HAIR-LOSS EPIZOOTIC IN MOOSE (ALCES ALCES) ASSOCIATED WITH MASSIVE DEER KED (LIPOPTENA CERVI)...

HAIR-LOSS EPIZOOTIC IN MOOSE (ALCES ALCES) ASSOCIATED

WITH MASSIVE DEER KED (LIPOPTENA CERVI) INFESTATION

Knut Madslien,1,5 Bjørnar Ytrehus,1 Turid Vikøren,1 Jonas Malmsten,2 Ketil Isaksen,3

Hans Olav Hygen,3 and Erling J. Solberg4

1 Section for Wildlife Diseases, National Veterinary Institute, Pb 750 Sentrum, N-0106 Oslo, Norway2 Department of Pathology and Wildlife Diseases, National Veterinary Institute, SVA, SE-751 89 Uppsala, Sweden3 Climatology Division, Norwegian Meteorological Institute, Niels Henrik Abels vei 40, N-0313 Oslo, Norway4 Norwegian Institute of Nature Research, NO-7485 Trondheim, Norway5 Corresponding author (email: [email protected])

ABSTRACT: Deer keds (Lipoptena cervi) are blood-sucking flies in the family Hippoboscidae;moose (Alces alces) are their main host in Scandinavia. There are no detailed reports of thenegative impacts of deer keds on moose. In 2006 and 2007, hunters in southeastern Norway andmidwestern Sweden found several moose cadavers with severe alopecia; numerous moose hadextensive hair loss. Between February 2006 and June 2007, materials from 23 moose weresubmitted for laboratory examination and large numbers of deer keds were found in the coat ofmost animals. The body condition of the moose varied but was poor in animals with severealopecia. The findings of enormous numbers of deer keds in the coat of the majority of the affectedanimals and a consistent histologic image (acute to chronic, multifocal to coalescing, eosinophilic tolymphocytic dermatitis), concurrent with the absence of any other lesions, trace elementdeficiencies, or dermal infections which are known to cause alopecia, suggest that the hair-lossepizootic was linked to massive infestations with deer keds. The emergence of this hair-losssyndrome implies that the dynamics between parasite and host have been disrupted by a currentlyunknown environmental or ecological factor. A high moose density, combined with extraordinarilymild weather June 2006–June 2007 and a particularly long period with the absence of night-frost inautumn of 2006, may have been ideal for deer ked development, survival, and optimal hostacquisition.

Key words: Alces alces, climate, deer ked, dermatitis, hair loss, Lipoptena cervi, populationdensity, pathology.

INTRODUCTION

The deer ked (Lipoptena cervi) is ablood-feeding ectoparasite that infests sev-eral cervid host species (Hackman et al.,1983). Deer ked females are viviparous andproduce new prepupae throughout theyear. Fully developed pupae passively dropout of the coat to the ground where theydevelop into winged imagos in late summerand early autumn. When the imagos reachtheir hosts, they lose their wings andremain on the same host for the rest oftheir lives (Haarløv, 1964). Keds have beenpresent in continental Europe since thestone age (Gothe and Schol, 1994) andwere described in southern Sweden asearly as 1758 (Linne, 1758). This parasitehas expanded its distribution west andnorthward in Scandinavia over the lastfew decades and is now abundant insoutheastern Norway and central Sweden(Fig. 1) (Valimaki et al., 2010). Factors

contributing to the increase in deer keddistribution and abundance are not fullyelucidated, although increases in hostanimal populations and changes in climatehave been suggested (Valimaki et al., 2010).

The deer ked is not reported to causedisease in the host (Allan, 2001), althoughStrose (1916) blamed the parasite forcausing focal hair loss and eczema in reddeer (Cervus elaphus). Darling (1963)reported that red deer seemed not toreact strongly to the deer ked but arguedthat the effect on the host must beconsiderable, without further describingthe cases. Fatigue and growth retardationhave been seen in fallow deer (Damadama) experiencing massive infestations ofdeer keds (Ivanov, 1974). Laaksonen(2009) reported that semidomesticatedreindeer (Rangifer tarandus) showed pru-ritus and developed focal alopecia afterinfestation with deer keds.

