High winter loads of Oestrid larvae and Elaphostrongylus rangiferi are associated with emaciation in wild reindeer calves.

The Oestrid flies Cephemyia trompe and Hypoderma tarandi and the nematode Elaphostrongylus rangiferi are important parasites of Rangifer spp. The larvae of Oestrid flies develop in the throat (C. trompe) and skin (H. tarandi) of their host during winter while E. rangiferi develop in the CNS. Oestrid pupation, and development of E. rangiferi larvae from first- (L1) to infective third- stage in the environment during summer are highly temperature dependent. We investigated the possible negative effects of these parasites on the winter body-condition of wild reindeer calves. Two year-classes (generations) of calf, born in a warm (2014) and cold (2015) summer respectively, were examined for changes in body condition between autumn and spring, in relation to the parasite load determined in the spring. The body condition in the autumn was assessed as carcass weight, while the body condition in the spring was assessed as carcass weight, supplemented by an evaluation of fat reserves in various bodily locations. Oestrids were counted directly whereas the E. rangiferi quantification was based on faecal counts of L1 larvae. The abundance of infections for Oestrids and E. rangiferi were significantly greater in the 2014 generation than in the 2015 generation. The mean carcass weight decreased between autumn and spring for the 2014 generation but increased in the 2015 generation. Emaciation in the spring was documented (fat reserve evaluation) in 42% and 7% of calves in the 2014 and 2015 cohorts, respectively. There was a significant correlation between high parasite load and the probability of emaciation. The mean summer temperature in 2014 was 2.6 °C higher than the mean for 2015, and 1.0 °C higher than the mean for the last 30-years. Our findings suggest that following a warm summer, high loads of Oestrids and E. rangiferi may cause emaciation and potentially deaths among the calves.

Introduction

The Norwegian wild tundra reindeer (Rangifer tarandus tarandus) populations live in a harsh environment in the mountain areas of southern Norway (Fig. 1). During a short summer, the reindeer must build up body reserves to survive a long winter on poor food resources (lichen) covered in snow. Wild reindeer also face challenges related to climate change and human disturbance in their habitats (decades of hunting have led to high wariness of humans). Human disturbance (e.g., hiking trails, cabins, roads) triggers evasive behavior, flock aggregation and reduced pasture utilization (Strand et al., 2006, 2010; Gundersen et al., 2020). Animal aggregation in smaller areas may also increase the infection pressure of important reindeer parasites, such as the Oestridae Cephenemyia trompe (throat bots) and Hypoderma tarandi (warbles) and the nematode Elaphostrongylus rangiferi (brain worm). These parasites develop in the reindeer during winter and may cause loss of body condition and neurological disorders (E. rangiferi), especially among calves (Roneus and Nordkvist, 1962; Skjenneberg and Slagsvold, 1968; Cuyler et al., 2012). The development of the larval stages of Oestrids and E. rangiferi in the environment requires extended periods of relatively high temperature (Halvorsen and Skorping, 1982; Nilssen, 2006) and in semi-domesticated reindeer flocks in subarctic northern Norway, summer temperature is considered a limiting factor for infection (Halvorsen et al., 1980; Nilssen and Haugerud, 1995). In these areas, outbreaks of clinical elaphostrongylosis occur in autumn and winter, following hot summers (Handeland and Slettbakk, 1994). Oestrid and E. rangiferi infections are common in the Norwegian wild reindeer populations (Nilssen and Haugerud, 1995; Handeland et al., 2019) but the clinical impact during winter and the severity of infection in relation to summer temperature have not been investigated.

Fig. 1

Map of southern Norway showing the location of the 24 Norwegian wild tundra reindeer populations. The Hardangervidda population (No. 16) is marked with brighter tan.

