DIVERSITY AND ABUNDANCE OF TERRESTRIAL GASTROPODS IN VOYAGEURS NATIONAL PARK, MN: IMPLICATIONS FOR THE RISK OF MOOSE BECOMING INFECTED WITH PARELAPHOSTRONGYLUS TENUIS
Tim Cyr1, Steve K. Windels2, Ron Moen3, and Jerry W. Warmbold2,4
1Integrated BioSciences Graduate Program and Natural Resources Research Institute, University of Minnesota Duluth, Duluth, Minnesota 55811; 2Voyageurs National Park, 360 Highway 11 East, International Falls MN, 56649; 3Natural Resources Research Institute, 5013 Miller Trunk Highway, Duluth, Minnesota 55811; 4Present address: University of South Dakota, 414 East Clark St, Vermillion, South Dakota 57069.
ABSTRACT: Voyageurs National Park (VNP) has a stable population of about 40–50 moose (Alces alces). Recent declines in moose abundance in adjacent areas in northern Minnesota raise concerns about the long-term viability of moose in VNP. The parasitic nematode Parelaphostrongylus tenuis has been documented in moose in VNP and has been implicated in moose declines in other popula- tions. Terrestrial gastropods are the intermediate hosts for P. tenuis, and describing spatial and temporal differences in their abundance should increase understanding about the risk of P. tenuis infection for VNP moose at the individual and population levels. We used cardboard sheets to estimate species com- position and abundance of terrestrial gastropods in representative vegetation communities in VNP. We collected a total of 6,595 gastropods representing 25 species, 22 terrestrial snails and 3 slugs; 8 are known vectors of P. tenuis, including the slug Deroceras laeve, the most common species found. Gastropods were more abundant in September than July, and in upland forests (maximum = 555 gas- tropods/m2) more than in wetter lowlands (20 gastropods/m2). We used location data from GPS- collared moose in VNP to estimate the relative exposure of moose to gastropods that could be infected with P. tenuis larvae. The boreal hardwood forest and northern spruce-fir forest ecotypes had the high- est use by moose and high abundance of P. tenuis vectors in summer, and may pose the greatest risk for infection. Habitat use and the related risk of ingesting gastropod vectors varied by individual moose. Our method can be extended in moose range to estimate the relative risk of P. tenuis infection.
ALCES VOL. 50: 121–132 (2014)
Key Words: Alces, meningeal worm, Minnesota, moose, P. tenuis, parasite
INTRODUCTION Infections can be lethal and cause mortality The parasitic nematode Parelaphostron- indirectly through increased risk of predation gylus tenuis can be fatal to moose (Alces or accidents (Lankester et al. 2007, Butler et al. alces) (Anderson 1964), and was the prob- 2009, Wünschmann et al. 2014). Voyageurs able cause of 5% of mortality of radio-col- National Park (VNP) in northern Minnesota lared moose in northwestern Minnesota and maintains a stable, low-density population of >20% of incidentally-recovered moose in about 40–50 moose, and P. tenuis infection northern Minnesota (Murray et al. 2006, and associated mortality has been documented Wünschmann et al. 2014). The infection in and surrounding VNP (Windels 2014). causes weakness in the hindquarters, circling, Though the effect on moose at the popula- tilting of the head, and increased fearlessness tion level in VNP is unknown, previous of humans (Anderson and Prestwood 1981). studies suggest it is unlikely to be a major
121 GASTROPOD VECTORS OF P. TENUIS IN VNP – CYR ET AL. ALCES VOL. 50, 2014 mortality source at the currently low white- regions of Minnesota and the surrounding tailed deer (Odocoileus virginianus) density areas is possible (e.g., from northwestern (3–6 deer/km2) (Whitlaw and Lankester Minnesota [Nekola et al. 1999] or rock out- 1994b). crops in northeastern Minnesota [Nekola The normal lifecycle of P. tenuis 2002]). Gastropods exhibit habitat preferences includes white-tailed deer as the definitive that result in variation in presence or density host and terrestrial gastropods as intermedi- across vegetation communities or other habitat ate hosts (Lankester and Anderson 1968). features, and few studies have