Our study found a wide range of causes of death in reindeer on winter pasture and in calves during their first months of life. The main findings of our study include comparison of disease and predation related deaths to body condition metrics using both the bone marrow fat index [45] and visual fat score. Co-morbidities were seen in a number of diagnoses like bacterial sepsis subsequent to non-fatal predator wounds and poorer body condition with infections.
The comparison of visual fat score and bone marrow fat index correlated well in animals emaciated or in poor condition (index 0–1) as well as in good condition (index 4–5). However, the group of carcasses considered as fair (index 2–3), showed more variation and thus bone marrow fat index alone seems less suitable in this group. The bone marrow method does not distinguish between degrees of good condition (good – very good, levels 4 and 5) and between emaciated to very poor condition levels (levels 0 and 1) since the fat content in bone marrow will be the same [45]. Thus, three categories of fat index, based on bone marrow fat index, seems more appropriate than the five used in the visual fat score. Ideally, the bone marrow fat index should be used in combination with visual fat assessment of the carcass. This has also been the conclusion in other studies that evaluated measures of body condition in reindeer [45, 49].
Emaciation is an important cause of death in ungulates during winter even if the actual number of deaths are rarely documented. In winters with difficult pasture conditions, the reindeer population can decrease drastically, and emaciation is considered the most likely cause [50, 51]. Winter crises also influence the reproduction in the spring and thus have a negative impact on the number of calves available in the autumn. Calves born from females in poor condition in spring have reduced survival during spring and summer [52, 53], however, by autumn the calves’ condition seems to no longer be related to the mothers’ weight at birth [53]. No winter crises were registered during this study period. Obviously, winter conditions were variable and had, in all likelihood, an important impact on the animals dying from emaciation. However, documenting snow and weather conditions was outside the scope of this project.
Additional feeding was provided prior to death to most of the reindeer that died from emaciation in our study. Some of them had had access to feed for longer periods whilst for others it was only a few days. Emaciation in spite of feeding is not a new issue [37]. Reindeer herders today are better prepared for winter crises with the increased availability of commercial feedstuffs and greater experience with winter-feeding. These animals are, however, still primarily adapted to grazing on natural pastures, which highlights the importance of access to suitable grazing is even when feedstuffs are available.
In our study, 10 animals were considered as emaciated secondary to infectious disease. This highlights that although emaciation can be a result of hunger due to poor pastures or unfavourable snow conditions, other causes such as diseases, high parasite load, injuries as well as stress from predators contribute to nutritional imbalance [54, 55].
Building energy reserves during summer is the key for winter survival in the Arctic and fat metabolism will naturally increase during winter [56]. In our study, the emaciated animals were seen mainly in late winter/early spring, as expected. Young animals are always the most vulnerable having the highest nutritional needs [57], however we did not see any significant age differences between the emaciated animals in our study. This is likely due to bias in the sampling as the motivation for delivering carcasses for inspection in many cases was to confirm suspected predation. In addition, adults are prioritized when searching for lost animals [7] and calves are harder to find since they are quickly eaten by scavengers.
Traditionally, herds had more males and castrates who are able to dig through deep snow and ice, which the females then follow to take advantage of [58]. Females will keep their antlers during winter thus have a higher rank than the bulls and can chase them away from their grazing holes. One can question whether the herd structure incentivised by public administration policy, which has led to a population predominantly of females and calves, has led to a less robust populations during hard winters [59].
Eagles were the most important predator and responsible for 50% of the total predator killed reindeer. We do not claim that this percentage is representative for Troms and Finnmark, but it is close to the official statistics. However, calves were the main prey for eagles whilst wolverine prayed on both adults and calves is in our study, which is in accordance with public statistics [10].