Journal of Wildlife Diseases, 47(4), 2011, pp. 893–906# Wildlife Disease Association 2011

893

We describe the clinical and pathologicfindings associated with epizootic hair lossamong moose in areas of southeastern Nor-way and midwestern Sweden where the deerked is abundant. We discuss to what degreethe hair-loss syndrome was associated withdeer ked infestation and to what extent localmoose population densities and weatherconditions were factors in the outbreak.

MATERIALS AND METHODS

Study area

The study area was in southcentral Scandina-via (59u069–62u169N, 10u279–15u139E; Fig. 1).The elevation ranges from sea level in thesouthwest to about 600 m in the north, coveringboth the middle boreal, southern boreal, andboreonemoral vegetation zones (Moen, 1998).The landscape is undulating with forest-coveredhills and some farmland in intersecting valleys.Forests are dominated by Scots pine (Pinussylvestris) and Norway spruce (Picea abies) and,to some extent, birch (Betula spp.).

Affected population

The moose population of the study area ismainly limited (and regulated) by hunting.Predation by wolves (Canis lupus) and a few

brown bears (Ursus arctos) also may have someimpact on the population (Sand et al., 2008).

Body mass and reproductive rates of mooseare relatively high, but variable, throughout thestudy area. Observations by moose hunterssuggest a decline in body condition during thelast 15 yr, particularly in the north (Solberget al., 2010). The decline is associated withincreasing population density and is thought tobe caused by food limitation (Lavsund et al.,2003). Data from radio-collared moose indicatethat moose in this area are sedentary (Lavsundet al., 2003). Moose population density in thestudy area is higher than the average forScandinavia. On a regional (county) scale,hunters harvested, on average, about 0.3–0.6moose per km2 of forest and bogs in 2000–2007(Solberg et al., 2010). During the same period,we estimated the preharvest moose density wasabout 1.0–1.4 adult ($1 yr old) moose per km2

(E.J. Solberg, unpubl. data).

Data collection

Nonconfirmed observations of alopecicmoose were based on phone and email corre-spondence with the National Veterinary Insti-tutes in Oslo, Norway (NVI) and Uppsala,Sweden (SVA). To estimate the prevalence ofalopecia in the moose population in Septemberand October 2007 and 2008, moose hunters infive Norwegian counties, representing areaswithin and outside the deer ked distributionrange, were asked to complete a questionnaireduring the moose hunting season. They wereasked to note if they had observed moose withhair loss and to classify the pattern of alopecia ona scale from 0 (no hair loss) to 5 (complete hairloss) according to a figure (Fig. 2). In March2007, two cows and one subadult with severehair loss were fitted with radio collars in Arjang,Sweden (Fig. 3a). The development of hair losswas monitored in these three animals; bloodsamples for hematology were drawn from thejugular vein at the time radio collars were fitted.

Specimen analysis

The patho-anatomical part of the study wasbased on an examination of material fromcarcasses and biopsy material from alopecicmoose submitted to NVI and SVA from thestudy area from February 2006–June 2007(Fig. 1, Table 1). In the laboratory, wholecarcasses were carefully inspected and de-scribed before the hide was removed andexamined. A full necropsy was performed andsamples of lung, heart, liver, kidney, brain,lymph nodes, thyroid gland, adrenal gland,and skin were collected and fixed in 10%neutral buffered formalin, dehydrated and

FIGURE 1. A map of southeastern Norway andmidwestern Sweden. Dark grey color representsmunicipalities with laboratory-confirmed cases ofalopecia caused by deer keds (Lipoptena cervi) inmoose (Alces alces), 2006–2007. Light grey repre-sents municipalities with observed severe alopecicmoose in the field. The known distribution of deerked in Norway is east of the dotted line.

894 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011

embedded in paraffin, sectioned at 5 mm, andstained with hematoxylin and eosin and vanGieson for histologic examination. Standardbacteriologic examination on calf blood agarplates was performed on samples from liver(n512), spleen (n59), and skin (n514). Theplates were incubated aerobically at 37 C andexamined after 24–48 hr. Biopsies from bothaffected and normal skin were collected forroutine parasitologic (n511) and mycologic(n515) examination. All visible deer keds andpupae in the coat of four animals werecollected and counted. Liver samples from

FIGURE 3. (A) Adult, female moose (Alces alces)with typical pattern of alopecia, radio collared inMarch 2007 in Varmland county, Sweden. (B) Thesame moose, in September 2007, showing regrowthof the coat on neck and withers. Photo: GunnarGloersen, Swedish Hunters Association.

