ALCES VOL. 46, 2010 LANKESTER – IMPACT OF MENINGEAL WORM ON MOOSE
UNDERSTANDING THE IMPACT OF MENINGEAL WORM, PARELAPHOSTRONGYLUS TENUIS, ON MOOSE POPULATIONS
Murray W. Lankester
101-2001 Blue Jay Place, Courtenay, British Columbia V9N 4A8, Canada.
ABSTRACT: Declines in moose (Alces alces) populations have occurred repeatedly during the past century on the southern fringe of moose range in central and eastern North America, generally in the same geo-climatic regions. These prolonged declines, occurring over a number of years, are associated with higher than usual numbers of co-habiting white-tailed deer (Odocoileus virginianus). Numerous proximate causes have been hypothesized but none has gained widespread acceptance among cervid managers. However, current knowledge of the nature of moose declines and the biology of meningeal worm (Parelaphostrongylus tenuis) makes this parasite the most credible explanation. Other suggested disease-related causes are rejected, including infection with liver flukes (Fascioloides magna). There is no clinical evidence that flukes kill moose. As well, this parasite occurs at only moderate prevalence and intensity in some jurisdictions and is completely absent in others where moose declines are known. Winter ticks (Dermacentor albipictus), on the other hand, do kill moose but usually have a distinctly different and more immediate impact on populations. It is recognized that moose, albeit at lowered density, can persist for extended periods in the presence of P. tenuis-infected deer at moderate dens- ities. However, it is argued here that parelaphostrongylosis can, when conditions favour sustained high deer densities and enhanced gastropod transmission, cause moose numbers to decline to low numbers or to become locally extinct. Short, mild winters favour deer population growth in areas previously best suited for moose. Wetter and longer snow-free periods increase the numbers and availability of terrestrial gastropod intermediate hosts and the period for parasite transmission. It is hypothesized that these climatic conditions increase rates of meningeal worm transmission to moose and of disease, primarily among younger cohorts. Reports of overtly sick moose are common during declines but may not account for the total mortality and morbidity caused by meningeal worm. Other means by which the parasite may further lower recruitment and productivity causing slow declines still needs clarification. Managers in areas prone to declines should monitor weather trends, deer numbers, and the prevalence of meningeal worm in deer. Moose recovery will occur only after deer numbers are decidedly reduced, either by appropriate management or a series of severe winters. ALCES VOL. 46: 53-70 (2010)
Key words: Alces alces, climate, Dermacentor albipictus, Fascioloides magna, moose die-offs, moose sickness, Odocoileus, parelaphostrongylosis, white-tailed deer.
The neurological disease of moose (Alces Samuel 2007). alces) known as “moose sickness” has been Unequivocal, direct evidence identifying reported in eastern and central North America P. tenuis as a main cause of moose declines, for almost 100 years. Its cause, the menin- admittedly, is limited. This probably has en- geal or brain worm (Parelaphostrongylus couraged the continued search for alternative tenuis) from white-tailed deer (Odocoileus explanations including ticks with an attendant virginianus), has been known for almost 50 bacterium (Klebsiella paralyticum), competi- years (Anderson 1964). But the suggestion tion with deer, trace element deficiencies, a made long ago by Anderson (1965, 1972) that proposed virus, declining habitat quality, direct the resulting disease (parelaphostrongylosis) and indirect effects of warming climate and can cause moose populations to decline is heat stress, liver flukes (Fascioloides magna), still not generally accepted (Lankester and and a variety of other proposed, human- 53 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010 induced stressors (see review by Lankester densities exceeded 5/km2. Noted declines and Samuel 2007). None, however, can be were gradual, with moose population estimates as strongly argued as the meningeal worm going from high to low values over periods of hypothesis, albeit relying heavily on indirect 7-10 years. Analyses showed that high deer evidence including knowledge of the parasite’s numbers, high reporting rates of sick moose biology in gastropods, deer, and moose, its (# of cases/# of years with reported cases), known pathogenicity, and the reoccurring and declining moose numbers were coincident association of sustained high numbers of in- in at least 5 of 13 identified declines, despite fected deer with moose declines. The purpose concerns about the precision of historical den- of this paper is to characterize past and recent sities estimates and doubts that reporting rates moose declines and to highlight the biology were representative. As well, a possible time of the meningeal worm, P. tenuis, considered shift may confound such analyses. Increased here to be the most likely cause of periodic, rates of infection in gastropods may lag behind prolonged moose declines. a buildup in deer numbers and because some snails live 2-3 years (Lankester and Anderson MOOSE DECLINES 1968), the impact on moose could continue Declines in moose numbers have occurred after deer decline. repeatedly in several eastern North American Despite periodic moose declines, it has jurisdictions during the past century (Anderson long been evident that moose can persist with 1972, Whitlaw and Lankester 1994a, Lank- infected deer for extended periods. Karns ester and Samuel 2007). Declines typically (1967) suspected that moose could be man- occur, almost imperceptibly, over a number of aged in Minnesota at acceptable numbers years and only in the relatively narrow band provided deer did not exceed 12/mi2 (4.6/km2). of mixed coniferous-deciduous forest ecotone In Ontario, Whitlaw and Lankester (1994b) extending from the Atlantic, around the Great documented a 10-year period (up to 1992) Lakes Basin, and westward toward the edge of relative deer-moose population stability. of the central Great Plains. Pre-1900, much Managers surveyed in 45 game management of this area was covered with mature forests units indicated that deer and moose were and was the southern extent of recent moose co-habiting, despite occasional reports of and caribou (Rangifer tarandus) range. Since sick moose. Moose numbers were thought then, extensive habitat rejuvenation and/or to be increasing in 36 and declining slightly extended periods of shorter, less severe winters in only 5 management units. Nonetheless, have periodically created exceptional condi- moose densities were inversely related to deer tions allowing sustained high deer densities. densities and were greatest when deer were Otherwise, deer numbers in moose range are <4/km2. Moose density was also inversely kept relatively low (approximately ≤ 5/km2) by related to the intensity of P. tenuis larvae in periodic harsh winters, regulated hunting, and deer feces. predators (Whitlaw and Lankester 1994b). Other jurisdictions similarly reported Historical moose declines had certain moose and deer apparently co-existing in close characteristics; they occurred when moose proximity during the 1970s and 1980s, includ- sickness was being reported and deer numbers ing Maine (Dunn and Morris 1981), northern were unusually high. Examining long-term New Brunswick (Boer 1992), southern Que- (80 years) historical data beginning in 1912, bec (Dumont and Crete 1996), northern New Whitlaw and Lankester (1994a) found an York (Garner and Porter1991), and Voyageurs inverse relationship between moose and deer National Park in Minnesota (Gogan et al. numbers with moose declining when deer 1997). During this period, however, deer in
