Experimental & Applied Acarology, 21 (1997) 755–771
Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south–central Sweden Lars T¨alleklint and Thomas G.T. Jaenson* Medical Entomology Unit, Department of Entomology, Swedish University of Agricultural Sciences, Uppsala and Department of Zoology, Uppsala University, Villav¨agen 9, S-752 36 Uppsala, Sweden (Received 3 January 1997; revised 11 April 1997; accepted 12 June 1997)
ABSTRACT Infestation by Ixodes ricinus ticks on rodents, hares and cervids was examined at Bogesund, 10 km north of Stockholm, in south–central Sweden during 1991–1994 and on varying hares (Lepus timidus) at Stora Karls¨o and Gotska Sand¨on in the Baltic Sea during 1992–1993. At Bogesund, there were great differences between two consecutive years in the number of I. ricinus larvae infesting bank voles (Clethrionomys glareolus). The seasonal pattern of infestation by I. ricinus larvae and nymphs on bank voles was unimodal in 1991, with peaks in June–July and bimodal in 1992, with peaks in June and August. Male bank voles, compared to females and older voles, compared to young voles, harboured greater numbers of I. ricinus ticks. Apodemus mice, compared to bank voles, harboured greater numbers of I. ricinus ticks. Ixodes ricinus larvae engorged on Apodemus mice were heavier than larvae engorged on bank voles and resulted in larger nymphs. However, there was no difference in the proportions of viable nymphs resulting from larvae engorged on mice or voles. The ranges in the numbers of I. ricinus ticks infesting individual hosts were 1–451 for rodents, 16–2374 for hares and 428–2072 for roe deer (Capreolus capreolus). These ranges of tick numbers are estimated to represent potential blood losses from individual hosts of approximately 0.2–65% for rodents, 0.2–13% for hares and 0.3–9.0% for roe deer. Within the populations of all host species examined, the distributions of all stages of I. ricinus were clumped, with most host individuals harbouring few ticks and only a few individuals harbouring many ticks. The data suggest that, even though a small proportion of tick hosts may be severely affected, the direct effects of feeding by I. ricinus are unlikely to play an important role on mammal population dynamics. Keywords: Ixodes ricinus, mammals, population dynamics, infestation patterns, Sweden.
INTRODUCTION
Ectoparasitic ticks (Acari: Ixodoidea) may have several negative effects on their hosts, both direct effects, such as blood loss from tick feeding and tissue destruction from enzymes present in tick saliva and indirect effects, such as activation of the * To whom correspondence should be addressed at: Tel: 146 18 471 29 39; Fax: 146 18 559888; e-mail:
[email protected]
0168–8162 © 1997 Chapman & Hall
756
¨ L. TALLEKLINT AND T.G.T. JAENSON
host’s immune system or exposure of the host to pathogens (reviewed by Nelson et al., 1975, 1977; Kaufman, 1989; Lehmann, 1993). Regarding hard ticks (Acari: Ixodidae), relatively few studies have dealt with the interactions between three-host ticks and their natural hosts. These ticks leave the host after a completed blood meal and may, therefore, feed as larvae, nymphs and adults on three different host individuals. Some of these studies recorded negative effects on the hosts (Bolte et al., 1970; Keith and Cary, 1990; Gemmell et al., 1991; Hair et al., 1992) whereas others failed to find clear effects (Bauwens et al., 1983; Bull and Burzacott, 1993). The host defensive actions against feeding ticks include grooming activity and acquired resistance reducing tick attachment success, engorgement weight or moulting success (reviewed by Kaufman, 1989; Rechav, 1992; Sonenshine, 1993; Wikel, 1996). In the case of Ixodes ricinus, many aspects of the infestation of this tick on mammals have been studied. For instance, the risk of a mammal species being infested by I. ricinus varies both spatially and temporally (Mermod et al., 1973, 1974; Gray et al., 1978, 1992, 1995; Pruszynska, 1983; Gray, 1984; Randolph and Steele, 1985; Steele and Randolph, 1985; Nilsson, 1988; Matuschka et al., 1990, 1991, 1992, 1994; Doby et al., 1992; de Boer et al., 1993; Humair et al., 1993; T¨alleklint and Jaenson, 1994, 1996; Craine et al., 1995; Kurtenbach et al., 1995). Moreover, the host species, host sex and host age appear to affect infestation by I. ricinus (Brinck et al., 1967, 1984; Nilsson and Lundqvist, 1978; Pruszynska, 1983; Matuschka et al., 1990, 1991, 1992, 1994; Doby et al., 1992; de Boer et al., 1993; Humair et al., 1993; Craine et al., 1995; Kurtenbach et al., 1995). In addition, an acquired resistance against feeding I. ricinus ticks has been reported for voles, but appears absent in mice (Lebedeva, 1981; Dizij and Kurtenbach, 1995). However, data on the interactions between I. ricinus ticks and their mammal hosts have often appeared incidentally, usually in papers focusing on other topics, such as the transmission of tick-borne pathogens. The primary aims of this paper are to investigate and analyse the infestation patterns of I. ricinus ticks on individual mammal hosts and various mammal host populations, to estimate the potential impact of tick feeding on individual hosts and host populations and to discuss the factors determining the infestation patterns. MATERIAL AND METHODS
Field work Small mammals were live captured at Bogesund, 10 km north of Stockholm in south–central Sweden, for five successive days and nights monthly during June– September 1991 and 1992 and in July and September 1994, using Ugglan special traps (Allan Ahlgren, Marieholm, Sweden) baited with sunflower seeds and pieces of apple. Trapping was conducted in three quadratic 0.5 ha grids, each with 36 evenly spaced traps. The traps were inspected twice daily, at 0600–0700 h and 1800–1900 h. Trapped animals were brought into a field laboratory. Fed ticks were collected from live-trapped small mammals by suspending cages with trapped
INFESTATION OF MAMMALS BY I. RICINUS
757
