p37-48_3925.pdf ALCES VOL. 41, 2005 STÉEN ET AL. - DISEASES IN MOOSE 37 DISEASES IN A MOOSE POPULATION SUBJECTED TO LOW PREDATION Margareta Stéen1, Ing-Marie Olsson1, and Emil Broman2 1Veterinary Service and Food Control, County Administrative Board of Gaevleborg SE 801 70 Gaevle, Sweden; 2Department of Applied Environmental Science, Göteborg University, Box 464, SE 405 30 Gothenburg, Sweden ABSTRACT: Well-publicized studies on two moose diseases, elaphostrongylosis and moose wasting syndrome, conducted across Sweden from 1985 to 1994 resulted in an increased number of reports of sick and dead moose. A sample of 724 moose were investigated, including 426 females, 208 males, and 90 of unknown sex with an average age of 3.7 years (SD = 4.9, range 0-20). Prominent diagnoses were elaphostrongylosis (18%), moose wasting syndrome (11%), and accidental death (11%). Other important diagnoses were neoplasm (5%), parasitic (6%), nervous system (5%), infectious (4%), eye and ear diseases (4%), and predation (3%). From the beginning to the middle of the 20th century ap- proximately 10 wolves, 130 bears, 175 lynx, and 100 wolverines were present in Sweden (449,000 km2). Currently, the scene is quite different with wolf, bear, lynx, and wolverine populations all increasing. The total number of large predators and scavengers is estimated at 2,500-3,000. We believe that the diversity of moose diseases seen in the future will differ from that observed during the 1980s and 1990s by being less visible due to increasing predation. ALCES VOL. 41: 37-48 (2005) Key words: Alces alces, bear, Canis lupus, diseases, elaphostrongylosis, moose wasting syndrome, predation, Ursus ursus, wolf Statistics on regulated hunting (culled) of moose (Alces alces) have been recorded in Sweden since 1881, mirroring the population density. The population began to increase in the late 1920s, rose rapidly in the 1970s, and peaked in the 1980s (Cederlund and Markgren 1987, Cederlund and Bergström 1996). To- day, the summer population is estimated to be 300,000-400,000 animals (Stéen et al. 1998b) resulting in an approximate density of 1.0 – 1.5 moose/km2. The moose harvest in Sweden is sub- stantial with approximately 100,000 animals being culled each year and the meat annually comprising 4-5% of the country’s total meat production (Stéen et al. 1998b). Because moose are an important natural resource of considerable economic value to tourism, hunting, and meat production, a long-term overview of diseases affecting their health is of great societal interest. Routine investigations of wildlife dis- eases have a long history in Sweden (Stéen et al. 1997, 1998b). Diseases in moose have mostly been described as single or clusters of cases (Borg 1975, 1987; Stéen et al. 1998b). Climate, especially snow depth, and nutritional stress due to limited food resources have been regarded as the main causes of natural (i.e., - ing the 1980s another picture emerged, when large numbers of sick or dead moose were found throughout Sweden. Two diseases, elaphostrongylosis (ELA), caused by the parasite Elaphostrongylus alces, and moose wasting syndrome (MWS), the etiology of which is still unknown, gave rise to public concern and interest. In 1985, two projects were initiated at the Swedish University of Ag- ricultural Sciences (SLU) to investigate both diseases and a number of reports and papers have subsequently been published (Stéen and DISEASES IN MOOSE – STÉEN ET AL. ALCES VOL. 41, 2005 38 Rehbinder 1986; Feinstein et al. 1987; Stéen and Diaz 1988; Stéen et al. 1989; Stéen and Johansson 1990; Stéen and Roepstorff 1990; Rehbinder et al. 1991; Stéen 1991; Olsson et al. 1993; Stéen et al. 1993; Frank et al. 1994; Merza et al. 1994; Stéen et al. 1994; Olsson et al. 1995; Stéen et al. 1997; Frank 1998; Lankester et al.1998; Olsson et al. 1998; Stéen et al. 1998a; Frank et al. 2000a, 2000b, 2000c, 2000d; Gajadhar et al. 2000; Olsson 2001; of disease in wild animals is in accordance with that of Wobeser (1981) who described diseases as any impairment that interferes with - tions, including responses to environmental factors such as nutrition, toxicants, climate, infectious agents, inherent or congenital de- fects, or combinations of these factors. An overview of the diseases seen in moose examined from 1985 to 1989, when non-human predators, including wolf (Canis lupus), brown bear (Ursus arctos), wolver- ine (Gulo gulo), and lynx (Lynx lynx), were few is presented in this paper. Diseases and other causes of morbidity and mortality were grouped into 19 diagnostic categories. The results are compared to previous reports of disease and mortality in moose. METHODS Study Period and Material Whole carcasses or organs from approxi- mately 1,000 moose were examined from 1985 to 1989. In this paper we describe moose examined by Stéen (Table 1). Data Collection and Necropsy Data describing where and how each animal was found or killed and the circum- stances surrounding the case accompanied each sample. Post-mortem and follow-up investigations