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FIGURE 2. Alopecia in moose (Alces alces), asassessed by hunters in the field during the 2007and 2008 hunting seasons in Norway and Sweden: 1)No visible hair-loss, 2) slight hair loss; spots ofalopecia affecting about 5 to 20%, especially thoraxand ventral neck, 3) moderate hair loss; about 30 to40% of coat lost and remaining coat sparse, 4) severehair loss, about 40 to 80% of coat lost, 5) nakedmoose; more than 80% hair loss. Figure inspired byfigure 1 in Samuel (1989).

MADSLIEN ET AL.—HAIR-LOSS EPIZOOTIC IN SCANDINAVIAN MOOSE 895

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12 moose were frozen at 220 C prior tocarrying out trace element analysis for copper,selenium, and cobalt (Vikøren et al., 2005).

Meteorologic data collection

We used meteorologic data from Garder-moen (elevation: 202 m) weather station,which is representative for the inland areasof southeastern Norway and adjacent areas ofSweden. Gardermoen is an automated weath-er station that provides hourly measurementsof precipitation, temperature, humidity, wind,and pressure. Prior to 2009, these variableswere measured manually every 3–6 hr, de-pending on weather and time of day. Wewanted to elucidate factors that may influenceoff-host survival and development of deerkeds, as well as host acquisition of wingedkeds. Temperature influences deer ked devel-opment (Harkonen et al., 2010) and repeatedfreezing and thawing may be unfavorable forparasite survival (Davidson et al., 2008), withthe pupal stage on the ground being mostvulnerable. Hence, we looked at the depth andduration of snow cover and temperaturefluctuations around zero degrees C. Warmand sunny weather may facilitate host acqui-sition by winged keds, while frost is probablyless beneficial; therefore, we also includeddegree-days (daily mean temperature multi-plied by the number of days), length ofgrowing season (sum of days with daily meantemperature .5 C), precipitation, and firstfrost in the autumn.

RESULTS

Field observations

Earlier reports of alopecia in moose inthe study area are scarce. On February 13,2006, wildlife managers in Marker munic-ipality, Norway (Fig. 1), reported a sub-adult, female moose with severe hair loss,emaciation, and abnormal behavior. Theanimal was euthanized after seeking shel-ter in a farm building and submitted toNVI for necropsy (moose 1, Table 1). InOctober 2006, wildlife managers in theneighboring municipality of Rømskog(Fig. 1) reported that five of 60 huntedmoose had severe hair loss and thatmoose, in general, were severely infestedwith deer keds. Skin samples from one ofthe alopecic moose were submitted to NVI(moose 2, Table 1). In November and

December 2006, 11 alopecic moose werereported in the same area; three werefound dead and eight were euthanized (J.Moen, pers. comm.). In Sweden, betweenArjang and Filipstad (Fig. 1), hunterseuthanized 12 and observed another 50moose with severe hair loss during theautumn of 2006 and winter of 2007 (G.Gloersen, pers. comm.). From December2006 to June 2007, skin samples or wholecarcasses from an additional 21 moose(moose 3–23), representing seven differ-ent municipalities in the study area inNorway and two in Sweden, were submit-ted to NVI and SVA (Table 1). During thisperiod, wildlife managers and laymen alsoreported observations of alopecic moose inanother nine municipalities; two in Feb-ruary, one in March, three in April, andthree in May (Fig. 1). According to thereports, severely alopecic moose seemedto be in poor condition and did notrespond to human activity. Pruritus, how-ever, was not observed.

Necropsy findings

Seventeen whole carcasses and biopsymaterial from six animals were submittedto NVI (n521) and SVA (n52) from thestudy area from February 2006–June 2007(Fig. 1). Twenty of the animals wereeuthanized because of severe alopecia,two were found dead, and one (moose 14)was a normally coated calf, shot simulta-neously with a female alopecic moose.

The necropsy of the index case (moose1, Table 1) revealed severe, bilateralalopecia and moderate, crusting dermatitisinvolving the cheeks, ventral neck, lateralthorax, abdomen, and haunch. A largenumber of deer keds were observed onthe carcass, most in areas that were stillcovered with hair. The lymph nodes of thebody were generally enlarged, but noother specific gross lesions were noted.Histologic examination of alopecic areasrevealed moderate and diffuse orthoker-atotic hyperkeratosis and diffuse, moder-ate hyperplasia of the epidermis, withmoderate formation of rete ridges (Fig. 4).


