Interspecific Variation in Climbing by Gastropods

The University of Notre Dame Interspecific Variation in Climbing by Gastropods: Implications for Transmission of Parelaphostrongylus tenuis Author(s): Karen D. McCoy and Thomas D. Nudds Source: The American Midland Naturalist, Vol. 137, No. 2 (Apr., 1997), pp. 320-328 Published by: The University of Notre Dame Stable URL: http://www.jstor.org/stable/2426851 Accessed: 21-04-2016 14:55 UTC Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://about.jstor.org/terms

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Am. Midl. Nat. 137:320-328

Interspecific Variation in Climbing by Gastropods: Implications for Transmission of Parelaphostrongylus tenuis KAREN D. MCCOYAND THOMAS D. NUDDS

Department of Zoology, University of Guelph, Guelph, Ontario NIG 2W1l ABSTRACT.-Most studies of the gastropod intermediate hosts of the nematode parasite Parelaphostrongylus tenuis used cardboard placed on the ground to collect host specimens.

We examined interspecific variation in climbing behavior of seven gastropod species from Algonquin Park, Ontario, to evaluate the potential for sampling bias and its implications (1) for inferences regarding which gastropods may be important in parasite transmission and

(2) for estimating parasite prevalence in gastropods. Gastropods were highly variable in the degree to which they climbed and when they did so. Zonitoides arboreus, Anguispira alternata

and Deroceras laeve climbed relatively infrequently; Stenotremafraternum and Mesodon sp. were most arboreal. Discus cronkhitei and Succinea ovalis were intermediate; they spent about as much time on the ground as they did climbing. Thus, the latter species are potentially most important as intermediate hosts because they frequent the ground where they can become

infected with the parasite, but also climb to where they may be more vulnerable to ingestion

by foraging deer and moose. A comparison of gastropod collections was made between studies that used cardboard to sample gastropods and studies where hand-searching was used. It

revealed that species from the families Zonitidae and Limacidae comprised the largest fractions of collections using cardboard, consistent with the idea that cardboard samples are

biased to terrestrial species. If collections are biased, prevalence levels detected for gastropod hosts of P tenuis may underestimate true levels. Therefore, the degree of arboreality among gastropod intermediate hosts could be important to consider when evaluating the potential for different species to serve as important vectors of transmission of P tenuis.

INTRODUCTION

Parelaphostrongylus tenuis, a metastrongyloid nematode typically found in white-tailed deer (Odocoileus virginianus), has been implicated as a limiting factor of moose (Alces alces)

populations, where moose are sympatric with white-tailed deer (Anderson, 1971; Gilbert, 1974; Kearney and Gilbert, 1978). Aspects of the biology of the parasite that are frequently estimated are the proportion of a sample of intermediate gastropod hosts parasitized by larvae (hereafter termed prevalence); the average number of larvae per intermediate host (hereafter termed intensity); and the distribution and abundance of various species of po-

tential gastropod hosts (Lankester and Anderson, 1968; Kearney and Gilbert, 1978; Maze and Johnstone, 1986; Upshall et al., 1986). Gastropods become infected when they come into contact with first stage larvae (LI) shed in deer feces. Parelaphostrongylus tenuis has been found in at least 18 species of gastropod (Anderson,

1963; Lankester and Anderson, 1968; Maze and Johnstone, 1986; Rowley et al., 1987). To determine local abundance and prevalence in these intermediate hosts, gastropods are often collected from under corrugated cardboard laid on the ground (Lankester and An-

derson, 1968; Gleich and Gilbert, 1976; Kearney and Gilbert, 1978; Samuel et al., 1985; Maze and Johnstone, 1986; Upshall et al., 1986). The cardboard is moistened, laid out in transects and checked every few days at dawn or dusk (Maze and Johnstone, 1986; Upshall et al., 1986). This method assumes that all gastropod species and age classes are equally

I e-mail: [email protected], [email protected] 320


1997 McCoy & NUDDS: CLIMBING BY GASTROPODS 321 attracted to cardboard and equally likely to be found when the cardboard is examined (Boag, 1982). This assumption may be violated, however, if some gastropod species are arboreal (climb), such that terrestrial species are more likely to be sampled by cardboard, and if there is diurnal variation in climbing behavior. Species of gastropods collected by the cardboard method, found to be abundant and to have a high prevalence of larvae, are usually inferred to be the species most important in

transmission (Lankester and Anderson, 1968; Kearney and Gilbert, 1978). For example, Upshall et al. (1986) suggested Deroceras laeve was important in the transmission of Pare-

laphostrongylus tenuis in central New Brunswick only because it was most heavily infected and most widespread; Rowley et al. (1987) further considered that the arboreal behavior of Deroceras laeve might make it especially vulnerable to accidental ingestion by deer. Here, we report on interspecific variation in the climbing behavior of various gastropod hosts of Parelaphostrongylus tenuis commonly found in Algonquin Park, Ontario, and infer