were performed as described in Stéen et al. (1997, 1998a). Evaluation of physical condition was done (n = 642) by visual inspection of the body fat, its loca- tion, and appearance. Condition categories included normal condition, below normal (poor), serous atrophy, or absence of adipose tissue (emaciated). Moose were aged by tooth wear and eruption (Skunke 1949, Reimers and Nordby 1968). Diagnosed causes of disease were categorized (Table 2). Statistics Inferential statistics were performed using SAS®. Analyses were considered statistically P < 0.05. RESULTS Samples originated from across Sweden, with the majority of cases being from north of Stockholm (59°N). Samples of sick or dead moose were submitted year-round, although - lowed by fall, winter, and summer (Table 1). Samples from hunter harvested animals were taken in the fall. Age and Sex The average age of moose examined was Table 1. Summary of moose samples examined in the study. Parameters Number of animals Total 724 Type of sample Carcass 315 Organ 405 Unknown 4 Sex Females 426 Males 208 Sex unknown 90 Season Fall 294 Winter 154 Spring 200 Summer 76 Manner of Death Euthanized 230 Found dead 304 Culling 171 Unkown 19 ALCES VOL. 41, 2005 STÉEN ET AL. - DISEASES IN MOOSE 39 3.7 years (SD = 4.9, range 0-20, n = 617). Grouped into 4 age classes, the distribution was: calf (41%), yearling (11%), adults 2-11 years (49%), and seniors 12-20 years (9%). The overall sex ratio was 1 bull/2cows, a female-biased adult ratio which makes cows more numerous than bulls (Fig. 1). The sex was unknown in 12% of the cases. Diagnoses Diagnoses were grouped into: blood, lymphatic and cardiovascular systems (BLC), digestive system (DIG), endocrine system (END), eye and ear (EE), infectious diseases (INF), metabolic disturbances (MET), muscle- skeletal system (MUS), neoplasm (NEO), nervous system (NER), parasitic diseases - tive and urinary systems (REP), respiratory system (RES), and skin and connective tissue (SKN) (Merck Veterinary Manual 1979). Ad- ditional diagnoses were malformation (MAL), elaphostrongylosis (ELA), moose wasting syndrome (MWS), predation (PRED), and miscellaneous causes (MIS). No pathological Of the 609 diagnosed cases, the most fre- quently diagnosed condition was ELA (22%), followed by MWS (14%), and accidental diagnoses were PAR, NEO, NER, INF, and EE. Predation was seen in 3% of cases and was comprised of 11 calves, 3 yearlings, 7 adults, 3 seniors, and 1 of unknown age. The age distribution of the predated cases did not differ from that of cases with other diagnoses 2 = 2.5280, 3 df, P = 0.4703). The relative risk (proportion of diagnosis Table 2. Number of animals diagnosed per disease category based on age classes. Disease category Calves Adults (2-11 years) Seniors (12-20 years) Unknown Total Blood, lymphatic and cardiovascular systems (BLC) 1 1 3 2 1 8 Digestive system (DIG) 7 1 6 1 1 16 Endocrine system (END) - - 3 - 1 4 Eye and ear (EE) 5 2 14 5 - 26 Infectious diseases (INF) 7 - 20 3 2 32 Metabolic disturbances (MET) - - 1 - - 1 Muscle-skeletal system (MUS) 3 1 13 1 2 20 Neoplasm (NEO) 1 3 24 6 5 39 Nervous system (NER) 11 - 24 3 - 38 Parasitic diseases (PAR) 11 12 16 1 3 43 25 12 36 3 2 78 Reproductive and urinary systems (REP) 2 - 4 1 - 7 Respiratory system (RES) 5 - 11 2 2 20 Skin and connective tissue (SKN) 1 - 1 - - 2 Malformation (MAL) 4 - 8 1 - 13 Elaphostrongylosis (ELA) 94 15 16 2 5 132 Moose wasting syndrome (MWS) 16 2 50 13 2 83 Predation (PRED) 11 3 7 3 1 25 Miscellaneous causes (MIS) 7 4 8 2 1 22 Total 211 57 265 48 28 609 DISEASES IN MOOSE – STÉEN ET AL. ALCES VOL. 41, 2005 40 among necropsied moose) from ELA was greater in calf/yearlings than in adults/seniors 2 = 73.4419, 1 df, P < 0.0001, 2 = 18.8946, 1 df, P < 0.0001, Fig. 2b). For MWS the opposite pat- tern was seen in respect to age classes (Fig. 2a,b), however differences were not statisti- 2 = 14.1872, 1 df, P 2 = 0.6691, 1 df, P = 0.4134, females and males, respectively). Animals with NEO and INF were over-represented in 2 = 17.0127, 1 df, P < 0.0001, 2 = 7.6095, 1 df, P = 0.0058, NEO and INF, respectively). Among calves, sex was not related to 2 = 0.1374, 1 df, P 2 = 0.2476, 1 df, P = 0.6188) (Fig. 2a, b). Two yearlings, 1 male and 1 female, were diagnosed with MWS and the relative risk did not differ between the sexes 2 = 0.0037, 1 df, P = 0.9516, Fig. 2a, b). Among older animals, adults and seniors together, bulls appeared to be more prone to 2 = 4.253, 1 df, P = 0.0392, Fig. 2a, b) but the opposite pattern was seen for MWS; i.e., the relative risk was higher for cows 2 = 6.3486, 1 df, P = 0.0117, Fig. 2a, b). The frequency of both ELA and MWS 2 = 33.1174, 3 df, P 2 = 13.699, 3 df, P = 0.0033, ELA and MWS, respectively). Moose with ELA were over-represented in springtime while cases with MWS were most prevalent in winter (Fig. 3). Predated carcasses were found most frequently in spring and in areas along the Norwegian border. The occurrence of animals with ELA and MWS differed geographically. The relative risk of ELA was greatest