54 ALCES VOL. 46, 2010 LANKESTER – IMPACT OF MENINGEAL WORM ON MOOSE these locations were not noted to be unusually the late 1980s, these same 2 jurisdictions have abundant and were likely constrained over the again experienced moose declines. In Nova longer term by weather, habitat, predators, Scotia, moose were declared an endangered and/or hunting. species in 2003 (Beazley et al. 2006), and It is clear, however, that moose co-habiting moose in northwestern Minnesota have all with infected white-tailed deer are less pro- but disappeared (Murray et al. 2006). ductive than elsewhere, although comparisons These recent studies in Nova Scotia and among identical circumstances are seldom Minnesota, as well as in North Dakota (Mas- possible. For example, on Isle Royale where key 2008), serve to further characterize the moose are constrained primarily by habitat and nature of moose declines and confirm their wolves, density ranges from approximately occurrence during prolonged periods of high 1-2/km2 (Vucetich and Peterson 2008). Mean deer densities. They also provide new informa- density approaching 3/km2, and often exceed- tion lacking in historical accounts, including ing 4/km2, is realized in Newfoundland where estimates of moose mortality rates, necropsy moose exist with bears (Ursus americanus) and findings, and better estimates of concurrent hunting (McLaren and Mercer 2005). In com- deer densities. Further insight into the plight of parison, over much of mainland eastern North moose facing rising deer numbers is provided America, where moose exist with infected by Dodge et al. (2004) in upper Michigan and white-tailed deer as well as with hunters and by anecdotal observations on the health of predators, moose densities typically are <0.4/ moose populations in northwestern Ontario km2 (Timmermann et al. 2002). Apparently, a and neighbouring southeastern Manitoba. strong interplay of limiting factors, effects of meningeal worm included, is already reflected Nova Scotia in lower moose densities where they persist The history of deer is well known (Patton in habitats with infected deer. 1991); after an introduction in the 1890s and Moose sickness has been reported his- likely immigration from neighboring New torically in the Canadian provinces of New Brunswick, deer numbers increased across the Brunswick, Nova Scotia, Quebec, Ontario, province and a “boom” occurred in the 1940s. Manitoba, and the northern states of Maine, By the early 1950s deer were more plentiful Vermont, New Hampshire, Michigan, and than ever, but 3 hard winters in the late 1950s Minnesota (Lankester 2001). Moose essen- depressed deer numbers and moose responded tially disappeared in Wisconsin by the early positively (Benson and Dodds 1977). For the 1900s (Parker 1990) and have re-colonized next 15 years deer numbers were fairly stable, only the highland areas of northern New York producing an annual harvest of about 20,000 (Hickey 2008); both states have had relatively deer. Three recognizable moose declines were high deer densities with regularity since the identified in the period 1930-1975 (Whitlaw early 1900s (Culhane 2006). Moose continue and Lankester 1994a). During these declines, to struggle in the Upper Peninsula of Michigan a total of 137 cases of moose neurological dis- despite 2 reintroductions (Hickie 1944, Dodge ease (6.5-10/yr) were noted; a record number et al. 2004). of cases for any single jurisdiction. By 1985 a Of nearly 500 reports of sick moose (lit- series of relatively mild winters had produced erature to 2001), most occurred in Nova Scotia another increase in deer numbers and a harvest (28%) during the 1940-1950s, and northern of 63,000 deer. Deer declined to one-quarter Minnesota (20%) during the 1930-1940s that number in 1990 and moose numbers may (Lankester 2001). More recently, during a pro- again have responded positively (Pulsifer and longed period of climate warming beginning in Nette 1995).
55 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010
Parker (2003), in an excellent review of highlands of Cape Breton) has a climate mod- the status of moose in mainland Nova Scotia, erated by proximity to the sea and is warmer suggested that numbers generally showed a and wetter than much of southern, continental somewhat continuous decline beginning as moose habitat. Although periodic hard winters early as the late 1920s, despite a partial hunt- along with coyote predation are known to ing closure in 1937 and a total ban in 1981 impact deer numbers (Patterson et al. 2002), (excluding Cape Breton Island). Agreeing extended periods of deer population growth with earlier authors (Dodds 1963, Telfer 1967, and a wetter climate conducive to gastropod Benson and Dodds 1977), he noted that a transmission may explain why moose numbers decline in the numbers of moose harvested outside of refugia have not recovered. It may clearly showed an inverse trend with increas- be significant that much higher prevalence ofP. ing deer harvests. tenuis infection has been found in gastropods Presently, moose remaining in mainland in Nova Scotia and southern New Brunswick Nova Scotia are largely confined to 5 remnant, (2.6% and 2.3%, respectively) than is found in localized groups, each with 50-600 animals northern New Brunswick and more continental (Beazley et al. 2008). They are mostly in parts of eastern Canada (<0.5%; see review elevated areas with early, deep-snow winters by Lankester 2001). and separated from deer, at least during winter. These areas are thought to serve as partial Northwestern Minnesota refugia from parelaphostrongylosis (Telfer A recent moose decline commencing about 1967, Pulsifer and Nette 1995, Lankester 2001, 1985 in an area including the Agassiz National Beazley et al. 2006). Although data are scant, Forest Wildlife Refuge, the Red Lake Wildlife calf survival in some of these groups was low, Management Area, and adjacent agricultural and parelaphostrongylosis was observed in land was studied by Eric Cox (deceased). the population (Beazley et al. 2006). These Data from related aerial moose surveys, authors, citing Benson and Dodds (1977), and necropsy of radio-collared (females and concluded that sufficient circumstantial evi- neonates) and accidentally killed moose from dence exists to suggest that a decline of the 1995-2000 were later analyzed by Murray et mainland moose population began following al. (2006). marked increases in deer numbers in the late The geography of the general area is rather 1920s-early 1950s, and continued in associa- atypical of moose habitat with much within tion with periodic high deer densities. the Northern Minnesota Wetlands Ecoregion Moose were almost extirpated on Cape that is characterized by standing water and Breton Island by the late 1800s, but an intro- permanent wetlands (Murray et al. 2006). It duction of animals from Alberta in the late comprises a mosaic of private farmlands and 1940s led to a hunted population of about 5000 protected areas, with marshes dominating (Beazley et al. 2006, Bridgland et al. 2007). natural areas along with lowland areas of Moose continue to prosper on the highlands of willow (Salix spp.), aspen (Populus spp.), and Cape Breton Island where deer do not winter, black spruce (Picea mariana), and uplands but are absent in southeastern lowland areas. with aspen and oaks (Quercus spp.). Beazley et al. (2008) concluded that moose Following an earlier decline in the 1940s, were not excluded from the lowlands by lack moose numbers in northwestern Minnesota of suitable habitat, but possibly by climatic and grew from an estimated 1300 animals in 1960- geological factors, including a role played by 61 to about 4000 by 1984-85 (Murray et al. meningeal worm in white-tailed deer. 2006). In 1971 the population was deemed Much of Nova Scotia (excluding the high enough to support the first hunt in 49 years