Cephenemyia trompe and H. tarandi are large flies that have obligatory larval development in Rangifer spp. Cephenemyia trompe eject first stage larvae (L1) towards the reindeer's nostrils (Anderson and Nilssen, 1990) whereupon the larvae enter the nasal cavities. Development to second (L2) and third (L3) larval stages takes place in the retro-pharynx in late winter and spring. Hypoderma tarandi lay eggs in the animal's coat and following hatching, L1 larvae penetrate the skin. Development to L2 and L3 stages takes place in the dorsal subcutis between late autumn and spring. Departure of Oestrid L3 from the host begins in late April (Nilssen and Haugerud, 1994). Pupation on the ground is dependent on temperatures of 10 °C or above (Nilssen, 2006). Oestrid flies (especially C. trompe) trigger reindeer flock aggregation and panic behaviour which reduces foraging and weight gain during summer (Skjenneberg and Slagsvold, 1968; Colman et al., 2003). It is also believed that the energy costs related to severe larval infections may lead to winter mortality (Skjenneberg and Slagsvold, 1968; Cuyler et al., 2012).

Reindeer with patent E. rangiferi infection shed L1 larvae in faeces and development to infective third stage larvae (L3), takes place in intermediate gastropod hosts (Mitsgevich, 1964; Skorping and Halvorsen, 1980). The temperature threshold for larval development in gastropods is 9–10 °C (Halvorsen and Skorping, 1982). Hosts become infected by ingestion of gastropods containing L3 larvae in late summer or autumn (Mitsgevich, 1964; Halvorsen et al., 1980). Adult development takes place within the CNS of the host and during this development, long-lasting neurological signs may occur (Handeland, 1994; Handeland et al., 1994). Generally, 3–6 months after infection the adult nematodes migrate to the skeletal muscles (Hemmingsen et al., 1993; Handeland, 1994), where eggs are deposited in blood vessels and passively transported to the lungs where the L1 larvae hatch. The pre-patent period is 3–5 months (Mitsgevich, 1964; Handeland et al., 1994) and patency of infection is several years (Halvorsen et al., 1985).

The objectives of this study were to investigate (a) the effect of Oestrid larvae and E. rangiferi on the winter body condition of two year-classes (generations) of wild reindeer calves, and (b) whether there was any connection between the parasite loads and temperatures during the preceding summers. The study was conducted in Norway's largest wild reindeer population, the Hardangervidda population (Fig. 1).

Materials and methods

Study population and summer pasture area

The study population of approx. 10,000 overwintering animals (Punsvik and Frøstrup, 2016) resides on the Hardangervidda mountain plateau (8130 km2). The calving period is in late May and early June and population control is achieved by targeted autumn hunting. Previously, there was an annual migration of the population from eastern wintering grounds to summer pastures in the west (see Fig. 2) in the spring (Skogland, 1994). Telemetry-studies of radio-collared females (Norwegian Institute for Nature Research) initiated in 2001 have revealed that the animals now remain within a relatively restricted area in the south during summer. This change in land use may be related to increased human traffic on the many hiking trails in the west (Strand et al., 2010; Gundersen et al., 2020). In the present study, we used GPS position data (n = 151,731) from 38 radio-collared females in the period 2001–2017 to determine the position, centre, and average altitude of the main summer pasture area (Fig. 2). The methods used are described in Handeland et al. (2019).

Fig. 2

Kernel Density Analysis, visualizing the main pasture area of radio-collared females in the wild reindeer population in Hardangervidda during June, July, and August 2001–2017. The darker the color, the larger number of GPS positions recorded. Calculated center at UTM 32V: 426706–6650377 and average altitude at 1283m. The center in the previously used summer area in the west (the mountain of Hårteigen) is marked with an asterisk. The red lines represent summer trails for hikers marked by the Norwegian Tourist Association. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Calves and body condition