in northern Sweden (Fig. 4a) while the relative risk of MWS was 0.00 0.20 0.40 0.60 0 4 8 12 16 20 Age (years) P ro p o rt io n o f m o o se Female Male Fig. 1. Age distribution of examined moose (female n = 426; males n = 208). Female 0.00 0.20 0.40 0.60 0.80 1.00 C a lv e s Y e a rl in g s A d u lts S e n io rs P ro p o rt io n s o f d ia g n o se s Others MWS ELA Male 0.00 0.20 0.40 0.60 0.80 1.00 C a lv e s Y e a rl in g s A d u lts S e n io rs P ro p o rt io n s o f d ia g n o se s Others MWS ELA Fig. 2. Proportion of moose diagnosed as ELA, MWS, and ‘Others’ based on age class and sex; (a) female (calves n = 125, yearlings n = 27, adults n = 220, and seniors n = 47) and (b) males (calves n = 96, yearlings n = 34, adults n = 69, and seniors n = 3). (a) (b) ALCES VOL. 41, 2005 STÉEN ET AL. - DISEASES IN MOOSE 41 highest in the south (Fig. 4b). Condition A disease was not always manifested by diminished body condition. Emaciation, poor, and normal condition were almost equally represented among the cases (33%, 31%, and 36%, respectively). Condition was related to season; poor/emaciated being most prevalent in spring, followed by winter, summer, and autumn. Excluding animals culled in the fall, this pattern did not change (Fig. 5). The poor/emaciated categories were over-repre- sented in moose showing ELA and MWS 2 = 28.0245, 1 df, P 2 = 10.237, 1 df, P < 0.05, respectively), but there was a tendency for INF to be under-represented 2 = 3.7057, 1 df, P = 0.0542). About 50% of animals with INF were in normal body condition, compared to other disease diagnoses where the corresponding value was < 40% (Fig. 6). Moose with tumors (NEO), as well as predated animals, were in all categories of body condition. DISCUSSION Diagnoses The proportion of different diagnoses (i.e., relative risks) varied between age-class and sex. MWS is more common among older animals and more common among cows than bulls. For ELA, the opposite pattern was ob- served. It appears that both age and sex can explain some of the variance in susceptibility such conclusions are equivocal, as we do not know the size and structure of the population from which the dead moose came, which is essential to estimate the absolute risk of death. Therefore, one can only estimate the relative risk of death. With reservations about discrepancies between relative and absolute risks, this study indicates that adult bulls were more prone to ELA than adult cows, but no differences were found between male and female calves and yearlings. Infections with Elaphostrongylus spp. normally occur in summer and fall, with (1986) studied ELA in reindeer and concluded that male calves belonging to dominant moth- ers are more heavily infected with E. rangiferi than females. The largest calves eat more and therefore experience a higher risk of ingesting gastropods with E. rangiferi. Stuve (1986) found a higher prevalence of ELA in male than female moose calves, also suggesting that males were more likely to be infected. moose calf weights were dependent on summer browse in the cows’ home range, the quality of which is related to the cows’ status. For older animals, Stuve (1986) attributed the difference in infection between the sexes to physiologi- cal changes during the rut in accordance with Age is related to ELA, with yearling and calves being most frequently infected. Earlier studies have shown that moose shed most E. alces - lowed by a sharp drop in larval shedding and reduced level of adult worms in older animals (Stuve 1986, Stéen 1991, Olsson et al.1995, Stéen et al. 1997). Our results show that emaciation is as- sociated with ELA. This could of course be a spurious correlation or a cause/effect of 0.00 0.20 0.40 0.60 0.80 1.00 S p ri n g S u m m e r A u tu m n W in te r P ro p o rt io n s o f d ia g n o s e s Others MWS ELA Fig. 3. Proportion of moose diagnosed as ELA, MWS, and ‘Others’ based on season (spring n = 200, summer n = 76, autumn n = 294, and winter n = 154). DISEASES IN MOOSE – STÉEN ET AL. ALCES VOL. 41, 2005 42 ELA. That emaciation might be an effect is supported by the fact that E. alces can cause a nervous disorder, with lack of co-ordina- Rehbinder 1986, Stéen et al. 1989, Stéen and Roepstorff 1990). Stuve (1986) found that general condition and he found that the dif- ference in carcass weights between infected and non-infected animals increased with age. Conversely, moose experimentally infected with E. alces retained their normal weight when fed ad libitum (Stéen et al. 1998a). INF differed from other diseases in being positively related to condition. Animals with INF probably die acutely before they loose condition or become emaciated, which is in contrast to animals with ELA and MWS. Health Status The disease pattern, including deaths caused by wild predators seen in our sample differs from that seen elsewhere (Lankester 1987, Guilazov 1998, van Ballenberghe and Ballard 1998), suggesting that moose popula- tions in Sweden might be different from other populations. For example, densities and hu- man harvest