Nymphal survival and habitat distribution of Ixodes scapularis and Amblyomma americanum
t l k , h ; 3 ~_r'lk, a l l . I A U l . l t l U a l i ~ J U l l l ' l l l i , , 18101,11H~ llli.,,trV '
York, USA
Howard S. Ginsberg a'b* and Elyes Zhioua a aCenter for Vector-Borne Disease, Woodward HalI-PLS, University of Rhode Island
Kingston, RI 02881, USA bNational Biological Service, Woodward Hall-PLS, University of Rhode Island
Kingston, RI 02881, USA (Received 17 February 1996; revised 21 May 1996; accepted 29 July 1996)
ABSTRACT The distribution and survival of Ixodes scapularis and Amblyomma americanum were studied in deciduous and coniferous wooded habitats and in open habitats on Fire Island, New York, USA. The survival of nymphal L scapularis in field enclosures was greater in forests than in open habitats, suggesting that greater survival contributes to the higher tick population in the woods. The nymphs of each species were more common in deciduous thickets (predominantly Aronia arbutifolia and Vaccinium corymbosum) than in coniferous woods (mostly Pinus rigida) in most but not all years. Larval L scapularis were more common in coniferous sites in 1994, while the same ticks, as nymphs, were more common in deciduous sites in 1995. The survival of the nymphs was not consistently greater in either the deciduous or coniferous woods. Therefore, factors other than nymphal survival (e.g. larval overwintering survival and tick movement on hosts) probably influenced the relative nymph abundance in different forest types. Overall, the survival of A. americanum was far higher than that of L scapularis.
Key words: Ticks, Ixodes scapularis, Amblyomma americanum, habitat distribution, survival, Fire Island
INTRODUCTION
The nymph of Ixodes scapularis Say ( - - L dammini Spielman, Clifford, Piesman and Corwin) (see Oliver et al., 1993) is the stage responsible for most transmission of Lyme Borreliosis spirochetes to humans in the United States (Hanrahan et al., 1984; Spielman et al., 1985; Fish, 1993). Therefore, public education programmes that help people avoid nymphal habitats or that provide self-protective measures for use in nymphal habitats, play an important role in
* To whom correspondence should be addressed. Fax: 40l 874 4017.
Lyme disease management (Schwartz et al., 1994). Knowledge of the habitat distribution of this species contributes to the design of these public education programmes.
Nymphal Amblyomma americanum (L.) often occur in extremely high densities (Hair and Bowman, 1986) and are suspected as vectors of several diseases, including Lyme disease (Schulze et al., 1984), Rocky Mountain OI,/ULI, K,U 1~¥~,1 ~UI.IAt~IAUIIK, I , 1 7 I J J , a [ I U ~ l l l l l ~ a l l l U ~ l B ~I~!¢YIII~ (ffL U t . } 1 7 2 J , l .au~,l~Lllalt
et al., 1996), although the evidence for transmission of these diseases in nature remains controversial (Goddard and Norment, 1986; Mather, 1993; Schriefer and Azad, 1994). Dense populations of this species have recently spread northwards into eastern Long Island, NY (Ginsberg et al., 1991), and Prudence Island, RI, USA (Mather and Mather, 1990).
In the northern United States, nymphal I. scapularis dwell primarily in leaf litter in forested areas (Ginsberg and Ewing, 1989; Siegel et al., 1991). They are far less common in open habitats, such as natural meadows (Ginsberg, 1992; Ostfeld et al., 1995) or lawns (Maupin et al., 1991). Amblyomma americanum nymphs occur primarily in woods and wood edges (Semtner and Hair, 1973; Sonenshine, 1993), but they are often found in grassy habitats as well (Semtner et al., 1971a). Both species are found in deciduous and coniferous woods, and though many field workers have had the impression that I. scapularis is more common in deciduous woods (Piesman and Gray, 1994), there have been recent reports of high abundances in coniferous woods, in some cases higher than in nearby deciduous sites (Lord, et al., 1992; Lord 1995). The activity and survival of A. americanum in different habitats is strongly influenced by microclimatic factors such as the temperature and humidity (Semtner et al., 1971b; Hair and Bowman, 1986), but the role of microclimate in I. scapularis distribution remains poorly understood.
