Parasitism of the deer ked,Lipoptena cervi,on the moose,Alces alces,in eastern Finland

The deer ked, Lipoptena cervi L. (Diptera: Hippoboscidae), is an ectoparasitic fly that spread to Finland in the early 1960s from the southeast across the Soviet border. It is currently a common parasite of the moose, Alces alces (Artiodactyla: Cervidae), in the southern part of the country and its area of distribution is gradually spreading to Finnish Lapland, where it will come into contact with another potential cervid host, the semi‐domesticated reindeer, Rangifer tarandus tarandus. The aim of this study was to determine the intensity of deer ked parasitism on the moose in eastern Finland. Whole skins of 23 moose were examined for the presence of deer keds, which were extracted and their total numbers estimated. The intensity of deer ked parasitism was correlated to the age, sex, skin area and anatomical region of the host. Bulls had the highest total number of keds (10616 ± 1375) and the highest deer ked density (35.7 ± 4.4 keds/dm² of skin). Cows had a higher total number of keds than calves (3549 ± 587 vs. 1730 ± 191), but ked densities on cows and calves were roughly equal (11.8 ± 1.7 vs. 9.4 ± 1.1 keds/dm² of skin). The density of keds was highest on the anterior back, followed by the posterior back, front limbs, abdomen, head and hind limbs. The sex ratio of deer keds was close to equal (male : female, 1.0 : 1.1). After they had consumed blood, male keds were heavier than females. As the total numbers and densities of deer keds were higher than reported previously on moose or for any other louse fly species, the effects of parasitism on the health of the host species should be determined.     

Salt licks do not increase local densities of the deer ked,Lipoptena cervi,an abundant ectoparasite of cervids

The deer ked, Lipoptena cervi (Diptera: Hippoboscidae), is a common ectoparasite of the moose, Alces alces (Artiodactyla: Cervidae). Salt licks are widely used to manipulate moose movements to prevent damage to saplings and traffic accidents. They may cause moose to gather in small areas, which could create aggregates of deer ked pupae as the parasite is a short‐distance flyer and its dispersion depends on its hosts. We investigated whether the population density of flying deer keds could be influenced by manipulating salt licks and how environmental variables affect parasite density. Densities were estimated in 40 experimental sites with four treatments (no salt licks, introduced salt licks, removed salt licks, permanent salt licks) in September during 2007–2010. Forest edges, mixed forests on mineral soil and coniferous forests on peat soil were the habitats with high numbers of parasites. The manipulation of salt licks seemed to be ineffective in reducing the density of deer keds as the only factor to show statistical significance with parasite numbers in the mixed‐model analysis was year of determination. Annual deer ked densities correlated with the abundance of moose in the region. Moreover, high spring and summer temperatures seemed to increase the numbers of flying imagos.     

Bartonella Infections in Deer Keds (Lipoptena cervi) and Moose (Alces alces) in Norway

Infections with Bartonella spp. have been recognized as emerging zoonotic diseases in humans. Large knowledge gaps exist, however, relating to reservoirs, vectors, and transmission of these bacteria. We describe identification by culture, PCR, and housekeeping gene sequencing of Bartonella spp. in fed, wingless deer keds (Lipoptena cervi), deer ked pupae, and blood samples collected from moose, Alces alces, sampled within the deer ked distribution range in Norway. Direct sequencing from moose blood sampled in a deer ked-free area also indicated Bartonella infection but at a much lower prevalence. The sequencing data suggested the presence of mixed infections involving two species of Bartonella within the deer ked range, while moose outside the range appeared to be infected with a single species. Bartonella were not detected or cultured from unfed winged deer keds. The results may indicate that long-term bacteremia in the moose represents a reservoir of infection and that L. cervi acts as a vector for the spread of infection of Bartonella spp. Further research is needed to evaluate the role of L. cervi in the transmission of Bartonella to animals and humans and the possible pathogenicity of these bacteria for humans and animals.     

Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness

Invasive generalist ectoparasites provide a tool to study factors affecting expansion rates. An increase in the number of host species may facilitate geographic range expansion by increasing the number of suitable habitats and by affecting local extinction and colonization rates. A geographic perspective on parasite host specificity and its implications on range expansion are, however, insufficiently understood. We conducted a field study to explore if divergent host specificity could explain the observed variation in expansion rates between Fennoscandian populations of the deer ked (Lipoptena cervi), which is a blood-feeding ectoparasitic fly of cervids. We found that the rapidly expanding eastern population in Finland appears to specialize on moose, whereas the slowly expanding western population in Norway breeds successfully on both moose and roe deer. The eastern population was also found to utilize the wild forest reindeer as an auxiliary host, but this species is apparently of low value for L. cervi in terms of adult maintenance, reproductive output and offspring quality. Abundant numbers of roe deer and white-tailed deer were observed to be apparently uninfected in Finland, suggesting that host use is not a plastic response to host availability, but rather a consequence of population-level evolutionary changes. Locally compatible hosts were found to be the ones sharing a long history with the deer ked in the area. Cervids that sustained adult deer keds also allowed successful reproduction. Thus, host use is probably determined by the ability of the adult to exploit particular host species. We conclude that a wide host range alone does not account for the high expansion rate or wide geographic distribution of the deer ked, although loose ecological requirements would increase habitat availability.     

Tick (Dermacentor albipictus)-induced winter hair-loss in captive moose (Alces alces)

Five captive moose calves each infested with 42,000 larval Dermacentor albipictus, six calves each infested with 19,000-21,000, and five control moose were observed for changes in hair-loss, body condition and number, stages, and distribution of the tick. Winter hair-loss was observed only in moose infested with ticks and was correlated positively with the total number of adult ticks. Hair-loss associated with ticks was minimal from October to January, but rapidly increased from February to April when up to 44% of hair had been removed. The pattern of hair-loss was similar in all moose with the neck, shoulders, withers, and perianal areas losing the most hair. Moose with extensive premature hair-loss had less pericardial and abdominal visceral fat than moose with little or no hair-loss.     

The moose throat bot fly <Emphasis Type="Italic">Cephenemyia ulrichii</Emphasis> larvae (Diptera: Oestridae) found developing in roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis>) for the first time

About fifty larvae of Cephenemyia ulrichii Brauer (Diptera: Oestridae), some of them nearly full-grown third instars, were found in the throat of a roe deer (Capreolus capreolus) in June 2007 near Helsinki in Finland. The parasite is considered to be host specific, occurring only in the moose (Alces alces), and this paper is apparently the first report of a successful infestation in an aberrant host.     

Effect ofDermacentor albipictus (Acari: Ixodidae) on blood composition,weight gain and hair coat of moose,Alces alces

The physiological effects of the winter tick,Dermacentor albipictus, on moose,Alces alces, were investigated. Blood composition, weight gain, food intake and change in the hair coat of moose calves, four infested withD. albipictus larvae, and eight uninfested, were monitored. Infested moose groomed extensively, apparently in response to feeding nymphal and adult ticks, and developed alopecia. Other clinical signs included: chronic weight loss, anemia, hypoalbumenemia, hypophosphatemia, and transient decreases in serum asparate transaminase and calcium during the period of nymphal and adult female tick engorgement. Infested animals did not become anorexic. Two moose with severe hair loss had increases in gamma globulin shortly after the onset of female tick engorgement. Results suggest that alopecia is associated with tick resistance. Animals that groom and develop hair loss likely carry fewer ticks and therefore suffer less severely from blood loss.     

Molecular identification and prevalence of Dictyocaulus spp. (Trichostrongyloidea: Dictyocaulidae) in Swedish semi-domestic and free-living cervids

Lungs of 102 roe deer (Capreolus capreolus), 136 moose (Alces alces), 68 fallow deer (Dama dama), and six red deer (Cervus elaphus) were examined during hunting seasons from 16 September 1997 to 1 March 2000. The aim was to determine the species composition and prevalence of Dictyocaulus lungworms in these hosts in Sweden. Worms were identified following polymerase chain reaction (PCR) amplification of the internal transcribed spacer of ribosomal DNA (ITS2), followed by hybridization with four species-specific oligonucleotides. In addition, 50 lungworms from five reindeer (Rangifer tarandus) from Norway were similarly analyzed. A total of 399 worms were recovered and analyzed representing a range of 29-128 worms per host species. All specimens from roe deer were identified as Dictyocaulus capreolus, whereas those from red deer and reindeer were identical with D. eckerti. From moose, 73 (81.1%) of the worms were identified as D. capreolus whereas 17 (18.9%) were D. eckerti. The ITS2 sequence of fallow deer lungworms differed significantly when compared with the ITS2 of D. viviparus, D. capreolus, and D. eckerti. This indicated that fallow deer in Sweden may be infected with a new genotype of Dictyocaulus spp. Consequently, a specific probe designed for the ITS2 from this Dictyocaulus sp. hybridized exclusively with samples from lungworms of fallow deer. Interestingly, no D. viviparus were found in any of these hosts. The prevalence of infection in each host was as follows: D. capreolus in roe deer (14.7%) and moose (10.6%); D. eckerti in moose (0.7%) and red deer (33.3%); and Dictyocaulus sp. in fallow deer (10.3%). Regardless of lungworm species, the overall prevalence of Dictyocaulus spp. in these hosts was 12.2%. Prevalence between male and female animals and among the different age groups did not differ significantly. Finally an enzyme linked immunosorbent assay (ELISA) specific for patent D. viviparus infection in cattle was utilized to analyze lung tissue fluids from infected animals. All samples from roe deer, red deer, and fallow deer were negative in the ELISA. However, three out of twelve (25%) samples from moose and 17 of 40 (43%) samples from cattle were positive. This indicated that moose anti-D. capreolus antibodies recognized the D. viviparus antigen and that anti-cattle immunoglobulin cross-reacted with moose antibodies.     

