Evidence of alphaherpesvirus infections in Alaskan caribou and reindeer

Background  

The reindeer (Rangifer tarandus tarandus) industry in Alaska began with animals imported from Siberia (Russia) in the 1890's. Cervid herpes virus 2 (CvHV2) is endemic in reindeer in Scandinavia. We sought to determine if the same virus, or similar herpesviruses, were circulating in Alaskan reindeer and caribou (Rangifer tarandus granti). Serum samples from 292 reindeer were collected during annual reindeer handlings (1988-2005) near Nome, Alaska. In 2005, swab samples were collected from 40 calves from this herd, near Nome, Alaska. In 2007, ocular and nasal swab samples were collected from 30 apparently healthy reindeer calves near Wales, Alaska. Samples of plasma and white blood cells were collected from three Alaskan caribou herds, Mulchatna (n = 24), Teshekpuk (n = 34) and the Western Arctic (n = 87) in 2009.     

Preliminary studies on the etiology of keratoconjunctivitis in reindeer (Rangifer tarandus tarandus) calves in Alaska

Keratoconjunctivitis outbreaks occur each summer in reindeer (Rangifer tarandus tarandus) herds in western Alaska, USA. This condition has not been well characterized nor has a definitive primary etiologic agent been identified. We evaluated the eyes of 660 calves near Nome, Alaska, between 29 June and 14 July 2005. Clinical signs of keratoconjunctivitis were observed in 26/660 calves (3.9%). Samples were collected from the conjunctival sac of both affected (n=22) and unaffected (n=24) animals for bacterial culture, enzyme-linked immunosorbent assay testing for Chlamydophila psittaci, and for polymerase chain reaction assays for Mycoplasma and Moraxella spp. No primary bacterial or viral etiologic agent(s) were isolated or identified. The cause of keratoconjunctivitis among reindeer calves was not determined, but it could involve an anaerobic bacteria, a difficult-to-isolate viral agent, stress associated with repeated handling, ocular foreign bodies, exposure to corral dust or arthropods, or a combination.     

Variation of plasma protein parameters in four free-ranging reindeer herds and in captive reindeer under defined feeding conditions

Plasma total protein (TP), albumin (ALB) and globulin (GLOB) concentrations and albumin/globulin ratio (A/G) were analysed from blood samples collected from free-ranging reindeer (Rangifer tarandus tarandus) herds at varying times of year. The same parameters were followed in nine captive reindeer with varying protein and energy intake. Variation in the blood constituents of free-ranging reindeer was analysed in relation to different extrinsic and intrinsic factors and compared to findings from captive animals, allowing the analysis of effects of protein and energy intake. There was large overall variation in TP, ALB, GLOB and A/G ratio in the free-ranging animals, ranging between 36-110 g/L, 18-59 g/L, 17-59 g/L and 0.5-2.1. The variation between months and years was significant for all variables except the A/G ratio, where no year effect was noted. Increase in live body mass was associated with a small significant increase and pregnancy with a small significant decrease in all dependent variables, except for the A/G ratio. Age did not have a significant effect on any of the blood constituents when body mass was included in the same model. In captive animals, feeding lichens with low protein content was related to a significant decline in TP, ALB and GLOB, but not in the A/G ratio, whereas feeding commercial ration increased plasma TP, ALB and GLOB significantly. Extrinsic factors such as season and year explained majority of variation in the blood constituents of free-ranging reindeer, whereas body mass, pregnancy and age had only a minor influence. It is concluded that plasma TP and ALB, and to a lesser extent GLOB and A/G ratio may serve as nutritional biomarkers of reindeer.     