In this paper, we compare the abundance of/. scapularis and A. americanum in deciduous and coniferous woods on Fire Island, NY, and examine the role of differential nymphal survival in determining the habitat distribution of these species.
MATERIALS AND METHODS
Study site Fire Island is a barrier island off the south shore of Long Island, New York, USA. Studies were conducted in the vicinity of the Fire Island Lighthouse (near the west end of the island), where a tract of natural vegetation includes extensive coniferous woods and deciduous thickets of approximately 3 m height. The coniferous woods are composed of pitch pine (Pinus rigida Miller) with only a limited shrub layer of poison ivy (Toxicodendron radicans (L.) Kuntze), catbrier (Smilax rotundifolia L.) and various ericaceous species and a
TICK SURVIVAL AND HABITAT DISTRIBUTION 535
substantial litter layer of pine needles. The deciduous thickets consist mostly of high-bush blueberry (Vaccinium corymbosum L.), chokeberry (Aronia arbuti- folia (L.) Elliot), American holly (Ilex opaca Alton) and bayberry (Myrica pensylvanica Mirbel), with a poison ivy and catbrier shrub layer and a thick layer of leaf litter. Between and to the south of these closed-canopy areas are extensive areas of open sand interspersed with low-growth patches of bayberry, poison ivy, beach heather (Hudsonia tomentosa Nuttall), beach plum (Prunus maritima Marshall) and beach grass (Ammophila breviligulata Fernald). The vegetation of Fire Island is described in greater detail by Art (1976) and Stalter et al. (1986).
Habitat distribution of ticks Three coniferous sites and three deciduous sites were selected for flagging samples. These sites were natural patches of vegetation of varying sizes, with two coniferous patches and one deciduous patch at the west end and one coniferous and two deciduous patches in the eastern portion of the natural area surrounding the Fire Island Lighthouse (approximately 0.7 km between the east end and west end sample sites). Larval and nymphal ticks were collected with a 1 x 0.5 m flag made of white pin-wale corduroy. The lower portion of the flag was drawn through the leaf litter and the upper portion of the flag contacted vegetation up to 0.5 m above the ground.
Flag samples (1 min each) were taken in each of the six sample sites during periods of peak nymphal and larval activity, based on previous sampling experience on Fire Island (Ginsberg and Ewing, 1989; Ginsberg 1992) and on phenology samples taken during this study. The nymph samples were taken on 22-23 June 1994, 16-17 June 1995 and 9-11 June 1996 and larva samples were taken on 2-4 August 1994. A total of 15 flag samples was taken from each of the six sites during each of the four sample periods. The sequence of samples was arranged to avoid any bias from the time of day (both coniferous and deciduous sites were sampled early and late each sample day) and were matched so that each sample site was sampled every sample day to avoid bias from day-to-day fluctuations in tick activity. Previous samples from Fire Island indicated that the tick questing activity declines when ambient temperatures are below 20°C (Ginsberg and LeBrun, 1996). Therefore, the ambient temperatures were measured during each sample with a field thermometer hung from a tree approximately 0.5 m above the ground at the study site. Nymphs were spot identified in the field, while larvae were collected and returned to the laboratory for identification. When flags had excessively large numbers of larvae, specimens were collected from each cluster of larvae on the flag and the rest of the larvae in the cluster were counted, then removed from the flag. The collected larvae were returned to the laboratory and identified, so the total number of larvae of each species on the flag could be estimated.