animals over pans with water for approximately 5 days. The ticks were removed from the water twice daily, at 0700 and 1900 h. During 1991–1992, 146 of 147 rodents survived the captivity and were released at the place of capture. The Swedish welfare regulations concerning trapping and maintaining animals were met and all the pertinent documents required by Swedish authorities are on file. In addition, skins from newly shot lagomorphs (August–September 1991, 1992 and 1993), roe deer, Capreolus capreolus (August–September 1990, 1991, 1993 and 1994) and moose, Alces alces (August–September 1991 and 1992) originating from the Bogesund area (T¨alleklint and Jaenson, 1994) and lagomorphs originating from the islands of Gotska Sand¨on and Stora Karls¨o (Jaenson and T¨alleklint, 1996) in the Baltic Sea (September 1992 and August–September 1993) were examined for ticks by suspending the skins over water until all ticks had detached. With the exception of a few Ixodes trianguliceps collected from rodents and one Ixodes hexagonus collected from a deer, all of the ticks were I. ricinus (Jaenson et al., 1994). During July and September 1994, detaching engorged larvae and nymphs were weighed on a digital scale (Cahn 29) 3–4 days after detachment. Larvae collected in July were held in humid chambers under natural temperature and light regimes until they had moulted to nymphs or died. The size of each resulting nymph was estimated by measuring the scutal area. This area was calculated according to the formula for that of a circle (pr2), where the radius can be estimated as the sum of the length and width of the scutum divided by four. A tick host’s potential blood loss caused by infesting I. ricinus ticks was estimated as (number of infesting larvae on the host 3 mean size of the larval blood meal 1 number of infesting nymphs on the host 3 mean size of the nymphal blood meal 1 number of infesting females on the host 3 mean size of the female blood meal) 4 total blood volume of the host. The blood volume (l) of the mammals can be estimated as (kg body weight)0.99 3 0.055 (Schmidt-Nielsen, 1975). The actual weight of each rodent was used. For the larger mammals, their weights were estimated at 4.5 kg for a European hare (Lepus europaeus), 3.9 kg for a varying hare (Lepus timidus), 18 kg for a roe deer buck, 8 kg for a roe deer fawn and 100 kg for a moose calf. The mean size of a tick blood meal was based on the data of Balashov (1972) for Ixodes persulcatus: 2.62 ml for a larva, 15.86 ml for a nymph and 732.8 ml for an adult female. Data analysis The differences in the numbers of I. ricinus larvae infesting different species of rodents and bank voles (Clethrionomys glareolus) of different sex and age were examined by Mann–Whitney U-tests, based on sampling occasions with similar median numbers of ticks infesting bank voles weighing .19 g, i.e. June and July 1991, July and September 1992 and July 1994 (data presented in Table 1). Similarly, the differences in nymphal infestation were examined by Mann–Whitney U-tests, based on sampling occasions with similar mean numbers of nymphs
Median number of larvae per host Mean (6 SD) number of larvae per host Proportion (%) of hosts infested by larvae Median number of nymphs per host Mean (6 SD) number of nymphs per host Proportion (%) of hosts infested by nymphs Number of hosts examined
July 1991
August 1991
September 1991
38 36 19 19.5 40 6 25 38 6 24 22 6 14 17 6 8 100 100 100 100 0 1 0 0 0.3 6 0.5 1.6 6 2.9 1.2 6 1.7 0 25 64 46 0 4 11 13 8
June 1991
July 1992
August 1992
September 1992
105 35 59 33 80 6 57 28 6 13 74 6 68 32 6 22 100 100 100 100 2 0 0 0 1.4 6 1.3 0.6 6 1.3 1.9 6 3.9 0.7 6 1.5 60 20 44 29 5 10 9 7
June 1992
September 1994 32 16 38 6 27 38 6 48 100 100 2 1 1.9 6 1.1 1.3 6 1.3 86 75 7 4
July 1994
Median and mean 6 SD numbers of I. ricinus larvae and nymphs infesting C. glareolus weighing .19 g and the proportion of infested hosts at Bogesund during June–September 1991–1992 and July and September 1994
TABLE 1
758 ¨ L. TALLEKLINT AND T.G.T. JAENSON
INFESTATION OF MAMMALS BY I. RICINUS
759
infesting bank voles weighing .19 g and similar proportions of voles infested, i.e. July and August 1991, June and August 1992 and July and September 1994. The differences in the proportion of hosts infested by I. ricinus larvae or nymphs were examined by the x2 test. Correlations between the body weight of female or male bank voles and the number of I. ricinus ticks on the voles and the numbers of different tick stages on individual hosts were examined by Spearman rank correlation. The mean weights of larvae engorged on voles or mice in July or September 1994 were calculated as the means weighted for the number of larvae infesting individual rodents (Sokal and Rohlf, 1981). The differences between mice and voles in the mean weight of engorged larvae or nymphs (log-transformed) or the mean area of the scutum of the nymphs resulting from engorged larvae (logtransformed) were examined by the t-test. The differences in the proportion of engorged larvae weighing .300 mg and the rate of moulting from engorged larvae to hungry nymphs were examined by the x2 test. The dispersion of ticks within a host population can, following Kitron et al. (1991), be expressed as mean crowding and patchiness, where mean crowding (mc), i.e. the mean number of other ticks per tick on its host, is calculated as mc 5 mean density (md) 1 [(variance/mean density) 2 1] and patchiness is calculated as the mean crowding divided by the mean density. When the distribution of ticks on hosts is random, mean crowding 5 mean density and patchiness 5 1. When ticks are aggregated on hosts, mean crowding . mean density and patchiness .1. Moreover, the basic unit of tick infestation can be measured as the intercept (a) in a simple regression of mean crowding on mean density (mc 5 a 1 bmd); a 5 0 when hosts are infested by a single tick at a time and a , 0 when hosts are infested by more than 1 tick at a time (Kitron et al., 1991).
