagopus. There was an age difference in prevalence of infection, and more adults (10.7%, n = 488, 95% cl 8.2-13.7%) than juveniles (5.0%, n = 721, 95% cl 3.6-6.8%) were infested. There was a significant age effect in the mean intensity index, and adult birds had more advanced infestations compared with juvenile birds. There were no significant changes in either the interannual prevalence of infection or the mean intensity index of infection. Of the feather types inspected, there was no age-related difference in selection of feathers, nor was there any preference of mites for any one of the inspected feather types. Body dispersants were all adult females. There was an age-related difference in mean intensities of infection of body dispersants; it was higher in adult birds. The methods used to determine presence or absence of M. lagopus were not 100% accurate especially for juvenile hosts, and this at least partly explains the difference in prevalence among age groups. There was no relationship between host body condition or host density and infection by M. lagopus.

Predator-prey feedback in a gyrfalcon-ptarmigan system?

Specialist predators with oscillating dynamics are often strongly affected by the population dynamics of their prey, yet they are not always the cause of prey cycling. Only those that exert strong (delayed) regulation of their prey can be. Inferring predator-prey coupling from time series therefore requires contrasting models with top-down versus bottom-up predator-prey dynamics. We study here the joint dynamics of population densities of the Icelandic gyrfalcon Falco rusticolus, and its prey, the rock ptarmigan Lagopus muta. The dynamics of both species are likely not only linked to each other but also to stochastic weather variables acting as confounding factors. We infer the degree of coupling between populations, as well as forcing by abiotic variables, using multivariate autoregressive models MAR(p), with p = 1 and 2 time lags. MAR(2) models, allowing for species to cycle independently from each other, further suggest alternative scenarios where a cyclic prey influences its predator but not the other way around (i.e., bottom-up scenarios). The classical MAR(1) model predicts that the time series exhibit predator-prey feedback (i.e., reciprocal dynamic influence between prey and predator), and that weather effects are weak and only affecting the gyrfalcon population. Bottom-up MAR(2) models produced a better fit but less realistic cross-correlation patterns. Simulations of MAR(1) and MAR(2) models further demonstrate that the top-down MAR(1) models are more likely to be misidentified as bottom-up dynamics than vice versa. We therefore conclude that predator-prey feedback in the gyrfalcon-ptarmigan system is likely the main cause of observed oscillations, though bottom-up dynamics cannot yet be excluded with certainty. Overall, we showed how to make more out of ecological time series by using simulations to gauge the quality of model identification, and paved the way for more mechanistic modeling of this system by narrowing the set of important biotic and abiotic drivers.

Gyrfalcons Falco rusticolus adjust CTNS expression to food abundance: a possible contribution to cysteine homeostasis.

Melanins form the basis of animal pigmentation. When the sulphurated form of melanin, termed pheomelanin, is synthesized, the sulfhydryl group of cysteine is incorporated to the pigment structure. This may constrain physiological performance because it consumes the most important intracellular antioxidant (i.e., glutathione, GSH), of which cysteine is a constitutive amino acid. However, this may also help avoid excess cysteine, which is toxic. Pheomelanin synthesis is regulated by several genes, some of them exerting this regulation by controlling the transport of cysteine in melanocytes. We investigated the possibility that these genes are epigenetically labile regarding protein intake and thus contribute to cysteine homeostasis. We found in the Icelandic population of gyrfalcon Falco rusticolus, a species that pigments its plumage with pheomelanin, that the expression of a gene regulating the export of cystine out of melanosomes (CTNS) in feather melanocytes of developing nestlings increases with food abundance in the breeding territories where they were reared. The expression of other genes regulating pheomelanin synthesis by different mechanisms of influence on cysteine availability (Slc7a11 and Slc45a2) or by other processes (MC1R and AGRP) was not affected by food abundance. As the gyrfalcon is a strict carnivore and variation in food abundance mainly reflects variation in protein intake, we suggest that epigenetic lability in CTNS has evolved in some species because of its potential benefits contributing to cysteine homeostasis. Potential applications of our results should now be investigated in the context of renal failure and other disorders associated with cystinosis caused by CTNS dysfunction.