56 ALCES VOL. 46, 2010 LANKESTER – IMPACT OF MENINGEAL WORM ON MOOSE
(Karns 1972). Numbers declined slightly after fluke (Fascioloides magna) in the population 1985 only to rise again by the early 1990s. was 89%, and the authors concluded that up Thereafter, moose began a step-wise decline to 32% of parasite-related death was due to that continued to 2000-01 when numbers this parasite. Meningeal worm was believed may have been as low as 500 (Murray et al. responsible for 5% of the deaths in a radio- 2006, Peterson and Moen 2009); the limited collared sub-sample, and 20% in a second hunting was stopped after 1996. After declin- submitted by the public. The cause of up to ing for almost 2 decades, an aerial survey in 25% of deaths was classified as “unknown” 2007 estimated the moose population at <100 but thought to be parasite-related. (Lenarz 2007b). Murray et al. (2006) classified moose as Deer numbers began to increase in the having died from liver flukes if severe organ 1970s, declined somewhat in the mid-1980s, and tissue damage was evident with no other but peaked again in the mid-1990s. Peak aerial overt cause of death; those without damage estimates of about 9/km2 in 1980 and 8/km2 in but with numerous flukes were considered 1994 were recorded in the Agassiz National “probable liver fluke deaths”; 89% percent Forest Wildlife Refuge (Peterson and Moen were infected. Given the absence of published 2009). Two severe winters in 1995-97 reduced evidence linking the death of moose to fluke deer numbers dramatically, but ensuing mild infection, their analyses may overstate the winters and restricted hunting allowed recov- importance of this parasite in the decline. ery by the early 2000s. Simulation models It should also be noted that Karns (1972) in 2007 estimated pre-fawning deer density sampled much the same area and found a at 5-14/km2 in the northwest forest hunting similar prevalence of fluke infection (87%) zones (Lenarz 2007a). 28 years earlier when the population had Initially during the moose decline (1984- grown to huntable numbers and continued to 1997), mid-winter calf survival was relatively do so, thereafter. Murray et al. (2006) consid- high (54-94 calves:100 cows; Murray et al. ered death was due to meningeal worm if at 2006). Only in subsequent years (1997-2001) least one P. tenuis was found in the cranium did mid-winter calf:cow ratios fall below and no other suspected cause of death was 50:100; the annual survival rate of male calves evident. Known difficulties in locating P. was half that of females. Pregnancy and twin- tenuis in moose heads (Lankester et al. 2007) ning rates in the declining population were suggest that deaths during the decline due low (<50%) for most female age classes and to this parasite were likely underestimated. correlated with nutritional state (bone marrow Overall, Murray et al. (2006) concluded that fat), and female reproductive senescence was the recent moose decline was primarily the apparent as early as 8 years old. Excessive result of climate change (increasing summer mortality generally was thought to begin and winter temperatures), possibly directly among the yearling age class and worsen pro- through summer heat stress or indirectly gressively with age. Population age structure through ecosystem changes including higher was skewed toward younger age classes and deer numbers and parasite-related disease and relatively few prime breeding-aged animals malnutrition. Inappetence and/or inanition (4-7 years old) were present (Murray et al. may have caused reduced condition since 2006). The population experienced a pooled food was not thought lacking and the growing mean annual mortality rate of 24% of which season over the study period had increased by 87% was attributed to pathology associated up to 39 days (Murray et al. 2006). with parasitic disease and related malnutrition (Murray et al. 2006). The prevalence of liver
57 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010
Northeastern Minnesota collared moose led Lenarz (2009) to suggest This area differs from northwestern Min- that a decline in the northeastern moose popu- nesota in it is largely mixed boreal forest with lation was occurring despite a lack of clear longer colder winters, and has yet to show evidence from annual aerial surveys. Using clear signs of a prolonged decline in moose data from the radio-collared animals, Lenarz numbers, although it may be imminent (Lenarz et al. (2009) found that warming January et al. 2009, Peterson and Moen 2009). Aerial temperatures above estimated physiological survey data (1983-2008; M. Lenarz, unpub- thresholds for moose were inversely correlated lished in Peterson and Moen 2009) indicate with subsequent annual survival. Tempera- that the moose population has fluctuated be- tures exceeding thresholds were considered tween 4,000-7,500 with no evident long-term to constitute heat stress by increasing energy trends. Over the last 12 years of this interval, expended to stay cool. They hypothesized calf:cow ratios and hunter success rates have that parasitic disease was likely a proximate both declined (Lenarz 2009). Limited hunting cause of mortality while lowered productivity has occurred annually since 1971 except in and increased mortality due to heat stress best 1991. Deer densities are lower than in north- explained what was occurring in this popula- western Minnesota; increasing numbers in the tion (Lenarz et al. 2009). late 1980s and 1990s were severely reduced during 2 harsh winters (1995-97). Estimates North Dakota of pre-fawning densities averaged 2.2/km2 in Maskey (2008) completed a hallmark dis- 1996, rose to about 4/ km2 by 2003, and have sertation study (University of North Dakota) remained fairly stable since (Lenarz 2007b). of factors likely to have been important in a An ongoing 6-year study of 116 radio- recent moose population decline in the Pem- collared adult bulls and cows indicates that bina Hills area of northeastern North Dakota. pregnancy and calf survival rates are nearly His findings are of particular interest because normal although twinning rates and mid-winter of this population’s close proximity to one in calf:cow ratios trend downward; the calf:cow neighboring northwestern Minnesota believed ratio was 0.32 in January 2009 (Lenarz et al. by Murray et al. (2006) to have declined due 2009). The estimated annual, non-hunter mor- to heat stress and liver flukes. Moose popu- tality rate was 21% over the 6-year period, or lations here experienced a period of growth about twice that expected, most in the southern beginning in the 1960s. By the mid-1990s, portion of the study area. Point estimates however, moose in the northeastern Pembina for the finite rate of increase averaged 0.86 Hills area began a steady, decade-long decline indicative of a long-term declining popula- to very low numbers (Johnson 2007). In a tion. About 60% of observed adult mortality sample of 32 moose dying, 19% had F. magna was classified as “unknown causes”, a good infection while 75% of the moose exhibited portion believed to be related to the effects of signs consistent with meningeal worm infec- parasites and disease worsened by warming tion (Maskey 2008). As in Minnesota, the climate and heat stress (Lenarz et al. 2009); decline in the Pembina Hills coincided with most deaths occurred in spring and fall. Liver an unprecedented increase in the range and fluke infection is much less common in moose abundance of white-tailed deer in northern in northeastern Minnesota than the northwest North Dakota (Smith et al. 2007), and with a and was not thought important, whereas men- long-term, wet climate cycle beginning around ingeal worm infections were detected in some 1993 (Todhunter and Rundquist 2004 cited in dead moose. Maskey 2008). Interestingly, moose numbers Annual mortality estimates of radio- in 2 other areas west of the Pembina Hills