examined their White-tailed deer ingest infected gastropods abundance and diversity at fine spatial scales while foraging and gastropods become (Moss and Hermanutz 2010). infected with P. tenuis by crawling over or The risk of P. tenuis infection is presum- near infected deer feces (Lankester 2001). ably influenced by vector density and could However, only 0.1–4.2% of gastropods col- vary within a population because individual lected in Minnesota and Ontario were moose demonstrate differential habitat use infected with P. tenuis larvae (Lankester (Gillingham and Parker 2008). Fine-scale and Anderson 1968, Lankester and Peterson habitat use derived from GPS collars can 1996). At those infection rates, a white-tailed help clarify the risk of P. tenuis infection to deer would need to consume up to 1000 gas- individuals and populations of moose. Com- tropods to encounter a single larva (Lenarz bined, individual differences in habitat use 2009). However, Lankester and Peterson and variability among habitat types in gas- (1996) reasoned that even at such low rates tropod diversity and abundance may result of infection in gastropods, the high rates of in differential risk of moose and other cer- infection measured in white-tailed deer in vids to P. tenuis infection (VanderWaal et al. the region (≤91%, Slomke et al. 1995) is 2014). explained by the large volume of vegetation In this study we surveyed terrestrial gas- eaten on and near the ground over a few tropod species on the Kabetogama Peninsula months in the autumn. Infection rates in in VNP. Our objectives were to 1) estimate white-tailed deer derived from winter fecal the abundance and diversity of terrestrial samples have ranged from 67–90% from gastropods in different ecotypes, with parti- the 1970s to the present in VNP (Gogan et al. cular focus on known vectors of P. tenuis, 1997, VanderWaal et al. 2014). White-tailed 2) document changes in gastropod abun- deer are the definitive host of P. tenuis but dance over the growing season, and 3) com- moose, an aberrant host, also ingest infected pare the use of cover types by GPS-collared gastropods during foraging and become moose to density of P. tenuis vectors to infected. Initial signs of P. tenuis infection estimate the encounter risk of individual can appear in moose as early as 20 days after moose. experimental infection (Lankester 2002). Gastropods are necessary for P. tenuis to STUDY AREA complete its life cycle. Therefore, knowledge Voyageurs National Park (48.50° N, of gastropod populations in VNP may help 92.88° W) is an 882 km2 protected area com- managers better understand the role of prised of a mixture of forested land (61%) P. te nu is in local moose population dynamics. and large lakes (39%) along the U.S.-Canada The distribution and habitat preferences border. Moose are primarily restricted to of terrestrial gastropods in VNP have not the Kabetogama Peninsula (Windels 2014), been studied previously. Extrapolation from a 300 km2 roadless area in the center of studies of gastropod communities in different VNP, and have remained relatively stable
122 ALCES VOL. 50, 2014 CYR ET AL. – GASTROPOD VECTORS OF P. TENUIS IN VNP since the 1990s with density ranging from Table 1. Area (km2) and % total area covered by 0.14–0.19 moose/km2 (Windels 2014). each of 6 terrestrial vegetation ecotypes sampled White-tailed deer density in winter during on the Kabetogama Peninsula, Voyageurs the study ranged between 3–6/km2 (Gogan National Park (VNP), Minnesota, USA, June- et al. 1997, unpublished data of VNP). Vege- September 2011. Area calculations exclude lakes and ponds. Ecotype classifications are according tation is a mix of southern boreal and Laur- to the US-National Vegetation Classification entian mixed conifer-hardwood forests System applied to VNP (Hop et al. 2001). comprised primarily of a mosaic of quaking Ecotype Area (km2)% aspen (Populus tremuloides), paper birch (Betula papyrifera), balsam fir (Abies balsa- Northern Spruce-Fir Forest 66 23 mea), white spruce (Picea alba), white pine Boreal Hardwood Forest 62 21 (Pinus strobus), red pine (P. resinosa), jack Northern