The hair follicles showed moderate kera-tosis, with the infundibulum of the major-ity of the follicles dilated with keratinplugs of exfoliated corneum and debris.The hair bulbs had the appearance of‘‘flame follicles’’ (i.e., follicles morpholog-ically characterized by excessive trichilem-

mal keratinization, giving the impressionof a flickering flame). Sebaceous andsweat glands appeared relatively normalbut had prominent, thickened basal mem-branes. The dermis showed increasedcellularity consisting of diffuse, mild tomoderate infiltrates of eosinophilic granu-

FIGURE 4. Skin histology of alopecic moose (Alces alces). (a) Sparse coat; inflammatory infiltrates indermis, flame follicles, and follicular keratosis. (b) Sparse coat; perivascular infiltration of eosinophils,macrophages, and plasma cells. (c) Alopecic skin, orthokeratotic hyperkeratosis, acanthosis, intracornealpustule, and follicular keratosis. (d) Sparse coat; orthokeratotic hyperkeratosis, perivascular infiltration ofeosinophils, macrophages, and plasma cells and a follicle filled with these cells. (e) Alopecic skin; acanthosis,dermal fibrosis, and perivascular infiltration of macrophages and lymphocytes. (f) Sparse coat; acanthosis, andfibrosis. a, b, c5moose 6 (see Table 1), d5moose 16, e5moose 18, f5moose 20. All are hematoxylin andeosin-stained sections, except for f, which is van Gieson stained. Bar5100 mm in all sections.


locytes, macrophages, plasma cells, andlymphocytes. A diffuse, mild edema and adiffuse, moderate increase in the amountof regularly organized connective tissue inthe dermis were also observed. The vesselsof the dermis appeared contorted andwere characterized by hypertrophic endo-thelium with prominent nuclei and athickened basal membrane. In areaswhere some hair was still present, the skinwas characterized by mild, diffuse ortho-keratotic hyperkeratosis, a mild focalhyperplasia of the epidermis, and occa-sional intraepidermal pustules. The chang-es in the dermis were similar to those inalopecic areas, but the increase in con-nective tissue was less prominent andcharacterized by irregularly organizedfibers.

The macroscopic changes in animalnumbers 2–23 showed large similaritieswith each other and with the casedescribed above. The general pattern wasbilateral, fairly symmetric alopecia on theventral neck, sides, and abdomen whilethe dorsal neck, back, and limbs showedless-prominent hair loss. Moose 14 did notshow alopecia but had skin changes asdescribed below. In the alopecic animals,the naked skin showed varying degrees ofhyperpigmentation (increasing with daylength) and was diffusely thickened andcovered by light, removable crusts butappeared otherwise relatively smooth anddid not show obvious papules, erythema,or erosive ulcerative lesions. Althoughsingle hairs were broken, the generalimpression was that hairs were eitherpresent at full length or not present. Selftrauma, consistent with scratching, wasnot a common finding. The remaining haircoat appeared dull and the hairs wereeasily epilated. Ked infestation was con-firmed in the majority of cases (17 of 23;Table 1). Keds were distributed through-out the animal, except distally on thelimbs, but only a few specimens werefound in alopecic areas. The keds aggre-gated in the axillae, neck, groin, andperineal region. In fresh carcasses, the

insects were located on the surface of theskin, their head oriented towards the skin,while they crawled out on the protectivehairs as the carcass cooled. The woolenhairs of severely infested animals weresmeared with a reddish-brown, dust-likematerial, probably deer ked feces mixedwith moose blood. The infestation inten-sity was highest in the animals examined inDecember–February (2006–2007), whilefew deer keds were found in May andJune 2007. The body condition of themoose varied, although it was poor in theanimals with severe alopecia, and therewere no consistent changes in the internalorgans.