Calves were collected during the autumn hunts of 2014 and 2015 (September 3-October 10), and extraordinary culls in the spring of 2015 and 2016 (March 30-April 17). Data relating to sex, carcass weight and date of harvest were recorded. The autumn sampling was carried out by selected hunters who collected heads and faecal samples from the calves. Cases lacking carcass weight data or with a registered teeth status incompatible with that of a calf were excluded. The spring culls were carried out by employees of the Norwegian Nature Inspectorate, after approval from the Norwegian Environment Agency. In addition to carcass weights, the body condition of the calves harvested in spring was evaluated on the basis of visually-evaluated and photo-documented fat reserves in five different bodily locations i.e. femur bone marrow (diaphysis), a knee joint, the vertebral canal, an orbital cavity and the surface of the heart. The fat reserves at each site were categorized into one of three categories: + clearly visible stiff, white fat; +÷ low amounts of soft fat, and ÷ complete absence of fat (serous adipose atrophy) (Fig. 3). Calves that scored +÷ or ÷ in four of the five bodily locations were defined as emaciated.

Fig. 3

Visualization of fat reserves in the bone marrow of femur (row 1), knee joint (row 2), vertebral canal (row 3), orbital cavity (row 4), and heart surface (row 5). The three categories used are illustrated from left to right: clearly visible white and stiff fat (+); low amounts of visible fat with a soft consistency (+÷); absence of visible fat (serous adipose atrophy) (÷). All figures are from wild reindeer calves killed on Hardangervidda in spring 2015, except for the heart to the bottom right which is from a moose that died from winter starvation.

Parasitological examinations

Cephenomyia trompe and Hypoderma tarandi

The nasal cavities of calves hunted in the autumns were exposed and the nasal mucosa inspected for the presence of C. trompe L1 larvae through a low power (5x) magnifying glass and the number of L1 larvae was counted semi-quantitatively (An accurate count would have required a complete and thorough examination of all nasal structures). The number of C. trompe larvae found in calves killed in the spring was counted after exposing the animals’ pharynx. Thereafter, the head was removed, cloven and the nose cavities inspected for larvae. For the calves examined in the spring of 2016, an additional washing of the nasal cavity and pharynx followed by filtering through a fine-mesh sieve was performed, to identify larvae overlooked on direct inspection. In some animals, C. trompe larvae were difficult to detect (and the number obviously underestimated) due to the presence of ruminal contents (following agonal regurgitation). The number of H. tarandi larvae in calves killed in the spring was counted in the visceral side of the skin.

Elaphostrongylus rangiferi

The studies of E. rangiferi included (a) microscopic examination for L1 larvae in the faeces of all calves collected, (b) macroscopical examination for adult nematodes in the CNS and skeletal muscles of the calves collected in spring, and (c) histological examination for the presence of E. rangiferi eggs in the lung tissue of the calves collected in spring.

The number of L1 larvae per gram (LPG) faeces was estimated, following a slightly modified Baermann technique (see Handeland et al., 2019). The larvae were confirmed as E. rangiferi by the presence of a dorsal spine on the tail and typical body length (Lancester and Northcott, 1979). Body length was measured for ten larvae per animal. The macroscopic examination for adult E. rangiferi in the CNS was carried out after exposing the brain case and brain meninges, the vertebral canal and spinal cord meninges. Examination for adult nematodes in the skeletal muscles was performed after exposing the fascial muscle surfaces. Histological examination for the presence of E. rangiferi eggs in the lungs was performed following standard procedures. Five lung tissue blocks per animal were fixed in a 10% buffered formalin, embedded in paraffin, sliced, and stained with haematoxylin and eosin.

Meteorological data

The mean daily summer (June–August) temperatures were calculated for the summers 2014 and 2015 and compared with the calculated summer temperatures for other years in the last 30-year-period (1989–2018). The calculations were based on interpolated long-term datasets from all weather stations in Norway (Lussana et al., 2019a, 2019b). These datasets have a 1 × 1km spatial resolution and a daily temporal resolution. Temperature was calculated as the mean temperature for several points in the terrain around the center of the main summer grazing area, adjusted to the average grazing altitude (1283m) (see p. 2.1 and Fig. 2).