Pine Forest 52 18 pine (P. banksiana), and black spruce (Picea Treed Rock Barrens 39 13 mariana) (Faber-Landgendoen et al. 2007). Northern Shrub Swamp 8 3 Soils range from thin, sandy loams over bed- Rich Conifer Swamp 5 2 rock to poorly draining clays at lower eleva- Total 232 80 tions (Kurmis et al. 1986). Beaver-created wetlands and associated seral stages are abundant (Johnston and Naiman 1990). representative of those across the entire − Temperatures vary from 40 to 36 °C, with Peninsula. At each site we sampled during an average annual temperature of 1.4 °C. a single over-night period at approximately Mean annual precipitation is 62 cm, with 1-month intervals in each of 4 periods: 6– most precipitation falling between May and 20 June, 29 July–3 August, 18–25 August, September (Kallemeyn et al. 2003). and 9–14 September. We used 0.25 m2 cardboard sampling METHODS squares (50 Â 50 cm) placed on ground We used the “ecotype”-level vegetation vegetation to collect gastropods (Lankester classification derived from the USGS-NPS and Peterson 1996, Hawkins et al. 1998, Vegetation Map (Hop et al. 2001) to select Nankervis et al. 2000, Maskey 2008). We the 10 most common terrestrial ecotypes on randomly selected a starting sample point the Kabetogama Peninsula to sample for gas- tropods. We excluded 4 of these because and direction within each polygon such that they were too wet to sample with our metho- a 100-m sampling transect would fit entirely dology: poor conifer swamps, rich hardwood within the polygon. We placed 10 corrugated swamps, wet meadows, and shrub bogs. The cardboard squares on the 100-m transect and remaining 6 ecotypes comprised 80% of verified that all were in the same ecotype. the non-aquatic vegetation communities The cardboard was placed directly on the (Table 1); 4 were dry uplands (rock barrens soil or duff layer after rocks and branches with trees, northern spruce-fir forests, boreal were cleared from the sampling site. The hardwood forests, and northern pine forests) cardboard was saturated with water and cov- and 2 wet lowland ecotypes (northern shrub ered with a 0.36 m2 sheet of 3-mm thick clear swamp and rich conifer swamp). We ran- plastic. domly selected 5 patches (polygons) within Sheets were set in the morning and each of the 6 ecotypes within a restricted retrieved ∼24 h later. The wetness of each area to facilitate access to sampling sites sheet was estimated as the percentage of the (Fig. 1) assuming that these sites were bottom that was visibly damp. All slugs
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Fig. 1. Primary moose range (dashed line) and terrestrial gastropod sampling area (cross- hatched area) in Voyageurs National Park, Minnesota, USA, 6 July-14 September 2010. and snails on the underside of the cardboard We considered the 100-m sample trans- were collected and stored in plastic jars with ect the sample unit and tested for the effects damp paper towels. Subsequent identifica- of ecotype and sample period on abundance tion was to the lowest taxonomic level possi- of gastropod groups (total gastropods, snails ble using available keys (Burch 1962, only, slugs only) using factorial ANOVA. Nekola 2007, J. Nekola, Minnesota Depart- We also tested for an interaction between ment of Natural Resources, pers. comm.). ecotype and sampling period. We used Bon- In 3 cases, we lumped 2 closely related spe- ferroni corrections when making post-hoc cies together that could not be reliably differ- comparisons between main effects (ecotype entiated by morphological characteristics: and sample period) and set statistical signifi- Zonitoides nitidus and Z. arboreus, Nesovi- cance at P = 0.05. trea electrina and N. binneyana, and Euco- We obtained GPS locations at 15-min nulus alderi and E. fulvous. We identified intervals from 11 adult moose (9F:2M) wear- potential gastropod vectors of P. tenuis based ing GPS collars to measure habitat use dur- on a literature review (Lankester and Ander- ing June-September 2010. Spatial data were son 1968, Gleich et al. 1977, Upshall et al. displayed using ArcGIS 10.1 with ArcGIS 1986, Rowley et al. 1987, Platt 1989, Lanke- Spatial Analyst (ESRI, Redlands, CA, USA ster and Peterson 1996, Whitlaw et al. 1996, 2012), and home ranges were calculated Nankervis et al. 2000, Lankester 2001). in the Geospatial Modeling Environment