58 ALCES VOL. 46, 2010 LANKESTER – IMPACT OF MENINGEAL WORM ON MOOSE were either steady or increasing, despite local The moose population on deer-free Isle increases in deer numbers. Significantly, deer Royale has behaved quite differently from in these areas had lower rates of meningeal that in the UP in the past 30 years. Reduced worm infection, presumably because of drier wolf numbers, following a canine parvovirus conditions less suitable for parasite transmis- outbreak about 1980, allowed moose numbers sion (Maskey 2008). to increase to about 2500 (3/km2) by the winter of 1995-96 (Vucetich and Peterson 2008); Michigan however, that severe winter and a delayed Moose were extirpated from lower Michi- spring reduced the population of poorly nour- gan by the late 1800s and most were gone ished animals to about 500. The population from the Upper Peninsula by 1900 (Dodge subsequently doubled by 2002 but declined et al. 2004). An attempt to reintroduce them again despite adequate food. Since 2002 in the 1930s failed. A second establishment moose have been subjected to high numbers of 61 animals brought from Ontario in 1985 of ticks and hair loss in spring, possibly due and 1987 has persisted but grown more slowly to a decade-long trend of warmer than average than expected. Despite meningeal worm ini- summers; however, late-winter mortality of tially causing 38% of observed mortality, this infested moose was not prominent. Instead, protected population, free of most predators, much mortality since 2002 is attributed to high showed some growth when deer were esti- predation on calves by a disproportionately mated at 4.3/km2 (Aho and Hendrickson 1989). high wolf population (Vucetich and Peterson However, rather than reaching a predicted 2008). Changes in the numbers of moose on population of 1000 by the year 2000, aerial Isle Royale over the past 50 years fluctuated, surveys conducted in 1996-1997 estimated sometime abruptly, largely in relation to winter <150 moose; radio-collaring subsequently severity, food constraints, and changes in wolf occurred in 1995-2001 to investigate the predation. By comparison, numbers of moose decline (Dodge et al. 2004). Of 17 deaths of confined in 2 other parks (Sleeping Giant and marked moose, more than half were attributed Algonquin Provincial Parks, Ontario) changed to meningeal worm and liver flukes. Survival slowly but dramatically when co-habiting with rates of adults, yearlings, and calves were all increasing numbers of unhunted deer with similar to those found in other non-hunted, meningeal worm (Whitlaw and Lankester lightly predated populations. They concluded 1994b). that poor population growth was due to low pregnancy and twinning rates, and no yearling Northwestern Ontario and Southeastern reproduction caused by less than optimal food Manitoba quality and supply (Dodge et al. 2004). The ranges of moose and deer first State-wide, deer increased dramatically overlapped in northwestern Ontario in 1900- after about 1985 (Frawley 2008) and by 2007 1920. Thereafter, deer increased provincially the harvest approached 484,000 animals. In until the late 1950s (Whitlaw and Lankester the Upper Peninsula (UP), peak populations 1994b) when they were as far north as Sioux of the early 1990s were reduced briefly by 2 Lookout. Moose declined during the 1940s severe winters (1995-97) but resumed their and the hunting season was closed briefly in increase until another severe winter in 2007- 1949. A series of deep snow winters began 08. Nankervis et al. (2000) found 44% of in the early1960s, but deer numbers remained deer heads sampled in the UP had meningeal robust until 2-3 extremely severe winters in worm and 0.7% of gastropods contained in- the mid-1970s reduced their populations by at fective larvae. least 50% (probably closer to 80%; B. Ranta,
59 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010 personal communication). Moose increased widely fluctuating deer population primarily during the early part of this period but appar- regulated by winter severity. In the early ently declined somewhat by the mid-1970s. 1970s, deer were numerous in much of the area From 1980-2007, winters were increasingly and sightings of sick moose with meningeal warmer and shorter, interrupted by only a few worm (and F. magna) were common (Lank- hard winters (1995-97 and 2007-09). Surveys ester 1974). More recently (1995-2008), deer in 1980-1992 of management units with both increased in number and northern distribution moose and deer indicated that moose numbers after several easy winters. Meanwhile, moose were stable to slightly increasing over much declined and virtually disappeared from the of the region, and were highest where deer extreme southeast corner of the Province, density was estimated at <4/km2 (Whitlaw south of Highway 1, and licensed hunting was and Lankester 1994b). discontinued in 2000 (V. Crichton, Manitoba By the mid-1990s, the Kenora District Wildlife & Ecosystem Protection Branch, had some of the highest moose populations personal communication). in the province at about 2/km2 on the Aulneau Peninsula in Lake of the Woods where only a MENINGEAL black powder and archery hunt was allowed WORM TRANSMISSION (B. Ranta, personal communication.). But The importance of climate in understand- by the early 2000s, deer were becoming ing rates of transmission of meningeal worm noticeably more abundant throughout much to deer and the risk of infection to moose of northwestern Ontario. This period of deer is under appreciated. Firstly, winter length increase was characterized by several years and severity are important determinants of of shorter, milder winters and large tracts of deer numbers at the northern limits of their forests in the region subject to blow-down range. Secondly, climate in summer (amount and insect damage (spruce budworm [Chori- of precipitation and length of summer) deter- stoneura fumiferana] produced a bonanza of mines 1) the survival of the parasite outside readily available forage when the dead and its host (as first-stage larvae), 2) the survival, dying balsam was colonized with arboreal abundance, and mobility of gastropods (the lichens, principally Usnea sp.). Deer peaked intermediate host), and 3) the suitability and at high numbers in the Kenora area in the length of the snow-free period when transmis- winter of 2006-07 and were again as far north sion is possible (Lankester 2001). Thusly, as Sioux Lookout. By 2007, moose were climate determines the density of deer and virtually absent on the Aulneau Peninsula. gastropods, and in turn, the rates at which each By the end of the 1990s, moose numbers in becomes infected. As emphasized by Wasel parts of northwestern Ontario were in decline, et al. (2003), the odds of encounter between especially south of Highway 17 between Ke- an infected gastropod and a white-tailed deer nora and Thunder Bay. Little information is (or moose) depend on the density and degree available on the demography of the current of spatial overlap of both. moose population but the trend in numbers was downward and poor calf productivity and Meningeal Worm in Gastropods recruitment was notable (A. Rodgers, Ontario Terrestrial gastropods (both snails and Ministry of Natural Resources, personal com- slugs) are required intermediate hosts of men- munication). ingeal worm. They become infected with P. Moose in southeastern Manitoba, east of tenuis by encountering first-stage larvae on Winnipeg and south of Lac du Bonnet, have deer feces or in soil where they are readily historically shared habitat with an infected and washed by rain and melting snow (Lankester