An epizootic of besnoitiosis in captive caribou (Rangifer tarandus caribou), reindeer (Rangifer tarandus tarandus) and mule deer (Odocoileus hemionus hemionus)

Besnoitia sp. was diagnosed in two caribou (Rangifer tarandus caribou) which died of pneumonia at the Assiniboine Park Zoo (Winnipeg, Manitoba, Canada) in 1983. During the following 3 yr besnoitiosis spread to an isolated herd of caribou, to mule deer (Odocoileus hemionus hemionus) and to reindeer (Rangifer tarandus tarandus). Reduction of exposure to biting insects appears to have reduced the transmission of besnoitiosis within the reindeer herd. The morbidity rate was approximately 82% in caribou and 67% in mule deer over the age of 2 mo. Most animals with clinical signs were euthanized; this precluded an estimation of the disease-related mortality rate. Twenty-eight caribou, 10 mule deer and three reindeer have been euthanized or died as a result of this epidemic. Attempts to artificially transmit the disease to potentially susceptible intermediate and definitive hosts were unsuccessful.     

Genetic variation in caribou and reindeer (Rangifer tarandus)

Genetic variation at seven microsatellite DNA loci was quantified in 19 herds of wild caribou and domestic reindeer (Rangifer tarandus) from North America, Scandinavia and Russia. There is an average of 2.0-6.6 alleles per locus and observed individual heterozygosity of 0.33-0.50 in most herds. A herd on Svalbard Island, Scandinavia, is an exception, with relatively few alleles and low heterozygosity. The Central Arctic, Western Arctic and Porcupine River caribou herds in Alaska have similar allele frequencies and comprise one breeding population. Domestic reindeer in Alaska originated from transplants from Siberia, Russia, more than 100 years ago. Reindeer in Alaska and Siberia have different allele frequencies at several loci, but a relatively low level of genetic differentiation. Wild caribou and domestic reindeer in Alaska have significantly different allele frequencies at the seven loci, indicating that gene flow between reindeer and caribou in Alaska has been limited.     

Induced orphaning reveals post-weaning maternal care in reindeer

A common by-product of human harvesting is orphaning of calves in autumn. Despite this, there are few studies in northern and temperate ungulates evaluating the fate of orphaned calves and the potential benefits to offspring and costs to mothers of post-weaning maternal care. We manipulated orphaning and forage distribution during winter for two herds of reindeer (Rangifer tarandus): one nonfed and the other supplementally fed to increase level of interference competition. Both herds consisted of females with and without calves at heel and orphaned calves. We measured survival and somatic losses during winter and distances between mother–calves and adult females–orphans within the herds. All females survived the winter, and there was no evidence of post-weaning maternal cost in terms of female’s mass loss. The winter mortality among calves was negligible and did not differ between orphans as compared to nonorphans. However, nonorphaned calves lost less mass and stayed closer to their mothers than orphans to adult females, suggesting that increased mortality might occur in harsher winters. This tended to be more marked in the fed group where interference competition was more likely due to feed being concentrated both in space and time. Reduced mass loss in nonorphans is therefore most likely due to mothers sharing and defending feeding resources and protecting their offspring from harassment by other herd members during their first winter. We conclude that hunting practise of northern and temperate ungulates where females having calf/calves at heel are intentionally or non-intentionally harvested, may have demographic side effects at least in harsh winters.     

Humoral immunity and output of first-stage larvae of Elaphostrongylus rangiferi (Nematoda, Metastrongyloidea) by infected reindeer, Rangifer tarandus tarandus

The use of an indirect immunofluorescence technique demonstrated that serum from reindeer, Rangifer tarandus tarandus, infected with Elaphostrongylus rangiferi (Nematoda, Metastrongyloidea) contained antibodies directed against antigen(s) on the cuticle of the parasites first-stage larvae (L1). Output of L1 from the male reindeer was low in the period June to August, but increased to a higher level during the rutting season (September to October). The titre of specific antibody showed an inverse pattern. In the female reindeer, larval output remained high throughout the sampling period from January to July. During this period antibody titre was low. A relationship between stress (rutting season or calving period), immunity and larval output is suggested.     