Large amounts of snow and temperatures above freezing, which may compact the snow and cause pasture icing problems, can have a negative effect on the body condition in winter (Strand, 2008). To investigate any differences in the snow conditions between the two calf generations, the mean daily temperature and total amount of precipitation (snow) (December–March) were calculated for the winters 2014/15 and 2015/16 (precipitation data was based on in situ observations from Mogen hydrological station on Hardangervidda).

Statistical analyses

Carcass weights for each calf generation were compared between autumn and spring by a t-test. A wilcox-test was used to compare the intensity of Hypoderma and Cephenemyia larval infection (summed) in the two calf generations. Spring carcass weights were then analyzed in a regression analysis as a function of larval intensity. By this analysis, the sum of larvae in each calf was log-transformed to normalize the variance. We also compared carcass weights by testing a two-level parameter of larval infection, high versus less-than high, defining a high level as those calves with a total number of larvae above or equal to the 0.75 quantile. In addition, we used a logistic regression model to analyze the number of emaciated versus non-emaciated calves in the spring. This model was run as a function of year or log intensity of Hypoderma and Cephenemyia infection. The prevalences of E. rangiferi infection in 2015 and 2016 were compared by a logistic regression analysis while abundance of infection (a measure of the level of infection in all hosts, including non-infected individuals) was compared using a wilcox test. We also tested all regression models by including potential covariates (sex, Julian day) and compared the models by AIC (Burnham and Anderson, 2002). The potential covariates did not reduce the AIC-value of the basic regression and no significant effects were found. Statistical analyses were performed in R version 4.0.3 (R Core Team, 2020).

Results

Body condition

In total, 50 calves fulfilled the sampling criteria. The number, sex and carcass weights for calves examined in autumn and spring from each calf generation are given in Table 1. The table also shows the results of the fat score evaluation (see Fig. 3) for the calves examined in spring. Fat reserves on the heart appeared last to disappear, with all but one calf displaying intact (white and stiff) fat reserves on the heart surface. For the 2014 generation, there was no significant difference in carcass weight between autumn and spring (p = 0.60), while there was a tendency towards higher spring than autumn carcass weights in the 2015 generation (p = 0.13). The number and percentage of calves classified as emaciated was markedly higher (p = 0.06) in the spring of 2015 (42%), compared to spring 2016 (7%).

Table 1

Number, sex, and carcass weight (kg) of 50 wild reindeer calves from two different generations (2014, 2015) from Hardangervidda, Norway. The calves were examined in the autumn of the year of birth, and in spring of the following year. The table also shows the results of a fat score evaluation, used to classify the calves harvested in spring in either a fair, or emaciated, bodily condition.

Season	No.	Females	Males	Carcass weighta			Bodily condition
				Mean	Range	SD	Fair	Emaciated
Autumn 2014	12	6	6	13.4	10.2–19.0	2.3
Spring 2015	12	1	11	12.9	10.1–16.2	2.0	7	5
Autumn 2015	12b	1	10	11.8	6.5–16.0	2.5
Spring 2016	14	6	8	13.2	9.8–16.0	1.8	13	1

Live weight minus head, skin, viscera, blood and metapodials.

One calf was of unknown sex.

Parasitological findings

Cephenemyia trompe and Hypoderma tarandi

Eighty-three % (10/12) and 75% (9/12) of the calves shot during the autumn hunt in 2014 and 2015, respectively, displayed L1 larvae of C. trompe in the nasal mucosa (Fig. 4). The number of larvae was generally higher in the autumn of 2014, with six calves having >50 larvae, whereas all calves examined in the autumn of 2015 had <30 larvae.

Fig. 4

Translucent white first stage Cephenemyia trompe larvae (1 mm) in the nasal mucosa of a calf killed on Hardangervidda in autumn 2014.