rates are higher in Sweden than in Russia and North America, but predation is lower. We believe that the disease patterns observed are masked worldwide by predation. The scenario of the Swedish moose loss, with the exception of hunting, will probably change over time and become more similar to the causes of deaths (e.g., predation) observed in other countries. Another difference between the Swedish Fig. 4. Proportion of moose examined between 1985 and 1989 with signs of (a) ELA and (b) MWS for each Swedish County. (a) (b) ALCES VOL. 41, 2005 STÉEN ET AL. - DISEASES IN MOOSE 43 and North American moose populations is the origin of the diseases (Borg 1956, Nils- son 1971, Borg and Nilsson 1985, Borg 1987, Lankester 1987, Lankester and Samuel 1998, Stéen et al. 1998b). An interesting and notable observation is that moose in North America have few Eurasian parasites but have acquired new parasites and diseases from indigenous wild ungulates and livestock (Lankester 1987, Lankester and Samuel 1998). The diseases observed in Sweden are, as far as we can - ted from livestock or deer, with the exception of malignant catarrhal fever (Warsame and Stéen 1989). Most of the diseases in American moose have not been diagnosed in Swedish moose. The viroses epizootic haemorrhagic disease, bluetongue, western equine and St. Louis encephalitis, Norway virus, California encephalitis virus, and contagious ecthyma have not been diagnosed in Swedish moose or bovine rhinotracheitis are, however, known in Swedish livestock (Moreno-Lopéz 1979, SJV 1994) and in reindeer (Rockborn et al. 1990) but not moose. Further, the bacterial and parasitic diseases in American moose (leptospirosis, brucellosis, necrobacillosis, Toxoplasma gondii, Entamoeba bovis, Param- phistomum spp., Fascioloides magna, Taenia ovis, T. krabbei, Echinoccocus granulosus, Thysanosoma actinioides, Orthostrongylus macrotis, Parelaphostrongylus tenuis, El- aeophora schneideri, Onchocerca cervipedis, Setaria yehi, , Derma- centor albipictus, Cephenemyia jellisoni, C. phobifera, and Haematobosca alcis), have not been found nor reported for Swedish moose (Nilsson 1971, Stéen et al.1998b). Despite all the diseases and parasites enu- merated, Lankester (1987) and Lankester and Samuel (1998) proclaim American moose to be generally healthy. They explain this status of health partly by the fact that American moose occur at a low densities (0.1-0.6/km2), which reduces the transmission rate of parasites and diseases. Also van Ballenberghe and Ballard (1998) state that moose host a variety of dis- eases and parasites that are seldom a major limiting factor for population growth. On the other hand, Wobeser (1994; 3) declared: “Although most infectious agents do not result in obvious disease, the host must pay a price for harboring parasites that live, grow, and reproduce at expense of the host. Interactions between parasites and other stress factors can in wild animals are often considered only in terms of death or obvious physical disability, parameters. In other words, the effect of dis- eases on wild populations may be much greater than is evident by simply counting the dead or 0.00 0.20 0.40 0.60 0.80 1.00 S p ri n g S u m m e r A u tu m n W in te r P ro p o rt io n s o f m o o se Emaciated Poor Normal Fig. 5. Proportion of moose in normal condition, poor condition, or emaciated split by season (spring n=183, summer n=73, autumn n=166, and winter n=131). Moose culled during regular sports hunting excluded. 0.00 0.20 0.40 0.60 0.80 1.00 E L A M W S IN F T o ta l P ro o ri tio n s o f m o o se Emaciated Poor Normal Fig. 6. Proportions of moose in normal condition, poor condition, or emaciated split by diagnosis (ELA n=126, MWS n=81, INF n=28, and ‘Total’ n=642). DISEASES IN MOOSE – STÉEN ET AL. ALCES VOL. 41, 2005 44 maimed. The Swedish moose population is dense, with up to 1.0-1.5 moose/km2, which may increase the risk of disease and parasite transmission as discussed by Lankester and Samuel (1998). It is unknown how our data relate to density, but for MWS there are indi- cations that density dependence might be the ultimate reason for its appearance (Broman et al. 2002a). Does the large number of diseased moose seen in Sweden during the latest 2 decades indicate anything about the health status of Swedish moose? The opportunity to see and report abnormal moose is greater in the intensely managed forests of Sweden than in the wilderness of North America and Russia. From 1985 to 1989, approximately 200 moose per year were necropsied and diagnosed in Sweden, compared to a total of 420 between 1947 and 1982 (Borg 1987, 1991). Currently, up to 100 moose per year are examined at the National Veterinary Institute, Uppsala, Sweden (Mörner 2001). If the necropsies - ever, the moose population increased sharply in the 1980s (Cederlund and Markgren 1987, Cederlund and Bergström 1996), making it Thus, increased observations do not necessar- ily indicate a higher absolute mortality risk. Broman et al. (2002b) estimated natural death < 4% for adults