from the degree and temporal pattern of arboreality, the potential for bias in the commonly used cardboard collection technique and the relative importance of various gastropod spe-

cies in the transmission of P tenuis. METHODS

Gastropods were collected from Algonquin Park, Ontario, using both hand collection (searching for and collecting every gastropod seen) and cardboard, between June and August 1994 (except for Deroceras laeve, which was collected in June and July 1995) and were maintained in laboratory terraria until beginning experiments. Terraria were kept moist by periodic misting with distilled water and lettuce was added regularly. Powdered calcium carbonate was also provided (Lankester and Anderson, 1968; Gray et al., 1985). Gastropods

were identified using keys by Burch (1962) and Pilsbry (1946). Two experiments were conducted. In the first, six species were used: Zonitoides arboreus

(family Zonitidae), Discus cronkhitei (family Endodontidae), Stenotrema fraternum (family

Polygyridae), Succinea ovalis (family Succineidae), Anguispira alternata (family Endodontidae) and Mesodon sp. (family Polygyridae). For each species, five 500-ml jars, with approximately 6 cm of potting soil in the bottom and cheesecloth over the top, were randomly arranged with jars containing the other species on a table. The number of individuals per jar varied among species depending on availability; that is, the size of the laboratory populations of each species (Z. arboreus, 10 individuals/jar; D. cronkhitei, 4 individuals/jar; S.

fraternum, 2 individuals/jar; S. ovalis, 2 individuals/jar; Mesodon sp., 3 individuals/jar; and A. alternata, 3 individuals/jar). Photoperiod in the windowless laboratory was set at 12L:

12D 1 wk before the onset of observations. Ambient temperature varied from approximately 20 to 30 C. Throughout the experiment, lettuce and water were supplied at random intervals to avoid introducing bias in climbing behaviors.

Between 25 October and 1 December 1994, observations were made four times daily (0800 h, 1200 h, 1600 h and 2000 h), every 2nd day, during two 2-wk periods, separated by 1 wk. During the first period, sampling occurred during daylight hours. Then, photoperiod was advanced 12 h and sampling occurred for 2 more wk during the "night". Since Bailey (1981) found that the snail, Helix aspersa, rephased its activity within 4 days of re-

versing the day/night cycles, we assumed that 1 wk between the day and night periods would be sufficient to "reset" the gastropods' circadian clock. The number of individuals in each jar that were climbing on the sides and the top of the jar ("up") was recorded. At the end of each 2-wk period, the number of individuals still alive in each jar was recorded. Dead individuals were assumed dead from the onset of the experiment, unless the climbing data indicated otherwise, because there was no way of knowing at what time they died


322 THE AMERICAN MIDLAND NATURALIST 137(2)

1.0

1.0

0.8

0.8

0

0.6

A

B

0.6

0

a)

0.4

0.2

0.4

0.2

SF M SO DC DL AA ZA M SF SO DC DL AA ZA

FIG. 1.-Average proportion of "up" observations in the day (A) and night (B) for seven gastropod

species (M-Mesodon sp.; SF-S. fraternum; SO-S. ovalis; DC-D. cronkhitei; DL-D. laeve, AA-A. alternata; ZA-Z arboreus). Student-Newman-Keul groupings indicated by straight lines below species codes

during the experiment; in that way no dead individuals were counted as terrestrial (or "down") observations. Individuals found dead after the first 2-wk period were replaced before the start of the second period for all species except Succinea ovalis, for which there

were not enough individuals in the laboratory population. In the second experiment, only Deroceras laeve (family Limacidae) was used. The experiment was identical to the first, with five jars and four individuals in each jar, except that

day and night observations were made over the same period between 17 and 29 September 1995. Photoperiod was again set for 12 h; lights were on between 0800 h and 2000 h daily.

Four observations were made every other day, two at "night" (0745 h and 2015 h) and two during the "day" (0815 h and 1945 h). The number of individuals alive in each jar was recorded each time lettuce and water were added.