All calves examined in the spring of 2015 and 2016 carried C. trompe larvae in the pharynx (Fig. 5) and H. tarandi larvae in the subcutis of the skin (Fig. 6). The results are summarized in Table 2. The intensity of Oestrid infection (both species together) was significantly higher in the spring of 2015, compared to spring 2016 (p = 0.02). There was a trend towards an association between increased Oestrid larval infection and low carcass weight (p = 0.09). The quarter of calves with the highest intensities of infection had significantly lower carcass weights (−1.7 kg (SE = 0.75), p = 0.03), compared to the calves with lower infection intensities. Similarly, the probability of an animal being classified as emaciated increased with the intensity of larval infection (p = 0.03): The average sum of larvae found in emaciated calves, versus calves with a fair body condition were 308 and 143, respectively.

Fig. 5

Cephenemyia trompe larvae in the pharynx/nasopharynx of a calf killed on Hardangervidda in spring 2015. Note the paired, swollen retropharyngeal lymph nodes (Ln).

Fig. 6

Photograph from the inside of the skin showing Hypoderma tarandi larvae removed from the lower part of the back of a calf killed on Hardangervidda in spring 2015.

Table 2

Oestrid larval findings in 26 wild reindeer calves from Hardangervidda, Norway. The calves belonged to two different generation (2014, 2015) and were examined in spring, the year after birth.

Season	No.	Hypoderma tarandi				Cephenemyia trompe
		Prevalence	Intensity of infection			Prevalence	Intensity of infection
			Mean	Range	SD		Mean	Range	SD
Spring 2015	12	100%	170	66–371	101	100%	64	25–196	47
Spring 2016	14	100%	119	21–422	135	100%	17a	1–48	13

32% of the C. trompe larvae found in spring 2016 were detected after rinsing with water. This complementary examination was not conducted in spring 2015.

As expected, none of the calves shot in the autumns of 2014 and 2015 excreted Elaphostrongylus L1 in faeces (calves normally do not develop patent infection until after the hunting season). The prevalence, intensity, and abundance of Elaphostrongylus larval faecal excretion in the calves killed in spring are shown in Table 3. The prevalence and abundance of infection were significantly higher (p = 0.003; p < 0.001) in the spring of 2015, compared to the spring of 2016. Histological examination of lung tissues from calves excreting E. rangiferi L1 larvae in faeces, revealed disseminated microgranulomas containing Elaphostrongylus eggs and hatching L1 larvae. Half of the calves displayed light-, and the remainder moderate to heavy- presences of microgranulomas. A massive and confluent presence of microgranulomas with extensive destruction of respiratory tissues was observed in the lungs of the most severely infected calf (Fig. 7).

Table 3

Results of examination for first stage larvae of Elaphostrongylus rangiferi in faeces (larvae per gram) in 26 wild reindeer calves from Hardangervidda, Norway. The calves belonged to two different generation (2014, 2015) and were examined in spring, the year after birth.

Season	No. examined	No. positive	Prevalence	Intensitya		Abundanceb
				Mean	Range	SD
Spring 2015	12	11	92%	347	24–1632	452	318
Spring 2016	14	3	21%	124	5–242	119	27

Number of larvae in infected individuals.

A measure of the mean level of infection in all hosts, including non-infected individuals.

Fig. 7

Verminous pneumonia in a calf killed on Hardangervidda in spring 2015. Numerous confluent granulomas containing Elaphostrongylus rangiferi eggs and hatched first stage larvae. Haematoxylin and eosin stain. Bar, 100 μm.

No adult Elaphostrongylus nematodes were detected in the CNS of any of the calves examined in spring, whereas 1–22 nematodes were successfully identified in the skeletal muscles (Fig. 8) of five of the calves excreting L1 larvae in faeces (detection of this hair-thin organism is challenging in skeletal muscle tissues). The calf with the highest number of recovered nematodes also excreted the most L1 larvae in faeces (LPG: 1632). Isolated nematodes were identified morphologically to the genus Elaphostrongylus (Cameron, 1931). Although not speciated, we conclude, based on the host species and fecal excretion of typical L1 larvae, that these nematodes were indeed E. rangiferi.

Fig. 8

Group of adult hair-thin, about 3–5 cm long Elahostrongylus rangiferi nematodes in the muscle fascia of a calf killed on Hardangervidda in spring 2015.