Polymorphisms and variants in the prion protein sequence of European moose (Alces alces), reindeer (Rangifer tarandus), roe deer (Capreolus capreolus) and fallow deer (Dama dama) in Scandinavia

The prion protein (PrP) sequence of European moose, reindeer, roe deer and fallow deer in Scandinavia has high homology to the PrP sequence of North American cervids. Variants in the European moose PrP sequence were found at amino acid position 109 as K or Q. The 109Q variant is unique in the PrP sequence of vertebrates. During the 1980s a wasting syndrome in Swedish moose, Moose Wasting Syndrome (MWS), was described. SNP analysis demonstrated a difference in the observed genotype proportions of the heterozygous Q/K and homozygous Q/Q variants in the MWS animals compared with the healthy animals. In MWS moose the allele frequencies for 109K and 109Q were 0.73 and 0.27, respectively, and for healthy animals 0.69 and 0.31. Both alleles were seen as heterozygotes and homozygotes. In reindeer, PrP sequence variation was demonstrated at codon 176 as D or N and codon 225 as S or Y. The PrP sequences in roe deer and fallow deer were identical with published GenBank sequences.     

Polymorphisms and variants in the prion protein sequence of European moose (Alces alces), reindeer (Rangifer tarandus), roe deer (Capreolus capreolus) and fallow deer (Dama dama) in Scandinavia

The prion protein (PrP) sequence of European moose, reindeer, roe deer and fallow deer in Scandinavia has high homology to the PrP sequence of North American cervids. Variants in the European moose PrP sequence were found at amino acid position 109 as K or Q. The 109Q variant is unique in the PrP sequence of vertebrates. During the 1980s a wasting syndrome in Swedish moose, Moose Wasting Syndrome (MWS), was described. SNP analysis demonstrated a difference in the observed genotype proportions of the heterozygous Q/K and homozygous Q/Q variants in the MWS animals compared with the healthy animals. In MWS moose the allele frequencies for 109K and 109Q were 0.73 and 0.27, respectively, and for healthy animals 0.69 and 0.31. Both alleles were seen as heterozygotes and homozygotes. In reindeer, PrP sequence variation was demonstrated at codon 176 as D or N and codon 225 as S or Y. The PrP sequences in roe deer and fallow deer were identical with published GenBank sequences.     

PCR detection of re-emerging tick-borne pathogen, <Emphasis Type="Italic">Anaplasma phagocytophilum</Emphasis>, in deer ked (<Emphasis Type="Italic">Lipoptena cervi</Emphasis>) a blood-sucking ectoparasite of cervids

Anaplasma phagocytophilum is an obligate intracellular bacterium, circulating in the natural foci in enzootic, vector-host cycle. In Europe, A. phagocytophilum is transmitted by Ixodes ricinus ticks. In Slovakia, cervids which are considered as naturally infected reservoirs of A. phagocytophilum are besides the ticks commonly infested with insects from the family Hippoboscidae. In this study, the presence of A. phagocytophilum was confirmed in deer keds (Lipoptena cervi) removed from deer by using of molecular approach. Detection of A. phagocytophilum in deer keds represents the remains of infected blood meal taken from infected deer host, what underlines the potential role of these blood-sucking insects in the mechanical transmission of pathogenic bacteria within the susceptible population of wild animals. Moreover, it may suggest the risk for the transmission of A. phagocytophilum or related pathogens to humans and healthy animals via the bite of infected hematophagous ectoparasites.     

