ALCES VOL. 48, 2012 SAMUEL ET AL. – KEDS ON

REVIEW OF DEER KED ( CERVI) ON MOOSE IN SCANDINAVIA WITH IMPLICATIONS FOR NORTH AMERICA

William M. Samuel1, Knut Madslien2, and Jessica Gonynor-McGuire3

11226 Kane Wynd NW, Edmonton, Alberta, Canada T6L 6X7, 2Norwegian Veterinary Institute, Pb 750 Sentrum, N-0106 Oslo, Norway, 3Warnell School of Forestry and Natural Resources, and Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, Georgia 30602, USA.

ABSTRACT: The deer ked (Lipoptena cervi) is an Old World dipteran ectoparasite of moose (Alces alces) and other Cervidae. It has undergone significant expansion in distribution on moose of Scan- dinavia in recent decades. This has been accompanied by much published research dealing with the range expansion and possible factors involved, problems for moose, exposure of northern populations of (Rangifer rangifer tarandus), and public health issues. Apparently, Lipoptena cervi was introduced into northeastern in the late 1800s, presumably on an unknown species of European deer, and it soon spread to white-tailed deer (Odocoileus virginianus). We review the cur- rent situation in Scandinavia and North America and document the first record ofL . cervi on moose in northeastern United States.

ALCES VOL. 48: 27-33 (2012)

Key words: Alces alces, distribution, deer ked, effect on host, Lipoptena cervi, moose, North America, Odocoileus virginianus, Scandinavia, white-tailed deer.

The deer ked, Lipoptena cervi (Insecta, including dermatitis on increasing numbers Diptera, ) is a widely distrib- of rural people bitten by deer keds (Härkönen uted, blood-sucking, reddish-brown, dorso- et al. 2009), exposure of northern reindeer ventrally flattened ectoparasite that occurs on (Rangifer rangifer tarandus) herds (Kaitala et Old and New World members of the Cervidae. al. 2009), as well as an epizootic of hair-loss Notable hosts include red deer (Cervus ela- and deaths of moose in southeastern Norway phus), (Capreolus capreolus), fallow and mid-western Sweden in 2006 and 2007 deer ( dama), and especially moose (Madslien et al. 2011). The objectives of (Alces alces) in Finland, Sweden, and Norway. this paper are to briefly review current issues Lipoptena cervi was described by Linnaeus involving deer keds on moose in Scandinavia (1758) as Pediculus cervi, probably basing and to provide information about its occurrence his description on examination of published in northeastern United States. figures, not specimens (see Bequaert 1957, pp. 488-489). It is an ancient found as- LIFE CYCLE sociated with the remains of a Late Neolithic All species of deer keds, including L. human mummy in an Italian glacier (Gothe cervi, are viviparous and produce one at a and Schöl 1994). time. Winged young adults of L. cervi emerge Lipoptena cervi has undergone rapid from pupae on the ground from late summer and ongoing west and northward expansion through autumn. They do not fly far in seeking of its distribution in Scandinavia in recent hosts, which in Scandinavia is usually moose. decades (Välimäki et al. 2010). This has Wings of males and females are lost once on been accompanied by emerging public health moose. Adults feed on blood and interstitial and conservation issues, mostly in Finland, fluid, mating and overwintering on the host. 27 DEER KEDS ON MOOSE – SAMUEL ET AL. ALCES VOL. 48, 2012