Statistical analysis.-The proportion of the total number of individual gastropods that

were "up" when observed was determined for each jar and normalized by arcsine transformation (Zar, 1984). For each of the sets of data collected during the day and during the night, interspecific variation in climbing behavior was tested by analysis of variance and Student-Newman-Keuls (SNK) test (SAS, 1990). Finally, for each species, we tested whether the proportion of individuals that were observed "up" differed between day and night with t-tests (Zar, 1984). RESULTS

There was significant interspecific variation in climbing behavior (Fig. 1) during both

day and night (F = 11.46, P = 0.0001 and F = 20.71, P = 0.0001, respectively). SNK tests (Fig. 1) separated species into three reasonably distinct groups. Mesodon sp. and Stenotrema

fraternum were always most arboreal. Similarly, Deroceras laeve, Anguispira alternata and Zonitoides arboreus were always most terrestrial. The tendency to climb varied with diurnal


1997 McCoy & NUDDS: CLIMBING BY GASTROPODS 323 TABLE 1.-Number of dead gastropods found at the conclusion of climbing experiment (dead/total individuals used). Note: one replication of Stenotrema fraternum was omitted from analysis in both the

day and night experiments because individuals were dead from the onset Day

Zonitoides Discus

arboreus

cronkhitei

Mesodon Anguspira

sp.

Night

7/50

10/20

0/15

alternata

7/50

12/18 0/15

0/15

1/15

Stenotrema fraternum 3/8 2/8 Succinea

ovalis

2/10

7/9

Deroceras lavae day and night 8/20

period for Succinea ovalis and Discus cronkhitei. Most species tended to climb more at night, but only Mesodon sp. and Anguispora alternata climbed significantly more at night (t =

-2.599, P = 0.0317; t = -2.336, P = 0.0477, respectively). The number of individuals that died over the course of the experiment varied with species (Table 1). Mortality was greatest for Discus cronkhitei (both day and night) and Succinea

ovalis (night). Observed climbing behavior would be inflated if individuals were falsely assumed dead from the start. Thus, for example, D. cronkhitei could be more terrestrial than our results indicate. In the terraria, however, D. cronkhitei were frequently observed climbing. In the case of S. ovalis, observations of climbing indicated that many of the dead individuals died close to the end of the experiment. Thus, our results are robust to variation among species with respect to mortality during experiments. DIscuSSION

Gastropod species varied considerably in the occurrence and timing of climbing behavior. These results have two implications with respect to the transmission dynamics of Parela-

phostrongylus tenuis. First, the technique commonly used for sampling gastropods potentially favors collecting those species with more terrestrial habits. Therefore, certain arboreal mem-

bers of the gastropod community may have been underrepresented in some earlier studies. Figure 2 shows the fractions of different families from total gastropod collections, compiled from four published studies that used cardboard and compared to four studies in which

gastropods were collected by hand. Because these studies ranged throughout the United

States and Canada, and there may be differences in the species found in each area, we averaged data, across studies, at the family level. Families containing species which our laboratory experiments indicated were relatively arboreal, such as Polygyridae, were sampled

less frequently by cardboard than were families with more terrestrial species, such as Zonitidae. Further, studies that used hand collection tended to report greater percentages of species from arboreal families.

Because there is a potential bias in regard to the distribution and abundance of gastropods in previous studies, there is also the potential that estimates of prevalence of Parela-

phostrongylus tenuis in the gastropod community, based on these collections, are also biased. Prevalence of P tenuis in gastropods, even in areas with very high prevalence in definitive hosts, is usually quite low (Nudds, 1990). A summary of studies completed for eastern North

America indicates that the prevalence of infection in deer is generally over 50%, whereas

that in the gastropod community is usually much less than 10% (Fig. 3). Ten percent of a snail population of a given area very likely includes a greater number of individual hosts


324 THE AMERICAN MIDLAND NATURALIST 137(2) 40

3 Cardboard

35

CHand 30

10

o5

10

Zonitidae Limacidae Endodontidae Polygyridae Succineidae

(ZA)

(DL)

(AA,

DC)

(SF,

M)

(SO)

FIG. 2.-Percent of gastropod collections by family, averaged across studies, for studies that used

cardboard to collect vs. studies that used hand search methods or, a combination of hand searching and cardboard. Species used in climbing experiment listed below corresponding family using codes as

in Figure 1. Data for cardboard-only collections from Gleich and Gilbert (1976), Kearney and Gilbert (1978), Rowley et al. (1987) and Upshall et al (1986). Data for hand searches, or a combination of hand search and cardboard from Lankester and Anderson (1968), Maze andJohnstone (1986), Platt (1989) and Raskevitz et al. (1991)

than would 50% of a deer population for the same area but, even so, prevalence in the intermediate hosts seems too low to account for the high prevalences observed in many

definitive host populations. It is possible that, due to the length of their lifespan and the nature of their foraging habits, deer eventually eat an infected gastropod (Anderson and