RESULTS
Yearly and seasonal variations in I. ricinus infestation on bank voles At Bogesund, there were differences between years in the number of I. ricinus larvae infesting bank voles weighing .19 g; the monthly median infestations during June–September ranged from 19–38 in 1991 to 33–105 in 1992 (Table 1). For nymphs, both the median infestation and proportion of hosts infested were similar in 1991 and 1992. The seasonal patterns of infestation by I. ricinus larvae and nymphs on bank voles weighing .19 g were unimodal in 1991, with peaks in June–July and bimodal in 1992, with peaks in June and August (Table 1).
Impact of host species, host sex and host age on the infestation of rodents by I. ricinus At Bogesund, Apodemus mice weighing .19 g harboured greater numbers of I. ricinus ticks than bank voles weighing .19 g, both for larvae (medians of 73.5 and
760
¨ L. TALLEKLINT AND T.G.T. JAENSON
33, respectively; U12, 39 5 88.5 and p 5 0.001) and nymphs (medians of 2.5 and 1, respectively; U22, 49 5 377 and p 5 0.04). All of the individual hosts examined were infested by larvae, whereas the proportion infested by nymphs tended to be higher for Apodemus mice (73% and n 5 22) than for bank voles (59% and n 5 49) (p 5 0.27). For bank voles weighing .19 g, males harboured greater numbers of I. ricinus larvae than females (medians of 39 and 24, respectively; U18, 19 5 104.5 and p 5 0.04), whereas the infestation by nymphs was similar for both sexes (medians of 1 in both cases; U20, 26 5 238 and p 5 0.63). All of the individual hosts examined were infested by larvae and the proportion infested by nymphs was similar for males (58% and n 5 20) and females (55% and n 5 26). Young voles weighing 10–19 g tended to be infested by lower numbers of I. ricinus larvae than female or male voles weighing .19 g (median numbers of 20, 24 and 39 larvae, respectively) but the differences between the juveniles and females or males were not significant (U9, 19 5 70.5 and p 5 0.46 and U9, 18 5 44.5 and p 5 0.06, respectively). In contrast, young voles were infested by lower numbers of I. ricinus nymphs than females and males (medians of 0 and 1, respectively; U5, 46 5 50 and p 5 0.04). All of the individual hosts examined were infested by larvae, whereas the proportion infested by nymphs was higher for males and females (57% and n 5 46) than for young ones (0% and n 5 6) (p 5 0.009). There were no correlations between the body weight of female or male bank voles weighing .19 g and the numbers of I. ricinus ticks on the voles, for either the larvae (rs 520.09, p 5 0.69 and n 5 19 and rs 520.35, p 5 0.15 and n 5 18, respectively) or the nymphs (rs 520.02, p 5 0.92 and n 5 26 and rs 5 0.33, p 5 0.15 and n 5 20, respectively). Weight and moulting success of I. ricinus ticks engorged on bank voles and Apodemus mice The mean weights of the engorged I. ricinus larvae detaching from Apodemus mice were greater than for the larvae detaching from bank voles, both in July 1994 (467 and 417 mg, respectively; t 524.03, p , 0.0001 and df. 5 126) and September 1994 (523 and 492 mg, respectively; t 523.94, p , 0.0001 and df. 5 251) (Table 2). Similarly, the mean weight of engorged I. ricinus nymphs detaching during July and September was greater for the 21 nymphs fed on mice than for the nine nymphs fed on voles (3.71 6 0.86 and 2.66 6 0.69 mg, respectively; t 5 3.24, p 5 0.003 and df. 5 28). Moreover, the mean weight of the larvae engorged in September was greater than for those engorged in July, both for mice (523 and 467 mg, respectively; t 525.70, p , 0.0001 and df. 5 198) and voles (492 and 417 mg, respectively; t 5 6.94, p , 0.0001 and df. 5 179) (Table 2). There were no significant differences in the engorgement rate (i.e. the proportion of larvae weighing .300 mg) between the larvae engorged on mice and voles during July or September; the engorgement rates were 100% in both July and September for mice (60 and 140 larvae examined, respectively) and 94% in July
INFESTATION OF MAMMALS BY I. RICINUS
761
TABLE 2 Number of larval I. ricinus per host and the mean weight 6 SD of engorged larvae for ticks engorged on female (F) and male (M) Apodemus mice and bank voles (C. glareolus) at Bogesund, Sweden, during July and September 1994 Tick host
Month
Sex/weight (g)
Number of larvae per rodent
Mean 6 SD weight of engorged larvae (mg)
Mouse Mouse Mean 6 SD
July July July
F/12 M/32 22 6 14
160 83 122 6 54
451 6 56 490 6 60 467 6 60
35 25 60
Mouse Mouse Mouse Mouse Mouse Mouse Mouse Mean 6 SD
September September September September September September September September
F/20 F/25 F/35 M/22 M/22 M/26 –/– 25 6 5
63 89 29 65 25 35 43 50 6 23
543 6 46 516 6 72 504 6 54 527 6 59 529 6 61 525 6 64 506 6 71 523 6 73
20 20 20 20 20 20 20 140
Vole Vole Vole Mean 6 SD
July July July July
F/29 M/24 M/24 26 6 3
24 88 32 48 6 35
423 6 68 416 6 71 415 6 87 417 6 74
24 24 20 68
Vole Vole Vole Vole Mean 6 S.D.