High genetic connectivity and introgression from domestic reindeer characterize northern Alaska caribou herds

Defining genetic populations and detecting hybridization with introduced or domestic taxa are two major concerns for the conservation of population-level diversity. We studied the genetic population structure of large, migratory caribou herds (Rangifer tarandus granti) on Alaska’s North Slope and their potential hybridization with introduced domestic reindeer (R. t. tarandus). Using a population genetics approach, we determined: (1) whether the four caribou herds could be differentiated; (2) how distance and population size appear to drive genetic population structure; and (3) how contact with reindeer has affected the genetic identity of herds. Samples from four caribou herds (n = 245) and reindeer (n = 67) were analyzed at 19 microsatellite loci. We found that North Slope caribou are isolated by distance, with no differentiation among herd pairs except for the most geographically distant herds (F _st  = 0.003, Jost’s D = 0.023; P-values < 0.001). We detected reindeer-caribou admixture in all populations except Kodiak Island, including 8 % of individuals in caribou herds and 14 % of individuals in Seward Peninsula reindeer herds. However, considering the stable or increasing trend in North Slope herds, reindeer introgression has had no apparent deleterious effect on herd demographics. Our findings indicate long-term genetic exchange among North Slope caribou herds when their ranges overlap, and suggest that herd size may influence susceptibility to reindeer introgression. As North Slope herd ranges are increasingly altered by industrial development, this study can provide a baseline for detecting potential future impacts to what are currently large, diverse, and naturally evolving herds.     

Obligate larval inhibition of Ostertagia gruehneri in Rangifer tarandus? Causes and consequences in an Arctic system

SUMMARY Larval inhibition is a common strategy of Trichostrongylidae nematodes that may increase survival of larvae during unfavourable periods and concentrate egg production when conditions are favourable for development and transmission. We investigated the propensity for larval inhibition in a population of Ostertagia gruehneri, the most common gastrointestinal Trichostrongylidae nematode of Rangifer tarandus. Initial experimental infections of 4 reindeer with O. gruehneri sourced from the Bathurst caribou herd in Arctic Canada suggested that the propensity for larval inhibition was 100%. In the summer of 2009 we infected 12 additional reindeer with the F1 and F2 generations of O. gruehneri sourced from the previously infected reindeer to further investigate the propensity of larval inhibition. The reindeer were divided into 2 groups and half were infected before the summer solstice (17 June) and half were infected after the solstice (16 July). Reindeer did not shed eggs until March 2010, i.e. 8 and 9 months post-infection. These results suggest obligate larval inhibition for at least 1 population of O. gruehneri, a phenomenon that has not been conclusively shown for any other trichostrongylid species. Obligate inhibition is likely to be an adaptation to both the Arctic environment and to a migratory host and may influence the ability of O. gruehneri to adapt to climate change.     

Growth and condition of three introduced reindeer herds on South Georgia: the effects of diet and density

The patterns of growth and seasonal changes in body weight and fat reserves of three herds of introduced reindeer on the sub-Antarctic island of South Georgia were investigated. Two of the herds, derived from the same stock, were at different densities but the higher density herd was on the better range. In this herd there was a significant growth advantage to the male reindeer, but not to females. The third herd, of a different stock, was also at a lower density on a range which had become overgrazed. The two lower-density herds showed the same annual changes in body weight and only slight differences in the fluctuation of their fat reserves. In addition, body weights in both these herds fluctuated to the same degree as those of a barren-ground caribou in the Northern Hemisphere but fluctuations in the fat reserves of South Georgia reindeer were considerably more severe. The results suggest that the South Georgia reindeer herds are limited by forage availability.     

No evidence of inbreeding avoidance in a polygynous ungulate: the reindeer (Rangifer tarandus)

In polygynous species, mate choice is an integrated part of sexual selection. However, whether mate choice occurs independently of the genetic relatedness among mating pairs has received little attention, although inbreeding may have fitness consequences. We studied whether genetic relatedness influenced females' choice of partner in a highly polygynous ungulate--the reindeer (Rangifer tarandus)--in an experimental herd during two consecutive rutting seasons; the herd consisting of 75 females in 1999 and 74 females in 2000 was exposed to three 4.5-year-old adults and three 1.5-year-old young males, respectively. The females' distribution during peak rut was not influenced by their genetic relatedness with the dominant males of the mating groups. Further, genetic relatedness did not influence the actual choice of mating partner. We conclude that inbreeding avoidance through mating group choice as well as choice of mating partner, two interconnected processes of female mate choice operating at two different scales in space and time, in such a highly female-biased reindeer populations with low level of inbreeding may not occur.     

Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter.

Living in the high Arctic, the Svalbard reindeer (Rangifer tarandus platyrhynchus) and its trichostrongyle nematodes experience a long cold winter from October to late May/early June. Over this period, transmission would be expected to be low. However, in culled reindeer the abundance of infection increased from autumn to late winter, providing evidence for continued transmission within this period. To our knowledge this is the first time this has been demonstrated in a climate with temperatures consistently below 0 degrees C. In one winter (1996-1997), the average fraction of nematodes found as larvae in the abomasal mucosa increased from around 10% to 50% between October and March. This suggests that arrested development took place throughout the winter. We found no evidence for an efficient acquired immune response towards the nematodes. The abundance of infection did not tend to decrease with increasing host age after an earlier peak, but levelled off instead, as predicted by a simple immigration-death model. In the late winter when the nutritional plane is low, both adult reindeer and calves had high worm burdens at intensities that may affect their condition and fitness.     

High Female Mortality Resulting in Herd Collapse in Free-Ranging Domesticated Reindeer (Rangifer tarandus tarandus) in Sweden

Reindeer herding in Sweden is a form of pastoralism practised by the indigenous Sámi population. The economy is mainly based on meat production. Herd size is generally regulated by harvest in order not to overuse grazing ranges and keep a productive herd. Nonetheless, herd growth and room for harvest is currently small in many areas. Negative herd growth and low harvest rate were observed in one of two herds in a reindeer herding community in Central Sweden. The herds (A and B) used the same ranges from April until the autumn gathering in October–December, but were separated on different ranges over winter. Analyses of capture-recapture for 723 adult female reindeer over five years (2007–2012) revealed high annual losses (7.1% and 18.4%, for herd A and B respectively). A continuing decline in the total reindeer number in herd B demonstrated an inability to maintain the herd size in spite of a very small harvest. An estimated breakpoint for when herd size cannot be kept stable confirmed that the observed female mortality rate in herd B represented a state of herd collapse. Lower calving success in herd B compared to A indicated differences in winter foraging conditions. However, we found only minor differences in animal body condition between the herds in autumn. We found no evidence that a lower autumn body mass generally increased the risk for a female of dying from one autumn to the next. We conclude that the prime driver of the on-going collapse of herd B is not high animal density or poor body condition. Accidents or disease seem unlikely as major causes of mortality. Predation, primarily by lynx and wolverine, appears to be the most plausible reason for the high female mortality and state of collapse in the studied reindeer herding community.     

Seasonal cycles in the output of first stage larvae of the nematode Elaphostrongylus rangiferi from reindeer,Rangifer tarandus tarandus

Summary The output of first stage larvae of the neurotrophic nematode Elaphostrongylus rangiferi was studied both in a herd of reindeer in the field and in reindeer held in captivity. There was a marked seasonal cycle in the output of larvae from infected reindeer. This seasonal cycle is dependent on host sex. After an initial phase of logarithmic increase from the onset of patency in late winter/spring, the larval output declines to a minimum in summer in both female and male reindeer. From then onwards a yearly cycle is repeated with a maximum density of larvae in autumn/early winter from male reindeer, and in late winter/spring from female reindeer. E. rangiferi has an adult longevity of several years in the reindeer, and it is probable that the seasonal cycle of parasite output is linked to seasonal changes in the degree of host stress.     