in the area where the highest incidences of natural moose mortalities were recorded (community of Mark) between 1991 and 1998. There were no wild predators in Mark during this period implying that natural mortalities were synonymous with mortality caused by disease. Without predators it ap- pears that the mortality risk due to disease has been quite low in the 1980s and 1990s, but the relative risk of ELA and MWS was high. Our description of diseases and natu- ral mortalities differs from that of Guilazov (1998) who described predation as the primary mortality factor in moose of Northern Russia. Based on our results, the risk of being killed by predators was low in the late 1980s. Only 25 of the moose in the entire sample were killed by wolves suggesting that predation was not common. Future Scenario Currently, winter populations of moose and roe deer in Sweden are approximately 250,000 and 1.5 million, respectively (Stéen et al. 1998b). Predators have increased sub- stantially in recent decades. Wolves were protected in Sweden when estimated num- approximately 67-81 (Aronsson et al. 2001). In the 1930s, 130 brown bears were known, and in 60 years (1996) they had increased to 800-1,300 (SOU 1999). It is realistic to believe that, despite future increase in numbers and range expansion, harvesting of predators will remain banned or be highly regulated by the from predation will no doubt result. Interactions between risk of disease and predation may result in compensatory rather than additive death. For moose, the risk of being killed by wolves or bears depends on age (e.g., van Ballenberghe 1987, Ballard and van Ballenberghe 1998, SOU 1999, Wikenros 2001). Ballard and van Ballenberghe (1998) showed that calves and old cows are the pri- mary target of wolves. Predation by bears was the most frequent cause of early calf mortality (Franzmann and Schwartz 1986; Boertje et al. 1987, 1988). Franzmann and Schwartz (1986) estimated bear density in Alaska to be 19.0/100 km2. This compares to a desirable density of at least 0.7/100 km2 anticipated outside the Swedish reindeer husbandry area (61°N to 69°N) (SOU 1999). Swedish studies of bear predation on moose calves indicate a 20-25% loss, while bears accounted for 0.5-1.5% of adult mortalities (SOU 1999). Studies in both Sweden and North America indicate that bear predation on calves is additive, at approxi- ALCES VOL. 41, 2005 STÉEN ET AL. - DISEASES IN MOOSE 45 mately 3 calves per bear/year (SOU 1999). SOU (1999) reports that natural mortality of adults was approximately 5% in an area with no predation and that the additive loss of adults by bear predation was 0.5-1.5% per bear/year. While predation on calves is mostly likely additive, van Ballenberghe (1987) stated that predation on adults was mostly compensatory, with the various mortality factors tending to substitute more for each other. Ballard and van Ballenberghe (1998) cite Mech et al. (1995) whose results show that wolf-predated calves and adults during winter have low marrow fat values, indicating poor condition. Also, Peterson (1977) reported that wolves from Isle Royale prey on heavily parasitized, diseased, or otherwise inferior moose. This information suggests that in the future, the weak, vulner- able, sick, and old moose will be preyed upon before dying from a disease. We suggest that the panorama of moose diseases seen in the future will differ from that seen during the 1980s and 1990s by being less visible due to increasing predation. REFERENCES ARONSSON, Å., P. WABAKKEN, H. SAND, O. K. STEINSET, and I. KOJOLA. 2001. Varg i Skandinavien. Statusrapport, för vintern 2000/2001. (The wolf in Scandinavia: status report of the 2000/2001 winter). (In Swedish with English summary). BALLARD, W. B., and V. VAN BALLENBERGHE. 1998. Predator/prey relationships. Pages 247-273 in A. W. Franzmannn and C. C. Schwartz, editors. Ecology and Man- agement of the North American Moose. Smithsonian Institution Press, Washing- ton, D.C., USA. BOERTJE, R. D., W. C. GASAWAY, D. V. GRANA- GAARD, and D. G. KELLEYHOUSE. 1988. Predation on moose and caribou radio- collared grizzly bears in East-central Alaska. Canadian Journal of Zoology 66:492-499. _____, _____, _____, _____, and R. O. STE- PHENSON. 1987. Factors limiting moose population growth in subunit 20 E. Fed- eral Aid in Wildlife Restoration Report. Alaska Department of Fish and Game, Juneau, Alaska, USA. BORG, K. 1956. Vilt och viltsjukdomar. Pages 314-342 in I. Lauritzon, editor. Lantbrukets djurbok III. Strömberg, Stockholm, Sweden. (In Swedish). _____. 1975. Viltsjukdomar. LTs förlag, Stockholm, Sweden. (In Swedish). _____. 1987. A review of wildlife diseases from Scandinavia. Journal of Wildlife Diseases 23:527-533. _____. 1991. Rådjur. Dödsorsaker, miljöpåverkan och rättsmedicin. Swed- ish Environmental Protection Agency, Naturvårdsverkets rapport 3921. (In Swedish). ____, and P. O. NILSSON. 1985. Silbenstumörer hos älg och rådjur (Ethmoid tumors in elk and roe deer). Nordique Veterinary Medecine 37:145-160. (In Swedish with English summary). BROMAN, E., K. WALLIN, M. STÉEN, and G. CEDERLUND. 