Histologic presentation varied depend-ing on the month of examination. Ingeneral, histologic examination of theskin revealed a mild to moderate diffuseorthokeratotic hyperkeratosis and mild tomoderate multifocal to diffuse hyperplasiaof the epidermis (acanthosis). In somecases, affected epidermis showed multifo-cal small ulcerations, micropustules, andserocellular crusts. The dermis was charac-terized by multifocal to coalescing, mild tomoderate infiltrates of inflammatory cells.The infiltrates had a perivascular distributionand were found in both the superficial andthe deep dermis. During the first half of theepizootic, they were dominated by eosino-philic granulocytes while lymphocytes, mac-rophages, and plasma cells were moreprominent in the spring and early summer.Blood vessels adjacent to inflammatoryinfiltrates were contorted and showed endo-thelial hypertrophy. Inflammatory changeswere most severe and acute in areas with aremaining coat, while alopecic areas wereoften characterized by milder, mononuclearinfiltrates. Increased amounts of irregularlyorganized connective tissue (fibrosis) weremost pronounced in chronic cases (i.e., in latewinter and spring) and in denuded areas.During autumn, winter, and early spring thehair follicles appeared as flame follicles.However, in May–June, a gradual shift toanagen follicles was observed (Table 2). Thedensity of follicles and dermal papillae did


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not show any obvious association withalopecia, deer ked infestation, or time of year.

Parasitologic examination

Seven of the 11 skin samples examinedfor ectoparasites other than deer keds werenegative, while low numbers of Chorioptesspp. were found in four animals.

Microbiologic culture results

Most skin samples had negative bacterialcultures, although Staphylococcus aureus(n56), Streptococcus agalactiae (n52),Pasteurella multocida multocida (n51)and Clostridium perfringens (n51) wereisolated from some skin samples. Mycolo-gic examinations were negative except forone moose on which Scopulariopsis brevi-caulis was isolated.

Trace elements

Liver concentrations (mg/g wet weight)of trace elements were (mean6SEM):cobalt 0.1160.01, selenium 0.9760.20,and copper 74.867.98.

Observations and blood analysis ofcaptured moose

Hemoglobin values from the capturedanimals in March 2007 were 124, 144, and145 g/l (normal range: mean6SD 125.5 6

9.9; Adolfsson, 1993). In September 2007,both radio-collared cows were observedand appeared healthy with a coat, al-though slightly sparse, covering formerdenuded areas (Fig. 3b).

Observations during hunting seasons 2007and 2008

In Norway, 16,845 moose were ob-served and reported in the questionnaireanswered by moose hunters in autumn2007. Twenty (0.12%) animals had alope-cia (nine adult females, eight adult males,two calves, and one animal with ageunclassified). Of these, 15 were scored ashaving grade 2 alopecia while the remain-ing five were scored as grade 3. In 2008,only one (subadult female) of 15,136(0.007%) was alopecic (grade 2).

Weather

Weather conditions for winter 2005–2006 were fairly normal, but summer andautumn 2006 were milder than normal(Table 3). The 365-day running mean airtemperature for the period from 11 June2006–10 June 2007 was by far the highestsince records at Gardermoen began in 1940(Fig. 5a). The temperature was threestandard deviations above the correspond-ing mean temperature of the normal period(1961–1990). Furthermore, autumn 2006was characterized by an extraordinarily latearrival of the first frost night after August 1(87 days, average is 47; Fig. 5b).

DISCUSSION

Based on the pathologic skin changes ofalopecic moose, the massive deer kedinfestation in affected animals, and theabsence of findings indicative of any otherconsistent factor (other ectoparasites, in-fectious agents, endocrine disorders, ordeficiencies) that could be a plausiblecause of such a condition, we concludethat severe deer ked infestation was a keyfactor in the current outbreak. However,deer keds were not found on two alopecicbulls from Rendalen, north of the deerked distribution range (Fig. 1) nor on four(one in March, three in June) alopecicanimals inside the deer ked area. Youngmoose bulls can disperse considerabledistances (up to 250 km) from their birtharea before they establish a more perma-nent home range (Hundertmark, 2007).Hence, the two bulls from Rendalen mayhave been born within the deer ked rangeand may have experienced massive deerked infestation as calves before dispersal.The hair loss in these two animals may, assuch, represent chronic, partially healedlesions. The absence of the parasite in thelast three cases may be explained by thedeer ked life cycle; the adult ectoparasitesare thought to die during spring andsummer (Haarløv, 1964).

In Canada, premature winter hair lossin moose associated with the presence of


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the winter tick (Dermacentor albipictus)has been described (McLaughlin andAddison, 1986). The winter tick wasreported once in Norway, found on animported horse from the USA, but theparasite is currently not present (Lillehauget al., 2002).