Demographics in an alpine reindeer herd: effects of density and winter weather

We examined how population density, winter weather, snow conditions, and 2 large-scale climatic indices (North Atlantic Oscillation, NAO, and Arctic Oscillation, AO) influenced demography (reproduction and mortality) in an alpine herd of semi-domesticated reindeer Rangifer tarandus between 1959 and 2000 in Finnish Lapland. The herd lived on heavily grazed lichen pastures, with winter densities between 0.8 and 3.9 individuals km⁻². Icing conditions occurred every 7th yr, on an average, and decreased reproductive rate (calves/females) by 49%. In general linear models icing remarkably increased the fit of snow models to reproductive rate. Incorporation of an interaction term between icing and the snow depth index provided better fit than a model without interaction. Delayed snowmelt decreased reproductive rate. For the day of snowmelt, however, the model without interaction was better than the interaction model. These 3 models provided the best fit to the data and accounted for 51–54% of the variation in reproductive rate. Winter mortality was related to density and large-scale climatic indices, but not to local winter weather except a slight increase in mortality during an icing winter. The best model for winter mortality, including reindeer density and NAO, accounted for 26% of variation in mortality. Three factors may be involved explaining weak density dependence or the lack of such dependence; climate change scenarios that predict higher winter temperature, more frequent thawing-freezing periods, and deeper snow would be expected to decrease reproductive rate and increase winter mortality of reindeer and thus to reduce profitability of reindeer husbandry. In contrast, early springs would be advantageous for reindeer in the short term.     

Pastoral Herding Strategies and Governmental Management Objectives: Predation Compensation as a Risk Buffering Strategy in the Saami Reindeer Husbandry

Previously it has been found that an important risk buffering strategy in the Saami reindeer husbandry in Norway is the accumulation of large herds of reindeer as this increases long-term household viability. Nevertheless, few studies have investigated how official policies, such as economic compensation for livestock losses, can influence pastoral strategies. This study investigated the effect of received predation compensation on individual husbandry units’ future herd size. The main finding in this study is that predation compensation had a positive effect on husbandry units’ future herd size. The effect of predation compensation, however, was nonlinear in some years, indicating that predation compensation had a positive effect on future herd size only up to a certain threshold whereby adding additional predation compensation had little effect on future herd size. More importantly, the effect of predation compensation was positive after controlling for reindeer density, indicating that for a given reindeer density husbandry units receiving more predation compensation performed better (measured as the size of future herds) compared to husbandry units receiving less compensation.     

Experimental trichinellosis in reindeer

Six female reindeer calves were inoculated intraruminally with various doses of Trichinella muscle larvae. Four calves were inoculated with T. nativa, receiving 15,000 (n = 1), 5,000 (1), and 2,500 (2) larvae each. Two calves were inoculated with 5,000 T. spiralis larvae each. Blood samples were collected twice per week for total white blood cell (WBC) and differential counts and for serology using enzyme-linked immunosorbent assay (ELISA) based on T. spiralis excretory-secretory antigen. On day 56, the calves were slaughtered and muscle samples were examined according to the standard digestion method for Trichinella larvae. Blood samples were also collected twice a week from 4 uninoculated, but otherwise similar, reindeer calves corralled separately. Both the total WBC and eosinophil counts of the inoculated animals were, on average, higher during the experimental period. All the inoculated calves seroconverted, showing an increase in the optical density (OD) in the ELISA starting between day 23 and day 27 postinoculation. Very few muscle larvae (<0.08 larvae/g [lpg]) were to be found from the animals inoculated with T. nativa, but about 4 and 6 lpg were recovered from the masseter muscles of those inoculated with T. spiralis.     

Variation in the load of the horn fly, Haematobia irritans, in cattle herds is determined by the presence or absence of individual heifers