2002a. A wasting syndrome in Swedish Moose (Alces alces): Back- ground and current hypotheses. Ambio 31:409-416. _____, _____, _____, and_____. 2002b. “Mass” deaths of moose Alces alces in southern Sweden: Population level characterization. Wildlife Biology 8:209- 218. CEDERLUND, G., and R. BERGSTRÖM. 1996. Trends in the moose-forest system in Fennoscandia, with special reference to Sweden. Pages 265-281 in R.M. De Graaf and R. I. Miller, editors. Conservation of Faunal Diversity in Forested Landscapes. _____, and G. MARKGREN. 1987. The develop- ment of the Swedish moose population, 1970-1983. Viltrevy, Swedish Wildlife Research Supplement 1:55-61. DISEASES IN MOOSE – STÉEN ET AL. ALCES VOL. 41, 2005 46 FEINSTEIN, R., C. REHBINDER, E. RIVERA, T. NIKKILÄ, and M. STÉEN. 1987. Intracy- toplasmic inclusion bodies associated with vesicular, ulcerative and necrotiz- ing lesions of the digestive mucosa of a roe deer (Capreolus capreolus L.) and a moose (Alces alces L.). Acta Veterinaria Scandinavica 28:197-200. FRANK, A. 1998. 'Mysterious' moose disease in Sweden: similarities to copper deficiency and/or molybdenosis in cattle and sheep. Biochemical background of clinical signs and organ lesions. Science of the Total Environment 209:17-26. _____, M. ANKE, and R. DANIELSSON. 2000a. Experimental copper and chromium de- ficiency and additional molybdenum sup- plementation in goats. I. Feed consump- tion and weight development. Science of the Total Environment 249:133-142. _____, R. DANIELSSON, and B. JONES. 2000b. The 'mysterious' disease in Swedish moose. Concentrations of trace elements in liver and kidneys and clinical chem- istry. Comparisons with experimental molybdenosis and copper deficiency in the goat. Science of the Total Environ- ment 249:107-122. _____, _____, and _____. 2000c. Experi- mental copper and chromium deficiency and additional molybdenum supplementa- tion in goats. II. Concentrations of trace and minor elements in liver, kidneys and - try. Science of the Total Environment 249:143-170. _____, V. GALGAN, and L. R. PETERSSON. 1994. Secondary copper deficiency, chromium deficiency and trace element imbalance in moose (Alces alces L.): Effects of an anthropogenic activity. Ambio 23:315- 317. _____, D. S. SELL, R. DANIELSSON, J. F. FOGARTY, and V. M. MONNIER. 2000d. A syndrome of molybdenosis, copper deficiency, and type 2 diabetes in the moose population of south-west Sweden. Science of the Total Environment 249:123-131. FRANZMANN, A. W., and C. C. SCHWARTZ. 1986. Black bear predation on moose calves in highly productive versus marginal moose habitat on the Kenai Peninsula, Alaska. Alces 22:139-153. GAJADHAR, A., T. STEEVES-GURNSEY, J. KEN- DALL, M. LANKESTER, and M. STÉEN. 2000. Differentiation of dorsal-spined elaphostrongyline larvae by polymerase chain reaction amplification of ITS-2 of rDNA. Journal of Wildlife Diseases 36:713-722. GUILAZOV, A. S. 1998. Causes of reindeer (Rangifer tarandus) and moose (Alces al- ces) mortality in the Lapland Reserve and its surroundings. Alces 34:319-327. HALVORSEN, O. 1986. Epidemiology of reindeer parasites. Parasitology Today 2:334-339. LANKESTER, M. 1987. Pests, parasites and diseases of moose (Alces alces) in North America. Swedish Wildlife Research Supplement 1:461-490. _____, I-M. OLSSON, M. STÉEN, and A. A. GAJADHAR. 1998. Extra-mammalian larval stages of Elaphostrongylus alces (Nematoda: Protostrongylidae), a parasite of moose (Alces alces) in Fennoscandia. Canadian Journal of Zoology 76:33-38. _____, and W. SAMUEL. 1998. Pests, parasites and diseases. Pages 479-517 in A. W. Franzmannn and C. C. Schwartz, editors. Ecology and Management of the North American Moose. Smithsonian Institution Press, Washington, D.C., USA. MECH, L. D., T. J. MEIER, J. W. BURCH, and L. G. ADAMS. 1995. Patterns of prey selec- tion by wolves in Denali National Park, Alaska. In D. Seip, editors. Ecology and Conser- vation of Wolves in a Changing World. Proceedings of the 2nd International Wolf Symposium. Canadian Circumpolar In- stitute, University of Alberta, Edmonton, ALCES VOL. 41, 2005 STÉEN ET AL. - DISEASES IN MOOSE 47 Alberta, Canada. MERCK VETERINARY MANUAL - book of Diagnosis and Therapy for the Veterinarian. Fifth Edition. Merck & Co., Inc., Rahway, New Jersey, USA. MERZA, M., E. LARSSON, M. STÉEN, and B. MOREIN. 1994. Association of a retrovirus with a wasting condition in the Swedish moose. Virology 202:956-961. MORENO-LOPÉZ, J. 1979. A serosurvey of viruses during outbreaks of acute respi- ratory and/or enteric disease in Swedish B 26:634-640. MÖRNER, T. 2001. Var tog Älvsborgssjukan vägen? (Where did “the Älvsborg disease” disappear?) Svensk jakt 11:64-65. (In Swedish). NILSSON, O. 1971. The interrelationship of endoparasites in wild cervids (Capreolus capreolus L. and Alces alces L.) and domestic ruminants in Sweden. Acta Veterinaria Scandinavica 12:36-68. OLSSON, I.