Other findings

The reindeer sinus parasite, Linguatula arctica (Riley et al., 1987) was detected in the maxillary sinuses of three calves. Six calves displayed eye lesions compatible with chronic keratitis.

The calculated mean summer temperatures in the pasture area for 2014 and 2015 were 1.0 °C above and 1.7 °C below the average (7.4 °C) for the last 30-year-period (Fig. 9). Fig. 10 shows the number of summer days with a mean air temperature ≥12 °C for this period, and for the years 2014 and 2015, as well as for the five individual years with a higher mean temperature than in 2014.

Fig. 9

Calculated mean air temperature (°C) in the main summer pasture area of the Hardangervidda wild reindeer population for individual summers (June–August) 1989–2018. The summers of 2014 and 2015 are marked with a black circle. The dotted horizontal line shows the mean (7.4 °C) for the 30-year-period.

Fig. 10

Calculated number of summer days (June–August) with a mean air temperature ≥12 °C in the main summer pasture area of the wild reindeer population on Hardangervidda. The figure shows the mean and range for the 30-year period 1989–2018, and the mean for individual years 2014 and 2015 as well as for the five years with a higher mean temperature than in 2014.

The total snow precipitation (measured as mm water) for the winters 2014/15 and 2015/16 was high, but similar (284–296 mm). The number of days with a calculated mean air temperature >0 °C was however higher in the winter of 2015/21016 (11 days), compared to winter 2014/15 (3 days). Based on these results, it could be suggested that winter conditions were in favor of the 2014 generation.

Discussion

This study found a significant relationship between high winter loads of Oestrids and E. rangiferi, low carcass weights and cases of emaciation in wild reindeer calves on Hardangervidda. The parasite loads were significantly higher for the calves born in the summer of 2014, compared to those born in 2015. We consider these differences in parasite loads to be closely related to differences in summer temperature and possibility of successful Oestrid pupation and development of E. rangiferi L3 larvae in the environment. The mean summer temperature in 2014 was 2.6 °C higher than the mean for 2015.

The developmental time of Oestrid pupae and L3 larvae of E. rangiferi in gastropods decreases proportionally with temperatures above 10 °C and at 12 °C the minimum developmental period for Oestrids and E. rangiferi is about 1.5 and 2months, respectively (Halvorsen and Skorping 1982; Nilssen, 1997). Based on our calculations, these temperature requirements were not met at the average summer pasture altitude (1283m) for either of the two summers (see Fig. 10). As air temperatures increase in mountain areas by almost 1 °C per hundred meters decrease in elevation, it is considered likely that fulfilled development of Oestrid pupae and Elaphostrongylus L3 larvae could been accomplished at a few hundred meters below the average summer pasture altitude in 2014, and many hundred meters below this level in 2015. However, it must be emphasized that in sites with a favourable microclimate, suitable temperatures may be reached at higher altitudes. Moreover, for E. rangiferi, it has been suggested that the parasite may compensate for low temperatures by fulfilling its larval development over two summers, by overwintering in gastropods (Halvorsen and Skorping, 1982).

We consider the prevalence (100%) and intensity of H. tarandi larval infection (mean 170 larvae) and C. trompe (mean 64 larvae) identified in the 2014 calf generation to be high. The real intensity of C. trompe larvae was obviously higher since an additional (water flushing) count, identifying 32% of the larvae found in the 2015 generation, was not performed for the 2014 generation. In comparison, studies carried out in semi-domesticated reindeer flocks in northern Norway reported mean intensities of 60 H. tarandi and 18 C. trompe larvae (Folstad, 1991; Nilssen and Haugerud, 1995). Oestrid larvae are rich in protein and fat, which originates from the host. The host's loss of energy to the larvae will peak in late winter and spring when the larvae grow to full size (1.5 g). Calves are especially vulnerable since they are frequently infected with more larvae and have lower fat reserves, than adults (Skjenneberg and Slagsvold, 1968). Cuyler et al. (2012) examined 10-month-old Greenland caribou calves with heavy Oestrid larval infections and estimated the energy costs for the heaviest infected calves to be equivalent to 12 days basal metabolic rate, or forgone fattening equivalent to 1.2 kg fat. They concluded that high larval burdens could negatively affect winter calf survival. We suggest that high and even moderate Oestrid larval infection levels may have fatal energy costs for calves balancing on a nutritional knife-edge during a long and harsh alpine winter and spring on Hardangervidda.