Host-Parasite Interactions and Population Dynamics of Rock Ptarmigan.

Populations of rock ptarmigan (Lagopus muta) in Iceland fluctuate in multiannual cycles with peak numbers c. every 10 years. We studied the ptarmigan-parasite community and how parasites relate to ptarmigan age, body condition, and population density. We collected 632 ptarmigan in northeast Iceland in early October from 2006 to 2012; 630 (99.7%) were infected with at least one parasite species, 616 (98%) with ectoparasites, and 536 (85%) with endoparasites. We analysed indices for the combined parasite community (16 species) and known pathogenic parasites, two coccidian protozoans Eimeria muta and Eimeria rjupa, two nematodes Capillaria caudinflata and Trichostrongylus tenuis, one chewing louse Amyrsidea lagopi, and one skin mite Metamicrolichus islandicus. Juveniles overall had more ectoparasites than adults, but endoparasite levels were similar in both groups. Ptarmigan population density was associated with endoparasites, and in particular prevalence of the coccidian parasite Eimeria muta. Annual aggregation level of this eimerid fluctuated inversely with prevalence, with lows at prevalence peak and vice versa. Both prevalence and aggregation of E. muta tracked ptarmigan population density with a 1.5 year time lag. The time lag could be explained by the host specificity of this eimerid, host density dependent shedding of oocysts, and their persistence in the environment from one year to the next. Ptarmigan body condition was negatively associated with E. muta prevalence, an indication of their pathogenicity, and this eimerid was also positively associated with ptarmigan mortality and marginally inversely with fecundity. There were also significant associations between fecundity and chewing louse Amyrsidea lagopi prevalence (negative), excess juvenile mortality and nematode Capillaria caudinflata prevalence (positive), and adult mortality and skin mite Metamicrolichus islandicus prevalence (negative). Though this study is correlational, it provides strong evidence that E. muta through time-lag in prevalence with respect to host population size and by showing significant relations with host body condition, mortality, and fecundity could destabilize ptarmigan population dynamics in Iceland.

Morphological characteristics of Mesocestoides canislagopodis (Krabbe 1865) tetrathyridia found in rock ptarmigan (Lagopus muta) in Iceland.

Necropsies of 1010 rock ptarmigans (Lagopus muta) sampled in autumn 2006-2015 in northeast Iceland revealed Mesocestoides canislagopodis tetrathyridia infections in six birds (0.6 %), two juvenile birds (3 month old), and four adult birds (15 months or older). Four birds had tetrathyridia in the body cavity, one bird in the liver, and one bird both in the body cavity and the liver. There were more tetrathyridia in the body cavity of the two juveniles (c. 50 in each) than in three adults (10-40), possibly indicating a host-age-related tetrathyridia mortality. Approximately, half of tetrathyridia in the body cavity were free or loosely attached to the serosa, the other half were encapsulated in a thin, loose connective tissue stroma, frequently attached to the lungs and the liver. Tetrathyridia in the liver parenchyma incited variably intense inflammation. Tetrathyridia from the juvenile hosts were whitish, heart-shaped, and flattened, with unsegmented bodies with a slightly pointed posterior end. In the adult hosts, tetrathyridia were sometimes almost rectangular-shaped, slightly wider compared to those in the juveniles, but more than twice as long as the younger-aged tetrathyridia. Tetrathyridia infections are most likely acquired during the brief insectivorous feeding phase of ptarmigan chicks, and the tetrathyridia persist throughout the lifespan of the birds.

Occurrence of Mesocestoides canislagopodis (Rudolphi, 1810) (Krabbe, 1865) in mammals and birds in Iceland and its molecular discrimination within the Mesocestoides species complex.