The developing larva is retained in the uterus keds currently occupy a small part of Norway of the adult female. Females extrude white near and north of Oslo, the southern half of mature larva, the prepupa, one at a time, from Sweden, and approximately the southern 75% autumn until the next summer (Härkönen et al. of Finland. 2010). The skin of prepupa fattens and hard- There has been progress in identifying ens into a seed-like dark case as the prepupa factors involved in the expansion of L. cervi transforms to the and drops to the ground distribution. Changes in moose numbers and on vegetation or snow. Pupae remain on the climate are likely key factors. Numbers of ground until autumn (for details see Bequaert moose began to increase rapidly in Norway, 1953, Haarløv 1964, and a life cycle diagram Sweden, and Finland in the 1960s, owing to in Samuel and Madslien 2010). increased clear-cutting practices by the forest industries and changes in management strate- STATUS IN SCANDINAVIA gies to sex and age-specific harvests (Lavsund Expanding distribution and consequences et al. 2003). Lavsund et al. (2003) documented for hosts that harvest of moose, which likely reflects Lipoptena cervi has expanded its distri- population density, was highest in the early bution west- and northward in Scandinavia 1980s (Sweden and Finland), again in Finland in recent decades (see distribution maps in in the late 1990s and early 2000s (also see Selby Kaunisto et al. 2011 and Välimäki et al. 2010). et al. 2005), and in the 1990s in Norway (also Summarizing this expansion, Välimäki et al. see Lykke 2005). In 2003, moose densities in (2010) state that L. cervi “has been resident in all 3 countries “were lower in the north than in Sweden for more than two centuries, whereas the south and higher in Norway and Sweden in Finland (~50 years) and Norway (~30 years) than in Finland” (Lavsund et al. 2003). The it has established itself relatively recently.” 2008 moose population in Finland stabilized There are two fronts of ked expansion: one at 90,000 (Pusenius et al. 2008, in Kaitala that began in 1960 in southernmost Finland et al. 2009). Kaitala et al. (2009) suggested (59-60o N) with source keds from Russia, and that increase in moose densities in Finland one that began on or perhaps slightly before has been the main reason why deer keds have 1983 in southeastern Norway (~59o N) with been able to expand their range and increase source keds from Sweden. By the end of in numbers. Välimäki et al. (2010) point out 2008, deer keds in Norway had spread from that there was little or no range expansion of the first known source south and east of Oslo L. cervi in Fennoscandia when densities of and the Oslo Fiord (~59 o N), west and north moose were relatively low. at ~7 km/yr. Northward expansion along Northern range expansion of L. cervi the border of Sweden and Norway reached should be limited by colder temperatures and ~62o N by end of 2008. Northern expansion shorter growth season that would most affect in Sweden is less well documented, but has off-host life stages, because it is the pupae been relatively slow. In the early 1960s keds on the ground and recently emerged young were as far north as 59o, ~420 km from the winged adults, not adult keds on moose, southern tip of Sweden, and by 2008 keds that are exposed to changing and potentially were found as far north as ~62.5o. Northern adverse northern environmental conditions expansion in Finland has been more rapid, (Härkönen et al. 2010, Välimäki et al. 2010). spreading at a rate of 11 km/yr, and now is Härkönen n et al. (2010) studied development close to the Arctic Circle (~66o N) where it of pupae and timing of adult emergence along overlaps with the southern edge of reindeer a latitudinal gradient from boreal taiga in herding areas (Kaitala et al. 2009). Thus, deer central Finland to Arctic tundra in northern