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(2012 Spatial Ecology LLC) running via the gastropods because they were damaged ArcGIS 10.1 and R 3.0.1. We calculated the beyond recognition during collection and sto- proportion of locations in each ecotype for rage, or were juveniles that can be difficult to individual moose. We calculated a relative identify accurately even to the family level (J. measure of P. tenuis transmission risk to Nekola, pers. comm.). The total number of moose in different ecotypes by comparing snails/m2 (including unidentified) increased the abundance of gastropods in each ecotype from July to September in all ecotypes com- to habitat use in each ecotype. Mean bined (ANOVA, F3,29 = 8.7, P < 0.001). The monthly habitat use (i.e., proportion of all treed rock barren cover type had the lowest locations within an ecotype) varied little snail density (7.1/m2) for all sampling periods from June to September; all differences combined. The northern pine forest and were <5% between months for any ecotype. northern spruce-fir forest ecotypes had the We therefore used the mean proportion of most snails for all periods combined, increas- use for the entire June-September period to ing from 7.3 and 10.2 snails/m2 in July to 23.7 estimate an overall risk of P. tenuis infection and 22.8 snails/m2 in September, respectively by ecotype during summer. (Fig. 2). We also evaluated variation in relative Overall, slug density was relatively con- risk of P. tenuis infection to individual stant over time within each ecotype, and at moose. Risk Value was calculated by multi- lower density than snails. Slug density plying the proportion of each ecotype used (including unidentified) was more variable by a moose by the mean density of potential over time than snail density (Fig. 3). Slug P. tenuis gastropod vectors measured in each density in all 4 sampling periods combined ecotype. We scaled the Risk Value for each was lowest (1.3/m2) in the rich conifer moose to the highest individual Risk Value swamp ecotype and highest in the northern to compare relative risk of infection among pine (6.2/m2) and northern spruce-fir forests individual moose. Our indices of risk assume (6.9/m2). Northern shrub swamp (3.3/m2) that 1) gastropod infection rates (i.e., propor- and rich conifer swamp (1.3/m2) had lower tion of gastropods infected with P. tenuis lar- slug densities than the other 4 ecotypes vae) did not vary among gastropod species, (ANOVA, F5,29 = 20.88, P < 0.001). among habitat types, or over the sampling Cardboard wetness increased as the sur- time, and 2) the likelihood of a moose ingest- vey progressed (ANOVA, F3,29 = 165.8, P ing a potentially infected vector gastropod in < 0.001); for example, mean wetness was a given ecotype is proportional to the density 47% in Survey 1 and 90% in Survey 4. of known vectors of P. tenuis in that ecotype. Within ecotypes, cardboard wetness in the Our index of risk does not consider morbid- treed rock barren ecotype was lower (51%) ity or mortality for infected moose, because than in the other 5 ecotypes (range = 75– the severity and duration of the infection 82%; ANOVA, F5,29 = 44.3, P < 0.001). can be highly variable (Lankester Eight of the collected species are known 2002, 2010). vectors of P. tenuis and comprised 32% of the sample. The slug Deroceras laeve was RESULTS the most common vector collected (26% of We collected 6,595 gastropods represent- total captures), was present in every ecotype, ing 9 families and 25 species (3 slug species and most common in the northern spruce-fir and 22 snail species; Table 2), and success- forest ecotype. Two other slug vectors were fully classified 62% of slugs and 50% of Pallifera hemphili and a Deroceras specimen snails. We could not identify 3,116 (47%) of that we could not identify to species, but