536 H . S. G I N S B E R G A N D E . Z H I O U A
Survival experiments To determine the survival in different habitats, nymphal I. scapularis and A. americanum were placed in enclosures in coniferous woods, deciduous thickets and open sites. Ticks were placed in stockings and in snap-cap vials. The toe ends of off-white stockings (No nonsense, Sheer to waist pantyhose, M58, Off White Sandalfoot, Kayser-Roth Corporation, Burlington, NC) were cut off at ta~l, l l - l t a V k , l a l l t d V Y ~ I ~ Z U I t £ ~ . J U a l l l d ~ a l ~ u W I L I I a ~11[ .1 a U t l l ~ k~OtlJt--Kalll.~. 111 a k t t , t l U l U I l ,
ticks were confined in plastic snap-cap vials (caps had holes covered with screening) that were placed in stockings at the same sites. The stockings were secured at ground level (with marking stakes placed through holes in the clips) and covered with leaf litter (where litter was present). Ten nymphs were placed in each stocking or vial. Five stockings and five vials in stockings with each tick species were placed in each habitat type. Thus, for each species ten ticks were placed in each of 15 stocking enclosures and 15 vial enclosures (five replicates in each of the three habitat-types) for a total of 300 ticks of each species. The enclosures were placed on 24 May-9 June and each was checked for tick survival approximately 4 weeks after placement (23 June-6 July 1995). In 1995 the nymphal phenology was determined by taking 15 flagging samples, 1 min each, at a centrally located deciduous site each week throughout the experiment (these were separate from the habitat-distribution samples described above). Ticks from phenology samples were released at the site of capture immediately after counting.
Statistics The abundances of the ticks in different habitats were compared by ANOVA using the SYSTAT subprogram 'General Linear Model' (SYSTAT for the Macintosh, 1992, Evanston, IL). The data were tested for heteroscedasticity using Fm~ tests (Rohlf and Sokal, 1981; Sokal and Rohlf, 1981). The proportions of individuals of each species surviving in each habitat were compared by ANOVA using log-linear models (SYSTAT Tables subprogram) and G-tests (BIOM statistical package, subprogram RXC; Sokal and Rohlf, 1981). Comparisons of the temperatures in the different habitats were performed using SYSTAT (General Linear Model subprogram).
RESULTS
Natural tick densities in different habitats A total of 3621 nymphal ticks and 4972 larvae was collected in the habitat distribution samples. The densities of 1. scapularis and A. americanum nymphs in the deciduous and coniferous habitats are given in Table 1. The variances of the untransformed data were heterogeneous, so a ln(x + 1) transformation was used to stabilize the variances (Fma x tests for heterogeneity of variances, d f= 14 with six groups in all cases: 1. scapularis 1994, Fmax =4.458, p > 0.05; 1995,
TICK SURVIVAL AND HABITAT DISTR/BUTION
TABLE 1
Number of nymphal ticks per flagging sample in deciduous and coniferous habitat
~Entdes are least-squares mean numbers of nymphs collected per 1 rain flagging sample (for each mean, n = 45). Each entry is back-transformed from the mean of ln(x + 1) transformed data.
Fmax-- 3.742, p > 0.05; 1996, Fm~x = 2.035, p > 0.05; A. americanum 1994, Fmax=5.938, 0.05 >p>0 .01 ; 1995, Fm~x=3.376, p > 0.05; 1996, Fmax = 4.166, p > 0.05). The densities of I. scapularis were significantly greater in the deciduous than in the coniferous sites in both 1994 ( F = 7.205, d f= 1,86) and 1995 (F--- 19.350, df-- 1,86), but not in 1996 (F=0.181, d f= 1,86). The densities of A. americanum were significantly greater in the deciduous than in the coniferous sites in 1995 (F=37.030, d f=l ,86) and 1996 (F=13.900, d f = 1,86), but not in 1994 ( F = 1.067, d f= 1,86, but note the heterogeneous variances, and that the difference was in the right direction). There were no significant effects of location (east versus west plots) and no significant interactions of location and habitat (in all cases, p > 0.05), except for /. scapularis in 1996. This species was characteristically uncommon in the west coniferous plots, but was exceptionally abundant in the east coniferous plot (location × habitat interaction, F = 25.074, d f= 1,86, p = 0.000003).