Prestwood, 1981). However, 48% of fawns have been found infected in certain areas (Gilbert, 1973), so it is also possible that prevalence in gastropods is actually higher than reported. For example, species like Mesodon sp., in the family Polygyridae, have been found to be more susceptible to Parelaphostrongylus tenuis infections than other species (Lankester and Anderson, 1968) and species in this family are potentially underrepresented by the cardboard collection technique. In the Himsworth Game Preserve in Ontario, 16,498 gastropods

were collected; prevalence of parasitic larvae was only 0.06% (Kearney and Gilbert, 1978). Of the gastropods collected, only 0.8% were from the family Polygyridae. If, by the nature of the sampling technique, individuals of this family were missed, the calculated prevalence may greatly underestimate the true prevalence. The second implication that variable climbing behavior has is with respect to the deter-

mination of which gastropod species are important in the transmission of the parasite. Schmitz and Nudds (1994) modeled the effects of Parelaphostrongylus tenuis on moose populations and found that model solutions were most sensitive to the intrinsic rate of increase of the gastropod host. Because the different species can have very different life histories (Ingram, 1944; Getz, 1959), it is important to determine which gastropod species


1997 McCoy & NUDDS: CLIMBING BY GASTROPODS 325

gastropods

20

0

deer

~15 '4-

0

z

5

0

0 10 20 30 40 50 60 70 80 90 100 PREVALENCE FIG. 3. Distribution of prevalence estimates (% infected) of Parelaphostrongylus tenuis in deer (n = 67 studies) and gastropod (n = 26 studies) populations. Values for deer are from Anderson and

Prestwood (1981), Bogaczyk et al (1993), Dew (1988), Garner and Porter (1991),Jarvinen and Hedberg (1993), Kocan et al. (1982), Peterson and Lankester (1991), Pitt and Jordan (1994), Slomke et al. (1995), Thomas and Dodds (1988), Upshall et al. (1987) and Whitlaw and Lankester (1994). Gastropod prevalence values were taken from Gleich et al. (1972), Kearney and Gilbert (1978), Lankester and Anderson (1968), Maze and Johnstone (1986), Pitt and Jordan (1994), Platt (1989), Raskevitz et

al. (1991), Rowley et al. (1987), and Upshall et al. (1986). Prevalence in gastropods did not exceed

10% except when total collections were separated into groups (i.e., mature slugs only)

are the principal vehicles of transmission in order to better determine the effect of the parasite on cervid populations. Many previous studies have tried to determine which gastropod species are important in

transmission by inferring it from the abundance and prevalence of infection in the different species (Lankester and Anderson, 1968; Platt, 1989). The degree of arboreal behavior, how-

ever, may have important implications for which species are actually important. Species which are more terrestrial in nature, like Zonitoides arboreus, are perhaps more likely to be

infected since they have a greater chance of coming into contact with LI larvae compared with more arboreal species, such as Mesodon sp. Even if a large number of terrestrial species are infected, unless they climb to browse height (or cervids feed on low vegetation), they


326 THE AMERICAN MIDLAND NATURALIST 137(2) are unlikely to be ingested by the definitive host and, therefore, would not be important in transmission. Some have noted that deer graze at ground level during certain times of the season (Lankester and Anderson, 1968), but many of these terrestrial species are found deep within the litter layers of the forest floor (pers. observ.), a place unlikely for deer to graze. It could be that there are a few gastropod species which are intermediate in their arboreal/terrestrial behaviors, that can both pick up the parasite and transfer it to the definitive host. Based on our experiments, it appears that these are Discus cronkhitei and Succinea ovalis. Within their range, these species have been found to be intermediate with respect to prevalence of the parasite (Lankester and Anderson, 1968; Maze andJohnstone, 1986; Platt, 1989).

Many parasites have been shown to alter the behavior of intermediate hosts, thereby increasing the likelihood of transmission to the next host (Carney, 1969; Moore, 1983;

Curtis, 1987; Levri and Lively, 1996). If Parelaphostrongylus tenuis alters the climbing behavior of its gastropod host, a possibility we are currently examining, then the climbing behaviour of the different species may change and therefore, the relative importance of the different species in transmission of the parasite may be altered from that which we inferred from our observations of uninfected gastropods.

The variable nature of the climbing activity of different gastropod species indicates that one collection procedure may not be sufficient to obtain an accurate estimate of gastropod distribution and abundance. The assumption that all species are equally attracted to card-

board traps is likely false. Although more time-consuming and tedious, other methods should also be employed to ensure a better representation of the gastropod community of a given area. In order to determine which species may be the most important in transmission, the arboreal nature of the gastropod hosts, as well as the feeding nature of the definitive hosts need to be examined. With these considerations, it should be possible to obtain a clearer indication of the effect that variable behaviors of potential intermediate hosts might have on the transmission of Parelaphostrongylus tenuis and the risk the parasite may pose to cervid hosts. Acknowledgrments.-Thanks go to the following people for their generous assistance with various parts

of this study: Alison Stuart, Sheila MacLeod, Derek Potter, Heather Hager, the staff and researchers at the Wildlife Research Station in Algonquin Park, Ontario, and two anonymous reviewers. This research

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