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Table 2. Composition of terrestrial gastropods collected in Voyageurs National Park, Minnesota, USA, June-September 2011. Gastropod species were identified to the lowest taxonomic level possible; 62% of slugs and 50% of snails were classified. Group Family Species Count % Total Captures P. tenuis Vectors Slug Limacidae Deroceras laeve 906 26.0 Slug Limacidae Deroceras sp. (but not D. leave) 13 0.4 Slug Philomycidae Pallifera hemphili 6 0.2 Snail Endodontidae Discus cronkhitei 55 2.0 Snail Strobilopsidae Strobilops spp. 145 4.0 Snail Valloniidae Cochlicopa sp. 6 0.2 Snail Zonitidae Zonitoides (nitidus+arboreas) 159 4.6 Total 1290 37.4 Non-vectors Snail Endodontidae Helicodiscus parallelus 7 0.2 Snail Endodontidae Punctum californicum 7 0.2 Snail Endodontidae Punctum minutissimum 2 <0.1 Snail Endodontidae Punctum spp. 4 0.1 Snail Oxychilidae Nesovitrea (electrina+binneyana) 105 3.0 Snail Pupillidae Columella simplex 6 0.2 Snail Pupillidae Gastrocopta pentodon 6 0.2 Snail Pupillidae Gastrocopta sp. 11 0.3 Snail Pupillidae Vertigo spp. 319 9.0 Snail Pupillidae Unknown 143 4.0 Snail Succineidae Oxyloma retusa 19 0.5 Snail Valloniidae Cochlicopa lubricella 11 0.3 Snail Valloniidae Zoogenetes harpa 62 2.0 Snail Zonitidae Euconulus (alderi + fulvous) 638 18.0 Snail Zonitidae Guppya sterkii 6 0.2 Snail Zonitidae Striatura milium 29 0.8 Snail Zonitidae Striatura exigua 7 0.2 Snail Zonitidae Striatura ferrea 6 0.2 Snail Zonitidae Vitrina limpida 326 9.0 Snail Zonitidae Unknown 461 13.0 Total 2175 61.4 assumed was a P. tenuis vector like its con- Risk of P. tenuis infection was highest in gener D. leave. The snails Discus cronkhitei, northern spruce-fir forests (Fig. 4). The Zonitoides nitidus+arboreas, Strobilops northern spruce-fir ecotype had the highest spp., and Cochlicopa sp., known vectors of use by moose (35% of total locations) and P. tenuis, were ∼11% of the sample and also had the second highest estimated den- found across all surveys and sample sites sity of P. tenuis vectors. Treed rock barrens (Table 2). had the fourth highest use by moose (8%)
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Fig. 2. Mean (+SE) number of snails/m2 (including unidentified) measured in each of 6 ecotypes for a single over-night period in each of 4 sampling periods in June- September, 2011 in Voyageurs National Park, Minnesota, USA. Sample periods were: Survey 1 = 6–20 June, Survey 2 = 29 July – 3 August, Survey 3 = 18–25 August, Survey 4 = 9–14 September.
Fig. 3. Mean (+SE) number of slugs/m2 (including unidentified) measured in each of 6 ecotypes for a single over-night period in each of 4 sampling periods in June- September, 2011 in Voyageurs National Park, Minnesota, USA. Sample periods were: Survey 1 = 6–20 June, Survey 2 = 29 July – 3 August, Survey 3 = 18–25 August, Survey 4 = 9–14 September. and the third highest P. tenuis vector density, based on their relatively high use and low suggesting moderate risk. Boreal hardwood vector density. Rich conifer swamps and forests were also a moderate risk ecotype northern shrub swamps were low risk
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17
15 Northern Pine Forest of Trap
2 13 Northern Spruce- Treed Rock Barren Fir Forest 11 Boreal Hardwood Forest
9
Gastropod Vectors/m 7 Rich Conifer Northern Shrub Swamp Swamp 5 0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 Propor on of Habitat Use
Fig. 4. Relative risk of moose encountering P. tenuis gastropod vectors in 6 ecotypes in Voyageurs National Park, Minnesota, USA, July-September 2010. ecotypes because of their relatively low use of P. tenuis. Most larvae in infected gastro- (5% and 7%) and low density of P. tenuis pods are presumably in the infective stage vectors (Fig. 4). (i.e., third stage) by early July (Lankester Moose displayed variability in indi- and Peterson 1996) corresponding to our vidual risk of infection as a result of dif- sampling period between mid-June and ferential habitat use. Ten of 11 moose had September. Relative Risk scores of 0.68–1.0, and Rela- The cardboard sampler method is meant tive Risk differed by ≤32% for the majority to provide a relative measure of