The life cycle of Mesocestoides tapeworms (Cestoda: Cyclophyllidea: Mesocestoididae) requires three hosts. The first intermediate host is unknown but believed to be an arthropod. The second intermediate host is a vertebrate. The primary definitive host is a carnivore mammal, or a bird of prey, that eats the tetrathyridium-infected second intermediate host. One representative of the genus, Mesocestoides canislagopodis, has been reported from Iceland. It is common in the arctic fox (Vulpes lagopus) and has also been detected in domestic dogs (Canis familiaris) and cats (Felis domestica). Recently, scolices of a non-maturing Mesocestoides sp. have also been detected in gyrfalcon (Falco rusticolus) intestines, and tetrathyridia in the body cavity of rock ptarmigan (Lagopus muta). We examined the taxonomic relationship of Mesocestoides from arctic fox, gyrfalcon, and rock ptarmigan using molecular methods, both at the generic level (D1 domain LSU ribosomal DNA) and at the specific level (cytochrome c oxidase subunit I (COI) and 12S mitochondrial DNA). All stages belonged to Mesocestoides canislagopodis. Phylogenetic analysis of the combined 12S-COI at the specific level confirmed that M. canislagopodis forms a distinct clade, well separated from three other recognized representatives of the genus, M. litteratus, M. lineatus, and M. corti/vogae. This is the first molecular description of this species. The rock ptarmigan is a new second intermediate host record, and the gyrfalcon a new primary definitive host record. However, the adult stage seemed not to be able to mature in the gyrfalcon, and successful development is probably restricted to mammalian hosts.

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.

The Parasite Fauna of the Gyrfalcon (Falco rusticolus) in Iceland.

We examined 46 Gyrfalcon (Falco rusticolus) carcasses from Iceland for parasites, including 29 first-year birds and 17 second-year birds and older. Endoparasites observed were the trematodes Cryptocotyle lingua (prevalence 8%), Cryptocotyle concavum (4%), and Strigea sp. (8%); the cestode Mesocestoides sp. (27%); and the nematodes Eucoleus contortus (76%) and Serratospiculum guttatum (7%). Ectoparasites included the astigmatan mite Dubininia accipitrina (47%), a mesostigmatan rhynonyssid mite (4%), the tick Ixodes caledonicus (20%), the mallophagans Degeeriella rufa (90%) and Nosopon lucidum (7%), the flea Ceratophyllus vagabundus (7%), and the louse fly Ornithomya chloropus (7%). Cryptocotyle lingua, C. concavum, S. guttatum, D. accipitrina, I. caledonicus, and N. lucidum are new host records. Of the five most common parasites (prevalence ≥ 20%) only Mesocestoides sp. showed a significant age relationship, being more prevalent in adult falcons (P = 0.021). Eucoleus contortus was also more prevalent in adults with marginal statistical significance (P = 0.058). Frounce, caused by E. contortus (possibly also by Trichomonas gallinae, which was not searched for in the survey) was highly prevalent (43%), but did not show a relationship with host age (P = 0.210). Birds with frounce were in poorer body condition than healthy birds (P = 0.015).

Feather mites (Astigmata: Psoroptidia) parasitising the rock ptarmigan Lagopus muta (Montin) (Aves: Galliformes) in Iceland.

Four new species of feather mites are described from the Icelandic rock ptarmigan Lagopus muta islandorum (Faber) in Iceland. These are Metamicrolichus islandicus n. sp., Myialges borealis n. sp. (Epidermoptidae), Strelkoviacarus holoaspis n. sp. (Analgidae) and Tetraolichus lagopi n. sp. (Pterolichidae). This is the first report on feather mites associated with the Icelandic rock ptarmigan. Brief comments on the systematics and biology of corresponding feather mite genera are given. For two species, originally described in Pterolichus Robin, 1868 (Pterolichidae), new combinations are proposed, i.e. Tetraolichus gaudi (Cerný, 1971) n. comb. and T. microdiscus (Trouessart, 1887) n. comb.