Hair-loss syndrome in black-tailed deer of the Pacific Northwest

A widespread hair-loss syndrome (HLS) has affected Columbian black-tailed deer (Odocoileus hemionus columbianus) in western Oregon and Washington (USA) since 1996. In order to better characterize the condition, 21 HLS-affected black-tailed deer (BTD) were necropsied, and body condition, parasite burdens, and significant lesions were noted. All deer were in poor body condition, and at least 17 had severe internal parasite burdens. A consistent finding was the presence of large numbers of chewing lice, identified as an indeterminate species of Damalinia (Cervicola). Four animals were infested with intrafollicular Demodex sp., the first report of this genus of mites in BTD. We postulate that the hair loss is largely due to ectoparasitism by a species of chewing louse that represents a new pathogen for BTD. This loss of pelage also may be an important contributor to the poor body condition of these animals.     

Presumptive gangrenous ergotism in free-living moose and a roe deer

Presumptive gangrenous ergotism in 10 moose (Alces alces) and one roe deer (Capreolus capreolus) is reported. Three of the moose came from a municipality in southeastern Norway where the disease occurred as a cluster in 1996. The other moose represented solitary or sporadic cases diagnosed in four municipalities in northwestern Norway between 1996 and 2004. Affected moose (seven calves, three yearlings) were found between October and June, showing distal limb lesions on one to three limbs. The lesions in the moose found during October and November presented as dry gangrene, whereas moose found between December and June presented with loss of the distal part of the limbs or open lesions close to sloughing. Four of the moose also had bilateral ear lesions affecting the outer third of the pinnae. A retrospective diagnosis of ergotism (June 1981) was made in a 1-yr-old roe deer from northwestern Norway showing loss of the distal part of all four limbs.     

Parelaphostrongylus tenuis in New Brunswick: the parasite in white-tailed deer (Odocoileus virginianus) and moose (Alces alces)

Research was initiated in 1983 to investigate the ecology of Parelaphostrongylus tenuis in New Brunswick. The objectives were to determine the prevalence and intensity of infection in white-tailed deer, and to determine whether or not moose feces contained first stage larvae, signifying the completion of the life cycle of P. tenuis in this host. Forty-nine percent of deer pellet samples were positive and 60% of deer heads contained adults of P. tenuis. None of the moose pellet samples contained first stage larvae.     

Experimental Narthecium ossifragum nephrotoxicity in cervids from Norway

One moose (Alces alces), two red deer (Cervus elaphus), two reindeer (Rangifer tarandus) and two fallow deer (Dama dama) were dosed intraruminally with an aqueous extract made from 30 g of bog asphodel (Narthecium ossifragum) (wet weight) per kg live weight. The moose and one of the two reindeer were mildly depressed and had reduced appetite 3 to 7 days and 1 to 4 days after dosing, respectively. The serum creatinine and urea concentrations increased markedly in the moose and red deer, and moderately in the reindeer. No increase in serum creatinine and urea was observed in the fallow deer. Histopathological examination of the kidneys of the animals, killed 8 to 10 days after dosing, revealed tubular epithelial cell degeneration, necrosis, and regeneration in the moose, red deer and reindeer. The renal lesions were severe in the moose, moderate in the red deer and mild in the reindeer. No histopathological lesions were seen in the kidneys of the fallow deer.     

Antibodies to ruminant alpha-herpesviruses and pestiviruses in Norwegian cervids

A serologic survey revealed that Norwegian populations of free-ranging reindeer (Rangifer tarandus tarandus), roe deer (Capreolus capreolus), red deer (Cervus elaphus), and moose (Alces alces) have been exposed to alpha-herpesviruses and pestiviruses. A total of 3,796 serum samples collected during the period 1993-2000 were tested in a neutralization test for antibodies against bovine herpesvirus 1 (BHV-1) or cervid herpesvirus 2 (CerHV-2), and 3,897 samples were tested by a neutralization test and/or enzyme-linked immunosorbent assay for antibodies against bovine viral diarrhea virus (BVDV). Antibodies against alpha-herpesvirus were found in 28.5% of reindeer, 3.0% of roe deer, and 0.5% of red deer, while all moose samples were negative. In reindeer, the prevalence of seropositive animals increased with age and was higher in males than females. Antibodies against BVDV were detected in 12.3% of roe deer, 4.2% of reindeer, 2.0% of moose and 1.1% of red deer. The results indicate that both alpha-herpesvirus and pestivirus are endemic in reindeer and pestivirus is endemic in roe deer in Norway. The viruses may be specific cervid strains. Seropositive red deer and moose may have become exposed as a result of contact with other ruminant species.     