gastropod of moose. Moose V09 was an exception as diversity and abundance, and it is critical it spent little time in gastropod rich habitats that they be as uniform as possible in shape, and had a much lower risk of infection thickness, and wetness. All were saturated (0.21) relative to the other moose (Table 3). with water at the time of deployment but dried at different rates depending on habitat DISCUSSION features (e.g., soil moisture, rockiness, expo- Gastropod density, and more specifically sure) and weather conditions (e.g., dry and density of known vectors of P. tenuis, dif- windy vs. calm and humid). Cardboard wet- fered among the ecotypes and sample peri- ness varied from 0–100% at collection and ods. Similar to previous studies, ecotypes this wide variation could skew the estimates of mixed conifer-deciduous forest types had of gastropod abundance because they are the highest gastropod densities (Gleich et al. less likely to be found on dry cardboard 1977, Kearney and Gilbert 1978, Nankervis (unpublished data, VNP). et al. 2000). The increasing density of gas- Variation in cardboard wetness could be tropods and potential P. tenuis vectors from minimized by distributing the cardboard summer to fall is also consistent with pre- after the warmest part of the day and check- vious studies in northern Minnesota (Lanke- ing them before the warmest part of the next ster and Peterson 1996). D. laeve was the day, which would be especially important in most abundant gastropod found in our study the longer and warmer days in July and early area, and is likely the most important vector August. Past studies indicate lower
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Table 3. Proportional habitat use and individual risk of moose encountering P. tenuis infected gastropods in the Kabetogama Peninsula, Voyageurs National Park, Minnesota, USA, June-September 2010. Risk value is calculated by multiplying the proportion of each ecotype used by a moose by the mean density of P. tenuis gastropod vectors measured in each ecotype. The Relative Index of Risk is the Risk Value scaled to the highest Risk Value found for an individual moose in 2010 (i.e., Moose V05). Proportion Habitat Use
Northern Northern Treed Boreal Northern Rich Relative Moose Pine Spruce- Fir Rock Hardwood Shrub conifer Risk Index # Forest Forest Barren Forest Swamp Swamp Value of Risk V05 0.43 0.18 0.02 0.24 0.00 0.03 9.50 1.00 V06 0.42 0.10 0.02 0.17 0.03 0.05 8.96 0.94 V07 0.09 0.34 0.11 0.18 0.07 0.04 8.91 0.94 V14 0.05 0.35 0.14 0.19 0.10 0.04 8.76 0.92 V07 0.04 0.37 0.10 0.18 0.06 0.03 7.80 0.82 V10 0.05 0.33 0.10 0.19 0.06 0.03 7.66 0.81 V18 0.07 0.19 0.26 0.19 0.02 0.00 7.64 0.80 V17 0.13 0.25 0.08 0.18 0.03 0.02 7.44 0.78 V12 0.10 0.32 0.03 0.21 0.06 0.05 7.23 0.76 V08 0.01 0.37 0.00 0.27 0.02 0.01 6.49 0.68 V09 0.00 0.17 0.00 0.13 0.09 0.11 2.04 0.21 gastropod abundances in early summer (Lan- need to be considered carefully because sea- kester and Anderson 1968, Kearney and Gil- sonal variation of infection rates in gastropod bert 1978, Lankester and Peterson 1996), hosts is not well understood (Lankester and and although these studies did not report Anderson 1968, Kearney and Gilbert 1978, the relative wetness of cardboard sheets, Lankester and Peterson 1996). High white- they may be biased low if sheets were drier tailed deer density has been correlated with in early summer. Cardboard samplers may increased infection rates of gastropods (Lan- underestimate the total density of gastropods kester and Peterson 1968) and moose (Whit- in an area, as the number of gastropods in the law and Lankester 1994a) at larger spatial soil underneath cardboard samplers has been scales. A recent study found no correlation reported higher than those attached between white-tailed deer abundance and to the cardboard samplers (Hawkins et al. P. tenuis infection at smaller spatial scales 1998). within VNP (VanderWaal et al. 2014), By combining information about gastro- although the range of deer abundance was pod density and relative habitat use, we limited across sites. assessed the relative risk of P. tenuis infec- Risk