Reports have also concluded that that eagles kill calves predominately during the first months of life [15, 16, 60] and newborn calves with lower body weight seem to be particularly vulnerable to predation [15, 16]. Nieminen et al. (2011) also found that calves born from young females, late in the spring, were lighter and had a higher risk of predation [61]. Open landscape seems to be a risk factor for predation of young calves [15, 16]. Eagles are also capable of killing adult reindeer, predominantly by puncturing the chest/thorax with their talons [36, 61]. One adult female was confirmed as killed by eagle in October in our study. Relatively few such cases are reported in the official statistics [10].
Our findings not only confirm that the eagles kill newborn calves but that they also continue to kill calves during the whole first year of their life. This is in accordance with official statistics, showing that eagles were responsible for 49% of documented predator killed carcasses in western Finnmark in 2016-19, with calves being the dominant prey, while lynx and wolverine amounted for 24% and 25% [10]. In our study, the eagle-killed calves were found mainly in the period January-March. This may be a bias of the study rather than a true reflection of the level of eagle predation. These months have light and snow conditions suitable for searching for carcasses.
Our study showed that calves, mostly from the winter pasture in Western Finnmark, were in both poor and good condition when killed by eagles. Josefsen et al. (2014) also found that predator killed reindeer had normal body condition [35]. An important aspect is also that poorer body condition is a normal finding in late winter. This might suggest that predator losses in reindeer in Norway are a combination of both compensatory and additive, and not just compensatory losses as suggested by others [17, 40]. An important aspect is also that long-term stress can have negative effects on an individual’s growth, health, and reproduction and this stress should therefore be considered as a negative effect from predators in addition to the fatalities [54, 55]. Assessing the cost of predation and evaluating mitigation measures needs to go beyond the current focus of body condition as a main risk factor and would benefit from a more nuanced approach.
There were few only five killings by lynx in our material. Lynx can kill both adults and calves, but seem to prefer calves [62].
Official statistics from Western Finnmark show documented wolverine kills in 34% of the adults during the herding years 2017/18 and 2018/19 [10]. We found that wolverine killed mainly adults in good body condition (10/14). Some of these adults (n = 3) had non-deadly wounds, but were either euthanized or died subsequently from bacterial infection in association with these non-fatal wounds. It is interesting though that wolverine, despite being a rather small animal, attacks adult males and females in good body conditions weighing 60–80 kg. Killing of adults in a prey population may have a larger impact on the population than predators selecting mainly juveniles [20, 62].Traditional Sámi knowledge tells about the impact of snow condition on wolverine predation strategies. It describes how wolverine take advantage of deep snow and attack adult reindeer, which find it difficult to escape, as well as sneaking up on reindeer digging grazing pits. Herders have also experienced that reindeer with non-fatal wounds from wolverine would likely die [63]. Bacterial infections in wounds from attacks as seen in a few individuals in our study are likely underreported.
Changing herding practice with supplementary feeding and combination with corralling in particular, as a response to predation or poor grazing availability, can lead to increased risk of infectious diseases [30]. Outbreaks of diseases seems to be an increasing problem in Finland and in Sweden [29, 30], but to much lesser extent in Norway with only a few published reports [31, 32]. In this project, we did not discover any outbreaks of infectious disease in combination with feeding or corralling.
Infections were, however, still the third most common diagnostic category and were found as the direct, or indirect, cause of death in 14% (20/138) of the individuals in our study. Emaciation was also seen in combination with infections and bone marrow fat index was significantly lower in animals dying of infections than of trauma, or of other causes. Infections can lead to general weight loss [64] and reindeer, being in a negative energy balance during winter [65], will be particularly vulnerable to emaciation if exposed to disease. On the other hand, animals in poor condition also have increased susceptibility to infections [66].