60 ALCES VOL. 46, 2010 LANKESTER – IMPACT OF MENINGEAL WORM ON MOOSE
2001). Although the prevalence of infection of the southeastern United States (Lankester in gastropods can be quite low (e.g., 1/1000), 2001). These higher values probably reflect a transmission is, nonetheless, very efficient. warmer, moister climate with longer periods Because of the large amounts of vegetation of gastropod activity, and probably higher deer consumed daily by deer, a low prevalence densities as well (Lankester 2001). Presum- of infection in gastropods can still result in ably, climatic conditions that favor gastropod almost all deer becoming infected and at a numbers and mobility not only increase their young age (Slomke et al. 1995, Lankester and rates of encountering larvae on feces or in Peterson 1996). soil, but also the likelihood that they will be A variety of gastropod species can serve ingested by cervids. as sources of infection but one in particular Infection of gastropods also reflects the is most important, the small, ubiquitous dark density of infected deer. There was a 4-fold slug Deroceras laeve (Lankester and Anderson difference (0.04% versus 0.16%) in the 1968, Lankester 2001). It is often the most prevalence of meningeal worm larvae between frequently infected species and the one with summer range in northern Minnesota (4 deer/ the most meningeal worm larvae, probably km2) and winter range where they aggregate because it is very mobile. It is one of the first (50 deer/km2) for a few months (Lankester land gastropods to become active in spring and and Peterson 1996). Likewise, gastropods on one of the last to cease movement in autumn Navy Island where deer exist year-round at (Lankester and Peterson 1996). Terrestrial density of about 90/km2, were 100 times more gastropod populations respond to wet climate; frequently infected (4.2%) than gastropods moisture (precipitation and dew) determines on summer range in Minnesota. Unusually their reproductive success and survival as well high prevalence in gastropods is realized only as mobility in ground litter and on low vegeta- where deer density is exceptionally high for tion. Hawkins et al. (1997, 1998) demonstrated long periods (Lankester 2001). their potential to become more numerous on surface vegetation during wet periods. For Meningeal Worm in Deer every snail sampled on the surface during The importance of winter to deer survival moderately dry periods, almost 50 more were is well known (Karns 1980) but there is a present in the first 5 cm of underlying duff and lack of reliable data needed to test suspected soil (Hawkins et al. 1998). Further, models relationships between climate, deer density, describing the potential impact of meningeal and P. tenuis-infection rate. Measuring deer worm on moose were most sensitive to changes density with acceptable precision is notori- in the intrinsic rate of increase in gastropods ously difficult and continues to be attempted (Schmitz and Nudds 1994). by only a few jurisdictions. As well, accurately Infection of gastropods is affected by measuring the prevalence and intensity of climate; for example, snails and slugs in a meningeal worm in deer requires proper tech- wet forested area on Navy Island, Ontario, niques and an understanding of the parasite’s were >6 x (5.1 versus 0.8%) more likely to developmental biology (Slomke et al. 1995, be infected with P. tenuis than those in a dry Forrester and Lankester 1997). upland forest habitat (Lankester and Anderson Of exclusive interest here is the biology of 1968). A number of studies report overall meningeal worm in deer near the northern lim- prevalence in gastropods in many deer/moose its of their distribution where they periodically areas to be much less than 1%, yet higher mean share habitat in large numbers with moose. values of 2.6-9.0% occur in the Canadian Valuable information comes from a study of maritime provinces and in deer-only areas heads and feces from road-kill deer collected in
61 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010 mid- to late winter within a deer wintering area mune to further infection by the time snow near Grand Marais, Minnesota (Slomke et al. melts the following spring when gastropods 1995). Deer density (pre-fawning) at that time resume activity. This so-called concomitant was estimated conservatively at about 2/km2 immunity no doubt protects deer from acquir- (Lenarz 1993) and the moose population was ing too many worms that will eventually reside deemed fairly stable. Maturing worms were close to the brain. detected in the heads of a large percentage of Many deer initially pick up only a single fawns in early winter (December-February) infective larva (or 2 of the same sex) and do indicating that deer are exposed to the para- not encounter another before the immune site early in life (Slomke et al. 1995); >90% response becomes protective. As a result, up had encountered the parasite by their second to one-third of all infected deer may never autumn. Infected deer retain the same live pass larvae because a mature worm of the worms in their cranium for life, young animals opposite gender cannot gain foothold (Slomke pass twice as many larvae as older animals, et al. 1995). Hence, the rates of infection in and larval output is highest in spring. deer, mean numbers of mature worms, and the In deer, the parasite requires 3-4 months proportion of sterile infections in a population before first-stage larvae occur in feces. Tradi- are determined by the rate of initial acquisition tionally, deer heads used for assessing infection of infective larvae by fawns and yearlings. rates are collected during the autumn deer Therefore, year-to-year changes in infection hunting season, but this is not the ideal time to rates and the factors responsible can only be de- obtain an accurate estimate of infection rates tected by examining successive fawn cohorts because a large portion of the harvest could (Peterson et al. 1996). Or, if the protection be fawns and yearlings with recent infections. against re-infection is as strong as believed, Because some worms will still be developing past differences in annual transmission rates inside the spinal cord and be difficult to detect, might be revealed using cohort studies of heads of fawns in hunter-killed samples should worm numbers in adult deer. either be excluded or analyzed separately. Considerable data support the prediction Deer feces to be examined for larvae are best that the prevalence of meningeal worm in deer collected in late winter when most viable increases with increased deer density (Karns infections will be patent, and feces can be 1967, Behrend and Witter 1968, Slomke et al. collected off snow and not be contaminated 1995, Peterson et al. 1996, Wasel et al. 2003, with soil nematodes. Maskey 2008). The mean number of larvae in Only low numbers of adult worms are feces of fawns after their first winter (intensity found in the heads of deer living in moose of infection) is also positively correlated with range (e.g., x = 3.2, range = 1-13; Slomke et deer density (Whitlaw and Lankester 1994b, al. 1995) because infection rates in gastropods Slomke et al. 1995, Peterson et al. 1996). are low and many have only a single larva. The importance of climate in meningeal And, shortly after becoming infected, deer worm transmission deserves more emphasis. develop an immune protection against further The prevalence in deer is positively correlated infection even if exposure is to only a single with summer and autumn precipitation that infective larva (Slomke et al. 1995). Only presumably favours gastropod infection rates those worms acquired within a few months of and availability (Gilbert 1973, Brown 1983, the first exposure are able to reach the cranium Bogaczyk 1990, Bogaczyk et al. 1993, Pe- and mature before protection develops against terson et al. 1996, Wasel et al. 2003, Maskey further infection. Hence, fawns infected in 2008). Using 9 years of fecal data, Peterson late summer or autumn are likely to be im- et al. (1996) found that the prevalence in