September September September September September
F/33 F/20 M/20 –/24 24 6 6
10 12 20 110 38 6 48
487 6 51 440 6 45 484 6 61 500 6 63 492 6 62
10 12 20 71 113
Number of larvae examined
and 100% in September for voles (68 and 113 larvae examined, respectively). There was no difference in the proportion of successful moults to the nymphal stage between the larvae engorged on voles and mice in July 1994 (92% in both cases; n 5 265 and 474, respectively). However, the nymphs originating from the larvae engorged on mice were larger than those engorged on voles (mean scutal areas of 0.275 6 0.025 and 0.240 6 0.031 mm2, respectively; t 527.35, p , 0.0001 and df. 5 154). Infestation by I. ricinus ticks on individual hosts and within host populations The ranges of numbers of I. ricinus ticks (all stages) infesting individual hosts at Bogesund during 1991–1994 were 1–219 for bank vole, 4–174 for short-tailed vole (Microtus agrestis), 4–185 for wood mouse (Apodemus sylvaticus), 4–451 for yellow-necked field mouse (Apodemus flavicollis), 16–1162 for European hare, 458–1725 for varying hare and 428–2072 for roe deer. In terms of potential blood loss for individual hosts (i.e. the volume of blood taken by infesting ticks divided by the total blood volume of the host, not considering production of new blood)
¨ L. TALLEKLINT AND T.G.T. JAENSON
762
these ranges represent losses of 0.2–57% for bank vole, 1.6–35% for short-tailed vole, 1.2–65% for wood mouse, 1.0–52% for yellow-necked field mouse, 0.2–4.2% for European hare, 3.2–13% for varying hares and 0.3–9.0% for roe deer (Table 3). For varying hares at Stora Karls¨o and Gotska Sand¨on, the range of infesting ticks was 87–2374 (Jaenson and T¨alleklint, 1996), representing potential blood losses of 0.5–8.0%. Within the populations of all host species examined, the distributions of all stages of I. ricinus ticks were clumped, i.e. the mean crowding (mc) was greater than the mean density (md) and patchiness was .1 (Table 4). Thus, the frequency distributions of I. ricinus larvae, nymphs and adults on individual hosts were skewed, with most host individuals harbouring few ticks and only some individuals having many ticks. This was true for all tick stages on roe deer, European hares, varying hares and rodents (Figs 1a–d, 2a–d and 3a–c), the possible exception being nymphs on European hares (Fig. 2b). Despite harbouring greater numbers of ticks, relatively large mammals such as hares and cervids appear to be proportionately less affected than rodents by pure blood loss than (Table 3). At Bogesund there were positive correlations between the numbers of I. ricinus larvae and nymphs infesting bank vole (rs 5 0.46, p , 0.0001 and n 5 106), Apodemus spp. mice (rs 5 0.59, p , 0.0001 and n 5 50), European hare (rs 5 0.94, p , 0.0001 and n 5 23), varying hare (rs 5 0.94, p 5 0.01 and n 5 8) and roe deer (rs 5 0.40, p 5 0.02 and n 5 37). For larger mammals, there were also positive correlations between the numbers of subadult and adult I. ricinus ticks; European TABLE 3 Estimated blood loss (not considering the production of new blood) due to infestation by I. ricinus ticks of rodents, hares and cervids at Bogesund during 1991–1994a and varying hares at Stora Karls¨o and Gotska Sand¨on in 1992–1993b Host species
Number of hosts (%) with blood losses within the ranges 0–5%
6–10%
Bogesund C. glareolus M. agrestis A. sylvaticus A. flavicollis L. europaeus L. timidus C. capreolus A. alces
55 (52%) 29 (28%) 6 (29%) 7 (33%) 6 (31%) 2 (11%) 9 (31%) 6 (21%) 23 (100%) 0 4 (50%) 2 (25%) 32 (86%) 5 (14%) 7 (100%) 0
Stora Karls¨o and Gotska Sand¨on L. timidus
11 (73%)
a b
4 (27%)
11–20%
21–50%
.50%
Median blood loss (%)
13 (12%) 5 (24%) 8 (42%) 9 (31%) 0 2 (25%) 0 0
7 (7%) 3 (14%) 2 (11%) 4 (14%) 0 0 0 0
1 (1%) 0 1 (5%) 1 (3%) 0 0 0 0
5.4 9.4 12.0 9.4 0.9 5.6 2.0 0.2
0.2–56.8 1.6–35.1 1.2–65.1 1.0–52.4 0.2–4.2 3.2–13.3 0.3–9.0 0.1–0.4
0
0
2.4
0.5–8.0
0
Partly published in T¨alleklint and Jaenson (1994). Partly published in Jaenson and T¨alleklint (1996).
Range (%)
1119
Stora Karls¨o and Gotska Sand¨on L. timidus 412 2.7
2.0 1.6 1.9 2.6 3.3 1.3 2.1
p
53.0
0.9 4.1 1.2 1.8 59.0 255.0 93.0
md
b
70.0
3.3 10.0 1.8 2.9 81.0 378.0 178.0
mc
Nymphs
Partly published in T¨alleklint and Jaenson (1994). Partly published in Jaenson and Talleklint (1996). c Ratio of md (larvae) : md (nymphs) : md (adult females).
a
69 95 99 175 466 815 554
34 61 51 68 141 630 265
Bogesund C. glareolus M. agrestis A. sylvaticus A. flavicollis L. europaeus L. timidus C. capreolus
mc
md
Host
Larvae
1.3
4.0 2.4 1.5 1.6 1.4 1.5 1.9
p
6.0
0.0 0.0 0.0 0.0 2.0 13.0 30.0
md
Females
10.0
4.8 16.0 55.0
mc
1.7
2.4 1.3 1.8
p
5.0
0.0 0.0 0.0 0.0 1.8 15.0 17.0
md
Males
8.0
2.4 20.0 27.0
mc
1.6
1.4 1.3 1.6
p
7.8 : 1 : 0.1
37.8 : 1 : 0 14.9 : 1 : 0 42.5 : 1 : 0 37.8 : 1 : 0 2.4 : 1 : 0.03 2.5 : 1 : 0.05 2.8 : 1 : 0.3
L : N : F ratioc
15
106 21 19 31 23 8 37
Number of hosts examined
Mean density (md), mean crowding (mc) and patchiness (p) of I. ricinus larvae, nymphs, females and males infesting rodents, hares and roe deer at Bogesund during 1991–1994a and varying hares at Stora Karls¨o and Gotska Sand¨on in 1992–1993b
TABLE 4
INFESTATION OF MAMMALS BY I. RICINUS
763
764
¨ L. TALLEKLINT AND T.G.T. JAENSON
Fig. 1. Frequency distribution of the numbers of I. ricinus larvae (a) infesting roe deer, (b) European hares, (c) varying hares and (d) rodents.