-M. 2001. Elaphostrongylus alces – transmission, larval morphology and tissue migration. M.Sc. Thesis, Swedish University of Agricultural Sciences, Up- psala, Sweden. _____, R. BERGSTRÖM, M. STÉEN, and F. SAND- GREN. 1995. A study of Elaphostrongylus alces in an island moose population with low calf body weights. Alces 31:61-75. _____, M. W. LANKESTER, A. A. GAJADHAR, and M. STÉEN. 1998. Tissue migration of Elaphostrongylus spp. in guinea pigs (Cavia porcellus). Journal of Parasitology 84:968-975. _____, M. STÉEN, and H. MANN. 1993. Gas- tropod hosts of Elaphostrongylus spp. (Protostrongylidae, Nematoda). Rangifer 13:53-55. PETERSON, R. O. 1977. Wolf ecology and prey relationships on Isle Royale. U.S. National Park Service, Science Mono- graph Series 11. REHBINDER, C., K. GIMENO, K. BELAK, S. BELAK, M. STEEN, M. RIVERA, and T. NIKKILÄ. 1991. A bovine viral diarrhoea/mucosal disease-like syndrome in moose (Alces alces): investigations on the central nervous system. Veterinary Record 129:552-554. REIMERS, E., and O. NORDBY. 1968. Relation- ship between age and tooth cementum layers in Norwegian reindeer. Journal of Wildlife Management 32:957-961. ROCKBORN, G., C. REHBINDER, B. KLINGEBORN, M. LEFFLER, K. KLINTEVALL, T. NIKKILÄ, A. LANDÉN, and M. NORDKVIST. 1990. The demonstration of a herpesvirus related to bovine herpesvirus 1, in reindeer with ulcerative and necrotizing lesions of the upper alimentary tract and nose. Rangifer 10:373-384. SAETHER, B.-E., and M. HEIM. 1993. Ecological correlates of individual variation in age at maturity in female moose (Alces alces); the effects of environmental variability. Journal of Animal Ecology 62:482-489. (SJV) SWEDISH BOARD OF AGRICULTURE. 1994. Viktiga smittsamma sjukdomar. Swedish Board of Agriculture, Jönköping, Sweden. (In Swedish). SKUNKE, F. 1949. Älgen. Studier, jakt och vård. Stockholm, Sweden. (In Swedish). (SOU) STATENS OFFENTLIGA UTREDNINGAR. 1999. Sammanhållen rovdjurspolitik. Slutbetänkande av rovdjursutredningen. Statens offentliga utredningar (SOU 1999:146) and appendix, The Swedish government, Stockholm, Sweden. (In Swedish). STÉEN, M. 1991. Elaphostrongylosis. A clini- cal, pathological, and taxonomical study with special emphasis on the infection in moose. Ph.D. Thesis, Swedish Univer- sity of Agricultural Sciences, Uppsala, Sweden. _____, C. G. M. BLACKMORE, and A. SKORPING. 1997. Cross infection of moose (Alces alces) and reindeer (Rangifer taran- dus) with Elaphostrongylus alces and DISEASES IN MOOSE – STÉEN ET AL. ALCES VOL. 41, 2005 48 Elaphostrongylus rangiferi (Nematoda, Protostrongylidae): Effects on parasite morphology and prepatent period. Vet- erinary Parasitology 71:27-38. _____, A. G. CHAUBAUD, and C. REHBINDER. 1989. Species of the genus Elaphostron- gylus parasite of Swedish cervidae. A description of E. alces n.sp. Annales de 64:134-142. _____, and R. DIAZ. 1988. Studies of a bovine virus diarrhea/mucosal disease like syn- drome in Swedish moose (Alces alces L.). M.Sc Thesis, Swedish University of Agri- cultural Sciences, Uppsala, Sweden. _____, _____, and W. E. FABER. 1993. An erosive/ulcerative alimentary disease of undetermined etiology in Swedish moose (Alces alces L.). Rangifer13:149-156. _____, W. E. FABER, and A. OKSANEN. 1998b. Disease and genetical investigations of Fennoscandian cervids – A review. Alces 34:287-310. _____, and C. JOHANSSON. 1990. Elaphostron- gylus spp. from Scandinavian cervidae – a scanning electron microscope study (SEM). Rangifer 1:39-46. _____, S. PERSSON, and L. HAJDU. 1994. Protostrongylidae in Cervidae and Ovibos muscatus: A clustering based on isoelec- tric focusing on nematode body proteins. Applied Parasitology 35:193-206. _____, and C. REHBINDER. 1986. Nervous tissue lesions caused by Elaphostrongylus in wild Swedish moose. Acta Veterinaria Scandinavica 27:336-342. _____, and L. ROEPSTORFF. 1990. Neurological disorder in two moose calves (Alces alces L.) naturally infected with Elaphostron- gylus alces. Rangifer 3:399-406. _____, I. WARSAME, and A. SKORPING. 1998a. Experimental infection of reindeer, sheep and goats with Elaphostrongylus spp. (Nematoda, Protostrongylidae) from moose and reindeer. Rangifer 18:73-80. STUVE, G. 1986. The prevalence of Ela- phostrongylus cervi infection in moose (Alces alces) in southern Norway. Acta Veterinaria Scandinavica 27:397-409. VAN BALLENBERGHE, V. 1987. Effects of preda- tion on moose numbers: A review of recent North American studies. Swedish Wildlife Research Supplement 1:431-460. _____, and W. B. BALLARD. 1998. Popula- tion dynamics. Pages 223-246 in A. W. Franzmannn and C. C. Schwartz, editors. Ecology and Management of the North American Moose. Smithsonian Institution Press, Washington, D.C., USA. WARSAME, I. Y., and M. STÉEN. 1989. Ma- lignant catarrhal fever in Swedish moose (Alces alces L). Rangifer 9:51-57. WIKENROS, C. 2001. Wolf winter predation on moose and roe deer in relation to pack size. Department of Conservation Biol- ogy, Grimsö Wildlife Research Station, Riddarhyttan, Sweden, No. 75. WOBESER, G. 1981. Diseases of Wild Water- fowl. Plenum Publishing Corporation, _____. 