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10-month-old fawns correlated positively with observed in moose with only a single worm, the number of days in autumn when deer could and sometimes none. Failure to locate worms still access ground vegetation. may relate to the body site and/or killed worms, Low rainfall, and possibly lower deer or host inflammatory response (i.e., meningitis density, probably determine the westernmost and perineuritis). In addition, it is suspected limit of meningeal worm and have prevented that some infected animals may experience its spread to vulnerable cervid communities in unobservable, physiological or behavioural western Canada (Wasel et al. 2003). Unfavour- abnormalities. The difficulty of finding adult able conditions for transmission in western worms at necropsy often makes a definitive Manitoba and central North Dakota resulted diagnosis elusive. For example, in a sample in low rates of infection (<20% with worms of 34 moose showing typical clinical signs in the head). Of equal importance was the of parelaphostrongylosis, adult meningeal remarkably high proportion (44%) of deer that worms were found in only 44% (Lankester had only a single worm in the cranium; this et al. 2007). is an expected consequence of low transmis- Moose of all ages are affected but younger sion rates. A large number of deer with only animals certainly predominate. The mean age a single worm are effectively immunized and of animals showing signs in the above study thought never to develop patent infections was 3.6 years (range = 0.6-14). Those with (Slomke et al. 1995). worms detectable in the cranium were younger (1.8 ± 0.5 years) than those with signs but Meningeal Worm in Moose without worms in the head (5.2 ± 1.2 years). The meningeal worm rarely matures to Females made up 76% of sick animals >3 produce larvae in moose, hence, infection years old. The sexes were more balanced (10 depends on the presence of infected deer. male:7 female) among younger animals (<3 Infected moose show behavioral and neuro- years). There was no indication that females motor disease of varying severity (Lankester acquire fewer worms than males, but results et al. 2007). Some animals show almost suggest that over time, worms are overcome imperceptible or intermittent motor deficien- by moose and that females may survive infec- cies with slight toe-dragging or stumbling. tion longer. Results were similar in a smaller Severely affected animals can exhibit profound sample of 10 sick moose from southeastern weakness of the hind quarters and may be Manitoba (Lankester 1974). unable to rise. Others that become laterally Only one experimental study has investi- recumbent and flail their legs probably die. gated the response of moose to low numbers of Some animals exhibit chronic debility includ- infective larvae, similar to that encountered in ing loss of fear of humans and weight loss, nature (Lankester 2002). All 5 moose (5-9.5 and may remain within a restricted area for months) given 3-10 larvae showed abnormal an extended period; those escaping predation locomotory signs after 20-28 days. Symptons may recover eventually. became progressively more pronounced with Overtly sick moose show a typical suite front limb lameness and hindquarter weakness. of neurological signs, but the severity of However, after 77-130 days, marked signs signs manifest is not necessarily reflective of persisted in only one animal, were diminished the number of worms found on examination. markedly in 2, and disappeared in 2. Two Moose usually acquire <10 worms (x = 2.5 animals were challenged with 15 larvae (199 ± 0.6; Lankester et al. 2007). Those with days after initial infection) with no noticeable >3-4 in the cranium invariably show severe effects; at necropsy, one had a single worm neurological impairment, but severe signs are believed to be from the challenge. Results
63 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010 indicate that all young moose ingesting a few and a few locations in western Canada (Pybus larvae show some impairment, even if inter- 2001). The parasite has a water-based life mittent and temporary. Worms in the cranium cycle and is found only where aquatic snails were overcome and some animals recovered, of a particular genus (Lymnaeus spp.) occur. at least for the short-term, and such animals White-tailed deer and elk (Cervus elaphus) are appeared to have a degree of protection that its principal hosts and the source of infection may reduce the impact of subsequent infec- to moose. It is acquired by eating an inter- tions. How long-lasting such protection might mediate larval stage that emerges from snails be in naturally infected moose is unknown. and encysts on aquatic vegetation. Moose An enzyme-linked immunosorbent assay are a dead-end host and do not propagate the (ELISA) developed using excretory products parasite. Their risk of infection presumably of P. tenuis larvae was positive for all of the is directly related to the density of co-habiting animals infected above (Ogunremi et al. 2002). infected deer and to the densities of suitable The level of antibody response was strongly aquatic snails. correlated with the inoculating dose, and lev- There is no clinical evidence that flukes els remained high in all animals that still had kill or debilitate moose. However, the consid- worms in the cranium when euthanized. But, erable tissue pathology seen in some heavily titers diminished in 2 and were undetectable infected livers has led to the suggestion that in a third animal that had overcome worms flukes may cause mortality when moose are by the time of necropsy (186 days after in- stressed (see reviews by Pybus 2001, Lankester fection). Antibodies became elevated after and Samuel 2007). In moose, like in domestic challenge infection. More serological study cattle, migrating flukes cause bloody tracts, and accompanying, competent necropsy of extensive fibrosis and compensatory liver sick moose is needed to fully appreciate the tissue hypertrophy; infected livers may be utility of the ELISA in measuring and monitor- more than double normal size. ing the impact of meningeal worm on moose Moose experimentally infected with F. populations. magna and observed for >12 months showed no outward signs of disease (M. Lankester OTHER POTENTIAL and W. Foreyt, unpublished). Two calves and DISEASE-CAUSING PARASITES a yearling were given 50-225 metacercariae Of several parasites known in moose and observed for up to 16 months. The liver (Lankester and Samuel 2007), only 2 (liver of animals infected as calves were enlarged fluke and winter tick [Dermacentor albipic- and contained bloody tracks, extensive fi- tus]) have come to be associated with dead brosis, and walled capsules; 1 and 11 flukes or sick animals during moose population were recovered. That of the yearling had 3 declines. For several reasons, neither is likely large, thick-walled cysts but no flukes were to be the cause of gradual moose declines found at necropsy. Growth, weight gain, and discussed here. behaviour of all 3 were similar to uninfected, farm-reared moose. Liver Fluke In most hosts studied (deer, elk, caribou The giant liver fluke, or deer fluke, has a and cattle [Bovus spp.]), the prevalence of spotty and limited distribution across moose fluke infection increases with host age and range. It occurs in the Great Lakes Basin plateaus in older age classes (Pybus 2001); including central and northwestern Ontario, young-of-the-year are rarely infected. Mean southeastern Manitoba, northern Minnesota, intensity generally is similar within each in- the Upper Peninsula of Michigan, Quebec, fected age class suggesting that an acquired,