hare rs 5 0.62 (p 5 0.004 and n 5 23), varying hare rs 5 0.74 (p 5 0.049 and n 5 8), but not for roe deer rs 5 0.28 (p 5 0.10 and n 5 37). A statistically significant regression coefficient of mean crowding on mean density for I. ricinus larvae on bank voles (r 2 5 0.86, p 5 0.0001 and df. 5 9), based on 10 months’ data from Bogesund during 1991–1994, resulted in an intercept (a) of 29.5, suggesting that the basic unit of larval infestation for bank voles at this locality is one single larva.
DISCUSSION
Density and seasonality of I. ricinus ticks This and other European studies show that the risk of a mammal species becoming infested by I. ricinus can vary significantly both spatially and temporally. In European studies published after 1990, the mean densities of I. ricinus larvae and nymphs infesting rodents in different areas vary from less than five to .30 larvae and from none to more than one nymphs (Doby et al., 1992; Gray et al., 1992,
INFESTATION OF MAMMALS BY I. RICINUS
765
Fig. 2. Frequency distribution of the numbers of I. ricinus nymphs infesting (a) roe deer, (b) European hares, (c) varying hares and (d) rodents.
1995; Matuschka et al., 1992, 1994; de Boer et al., 1993; Humair et al., 1993; T¨alleklint and Jaenson, 1994; Craine et al., 1995; Kurtenbach et al., 1995). Tick infestations presumably also vary on a microgeographical scale since the distribution of questing ticks within small areas is usually clumped (Mermod et al., 1973; Gigon, 1985). The number of infesting ticks can change significantly between different years in a locality; 2-fold changes in the numbers of I. ricinus larvae and nymphs on rodents have been recorded for consecutive years (Table 1; Kurtenbach et al., 1995). Tick infestation can also vary during the season of tick activity. In northern Europe, the seasonal patterns of peak infestation by I. ricinus on mammals can be unimodal, with a peak in May–July or August–September for the larvae and April–July or July–September for the nymphs or bimodal with peaks in May–June and August–September (Table 1; Mermod et al., 1973, 1974, Gray et al., 1978; Pruszynska, 1983; Gray, 1984; Steele and Randolph, 1985; Nilsson, 1988; Matuschka et al., 1990, 1991; Doby et al., 1992; Humair et al., 1993; Craine et al., 1995). The seasonal infestation pattern by adult I. ricinus can be unimodal with peaks in April–July or August–September or bimodal with peaks in April–May and August–September (Gray et al., 1978; Gray, 1984; Randolph and Steele, 1985).
766
¨ L. TALLEKLINT AND T.G.T. JAENSON
Fig. 3. Frequency distribution of the numbers of I. ricinus adults infesting (a) roe deer, (b) European hares and (c) varying hares.
Impact of host movement patterns on the infestation by I. ricinus ticks In previous European studies and in the present study, greater numbers of I. ricinus larvae and nymphs were recorded on Apodemus mice than on bank voles (Brinck et al., 1967; Nilsson and Lundqvist, 1978; Pruszynska, 1983; Matuschka et al., 1990, 1991, 1994; Doby et al., 1992; Humair et al., 1993; Kurtenbach et al., 1995). Similarly, our findings that male compared to female and adult compared to juvenile rodents generally harbour greater numbers of I. ricinus larvae and nymphs conform to previous European studies (Nilsson and Lundqvist, 1978; Brinck et al., 1984; Doby et al., 1992; Matuschka et al., 1992; de Boer et al., 1993; Craine et al., 1995). Sonenshine and Stout (1968) reported that the numbers of Dermacentor variabilis ticks infesting white-footed mice (Peromyscus leucopus) were related to the distance the mice travelled between successive recaptures. Similarly, the infestation levels recorded by us and others in Europe appear to be related to the host home range. Apodemus mice have larger home ranges than bank voles (e.g. the home ranges of males in British woodland of approximately 0.6 ha for wood mice and approximately 0.2 ha for bank voles; MacDonald and Barret, 1993). In
INFESTATION OF MAMMALS BY I. RICINUS
767
addition, male Clethrionomys, Microtus and Apodemus rodents have greater home ranges than females, in particular during the breeding season and, since the home ranges tend to increase with sexual maturity, adults range further than juveniles (e.g. Myllam¨aki, 1977; Randolph, 1977; Bondrup-Nielsen and Karlsson, 1985; Viitala and Hoffmeyer, 1985; Erlinge et al., 1990; Yl¨onen and Viitala, 1991; MacDonald and Barret, 1993). Moreover, some studies have indicated that the home range size for a given rodent species and, thus, presumably also the level of tick infestation, may vary with the density of both the same species and other rodent species competing for similar food resources; home ranges tend to be greater at low rodent densities and smaller at high rodent densities (e.g. Grant, 1972; BondrupNielsen and Karlsson, 1985; Viitala and Hoffmeyer, 1985; Erlinge et al., 1990). A positive correlation between the body size of Apodemus mice and the numbers of infesting I. ricinus (Craine et al., 1995) was not found for the numbers of larvae or nymphs infesting female or male bank voles at Bogesund. In fact, in three out of four cases the potential correlations between the host weight and number of infesting larvae or nymphs tended to be negative. Impact of host defences on the infestation by I. ricinus ticks In general, acquired resistance has been considered to be of little consequence in long-established host-tick systems since ticks should have evolved mechanisms to suppress or evade the immune response of frequently encountered hosts (reviewed by Rechav, 1992; Wikel, 1996). However, it has recently been demonstrated in laboratory studies that bank voles, but not Apodemus mice, can acquire resistance against feeding I. ricinus and I. trianguliceps. This resistance may manifest itself as a lower attachment success of the subadult ticks on voles than on mice (Nilsson and Lundqvist, 1978; Lebedeva, 1981; Matuschka et al., 1990), reduced weights