The densities of larval I. scapularis in the six sample sites in 1994 and the nymphal densities in 1995 (the same generation of ticks at a later stage) are shown in Table 2. The variances of the untransformed larval samples were heterogeneous, so a ln(x + 1) transformation was used to stabilize the variances (Fmax -- 3.762, p > 0.05). Despite a significant interaction between the habitat and location (F----6.646, d f= l ,86 , p=0.012), larvae were generally more abundant in the coniferous than the deciduous sites (F--6.088, df--1,86, p = 0.015). The distribution of nymphal ticks among the sample sites in 1995 clearly differed from the distribution of these same ticks as larvae the previous year (Table 2). Overall, the larvae were more abundant in the coniferous sites, while as nymphs they were more abundant in the deciduous sites.
Differences in the ambient temperature at the time of sampling could potentially influence the apparent trends in the tick densities in the different habitats. We tested this possibility by comparing the ambient temperatures during the samples in different habitats and locations during larval samples in 1994 and nymph samples in 1994, 1995 and 1996. The temperature was
538 H.S. GINSBERG AND E. ZHIOUA
TABLE 2
Distribution of larval and nymphal L scapularis of the same generation among sample sites
Site Habitat Location Larvae in 1994 Nymphs in 1995
1 Coniferous West 3.107 (1.164-6.791) 1.234 (0.537-2.248) 2 West 27.514 (11.846-62.244) 0.735 (0.320-1.280) 3 East 28.902 (16.743-49.400) 0.865 (0.388-1.5117) 4 Deciduous West 10.167 (4.523-21.579) 3.623 (2.343-5.392) 5 East 7.684 (4.760--12.092) 1.411 (0.664-2.494) 6 East 4.845 (2.056-10.179) 2.776 (1.228-5.404)
Entries are mean numbers of ticks collected per 1 min flagging sample (for each mean, n = 15). Each entry is back-Wansformed from the mean of ln(x + 1) transformed data, with 95% confidence intervals in parentheses.
not significantly different in the different habitats during larval samples in 1994 (F--2.119, d f - l , 8 6 , p=0.149) or the nymphal samples in 1995 (F= 0.926, d f= 1,86,p=0.339) or 1996 (F= 3.171, d f= 1,86,p = 0.078), but were higher in the coniferous than the deciduous habitat during the nymphal samples in 1994 (F=5.160, d f= 1,86, p=0.026). However, the difference in the mean temperatures was small (26.0 versus 25.3°C) and the temperatures were well above the level at which tick activity declines on Fire Island (Ginsberg and LeBrun, 1996). Furthermore, the number of nymphs per sample was greater in the cooler habitat and the habitat distribution was consistent with the 1995 samples when there was no temperature difference between the habitats. Therefore, differences in ambient temperature do not account for the habitat differences documented in Tables 1 and 2.
Survival in different habitats The phenology of the nymphal I. scapularis and timing of the survival experiment are displayed in Fig. 1. The survival of nymphal/, scapularis and d. americanum in different habitats during this period are shown in Fig. 2. Three- way ANOVAs of the proportion of ticks alive using log-linear models showed significant interactions between the species and habitat type (ticks in stockings, Pearson ~2= 15.64, df=2, p < 0.001; ticks in vials, Pearson Z2= 7.95, df=2, p=0.019), so the survival in different habitats differed between species. Overall, the survival ofd. americanum was higher than for 1. scapularis (Fig. 2) (ticks in stockings, Mantel-Haenszel Z2-49.635, p<0.0001, ticks in vials, Mantel-Haenszel ;t 2 = 103.911, p < 0.00001) (SYSTAT, Tables subprogram).
The survival of 1. scapularis in the stockings differed significantly between the habitats (G=29.405, df=2, p <0.001) with no non-significant subsets, while the survival of A. americanum in stockings did not differ significantly among habitats (G=4.684, df=2, p~,0.10). In contrast, the survival of the ticks in the vials differed significantly between the habitats for both I. scapularis
TICK SURVIVAL AND HABITAT DISTRIBUTION 539
03
o3
(5 Z
10
8-
6 -
4 -
2 -
0 125
I~XPERIMENT
T
150 175 200 225
MAY JUNE JULY AUG
250
DAY OF YEAR, 1995
Fig. 1. Phenology of nymphal I. scapulans in a deciduous site within the Lighthouse tract, Fire Island National Seashore, New York, USA (means of 15 1 min flag samples + 1 SE). The horizontal bar is the timing of the survival experiment.