Chorioptes spp. may cause skin lesionsin the outer ear canal of moose (Hestvik etal., 2007) and have also been associatedwith single cases of generalized alopecia inmoose in Norway and Sweden. Histolog-ically, the ear skin lesions caused by this

mite seem quite similar to those seen inour study. However, moose with massiveChorioptes infestation typically show apatchy pattern of alopecia, compared tothe confluent pattern seen in the currentoutbreak. Also, Chorioptes was not foundin the majority of our cases. Otherectoparasites known to cause alopecia incervids, including chewing lice (Cervicolasp.; Bildfell et al., 2004), sarcoptic mange(Sarcoptes scabiei; Bornstein et al., 2001),and mites of the genus Demodex (Genteset al., 2007) were not found in our study.

Several endocrine dermatopathiescause alopecia in cattle, among themhypovitaminosis A and hypothyroidism(Ginn et al., 2007). Blood plasma levelsof vitamin A and thyroxin were notexamined in our material, but the histo-logic changes were not consistent with anendocrine dermatopathy. Deficiencies ofcopper (Frank, 1998) and cobalt (Kennedyet al., 1997), and selenium intoxication(Kaur et al., 2003), are reported to beassociated with alopecia in animals. In ourstudy, these trace elements were not attoxic or deficient levels based on the NVI’scriteria set for cattle.

In Belarus, Ivanov (1974) reported thatall moose hunted during the autumnharbored deer keds in their coat with anaverage of about 1,000 keds per moose. InFinland, average numbers of keds innormally coated cows and calves were3,549 and 1,730, respectively (Paakkonenet al., 2010). We found 16,496, 11,014,and 5,938 keds in the coats of three cowswith severe hair loss and 10,687 in the coatof a calf with a normal coat (Table 1). Weconsider these numbers to be very high,taking into account that keds preferhabitats with hair-covered skin (Haarløv,1964), and it can be presumed that amajor proportion of the initial ked popu-lation may have been lost together withthe hair. Consequently, perhaps the highdensity of deer keds, biting and feeding15 to 20 times per day (Ivanov, 1974),exceeded a threshold of what moose skincould tolerate, thus triggering a cascade of

FIGURE 5. Meteorologic data from the Garder-moen weather station (elevation: 202 m), which isrepresentative for inland areas of eastern Norwayand midwestern Sweden (see www.met.no). Thethick black line and the thin grey lines display,respectively, the mean and 30-yr standard deviationsfor the normal period 1961–1990. (a) Series of 365-day running mean air temperature for 1990–2009.The black arrow marks the maximum 365-day meantemperature in the series corresponding to theperiod 6 November 2006 to 6 October 2007. (b)Number of days after 1 August before the minimumtemperature drops below 0 C for 1990–2008. Theblack-filled circle marks the year 2006.


skin inflammatory reactions as seen inthe majority of our skin samples. Why thisinflammatory reaction should induce hairloss without causing simultaneous pruritusis not clear. In experiments with sheep,Nelson (1963) suggested that the skininflammatory response to the sheep keds(Melophagus ovinus) resulted in reduceddermal blood supply. Hence, it is possiblethat changes in blood supply, induced bydeer ked bites, could affect the hairpapillae and thereby cause hair loss.Further research is needed.

The prevalence and extent of the hairloss in the moose population in 2006–2007is difficult to estimate due to the lack ofsurveillance data. Finding diseased ordead animals is the most direct evidencethat disease is occurring in an area orpopulation, but this technique has limitedapplication and, invariably, results in anunderestimation of the occurrence ofdisease (Wobeser, 2006). The number ofsubmitted and reported animals is, there-fore, not a good measurement of preva-lence of disease. However, during theattempt to immobilize moose in March2007, three of 15 moose (20%) observedfrom a helicopter had severe hair loss(Gunnar Gloersen, pers. comm.). Also,based on the pattern and severity of thealopecia seen in the moose and theassumption that the hair loss was progres-sive, it is plausible that a major proportionof the population experienced significant,but not clinically obvious, hair loss and,therefore, were not observed. We found alow prevalence of alopecia among moosein autumn 2007 (0.12%) and 2008(0.007%), indicating a termination of thehair loss epizootic in spring 2007. Wecannot rule out cases of deer ked-relatedhair loss prior to 2006, given the potentiallylow detection rate for the condition and thefact that moose alopecia was not of publicconcern prior to the hair-loss epizootic.