of the larvae after repeated infestations on voles but not on mice (Randolph, 1979, 1994; Dizij and Kurtenbach, 1995) and a reduced moulting success of the larvae engorged on previously tick-exposed voles (compared to naive voles and Apodemus mice) (Dizij and Kurtenbach, 1995). However, it remains to be investigated to what extent voles will acquire resistance under natural conditions. Lower weights of larvae and nymphs engorged on field-caught voles than on mice have been reported (Table 2; Nilsson and Lundqvist, 1978; Matuschka et al., 1992). At Bogesund, a mean weight difference of 6–11% did not result in a lower moulting success for larvae engorged on voles, but in nymphs from larvae fed on mice having an, on average, 13% larger scutum than those fed on voles. These data from Bogesund, with the infestation levels of I. ricinus ticks on rodents being among the highest recorded in Europe, indicate that acquired resistance in these host–parasite systems may be a relatively unimportant phenomenon in nature. There are several possible explanations as to why acquired resistance could be present in some bank vole populations but absent from others. For instance, selection for acquired resistance in voles is probably weak – or has been so until recently – in areas where the tick-free period of the year is approximately the length of or exceeds the mean lifespan of the voles as well as in areas where the numbers of I. ricinus ticks infesting voles have only increased
768
¨ L. TALLEKLINT AND T.G.T. JAENSON
strongly during the last few decades. The fact that, at any given time, most individual voles carry few I. ricinus ticks and only a few voles carry heavy tick loads should also contribute to a weak selection pressure for acquired resistance. Thus, strong selection for acquired resistance against feeding I. ricinus ticks is likely to occur in vole populations in areas where ticks have been abundant for a long time, where they are active for most of the year and where the reproducing host population is small and isolated. Other tick species, such as I. trianguliceps or even other ectoparasites may contribute to the selection for acquired resistance that would reduce the feeding success of I. ricinus.
Tick infestation of individual hosts and host populations At any given time during the season of tick activity, there are great differences in the numbers of I. ricinus ticks infesting individual mammals of a particular species. These differences are reinforced by the fact that the numbers of larvae, nymphs and adults on individual hosts are usually positively correlated (as shown by the data from Bogesund in the Results section; Craine et al., 1995). It is evident from this study that, in general, individual hares and cervids do not suffer extensive blood losses due to I. ricinus infestation, despite infestation levels of .2000 ticks on some individual hosts. In contrast, some individual rodents were estimated to suffer blood losses of .50% of their total blood volume (not considering the production of new blood) over a 2–3 day period due to I. ricinus infestation. However, it remains to be investigated what effects such a blood loss and the immune response elicited against feeding ticks may have on the well-being of a rodent. Moreover, since the rodents were not marked, it is uncertain whether individuals with high tick loads harbour high numbers of ticks most of the time or if they harbour low numbers of ticks most of the time and high numbers only occasionally. In the latter case, occasional severe blood losses may not severely affect the host individual. Interestingly, the regression of mean crowding on mean density for I. ricinus larvae infesting bank voles suggests that, in accordance with a study on whitefooted mice by Kitron et al. (1991), the basic infestation unit for bank voles at Bogesund is one single tick. This is somewhat surprising, since the mean monthly number of infesting larvae is much higher for the voles at Bogesund than for the mice studied by Kitron et al. (1991), i.e. 17–80 and 0.2–7.5 larvae, respectively. If the basic infestation unit is one larva for bank voles at Bogesund, occasional infestations of .100 larvae on a particular host individual is, presumably, because such a rodent has crossed one or a few larval aggregations many times, rather than crossing a large number of different larval aggregations. The distribution of I. ricinus and I. scapularis ticks within populations of mammal hosts is aggregated, with most hosts harbouring few ticks and few hosts harbouring many ticks (Table 4 and Figs 1–3; Nilsson and Lundqvist, 1978; Kitron et al., 1991; Doby et al., 1992; Manelli et al., 1993; Brunet et al., 1995; Craine et al., 1995). Thus, based on potential blood losses and inflammatory responses to feeding ticks, it seems unlikely that infestation by these tick species should have a
INFESTATION OF MAMMALS BY I. RICINUS
769
great direct impact on the population dynamics of their mammal hosts, even if some individual hosts may succumb due to the direct effects of tick infestation. In contrast, indirect effects from tick feeding, i.e. the transmission of pathogens, could potentially have dramatic effects on host populations. ACKNOWLEDGEMENTS