(G=l l .301 , df=2, p < 0.001) and A. americanum (G---9.208, df=2, p < 0.005).
DISCUSSION
Several investigators have documented the greater abundance of L scapularis nymphs in forests than in open habitats (Ginsberg and Ewing, 1989; Maupin et al., 1991; Siegel et al., 1991; Adler et al., 1992). The lower survival of nymphs in open than in wooded sites in our study (Fig. 2) indicates that survival plays a role in this distribution.
In contrast, few researchers have studied the differences in L scapularis abundance between forest types. Lord (1995) found a greater abundance in coniferous than deciduous sites in New Jersey, USA, which contradicted the impression of many field workers that these ticks are more common in deciduous habitats. In our samples, the nymphs were generally more abundant in deciduous sites than in coniferous woods. Our deciduous sites were chokeberry/highbush blueberry thickets and our coniferous sites were pitch pine woods. Lord's (1995) deciduous sites included sassafras, mixed deciduous, oak and spicebush woodlands and the coniferous sites included white pine and red cedar woods. Perhaps lumping these various sites as 'deciduous' versus 'coniferous' obscures other characteristics of the individual sites that contribute to tick abundance.
Ostfeld et al. (1995) discussed four possible mechanisms for differential tick abundances in different habitat types: differential mortality, differential natality,
540 H, S. GINSBERG AND E. ZHIOUA
A) TICKS IN STOCKINGS
100
z 7 5 -
0'~ 5 0 -
k) 2 5 - t~
0 -
PINE DECIDUOUS
HABITAT
OPEN
[] Ixodes scapularis
• Amblyorama americanum
B) TICKS IN VIALS
Z
[] lxodes scapularis
• Amblyomma araericanum
PINE DECIDUOUS OPEN
HABITAT
Fig, 2. Survival of nymphal I. scapularis and A. americanum in various habitats on Fire Island, New York, USA (n = 50 ticks of each species in each type of enclosure in each habitat).
the movement by ticks between habitats and the movement of ticks on vertebrate hosts. In addition, the differential efficiency of the sampling methods in different habitats could account for apparent differences in abundance (Wilson, 1994).
Larval and nymphal 1. scapularis both quest in leaf litter (Ginsberg and Ewing, 1989) and attach to most of the same hosts (Anderson, 1988). Therefore, any sampling biases between the habitats should be similar for the larvae and nymphs. The differences in the distribution between the larvae in 1994 and the nymphs in 1995 (Table 2) therefore suggest that sampling biases do not account
T I C K S U R V I V A L A N D H A B I T A T D I S T R I B U T I O N 541
for the habitat differences documented in the Fire Island samples. These differences between the distributions of the larvae and nymphs of the same generation also suggest that differential natality does not explain the nymphal distribution. Furthermore, I. scapuIaris crawls only short distances in nature (Ginsberg and Ewing, 1989; Falco and Fish, 1991), so immatures are unlikely to move between habitat patches on their own. This leaves differential mortality a l l U . IA[I~ l l L ~ ¥ r ~ l l l ~ l l L K / I L I ~ K 3 ~ t l t t t J i 3 t ~ 0~13 I,lt~.~ L I I U ~ L l l l ~ K a l f f l l l~ . , l , a l I Q l l l ~ I l l ~ IK31 t t ~ U I L a t
differences in tick abundance. We did not measure the movement of ticks on vertebrate hosts, but several
indirect lines of evidence suggest that this factor contributes to the tick distribution. Wilson et al. (1990) found that the numbers of immature ticks per mouse were correlated with deer abundance in 0.25 ha quadrants in a wildlife refuge on Long Island, NY. Adler et al. (1992) reported that the relationships between the tick burdens on mice and the habitat structure changed after deer were removed from Great Island, MA. Lord (1995) noted abundant deer activity in a coniferous site with the higher tick abundance than nearby deciduous sites in New Jersey. Year to year changes in tick abundance in sites in New York state (Ostfeld et al., 1995) could have resulted from the changes in deer forage abundance that resulted in the movement of deer between sites. Thus, host movement appears to play a role in nymphal distribution, but this role remains to be quantified. Deer were abundant at our study site and moved freely between the sites. The quantification of the movement patterns of deer and other mammals at this site is currently under way.