28 ALCES VOL. 48, 2012 SAMUEL ET AL. – DEER KEDS ON MOOSE

Finland, and found success of pupae emerging Some were found dead and others in obvi- to young adults was higher (19% emerged at ous severe distress were humanely killed. the southernmost site at 62o N) and earlier in Madslien et al. (2011) felt the main cause the south and much lower (<2% emerged at of the outbreak, high numbers of deer keds, the high Arctic site at 70o N) and later in the far was in response to extremely high summer north. However, a few pupae emerged in the and autumn temperatures in 2006, providing high Arctic, nearly 500 km north of its current good development and survival of pupae. In northern range. Thus, at 70o N, fewer young Finland, numbers of keds averaged 10,616, winged adults had less time before winter to 3,549, and 1,730 on bulls, cows and calves, find a host, but the results from 5 sites at dif- respectively, with full coats of hair (n = 23) ferent latitudes suggest that “spread of deer (Paakkonen et al. 2010). keds to cervids in the southern parts of the reindeer herding area seems inevitable.” This Public Health Issues indicates that L. cervi has broad ecological Newly emerging young adult keds attack tolerances (Kaunisto et al. 2011) and suggests humans as well as ruminants, especially in that the colder and shorter growing season in Finland. Keds do not reproduce on humans, the north may slow, but not stop the northern but infestation is a nuisance for rural people spread of deer keds. such as hunters, berry pickers, and forestry Moose are numerous in southern parts workers (Härkönen et al. 2009, Kortet et al. of Finnish Lapland (Pusenius et al. 2008, in 2009). Apparently it is not the ked bite that Kaitala et al. 2009) and are considered the is the problem, but rather the inconvenience main host for deer keds (Kaitala et al. 2009). of removing “dozens of keds from hair and Thus, it is likely that reindeer will be attacked clothes.” More serious health issues have by adult ; in addition, they are a suitable emerged and increasing numbers of people host. Kynkäänniemi et al. (2010) experimen- in Finland suffer from chronic dermatitis tally infested reindeer with L. cervi, and a few and occupational allergic rhinoconjunctivitis keds survived and reproduced. Kaunisto et al. following bites by deer keds. It is estimated (2009) found that deer keds occasionally infest that several thousand people have ked-caused semi-domesticated reindeer and wild Finnish dermatitis and growing numbers of forest forest reindeer, R. t. fennicus. Bequaert (1957) workers have become sensitized to ked bite. reported that reindeer introduced to Scotland A recent twist has been added to this from Lapland became “heavily infested with subject. Several of the many newly-described L. cervi” shortly after their arrival. species in the bacterial genus Bartonella Keds can be numerous on moose and they cause diseases in humans (Jacomo et al. 2002, might be associated with mortality of moose. Chomel et al. 2009). Bartonella henselae, Madslien et al. (2011) found up to 16,500 keds for example, was identified in 1990 and is on moose during an outbreak of ked-caused now known to cause several clinical diseases hairloss in moose in eastern Norway and mid- including cat scratch disease. It is transmitted western Sweden, 2006-2007. These numbers from cats to humans by the bite of an infected were considered conservative because keds cat flea or by a cat bite or scratch. Dehio et prefer hair-covered skin and many moose had al. (2004) found that L. cervi collected from severe alopecia. During the outbreak over roe and red deer in Germany were infected 100 moose were observed; most with severe with Bartonella schoenbuchensi. The twist loss of hair and varying degrees of emacia- is that Dehio et al. (2004) noticed that clinical tion, and some with atypical behaviour (e.g., signs and other aspects of cat scratch disease in farm buildings, unresponsive to humans). were similar to that of dermatitis in humans