We are indebted to Hans Mejlon for contributing to the data collection on tick infestation and the weights of fed ticks and to two anonymous reviewers for valuable suggestions. This study was financed by grants from the Swedish Natural Science Research Council (NFR), the Swedish International Development Cooperation Agency (Sida/SAREC) and the Royal Swedish Academy of Sciences. REFERENCES Balashov, Yu.S. 1972. [Bloodsucking ticks (Ixodoidea) – vectors of diseases of man and animals]. Misc. Publ. Entomol. Soc. Am. 8: 163–176 (English translation). Bauwens, D., Strijbosch, H. and Stumpel, A.H.P. 1983. The lizards Lacerta agilis and L. vivipara as hosts to larvae and nymphs of the tick Ixodes ricinus. Holarctic Ecol. 6: 32–40. Bolte, J.R., Hair, J.A. and Fletcher, J. 1970. White-tailed deer mortality following tissue destruction induced by lone star ticks. J. Wildl. Manage., 34: 546–552. Bondrup-Nielsen, S. and Karlsson, F. 1985. Movements and spatial patterns in populations of Clethrionomys species: a review. Ann. Zool. Fenn. 22: 385–392. Brinck, P., Johnels, A., Lundholm, B., von Zeipel, G. and Zetterberg, B. 1967. Small mammals as hosts of tick-borne encephalitis virus and vagrant ectoparasites. Oikos 18: 124–134. Brinck, P., Brinck-Lindroth, G., Edler, A., Lundqvist, L. and Nilsson, A. 1984. Ectoparasites (Insecta: Anoplura and Siphonaptera. Acari: Mesostigmata, Ixodoidea) on small mammals in Draved forest, Denmark. Entomol. Medd. 51: 103–11. Brunet, L.R., Sellitto, C., Spielman, A. and Telford, S.R., III 1995. Antibody response of the mouse reservoir of Borrelia burgdorferi in nature. Infect. Immunol. 63: 3030–3036. Bull, C.M. and Burzacott, D. 1993. The impact of tick load on the fitness of their lizard hosts. Oecologia 96: 415–419. Craine, N.G., Randolph, S.E. and Nuttall, P.A. 1995. Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochete, in a British woodland. Folia Parasitol. 42: 73–80. de Boer, R., Hovius, K.E., Nohlmans, M.K.E. and Gray, J.S. 1993. The woodmouse (Apodemus sylvaticus) as a reservoir of tick-transmitted spirochetes (Borrelia burgdorferi) in The Netherlands. Zentralbl. Bakteriol. Mikrobiol. Hyg. Ser. A279: 404–416. Dizij, A. and Kurtenbach, K. 1995. Clethrionomys glareolus, but not Apodemus flavicollis, acquires resistance to Ixodes ricinus L., the main European vector of Borrelia burgdorferi. Parasite Immunol. 17: 177–183. Doby, J.M., Bigaignon, G. and Degeilh, B. 1992. Importance potentielle compar´ee du mulot gris (Apodemus sylvaticus) et du campagnol roussˆatre (Clethrionomys glareolus) dans l’ e´ pid´emiologie de la borr´eliose de Lyme en mileu forestier dans l’ouest de la France, au travers de la relation rongeuers – Ixodes ricinus. Bull. Soc. Franç. Parasitol. 10: 271–293. Erlinge, S., Hoogenboom, I., Agrell, J., Nelson, J. and Sandell, M. 1990. Density-related homerange size and overlap in adult field voles (Microtus agrestis) in southern Sweden. J. Mammal. 71: 597–603.
770
¨ L. TALLEKLINT AND T.G.T. JAENSON
Gemmell, R.T., Cepon, G., Green, P.E. and Stewart, N.P. 1991. Some effects of tick infestation on juvenile northern brown bandicoot (Isodon macrourus). J. Wildl. Dis. 27: 269–275. Gigon, F. 1985. Biologie d’Ixodes ricinus L. sur le Plateau Suisse – une contribution a` l’ e´ cologie de ce vecteur. Th`ese pr´esent´ee a` la Facult´e des Sciences de l’Universit´e de Neuchˆatel. Gray, J.S. 1984. Studies on the dynamics of active populations of the sheep tick, Ixodes ricinus L., in Co. Wicklow, Ireland. Acarologia 25: 167–178. Gray, J.S., Turley, T. and Strickland, K.L. 1978. Studies on the ecology of sheep tick, Ixodes ricinus, in Co. Wicklow, Ireland. Irish Vet. J. February: 25–34. Gray, J.S., Kahl, O., Janetzki, C. and Stein, J. 1992. Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. J. Med. Entomol. 29: 915–920. Gray, J.S., Kahl, O., Janetzki, C., Stein, J. and Guy, E. 1995. The spatial distribution of Borrelia burgdorferi-infected Ixodes ricinus in the Connemara region of County Galway, Ireland. Exp. Appl. Acarol. 19: 163–172. Hair, J.A., Hoch, A.L., Buckner, R.G. and Baker, R.W. 1992. Fawn hematology and survival following tick infestation and theileriasis. J. Agricult. Entomol. 9: 301–319. Humair, P.F., Turrian, N., Aeschlimann, A. and Gern, L. 1993. Borrelia burgdorferi in a focus of Lyme borreliosis: epizootiologic contribution of small mammals. Folia Parasitol. 40: 65–70. Jaenson, T.G.T. and T¨alleklint, L. 1996. Lyme borreliosis spirochetes in Ixodes ricinus (Acari: Ixodidae) and the varying hare on isolated islands in the Baltic Sea. J. Med. Entomol. 33: 339–343. Jaenson, T.G.T., T¨alleklint, L., Lundqvist, L., Olsen, B., Chirico, J. and Mejlon, H.A. 1994. Geographical distribution, host associations and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden. J. Med. Entomol. 31: 240–256. Kaufman, W.R. 1989. Tick–Host interaction: a synthesis of current concepts. Parasitol. Today 5: 47–56. Keith, L.B. and Cary, J.R. 1990. Interaction of the tick (Haemaphysalis leporispalustris) with a cyclic snowshoe hare (Lepus americanus) population. J. Wildl. Dis. 26: 427–434. Kitron, U., Jones, C.J. and Bouseman, J.K. 1991. Spatial and temporal dispersion of immature Ixodes dammini on Peromyscus leucopus in northwestern Illinois. J. Parasitol. 77: 945–949. Kurtenbach, K., Kampen, H., Dizij, A., Arndt, S., Seitz, H.M., Schaible, U.E. and Simon, M.M. 1995. Infestation of rodents with larval Ixodes ricinus (Acari: Ixodidae) is an important factor in the transmission cycle of Borrelia burgdorferi s.l. in German woodlands. J. Med. Entomol. 32: 807–817. Lebedeva, N.N. 1981. Differences between various species of Muridae in the feeding of larvae of ixodid ticks (Ixodidae). Parasitologia 15: 436–440. Lehmann, T. 1993. Ectoparasites: direct impact on host fitness. Parasitol. Today 9: 8–13. MacDonald, D. and Barret, P. 1993. Mammals of Britain and Europe. HarperCollins Publishers, London Manelli, A., Kitron, U., Jones, C.J. and Slajchert, T.L. 1993. Role of the eastern chipmunk as a host for immature Ixodes dammini (Acari: Ixodidae) in northwestern Illinois. J. Med. Entomol. 30: 87–93. Matuschka, F.R., Lange, R., Spielman, A., Richter, D. and Fischer, P. 1990. Subadult Ixodes ricinus (Acari: Ixodidae) on rodents in Berlin, West Germany. J. Med. Entomol. 27: 385–390. Matuschka, F.R., Fischer, P., Musgrave, K., Richter, D. and Spielman, A. 1991. Hosts on which nymphal Ixodes ricinus most abundantly feed. Am. J. Trop. Med. Hygiene 4: 100–107. Matuschka, F.R., Fischer, P., Heiler, M., Richter, D. and Spielman, A. 1992. Capacity of European animals as reservoir hosts for the Lyme disease spirochete. J. Infect. Dis. 165: 479–483.