The distribution of horn flies, Haematobia irritans (L.) (Diptera: Muscidae), in herds of Danish Holstein-Friesian cattle was investigated in two studies conducted during two field seasons. In the first study, highly significant differences in fly distribution between the most and the least fly-susceptible heifers were observed. In one herd, the mean difference between the most fly-susceptible and the most fly-resistant heifers was 268 Ha. irritans specimens. The highest ratio between upper and lower mean fly number was 64.1:1, whereas the lowest was 3.1:1. In the second year, it was demonstrated that the heifers kept their rank in fly attraction over time. The trial clearly demonstrated that some heifers were attracting flies, whereas others, even in the same herd, only carried a few. In the second study, heifers were moved in and out of herds in an attempt to manipulate fly loads in the herds. In year 1, one herd (herd A) received four fly-resistant heifers from another herd (herd B), resulting in a drop in the mean number of flies, whereas herd B received four fly-susceptible heifers from herd A, resulting in an elevation of the mean number of flies. In year 2, a similar pattern emerged using herds C and D, and when the cattle were later returned to their original herds, the fly loads returned to their original distribution. The data presented here show unequivocally that, for horn flies, there can be considerable differences in fly loads for individual heifers within the Holstein-Friesian breed. Furthermore, the overall fly load within herds can be manipulated, and can be reversed. Thus, the distribution in the number of flies within a herd appears to depend on the number of fly-resistant or fly-susceptible heifers. The possible role of chemical factors emitted by heifers, i.e. volatile semiochemicals, in determining differences in fly loads is discussed, whereby attractants are emitted by fly-susceptible heifers and enable flies to locate their host, and repellents are emitted by fly-resistant heifers such that the flies are actively repelled from the herd.     

Genetic variation in domestic reindeer and wild caribou in Alaska

Reindeer ( Rangifer tarandus tarandus ) were introduced into Alaska 100 years ago and have been maintained as semidomestic livestock. They have had contact with wild caribou ( R. t. granti ) herds, including deliberate crossbreeding and mixing in the wild. Reindeer have considerable potential as a domestic animal for meat or velvet antler production, and wild caribou are important to subsistence and sport hunters. Our objective was to quantify the genetic relationships of reindeer and caribou in Alaska. We identified allelic variation among five herds of wild caribou and three herds of reindeer with DNA sequencing and restriction enzymes for three loci: a DQA locus of the major histocompatibility complex ( Rata-DQA1 ), K-casein and the D-loop of mitochondrial DNA. These loci are of interest because of their potential influence on domestic animal performance and the fitness of wild populations. There is considerable genetic variation in reindeer and caribou for all three loci, including five, three and six alleles for DQA , K-casein and D-loop respectively. Most alleles occur in both reindeer and caribou, which may be the result of recent common ancestry or genetic introgression in either direction. However, allele frequencies differ considerably between reindeer and caribou, which suggests that gene flow has been limited.     

Predator-driven fragmentation of fiddler crab droves into selfish miniherds of biased composition

An explanation for animal groups is the selfish herd, characterized by aggregation as each member tries to shield itself from a predator by moving into a tight gap between other members. We test the hypotheses that: (1) droves, the large feeding groups of fiddler crabs, are selfish herds; (2) the miniherds that form when droves fragment on approach of a large predator are selfish herds; (3) selfish herds form when refugia are unlikely to be reached before an approaching predator arrives; and (4) the composition of selfish miniherds is biased toward individuals most vulnerable to predation. The study was conducted in South Carolina (USA) by videotaping the movements of sand fiddler crabs Uca pugilator when approached by a human predator. In both droves and miniherds, interindividual distance decreases with predator approach, consistent with behavior in a selfish herd. However, two other expectations for selfish herds—herd cohesion and sacrificing distance from the predator in order to get closer to other herders—are only met in miniherds. Crabs farther from refugia are more likely to form and remain in miniherds, indicating that selfish herding is only favored when refugia cannot be quickly reached. The composition of the smallest miniherds, consisting of 2-18 crabs, is biased toward females and small males. These individuals may be more vulnerable to predation because they lack the enlarged claw of large males that deters some predators. The small miniherds are relatively homogeneous with respect to the size and sex of their members, which may enhance cohesion and effectiveness as selfish herds. Miniherds will be effective selfish groups when predator attack has a significant vertical component and when the strike distance is large relative to both the size of the prey and the distance between group members. Droves are not selfish herds but permit crabs to flee feeding grounds as members of selfish miniherds.