64 ALCES VOL. 46, 2010 LANKESTER – IMPACT OF MENINGEAL WORM ON MOOSE immunological resistance to further infection Newfoundland and north of approximately develops. As well, flukes have a highly aggre- 60° N latitude (Samuel 2004). Disease results gated distribution in normal cervid hosts. Most when moose acquire unusually large numbers have only a few flukes, while a small number and are subjected to a long, severe winter and of animals may carry large numbers. In dead possibly diminished food quality or avail- end hosts like moose and cattle, long-standing ability. Infested animals exhibit increased chronic infections are characterized by large grooming and restlessness due to the irrita- paste-filled, thick-walled, closed cysts with tion of blood-sucking ticks, lose weight, and few recoverable live flukes (Lankester 1974). experience extensive hair loss in late winter, Flukes are not considered important to the all of which can contribute to death. health of cattle despite infections that resemble Die-offs attributed to moose ticks have those in moose (Wobeser et al. 1985). particular characteristics. Relatively large Liver fluke infections were noted during numbers of infested moose, many with pre- earlier moose declines in Minnesota (Fens- mature hair loss, are found dead in late winter/ termacher and Olsen 1942), and flukes were spring. Such conspicuous mortality usually oc- found in livers of moose taken in the first hunt curs after a prolonged cold winter, and is often in many years; 17 and 87% were infected from reported in unusually high density populations the northeastern and northwestern regions, such as those protected in parks. Calves and respectively (Karns 1972). Moose popula- yearlings are thought to be the most severely tions in Minnesota continued to grow even affected but older animals may not be spared. with hunting, and more recently, as moose Die-offs often are widespread and rapid but in northwestern Minnesota experienced a short-lived (Samuel et al. 2000), continuing for marked decline (from about 1995-2005), the only 1-2 consecutive springs. Such epizootics prevalence of fluke infection was essentially are independent of deer density. unchanged at 89% (Murray et al. 2006). Flukes Moderate tick infestations presumably were common in the wetter habitat of north- have an on-going, sub-clinical impact on western Minnesota during population growth moose, but conspicuous die-offs most often and decline. occur when moose are dense, tick numbers Flukes are less common in northeastern are high, and nutritionally stressed animals Minnesota and not thought to play a primary have experienced a severe winter. Warmer, role in any decline there (Lenarz et al., unpub- shorter winters result in increased survival of lished data). In a study in adjacent northeastern adult females dropping off moose onto litter North Dakota, flukes were found in only18% in March and April and increased tick popula- of sick moose and were not considered respon- tions on moose the following winter (Drew sible for declining moose numbers (Maskey and Samuel 1986, Samuel 2007). Warm, 2008). In Nova Scotia, with a history of snow-free Octobers increase the survival of moose declines and where moose have been seed ticks and their likelihood of infesting declared “endangered”, liver fluke has never moose (Samuel and Welch 1991). been present. In total, these examples and Tick numbers generally correlate posi- data indicate that the deer liver fluke is not a tively with moose density (Samuel 2007). significant factor in moose declines. Over a 12-year study in Elk Island National Park, Alberta, there was a 1-year lag in tick Winter Tick numbers relative to moose numbers. Die-offs The winter tick can be found on virtu- occurred when moose approached 3/km2 and ally all moose wherever they occur in North mean numbers of ticks on moose reached America, with the exception of the island of 50-60,000. Since ticks generally have their
65 IMPACT OF MENINGEAL WORM ON MOOSE – LANKESTER ALCES VOL. 46, 2010 greatest impact on individual moose when ACKNOWLEDGEMENTS populations are high, this parasite is unlikely to I gratefully acknowledge the hard work be the cause of prolonged, relentless declines and inspiration of several graduate students in moose populations. and close colleagues in pursuing a better un- derstanding of an important and re-occurring Conclusions wildlife problem. Pronounced declines in moose numbers on the southern limits of their distribution in east- REFERENCES ern North America have occurred repeatedly Ah o , R. W., and J. He n d r i c k s o n . 1989. over the past century. The most conspicuous Reproduction and mortality of moose reductions have occurred generally in the same translocated from Ontario to Michigan. geo-climatic regions, the milder and moister Alces 25: 75-80. parts of eastern Canada (NS) and a central An d e r s o n , R. C. 1964. Neurologic disease in mixedwood, wetlands area, west of Lake moose infected experimentally with Pneu- Superior (comprising parts of northwestern mostrongylus tenuis from white-tailed Minnesota, northeastern North Dakota, south- deer. Veterinary Pathology 1: 289-322. eastern Manitoba, and northwestern Ontario). _____. 1965. An examination of wild moose The most recent declines were accompanied by exhibiting neurologic signs, in Ontario. a warmer and wetter period. Earlier declines Canadian Journal of Zoology 43: 635- (1930s-1950s) followed large-scale succes- 639. sional renewal of harvested mature forests, _____. 1972. The ecological relationships but also coincided with a lesser-known warm of meningeal worm and native cervids period (Le Mouel et al. 2008). It is concluded in North America. Journal of Wildlife here that extended periods of warmer, and Diseases 8: 304-310. possibly wetter climate provide conditions Be a z l e y , K., M. Ba l l , L. Is aa c m a n . S. Mc- conducive to moose declines resulting from Bu r n e y , P. Wi l s o n , and T. Ne t t e . 2006. increased winter survival of white-tailed deer Complexity and information gaps in re- and increased transmissibility of disease- covery planning for moose (Alces alces causing meningeal worm. Reports of overtly americana) in Nova Scotia, Canada. Alces sick moose are common during declines, but 42: 89-109. the number of recognizably sick animals may _____, H. Kwa n , and T. Ne t t e . 2008. An not represent the total mortality and morbidity examination of the absence of established caused by meningeal worm. Additional means moose (Alces alces) populations in south- by which the parasite may lower recruitment eastern Cape Breton Island, Nova Scotia. and productivity causing slow, insidious de- Alces 44: 81-100. clines still require clarification. Managers in Be h r e n d , D. F., and J. F.Wi t t e r . 1968. Pneu- areas prone to declines can lessen impending mostrongylus tenuis in white-tailed deer in harm to moose by monitoring weather trends, Maine. Journal of Wildlife Management deer numbers, and the prevalence of meningeal 32: 963-966. worm in deer. If retention of high quality Be n s o n , D. A., and D. G. Do d d s . 1977. Deer moose hunting is desired, deer numbers can of Nova Scotia. Nova Scotia Department be reduced where indicated by adjusting deer of Lands and Forests, Halifax, Nova harvest and banning supplemental winter feed- Scotia, Canada. ing that artificially elevates deer populations Bo e r , A. H. 1992. History of moose in relative to habitat. New Brunswick. Alces, Supplement 1: 16-21.