Infections with P. multocida was the dominant infectious disease in the project. Pasteurellosis is a known disease in semi-domesticated reindeer with a potential for large outbreaks [67]. It is probably under reported since single cases and smaller outbreaks and these are seldom diagnosed. Acute infections can affect animals in good condition, often in combination with stress, as seen in our data when calves in good condition died of acute pasteurellosis. Septic pasteurellosis was diagnosed in four calves; three were found dead after transport at the same slaughterhouse coral, whilst one died during transport. Bronchopneumonia due to P. multocida was found in a calf with rich fat reserves that died after showing clinical signs of respiratory disease. The bacteria was also found in individuals with septicaemia subsequent to a predator attack. In two of the cases, adults were found dead with non-fatal bite wounds caused by a wolverine. In another case, an adult reindeer was found alive with wolverine bite wounds and euthanized. The fourth case was in a young calf diagnosed as killed by lynx. Bacterial septicaemia in combination with the predator attack could have been due to activation of the animal’s own mucosal bacteria because of severe stress from being chased and attacked. The other explanation is the transfer of the bacteria from the predator’s oral cavity with a bite wound infection. Bite wounds from dogs and cats are the most common cause of infections with P. multocida in humans [68].
Other bacterial infections included three carcasses from which T. pyogenes was isolated. One calf had pneumonia and generalised bacteraemia, whilst an adult had purulent peritonitis caused by a perforating wound into the dorsal part of the abdominal cavity. Such puncture wounds could have been caused by an eagle attack, but this was not possible to document. The third case was a yearling with purulent arthritis. Streptococcus sp. was isolated from another calf with osteomyelitis, arthritis, and periarthritis, and Streptococcus suis was isolated from a liver abscess in an adult. Moraxella sp. was isolated from the eyes of two carcasses with mild purulent conjunctivitis and from a live animal with keratoconjunctivitis. The latter case was part of a small outbreak of eye infection in a herd during transport to winter pasture. Other bacterial diagnoses include beta toxic Staphylococcus sp. isolated from skin abscesses in the axillae of an adult and E. coli from a two week old calf found dead with acute, catarrhal enteritis.
Although elaphostrongylosis was diagnosed in only three calves from Trøndelag, these three cases were part of a large outbreak which included the loss of approximately 150 animals over a period of two years after an unusually warm summer and autumn in 2018 [69]. Single cases of elaphostrongylosis are regarded as common and seldom reported, but larger outbreaks have been documented. Outbreaks generally occurred in late autumn/early winter after unusually warm summers and the impact of temperature is well documented [33]. Elaphostrongylosis can also have milder, unspecific symptoms such as confusion, unusual tameness, lethargy and weight loss [33].
We also found mild meningitis in a yearling that died from ruminal acidocis. This yearling had withdrawn from the herd and stayed close to a house, which could be symptoms consistent with elaphostrongylosis.
Handeland et al. (2021) found that high number/load of the three parasites Cephenemyia trompe, Hypoderma tarandi and Elaphostrongylus rangiferi in wild reindeer influenced the body condition in calves and increased the risk of emaciation [49]. However, the mean load/range of these parasites were much higher than those seen in our results. Despite this, we also saw, that animals with higher H. tarandi burdens had significantly lower bone marrow fat index than those with lower burdens or no warbles. Infections with parasites were common in our study but mainly without pathology or reduced body weight.
We identified a calf with mandibular hypoplasia. This type of malformation is known to occur sporadically in reindeer [36]. One would expect such calves to have trouble with suckling as newborn and that they would die soon after birth [35]. However, this calf had managed for 8–9 months before it perished.
The results from this study are not representative for specific regions or districts. Most of the material came from the winter pastures of inner Finnmark. The carcasses and bone samples were mostly from material delivered to SNO for examination for predator damage/wounds. The organ samples were from animals that had either died before slaughter or were random findings during meat inspection at slaughterhouses. In Troms, the carcasses were mostly delivered when predator kills seemed unlikely. The month of submission varied with most being submitted during the winter period and early spring (December-May) except for a few newborn calves which were submitted in spring/early summer (May-July). The period during which the vast majority of carcasses were submitted (January-April) is a part of the winter with the best light and weather conditions for locating carcasses, and the cold weather helps preserve the carcasses. The few carcasses from Trøndelag were animals delivered due to clinical symptoms of brainworm infection. This makes a comparison of geographic and temporal trends challenging and was therefore not appropriate for this dataset.