of P. tenuis infection varies among tion for moose in different habitat types individual moose because of differences in (Fig. 4). We likewise calculated Risk Values habitat use within respective home ranges. for individual moose (Table 3). These meth- It will also be influenced by landscape com- ods can also be used to compare risk of position and the availability of different infection between different geographic areas habitats within an area. For example, the or populations. However, we caution that the western half of the Kabetogama Peninsula assumptions associated with our methods has more area covered by the higher risk
129 GASTROPOD VECTORS OF P. TENUIS IN VNP – CYR ET AL. ALCES VOL. 50, 2014 boreal hardwood and northern spruce-fir Tailed Deer. Pathologia Veterinaria 1: ecotypes, and conversely, the eastern half of 289–322. the park contains more of the drier, low risk ———, and A. K. PRESTWOOD. 1981. Lung- treed rock barrens and northern pine eco- worms. Pages 266–317 in W. R. David- types. VanderWaal et al. (2014) found that son, F. A. Hayes, V. F. Nettles, and F. E. P. tenuis infection rates in white-tailed deer Kellogg, editors. Diseases and Parasites increased as the proportion of vector-rich of the White-tailed Deer. Miscellaneous habitats such as mixed conifer-hardwood Publications Number 7, Tall Timbers Research Station, Tallahassee, Flor- forest increased within a local area. ida, USA. While our methods only considered BURCH, J. B. 1962. How to Know the Eastern coarse habitat use in our Risk Index, moose Land Snails. W. C. Brown Company, behavior within individual ecotypes is pre- Dubuque, Iowa, USA. sumably also important. Moose may prefer BUTLER, E., M. CARSTENSEN,M.SCHRAGE, to bed in certain ecotypes (e.g., in lowland D. PAULY,M.LENARZ, and L. CORNI- habitats in hot weather) and feed in others CELLI. 2009. Preliminary results from (Peek 1997), and even if gastropods are the 2007–2008 moose herd health assess- abundant in certain ecotypes, the risk of P. ment project. 2009 Summaries of Wild- tenuis infection should be less in areas less life Research Findings. Minnesota preferred for foraging. Risk of infection Department of Natural Resources, St. may also be affected by individual prefer- Paul, Minnesota, USA. ences for forage choice, previous exposure EZENWA, V., S. A. PRICE,S.ALTIZER,N.D. to P. tenuis, health status, genetics, body VITONE, and C. COOK. 2006. Host traits mass/longevity (Ezenwa et al. 2006), and and parasite species richness in even other factors not considered here. and odd toed hoofed mammals, Artiodac- tyla and Perissodactyla. Oikos 115: ACKNOWLEDGMENTS 526–537. We thank M. Lankester and two anon- FABER-LANDGENDOEN, D., N. AASENG,K. ymous reviewers for comments that HOP, and M. LEW-SMITH. 2007. Field improved our manuscript. We thank N. Guide to the plant community types of Walker, B. Olson, and W. Chen for project Voyageurs National Park. U.S. Geologi- assistance. Funding for this work was pro- cal Survey Techniques and Methods 2–A4. vided by Voyageurs National Park, USGS- GILLINGHAM, M. P., and K. L PARKER. 2008. NPS National Resource Preservation Pro- The importance of individual variation gram, the Environment and Natural in defining habitat selection by moose in Resources Trust Fund, the Integrated Bios- northern British Columbia. Alces 44: ciences Graduate Program at the University 7–20. of Minnesota Duluth, and the Natural GLEICH, J. G., F. F. GILBERT, and N. P. Resources Research Institute. The North KUTSCHA. 1977. Nematodes in terrestrial American Moose Conference and Workshop gastropods from Central Maine. Journal Newcomers Travel Grant provided a travel of Wildlife Diseases 13: 43–46. grant to the senior author. GOGAN, P. J. P., K. D. KOZIE, and E. M. OLEXA. 1997. Ecological status of moose and REFERENCES white-tailed deer at Voyageurs National ANDERSON, R. C. 1964. Neurologic disease Park, Minnesota. Alces 33: 187–201. in moose infected experimentally with HAWKINS, J. W., M. W. LANKESTER, and R. R. Pneumostrongylus tenuis from White- A. NELSON. 1998. Sampling terrestrial
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