Diversity of rickettsial pathogens in Columbian black‐tailed deer and their associated keds (Diptera: Hippoboscidae) and ticks (Acari: Ixodidae)

Cervids host multiple species of ixodid ticks, other ectoparasites, and a variety of rickettsiae. However, diagnostic test cross‐reactivity has precluded understanding the specific role of deer in rickettsial ecology. In our survey of 128 Columbian black‐tailed deer (Odocoileus hemionus columbianus (Richardson)) and their arthropod parasites from two northern Californian herds, combined with reports from the literature, we identified four distinct Anaplasma spp. and one Ehrlichia species. Two keds, Lipoptena depressa (Say) and Neolipoptena ferrisi Bequaert, and two ixodid ticks, Ixodes pacificus Cooley and Kohls and Dermacentor occidentalis Marx, were removed from deer. One D. occidentalis was PCR‐positive for E. chaffeensis; because it was also PCR‐positive for Anaplasma sp., this is an Anaplasma/Ehrlichia co‐infection prevalence of 4.3%. 29% of L. depressa, 23% of D. occidentalis, and 14% of deer were PCR‐positive for Anaplasma spp. DNA sequencing confirmed A. bovis and A. ovis infections in D. occidentalis, A. odocoilei in deer and keds, and Anaplasma phagocytophilum strain WI‐1 in keds and deer. This is the first report of Anaplasma spp. in a North America deer ked, and begs the question whether L. depressa may be a competent vector of Anaplasma spp. or merely acquire such bacteria while feeding on rickettsemic deer.     

The Prevalence of Elaphostrongylus Cervi Infection in Moose (Alces alces) in Southern Norway

The prevalence of Elaphostrongylus cervi infection in moose shot during the hunting season 1983 in 47 different municipalities in Southern Norway was studied. E. cervi seemed to occur endemically in the population, as infection was found in 35 % of 1,982 moose examined. Diagnosis was made on the basis of the presence of eggs and first-stage larvae (L1) and associated histopathological lesions in the lung, and on the presence of L1 in the faeces. The prevalence varied considerably between different municipalities. No relationship was found between the prevalence of E. cervi and the population density of moose. The highest prevalence was found in municipalities where red deer harbouring E. cervi were also present. The prevalence among males was higher than among females, and that among yearlings higher than among calves and adults. In no case was infection found in animals 51/2 years of age or older. Carcass weight in infected adult moose was significantly lower than in non-infected adults.     

Can androgen deficiency promote an outbreak of psoroptic mange mites in male deer?

Repeated outbreaks of infection by psoroptic mange mites (Psoroptes equi var. ovis) affecting most regions of the body and legs were observed in several male white-tailed deer (Odocoileus virginianus) suffering from hypoandrogenism (e.g., castrates, animals treated with antiandrogens or postprime). The massive infection was characterized by a severe alopecia and skin inflammation and began usually in early winter. One or two spray treatments of a 1% solution of Lindane was usually sufficient to eliminate the clinical signs of the disease and to restore a healthy hair coat. Neither healthy male or female deer have ever exhibited any external signs of this disease nor has the parasite been detected in the scrapings of their skin. We propose a possible relationship between the hormonal status of these animals and their resistance to this parasitic mite infection.     

Serologic survey for antibodies against Mycobacterium a vium subsp. paratuberculosis in free-ranging cervids from Norway

Affinity between protein-G and immunoglobulins from red deer (Cervus elaphus), moose (Alces alces), roe deer (Capreolus capreolus), and reindeer (Rangifer tarandus tarandus) was tested in a competition binding assay. Sera from red deer, reindeer, and moose inhibited the assay less than sera from cattle (less affinity), whereas sera from roe deer showed a slightly higher affinity to protein-G than did sera from cattle. The conclusion was made that protein-G could be used instead of anti-species antibodies for these cervid species, where the aim of the screening was to look for exposure or lack of exposure to mycobacteria in the tested populations. Serologic screening of 1,373 free-ranging cervids for antibodies against Mycobacterium avium subsp. paratuberculosis was conducted. All sera were tested by a protein-G-based antigen-absorbed enzyme-linked immunosorbent assay (ELISA). Seropositive moose (10/537; 1.9%), red deer (14/371; 3.8%), roe deer (6/49; 12.2%), and semidomesticated reindeer (11/325; 3.4%) were found, whereas wild reindeer (n = 91) were seronegative. In addition, the red deer sera were tested with a commercial ELISA, by which two animals tested positive and nine were suspicious of having M. avium subsp. paratuberculosis antibodies. Tissue samples and feces from 10 moose originating from a population with a clustering of seropositive animals were investigated by histology and bacteriology with negative results. Paratuberculosis has never been diagnosed in free-ranging or farmed cervid species in Norway. Thus, further studies are indicated to prove that the present findings reflect an infection with M. avium subsp. paratuberculosis.