Deer keds have been established in thestudy area for 15–20 yr (Valimaki et al.,2010). It is curious that hair-loss epidem-ics have not occurred previously. Gener-

ally, parasite abundance increases withincreasing host population density (Arne-berg et al., 1998). Balashov (1996) report-ed a strong correlation between highdensity of moose populations and abun-dance of deer keds. Moose populationdensity in the study area is high and, thus,favorable for deer ked survival and repro-duction. However, high density alonecannot explain the epizootic in 2006–2007, as moose density has been high andstable in the study area for the last decade.

Balashov (1996) argues that mild anddry summers are important for the devel-opment of pupae and winged keds. On theother hand, Kadulski (1974) proposes thata long, severe winter with heavy snowfall islinked to high deer ked infestation inten-sity on cervids the following autumn andwinter, due to weakening of the host. Analternative explanation for Kadulski’s ob-servations might be that frequent snow-falls will rapidly cover the pupae andprotect them from potential predators(birds and rodents), thus creating stablestorage conditions ideal for pupal survivalduring winter (Harkonen et al., 2010).

We consider the extraordinarily highsummer and autumn temperatures in2006 to be the most important factor formaximum pupal development and surviv-al. Additionally, in 2006, the first frostnight occurred late in autumn (Fig. 5b),possibly enabling winged keds to searchfor a host during a longer window of timethan normal. Therefore, more swarmingdeer keds might have managed to find ahost, causing unusually high deer keddensities on the moose in 2006–2007.

Independent of the cause of alopecia,moose lacking large proportions of haircoat will need to increase their metabolicrate to maintain body temperature(McLaughlin and Addison, 1986). Not-withstanding metabolic and behavioraladaptations, the basic metabolic energyrequirements of a moose losing 30% ofits winter coat may double at ambienttemperatures of 220 C (McLaughlin andAddison, 1986). Hence, hypothermia or


starvation might have been the proximatecause of the winter mortality of alopecicmoose in the study area in 2006–2007.Additionally, a transient negative effect ofblood loss cannot be excluded, even thoughhemoglobin levels from the alopecic cap-tured animals were normal and postmor-tems were not consistent with anemia. Nodecrease in moose population density orrecruitment rates were reported from thestudy area in 2007 compared to theprevious years, indicating that the outbreakdid not have substantial effects on the localmoose population (Solberg et al., 2010).There is still insufficient knowledge of theeffects of deer ked harassment and infes-tation on the health and fitness of wildlife.

ACKNOWLEDGMENTS

We thank Marthe Opland, Nina BrekkeTvedt, and Oddgeir Rissa Jacobsen at NVI forthe excellent technical assistance in the labora-tory. We are grateful to Rebecca K. Davidson,NVI, Professor Jon Teige, Norwegian School ofVeterinary Science and Preben Ottesen, andThe Norwegian Institute of Public Health forhelpful comments and Kjell Handeland, NVI,and Karin Bernodt, SVA, for performing someof the necropsies. Attila Tarpai, NVI, kindlyprepared the maps. We thank Jørn Daltorp,wildlife manager, for the excellent work withthe hair-loss questionnaire. We also thankGunnar Gloersen (Swedish Hunters Associa-tion), John Sigmund Moen (wildlife manager inRømskog), Atle Løvland (Indre Østfold Foodand Animal Health Authority), and all the otherhelpful wildlife managers and hunters forproviding important field reports and picturesof alopecic moose, submitting moose, andreporting alopecia. This work was supportedby the municipalities of Aurskog-Høland,Eidsberg, Eidskog, Elverum, Grue, Halden,Kongsvinger, Lørenskog, Marker, Nannestad,Sør-Odal, Trøgstad, Vestby, and Amot, theCounty Governor of Hedmark, the NorwegianForest Owners’ Federation, the NorwegianDirectorate for Nature Management, and theNational Health Surveillance Program forCervids (HOP) in Norway.

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Submitted for publication 23 December 2010.Accepted 9 April 2011.


HAIR-LOSS EPIZOOTIC IN MOOSE (ALCES ALCES) ASSOCIATED WITH MASSIVE DEER KED (LIPOPTENA CERVI)...

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