The prevalence of E. rangiferi infection in the 2014 calf generation was high (92%) whereas the intensity of infection, with reference to earlier studies in reindeer (Halvorsen et al., 1985) can be considered moderate to high. The calf with the highest intensity of infection (LPG 1632) was in an advanced stage of emaciation and 22 adult E. rangiferi were isolated from its skeletal muscles. This was similarly to the number of nematodes recovered from two experimentally infected reindeer calves that showed signs of ataxia and posterior paresis of several months' duration (Handeland, 1994; Handeland et al., 1994). On this basis, we consider it likely that the most heavily infected calf in our study would have suffered locomotory disturbances during the winter. The same calf also had a comprehensive verminous pneumonia caused by Elaphostrongylus eggs and L1 larvae, which may have hampered lung function. Verminous pneumonia can also create beneficial conditions for opportunistic pathogens e.g., Pasteurella multocida. This bacterium is commonly carried in the upper airways of reindeer and is a well-known cause of pleuropneumonia and septicaemia in semi-domesticated reindeer in northern Norway (Kummeneje, 1976). Pasteurellosis has also been diagnosed in wild reindeer populations (Handeland, 2016).

Although E. rangiferi infection is common in wild reindeer populations (Handeland et al., 2019) and may cause relatively heavy infections, as demonstrated in the present study, no outbreaks of clinical elaphostrongylosis have so far been recognized. This contrasts to semi-domesticated reindeer herds in northern Scandinavia where epidemics and severe losses, primarily in calves, have been reported (Roneus and Nordkvist, 1962; Bakken and Sparboe, 1973; Kummeneje, 1974). The apparent differences in clinical significance between semi-domesticated and wild reindeer could be related to differences in the probability of detecting disease. Semi-domesticated flocks are herded and thus more or less continuously monitored, whereas the wild reindeer populations, with the exception of the hunting season, are left to themselves in remote areas. Given a probable main time of infection in late summer or autumn (Mitsgevich, 1964; Halvorsen et al., 1980), and neurological signs normally starting 1–2 months after infection (Handeland et al., 1994), clinical disease in wild reindeer will not occur until after the hunting season, with small chances of detection. It should also be emphasized that even moderate infections with long-lasting slight or subtle locomotory disturbances may be fatal during the harsh alpine winter.

We assume that the high winter loads of Oestrids and E. rangiferi in wild reindeer calves on the Hardangervidda are related to the population's occupation of a limited area in the south during the summer (Fig. 2). This aggregation in the south in summer leads to higher concentrations of parasites on the ground, compared to previous years when the parasites were spread along a migratory route towards, and in larger summer pastures, in the west. The fact that Oestrid larvae are dropped and developed into adult flies within the same area, also probably increases Oestrid fly harassment. Harassment by Oestrid flies in summer is associated with reduced grazing time and low carcass weights in the autumn (Skjenneberg and Slagsvold, 1968; Colman et al., 2003). A gradual increase in the level of infection with Oestrids and E. rangiferi can also be expected in the face of climate warming. It has been shown that the average summer temperature in the Norwegian wild reindeer areas has increased by 0.6 °C from the previous, to the last, 30-year period (Handeland et al., 2019).

In conclusion, this study provided strong indications that Oestrid and E. rangiferi infections contribute to low body condition and cases of emaciation among wild reindeer calves in winter, particularly after a warm summer. We anticipate an increased future significance of these infections in wild reindeer populations due to climate warming and animal aggregation, following human pressure on their living areas.

Declaration of competing interest

None.