1994. Investigation and Management of Disease in Wild Animals. Plenum << /ASCII85EncodePages false /AllowTransparency false /AutoPositionEPSFiles true /AutoRotatePages /All /Binding /Left /CalGrayProfile (Dot Gain 20%) /CalRGBProfile (sRGB IEC61966-2.1) /CalCMYKProfile (U.S. Web Coated \050SWOP\051 v2) /sRGBProfile (sRGB IEC61966-2.1) /CannotEmbedFontPolicy /Warning /CompatibilityLevel 1.4 /CompressObjects /Tags /CompressPages true /ConvertImagesToIndexed true /PassThroughJPEGImages true /CreateJDFFile false /CreateJobTicket false /DefaultRenderingIntent /Default /DetectBlends true /DetectCurves 0.0000 /ColorConversionStrategy /LeaveColorUnchanged /DoThumbnails false /EmbedAllFonts true /EmbedOpenType false /ParseICCProfilesInComments true /EmbedJobOptions true /DSCReportingLevel 0 /EmitDSCWarnings false /EndPage -1 /ImageMemory 1048576 /LockDistillerParams false /MaxSubsetPct 100 /Optimize true /OPM 1 /ParseDSCComments true /ParseDSCCommentsForDocInfo true /PreserveCopyPage true /PreserveDICMYKValues true /PreserveEPSInfo true /PreserveFlatness true /PreserveHalftoneInfo false /PreserveOPIComments false /PreserveOverprintSettings true /StartPage 1 /SubsetFonts true /TransferFunctionInfo /Apply /UCRandBGInfo /Preserve /UsePrologue false /ColorSettingsFile () /AlwaysEmbed [ true ] /NeverEmbed [ true ] /AntiAliasColorImages false /CropColorImages true /ColorImageMinResolution 300 /ColorImageMinResolutionPolicy /OK /DownsampleColorImages true /ColorImageDownsampleType /Bicubic /ColorImageResolution 300 /ColorImageDepth -1 /ColorImageMinDownsampleDepth 1 /ColorImageDownsampleThreshold 1.50000 /EncodeColorImages true /ColorImageFilter /DCTEncode /AutoFilterColorImages true /ColorImageAutoFilterStrategy /JPEG /ColorACSImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /ColorImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /JPEG2000ColorACSImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /JPEG2000ColorImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /AntiAliasGrayImages false /CropGrayImages true /GrayImageMinResolution 300 /GrayImageMinResolutionPolicy /OK /DownsampleGrayImages true /GrayImageDownsampleType /Bicubic /GrayImageResolution 300 /GrayImageDepth -1 /GrayImageMinDownsampleDepth 2 /GrayImageDownsampleThreshold 1.50000 /EncodeGrayImages true /GrayImageFilter /DCTEncode /AutoFilterGrayImages true /GrayImageAutoFilterStrategy /JPEG /GrayACSImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /GrayImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /JPEG2000GrayACSImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /JPEG2000GrayImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /AntiAliasMonoImages false /CropMonoImages true /MonoImageMinResolution 1200 /MonoImageMinResolutionPolicy /OK /DownsampleMonoImages true /MonoImageDownsampleType /Bicubic /MonoImageResolution 1200 /MonoImageDepth -1 /MonoImageDownsampleThreshold 1.50000 /EncodeMonoImages true /MonoImageFilter /CCITTFaxEncode /MonoImageDict << /K -1 >> /AllowPSXObjects false /CheckCompliance [ /None ] /PDFX1aCheck false /PDFX3Check false /PDFXCompliantPDFOnly false /PDFXNoTrimBoxError true /PDFXTrimBoxToMediaBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXSetBleedBoxToMediaBox true /PDFXBleedBoxToTrimBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXOutputIntentProfile () /PDFXOutputConditionIdentifier () /PDFXOutputCondition () /PDFXRegistryName () /PDFXTrapped /False /Description << /CHS /CHT /DAN /DEU /ESP /FRA /ITA /JPN /KOR /NLD (Gebruik deze instellingen om Adobe PDF-documenten te maken voor kwaliteitsafdrukken op desktopprinters en proofers. De gemaakte PDF-documenten kunnen worden geopend met Acrobat en Adobe Reader 5.0 en hoger.) /NOR /PTB /SUO /SVE /ENU (Use these settings to create Adobe PDF documents for quality printing on desktop printers and proofers. Created PDF documents can be opened with Acrobat and Adobe Reader 5.0 and later.) >> /Namespace [ (Adobe) (Common) (1.0) ] /OtherNamespaces [ << /AsReaderSpreads false /CropImagesToFrames true /ErrorControl /WarnAndContinue /FlattenerIgnoreSpreadOverrides false /IncludeGuidesGrids false /IncludeNonPrinting false /IncludeSlug false /Namespace [ (Adobe) (InDesign) (4.0) ] /OmitPlacedBitmaps false /OmitPlacedEPS false /OmitPlacedPDF false /SimulateOverprint /Legacy >> << /AddBleedMarks false /AddColorBars false /AddCropMarks false /AddPageInfo false /AddRegMarks false /ConvertColors /NoConversion /DestinationProfileName () /DestinationProfileSelector /NA /Downsample16BitImages true /FlattenerPreset << /PresetSelector /MediumResolution >> /FormElements false /GenerateStructure true /IncludeBookmarks false /IncludeHyperlinks false /IncludeInteractive false /IncludeLayers false /IncludeProfiles true /MultimediaHandling /UseObjectSettings /Namespace [ (Adobe) (CreativeSuite) (2.0) ] /PDFXOutputIntentProfileSelector /NA /PreserveEditing true /UntaggedCMYKHandling /LeaveUntagged /UntaggedRGBHandling /LeaveUntagged /UseDocumentBleed false >> ] >> setdistillerparams << /HWResolution [2400 2400] /PageSize [612.000 792.000] >> setpagedevice