29 DEER KEDS ON MOOSE – SAMUEL ET AL. ALCES VOL. 48, 2012 caused by the bite of L. cervi and suggested tral (Bequaert 1957), it should that bartonellae are “pathogens that should be presumably occur on moose sympatric with considered possible etiological agents of deer white-tailed deer. Exact numbers of keds on ked dermatitis.” these hosts are unknown. Anecdotally, Be- quaert (1957) mentioned a heavily infested STATUS IN NORTHEASTERN white-tailed deer from Sullivan County, New UNITED STATES Hampshire in 1950, and one of us (Samuel)2 Apparently in the late 1800s L. cervi was saw many keds on an old male white-tailed introduced to northeastern United States on an deer killed in McKean County, Pennsylvania unknown deer transported from Europe, and by his father around 1950 (Samuel and Mad- later established on white-tailed deer (Bequaert slien 2010). Matsumoto et al. (2008) found 19531). Summarizing records from Bequaert only 6 keds on 4 of 27 white-tailed deer in (1937, 1942, and 1957), L. cervi was collected Worcester County, . from white-tailed deer in More recently, keds were collected op- (Grafton County in 1907, Sullivan County in portunistically from several moose and white- 1950) and a captive wapiti (Cervus canadensis) tailed deer at hunter check stations by one of in Sullivan County in 1942. It was collected us (Gonynor-McGuire) in 2007 and 2008. In from white-tailed deer in (Albany, October 2007, Gonynor-McGuire thoroughly Cattaraugus, and Hamilton Counties in 1938, examined harvested moose for ticks and keds 1949 and 1954, respectively), Massachusetts in New Hampshire; examinations were 5-10 (Dukes County in 1924), and Pennsylvania minutes in length. Several dozen keds were (Pike and Clinton Counties, no date; McKean collected and tentatively identified asL . cervi, and Cameron Counties in 1953). Keds also but were subsequently lost. In October 2008 were reported as being common on wapiti in cooperation with New Hampshire Fish and in Cameron County, Pennsylvania. Other Game Department personnel (K. Rines and reports of L. cervi in the United States are K. Gustafson), Gonynor-McGuire supplied from white-tailed deer in New York (Bump kits for collecting keds at harvest check sta- 1941), West Virginia (Kellogg et al. 1971), and tions. Fourteen keds were collected from 11 Worcester County, Massachusetts (Matsumoto white-tailed deer at stations in Cheshire, Coos, et al. 2008). Grafton, and Sullivan Counties, and 1 ked Given the above, L. cervi is probably more from each of 2 moose from stations in Coos prevalent on white-tailed deer and moose of and Grafton Counties. Keds from both species the northeastern United States than currently of host were identified by Samuel using keys known or assumed. If L. cervi survived on and descriptions of Bequaert (1937, 1957), wapiti sympatric with white-tailed deer in cen- and were subsequently compared with L. cervi 1In what we think is the only discussion of this intro- from moose in Norway. The keds from the 2 duction, Bequaert (1953) states “This parasite was, in moose from New Hampshire were deposited in my opinion, brought from the Old World by Man with the University of Alberta Parasite Collection; European Deer. From this host it strayed to the native Virginia deer, Odocoileus virginianus, on which it 2Hunters in northeastern United States must occasion- now breeds at several localities in the northeastern ally see keds on their killed deer, maybe their moose. United States...... The exact date of the introduction is Obviously my father did, but he thought they were unknown; it was first recognized in the United States ticks. Hunters mistaking keds for ticks is mentioned in 1907, when it was described as a new species by on fact sheets for this parasite on the internet (e.g., Coquillet (L. subulata) [later changed to L. cervi]. If http://ento.psu.edu/extension/factsheets/deer-keds). it were truly native, or autochthonous, it would be In 2007, many hunters at a New Hampshire deer found over a much wider territory and be more abun- check station near Berlin, NH said they thought keds dant; while its presence on native deer could scarcely were ticks (Gonynor-McGuire, personal observation). have escaped the early American entomologists.” 30 ALCES VOL. 48, 2012 SAMUEL ET AL. – DEER KEDS ON MOOSE accession numbers UAPC #11566 and #11572. surface of the hind leg and inguinal region) Several keds from each of 2 moose from the of white-tailed deer in southern Texas for Li- Madslien et al. (2011) study in Norway were poptena mazamae. They found no significant also deposited: UAPC #11563 and #11564. migration of keds to or from the area during Keds from 6 white-tailed deer were deposited the 2 hours following death of deer. Dead in the UAPC (#11565, #11567-11571), and deer were hung by the back legs, which were from 4 white-tailed deer in the University spread using a gambrel. After 2 hours, keds of Alberta E. H. Strickland Entomological began moving to extremities such as the nose, Museum (UASM213577-213580). This is ears, and lower legs. Given time constraints the first report of this parasite from moose in at hunter check stations, the technique used North America. by Sine et al. (2009) for detecting winter Keds are observed annually on harvested ticks on moose might be useful for detecting moose and white-tailed deer in New Hamp- deer keds. shire, with keds more common in recent years, but prevalence and numbers have not been REFERENCES monitored (K. Rines, pers. comm.). While Be q u a e r t , J. 1937. 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