INFESTATION OF MAMMALS BY I. RICINUS
771
Matuschka, F.R., Eiffert, H., Ohlenbusch, A. and Spielman, A. 1994. Amplifying role of edible dormice in Lyme disease transmission in central Europe. J. Infect. Dis. 170: 122–127. ´ Mermod, C., Aeschlimann, A. and Graf, J.-F. 1973. Ecologie et e´ thologie d’Ixodes ricinus Linn´e 1758 en Suisse (Acarina, Ixodoidea). Premi`ere note: fluctuations num´eriques. Acarologia 15: 197–205. ´ Mermod, C., Aeschlimann, A. and Graf, J.-F. 1974. Ecologie et e´ thologie d’Ixodes ricinus L, en Suisse. Deuxi`eme note: comparison des populations 1972 et 1973. Acarologia 16: 612–620. Myllam¨aki. A. 1977. Intraspecific competition and home range dynamics in the field vole Microtus agrestis. Oikos 29: 553–569. Nelson, W.A., Keirans, J.E., Bell, J.F. and Clifford, C.M. 1975. Host–Ectoparasite relationships. J. Med. Entomol. 12: 143–166. Nelson, W.A., Keirans, J.E., Bell, J.F. and Clifford, C.M. 1977. Interactions of ectoparasites and their hosts. J. Med. Entomol. 13: 389–428. Nilsson, A. 1988. Seasonal occurrence of Ixodes ricinus (Acari) in vegetation and on small mammals in southern Sweden. Holarctic Ecol. 11: 161–165. Nilsson, A. and Lundqvist, L. 1978. Host selection and movements of Ixodes ricinus (Acari) on small mammals. Oikos 31: 313–322. Pruszynska, I. 1983. Faunistic-ecological studies on the ectoparasites of the small mammals caught in the natural focus of tick-borne encephalitis in the region of Gdansk. Bull. Inst. Mar. Trop. Med. Gdynia 39: 91–107. Randolph, S.E. 1977. Changing spatial relationships in a population of Apodemus sylvaticus with the onset of breeding. J. Animal Ecol. 46: 653–676. Randolph, S.E. 1979. Population regulation in ticks: the role of acquired resistance in natural and unnatural hosts. Parasitology 79: 141–156. Randolph, S.E. 1994. Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti. Parasitology 108: 413–419. Randolph, S.E. and Steele, G.M. 1985. An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari: Ixodidae). II. The dynamics of the tick–host interaction. Bull. Entomol. Res. 75: 501–518. Rechav, Y. 1992. Naturally acquired resistance to ticks – a global view. Insect Sci. Appl. 13: 495–504. Schmidt-Nielsen, K. 1975. Animal Physiology. Cambridge University Press, Cambridge. Sokal, R.R. and Rohlf, F.J. 1981. Biometry. W. H. Freeman and Company, New York. Sonenshine, D.E. 1993. Biology of Ticks, Vol. 2. Oxford University Press, Oxford. Sonenshine, D.E. and Stout, J. 1968. Tick burdens in relation to spacing and range of hosts in Dermacentor variabilis. J. Med. Entomol. 5: 49–52. Steele, G.M. and Randolph, S.E. 1985. An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari: Ixodidae). I. A unimodal seasonal activity pattern. Bull. Entomol. Res. 75: 489–499. T¨alleklint, L. and Jaenson, T.G.T. 1994. Transmission of Borrelia burgdorferi. s. l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. J. Med. Entomol. 31: 880–886. T¨alleklint, L. and Jaenson, T.G.T. 1996. Seasonal variations in density of questing Ixodes ricinus (Acari: Ixodidae) nymphs and prevalence of infection with B. burgdorferi s.l. in southcentral Sweden. J. Med. Entomol. 33: 592–597. Viitala, J. and Hoffmeyer, I. 1985. Social organization in Clethrionomys compared with Microtus and Apodemus: social odours, chemistry and biological effects. Ann. Zool. Fenn. 22: 359–371. Wikel, S.K. 1996. Host immunity to ticks. Ann. Rev. Entomol. 41: 1–22. Yl¨onen, H. and Viitala, J. 1991. Social overwintering and food distribution in the bank vole Clethrionomys glareolus. Holarctic Ecol. 14: 131–137.