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Bismarck, North Dakota, USA. in A. W. Franzmann and C. C. Schwartz, Kar n s , P. D. 1967. Pneumostrongylus tenuis editors. Ecology and Management of in Minnesota and implications for moose. the North American Moose, 2nd edition. Journal of Wildlife Management 31: University Press of Colorado, Boulder, 299-303. Colorado, USA. _____. 1972. Minnesota’s 1971 moose hunt: Le Mo u e l , J.-L., V. Co u r t i l l o t , E. Bl a n t e r , a preliminary report on the biological and M. Sh n i r m a n . 2008. Evidence for a collections. Proceeding of the North solar signature in 20th- century temperature American Moose Conference and Work- data from the USA and Europe. Comptes shop. 8: 115-123. Rendus Geoscience 340: 421-430. _____. 1980. Winter – the grim reaper. Pages Le n ar z , M. 1993. The white-tailed deer of 47-53 in R. L. Hine and S. Nehls, editors. Minnesota’s forested zone: population White-tailed deer population management trends and modelling. Annual Report. in the north-central states. Proceedings of Minnesota Department of Natural Re- the 1979 Symposium of the North Central sources, Grand Rapids, Minnesota, Wildlife Society, The Wildlife Society, USA. Urbana, Illinois, USA. _____. 2007a. Population trends of white- La n k e s t e r , M. W. 1974. Parelaphostrongy- tailed deer in the forest zone – 2007. Pages lus tenuis (Nematoda) and Fascioloides 103-112 in M. H. Dexter, editor. Status of magna (Trematoda) in moose of south- Wildlife Populations, 2007. Unpublished eastern Manitoba. Canadian Journal of report, Division of Fish and Wildlife, Min- Zoology 52: 235-239. nesota Department of Natural Resources, _____. 2001. Extrapulmonary lungworms of St. Paul, Minnesota, USA. cervids. Pages 228-278 in W. M. Samuel, _____. 2007b. 2007 aerial moose survey. M. J. Pybus, and A. A. Kocan, editors. Pages 113-119 in M. H. Dexter, editor. Parasitic Diseases of Wild Mammals, Status of wildlife populations, 2007. 2nd edition. Iowa State University Press, Unpublished report, Division of Fish Ames, Iowa, USA. and Wildlife, Minnesota Department of _____. 2002. Low-dose meningeal worm Natural Resources, St. Paul, Minnesota, (Parelaphostrongylus tenuis) infections in USA. moose (Alces alces). Journal of Wildlife _____. 2009. 2009 Aerial moose survey. Min- Diseases 38: 789-795. nesota Department of Natural Resources, _____, and R. C. An d e r s o n . 1968. Gastropods St. Paul, Minnesota, USA.
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North Dakota, USA. Pe t e r s o n , R., and R. Mo e n . 2009. Report McLar e n , B. E., and W. E. Me r c e r . 2005. How to the Minnesota Department of Natural management unit license quotas relate to Resources (DNR) by the Moose Advisory population size, density, and hunter access Committee.
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Sm i t h , J.R., R. A. Sw e i t z e r , and W. F. Je n s e n . Wa s e l , S. M., W. M. Sa m u e l , and V. Cr i c h - 2007. Diets, movements, and consequenc- t o n . 2003. Distribution and ecology of es of providing food plots for white-tailed meningeal worm, Parelaphostrongylus deer in central North Dakota. Journal of tenuis (Nematoda), in northcentral North Wildlife Management 71: 2719-2726. America. Journal of Wildlife Diseases Te l f e r , E. S. 1967. Comparison of moose and 39: 338-346. deer winter range in Nova Scotia. Journal Wh i t l aw , H. A., and M. W. La n k e s t e r . of Wildlife Management 31: 418-425. 1994a. A retrospective evaluation of Ti m m e r m a n n , H. R., R. Go l l a t , and H. A. the effects of parelaphostrongylosis on Wh i t l aw . 2002. Reviewing Ontario’s moose populations. Canadian Journal of moose management policy – 1980-2000 Zoology 72: 1-7. – targets achieved, lessons learned. Alces _____, and _____. 1994b. The co-occurrence 38: 11-45. of moose, white-tailed deer and Parelap- To d h u n t e r , P. E. and B. C. Ru n d q u i s t . 2004. hostrongylus tenuis in Ontario. Canadian Terminal lake flooding and wetland ex- Journal of Zoology 72: 819-825. pansion in Nelson County, North Dakota. Wo b e s e r , G., A. A. Gaja d h ar , and H. M. Physical Geography 25: 68-85. Hu n t . 1985. Fascioloides magna: oc- Vu c e t i c h , J. A., and R. O. Pe t e r s o n . 2008. currence in Saskatchewan and distribution Ecological studies of moose on Isle Roy- in Canada. Canadian Veterinary Journal ale: Annual Report 2008-2009. Michigan 26: 241-244. Technological University, Houghton, Michigan, USA.
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