Tick survival can influence nymphal distribution in two ways: (1) the overwintering survival of the larvae might differ in different types of sites and (2) the survival of the nymphs might differ in different types of sites. The differential survival of overwintering larvae could have contributed to the changes in abundance between sites between the larval and nymphal ticks on Fire Island (Table 2). Dusb~ibek et al. (1971), for example, found that 87.5% of overwintered Ixodes ricinus larvae in a forest but only 71.1% in a meadow, remained active in late January. However, more comprehensive experimental evidence is needed to determine the role of larval survival, as compared to the movement of hosts, in explaining the change in the distribution on Fire Island.
Nymphal survival, on the other hand, clearly did play a role in the habitat distribution. Our results (Fig. 2) showed clear differences in the survival of/. scapularis nymphs in the same types of enclosures in different habitats. Of course, the nymphs in our trials were confined to stockings, whereas free-living nymphs may have been able to find refugia in the less favourable habitats, thus increasing the survival. Indeed, M.R. Bertrand and M.L. Wilson (1996) found a lower survival rate of adult ticks confined in nylon bags than of free-living ticks in outdoor enclosures and Daniel et al. (1972) reported differences in the survival of I. ricinus nymphs in outdoor cages made of different materials. Nevertheless, interpretation of our results is reasonably straightforward for I. scapularis in open habitats, where lower survival in open than in wooded
542 H.S. GINSBERO AND E. ZHIOUA
habitats is well correlated with the lower tick densities in open habitats reported in the literature (Ginsberg and Ewing, 1989; Maupin et al, 1991; Siegel et al., 1991). The comparison between the deciduous and coniferous habitats is less clear, however, because of disagreement between the results from the stocking and vial enclosures (see Fig. 2). We feel that in our experiment the survival data from the stockings are more realistic than from the vials because of I . / tJJJ.U~.sJLlk .~(~LI1L) I I JIJL tJ.JJb, Y l ~ l ~ (2~III~JL ~ O , J , / l l . . / ~ , / l l y L l ~ b , l l . . J ~ l ~ l ~,./11 1 . ~ . ~ ( . ~ ( ~ [ ] l , ~ l ( ~ l l L . ~ 1 1 1 L l l~b , Y I I ~ I ~ l l J .
the coniferous and open habitats. However, pathogenic fungi are present in Fire Island ticks (Ginsberg and LeBrun, 1996) and may be a natural mortality factor, so we report the data from the vials for the sake of completeness.
The densities of A. americanum in the Fire Island Lighthouse tract have increased dramatically since 1986, when this species was rare or absent at this site (Ginsberg, 1992). The relatively high survival of this species in all the habitats studied (Fig. 2) may partly explain its success. However, the rapidly increasing deer abundance at this site in the recent past (O'Connell and Sayre, 1989) has probably also contributed a great deal to the population increase of A. americanum, which attaches abundantly to deer in all three active life stages. Our results (Table 1 and Fig. 2) are compatible with those of previous studies, which demonstrated differential abundance and survival of A. americanum in different habitats (Semtner et al., 1971a,b, 1973; Koch, 1984), apparently related to differences in the microclimate. However, they also suggest that under the environmental conditions on Fire Island, A. americanum is a hardier species that is less restricted by habitat than is L scapularis.
ACKNOWLEDGEMENTS
The authors thank the staff of Fire Island National Seashore, who provided the use of facilities and logistical support for this study. Drs R.A. LeBrun, T.N. Mather and M.L. Wilson offered constructive comments on an early draft of the manuscript. This research was supported by the National Biological Service, administered through the Cooperative Park Studies Unit at the University of Rhode Island. This is contribution number 3172 of the College of Resource Development, University of Rhode Island, with support from the National Biological Service.
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