Ticks and Tick-borne Diseases 5 (2014) 69–74

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Original article

The patterns of seasonal activity of Ixodes vespertilionis (Acari: Ixodidae) on Rhinolophus hipposideros in nursery colonies Krzysztof Piksa ∗ , Andrzej Górz, Magdalena Nowak-Chmura, Krzysztof Siuda Department of Invertebrate Zoology and Parasitology, Institute of Biology, Pedagogical University of Cracow, Poland

a r t i c l e

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Article history: Received 4 February 2013 Received in revised form 14 August 2013 Accepted 28 August 2013 Available online 16 November 2013 Keywords: Ixodes vespertilionis Rhinolophus hipposideros Ixodidae Seasonal abundance Population Seasonality

a b s t r a c t The aim of this study was to describe the dynamics of the long-legged bat tick Ixodes vespertilionis infestation on the lesser horseshoe bat Rhinolophus hipposideros in 2 nursery colonies roosting in attics. Out of a total of 810 lesser horseshoe bats examined, 217 (26.8%) were found to be infested with a total of 464 I. vespertilionis individuals. The developmental stage most frequently found was the larva, followed by the nymph, and the adult female. Bats were significantly more frequently infested with I. vespertilionis ticks in the period April to May than in other months. In these months, all tick developmental stages were observed. During summer and autumn, only immature developmental stages were recorded, whilst in September and October larvae predominated. Considerable differences in tick load between nursery colonies were observed. The length of seasonal presence on bats, prevalence, and infestation intensity of I. vespertilionis on lesser horseshoe bats were higher in the nursery colony situated in close vicinity of a cave than in the colony situated far from the caves. The results suggest that the pattern of seasonal infestation of ticks on bats roosting in nursery colonies coincides with the seasonal activity of Rh. hipposideros in the caves. The first case of mixed infestation of the lesser horseshoe bat with I. vespertilionis and I. ricinus were also recorded. © 2013 Elsevier GmbH. All rights reserved.

Introduction Ticks (Acari: Ixodida) are obligate haematophagous arthropods that parasitize on domestic, farm and wild vertebrates worldwide (Sonenshine et al., 2002; Kolonin, 2007, 2008). Bats are among the wide range of wildlife hosting ticks. One of the tick species parasitizing these mammals is the long-legged bat tick, Ixodes (Eschatocephalus) vespertilionis Koch. It is an oligoxenous parasite of bats from the Hipposideridae, Rhinolophidae, and Vespertilionidae families (Arthur, 1956; Hoogstraal, 1956; Filippova, 1977; Kolonin, 1981; Walter and Kock, 1985; Bush and Robbins, 2012). Humans can also act as accidental hosts (Piksa et al., 2013b). This tick is a typical cave-dwelling species and occurs also in similar environments such as mines and cellars (Nuttall et al., 1911; Arthur, ˇ cík et al., 2010). 1956; Beaucournu, 1967; Siuda et al., 2009; Sevˇ Outside the caves and cave-like shelters, the tick can be found only attached to its hosts (Arthur, 1956; Hoogstraal, 1956; Beaucournu, 1967; Siuda, 1993). In temperate zones, bats use caves mainly as winter quarters, and they are usually attacked during the hibernation period when they are roosting (Arthur, 1956; Beaucournu, 1967). Only the immature stages of the tick and females parasitize

∗ Corresponding author at: Podbrzezie 3, 31-054 Kraków, Poland. Tel.: +48 12 6626702; fax: +48 12 6626682. E-mail addresses: [email protected], [email protected] (K. Piksa). 1877-959X/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ttbdis.2013.08.006

on hosts, as the males do not feed (Arthur, 1956; Hoogstraal, 1956; Siuda, 1993). In Central Europe, the lesser horseshoe bat Rhinolophus hipposideros (Borkhausen), which is a cave-dwelling species, is the most common host for I. vespertilionis (Arthur, 1956; Siuda et al., ˇ cík et al., 2010). In the moderate climate zone, it uses 2009; Sevˇ 2 principal types of shelters: (i) Caves, which are used almost throughout the whole year, are sites for overwintering and swarming, or – occasionally – as day, night, or transient quarters (Gaisler, 1963a, 1963b; Roer and Schober, 2001; Kokurewicz et al., 2008; Knight and Jones, 2009; Piksa et al., 2011b), and (ii) summer quarters, which are used by bats outside the hibernation season (April to October). One of the latter types includes the shelters where so-called nursery colonies congregate. In spring, pregnant females arrive at these shelters in groups ranging up to several hundreds and form the nursery colonies (Gaisler, 1963b; McAney and Fairley, 1988). The females stay in the shelters until September to October, where they deliver and raise their young, and where the young bats learn to become self-reliant. In Poland, these sites are mainly attics, as a rule, in sacred buildings, because they are spacious, have not been modified for long periods, and are relatively safe (Harmata, 1962; Szkudlarek et al., 2008). The foraging activity of females and their offspring is mainly in the vicinity of the nursery colony up to a maximum distance of 4.2 km (Bontadina et al., 2002; Kokurewicz et al., 2008). In this area, bats also use a variety of man-made structures and caves as night shelters (McAney

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K. Piksa et al. / Ticks and Tick-borne Diseases 5 (2014) 69–74

and Fairley, 1988; Roer and Schober, 2001; Kokurewicz et al., 2008; Knight and Jones, 2009). Caves and attics, the 2 basic types of shelter used by bats, offer disparate conditions. The caves are habitats with stable microclimatic conditions within which I. vespertilionis may live throughout the year (Beaucournu, 1967) whereas the attics of sacred buildings represent an extremely hostile environment where free-living ticks of this species cannot survive. The daily average temperature in the summer can often exceed 30 ◦ C (Reiter, 2004), sometimes reaching 40 ◦ C during the day (Harmata, 1962), and air relative humidity can fall below 60%. Such parameters markedly exceed the range of boundary values tolerated by this tick species (Beaucournu, 1967). The aim of this study was to check whether these ticks are present in lesser horseshoe bat nursery colonies situated in attics, and if so, for how long and if there are any differences in their seasonal activity between nursery colonies situated in the immediate vicinity of caves (living habitat of I. vespertilionis) and the colonies situated far from caves. Taking into account the aforementioned facts concerning this tick and its host, 2 scenarios can be envisaged. Firstly, the elimination of ticks in a relatively short time can be expected among bats occupying the summer quarters far from caves, after they arrive at the nursery colonies. In the second scenario, a longer residence by ticks can be expected, perhaps even for the entire time the nursery colony remains in an attic situated in the close vicinity of the cave – the main habitat of I. vespertilionis. Materials and methods Survey sites Two nursery colonies of the lesser horseshoe bat, which differed from each other in terms of localization between colonies and caves, with I. vespertilionis occurring were selected for field research. Bats and their ticks were surveyed at the following sites: (i) The church in Bukowiec (49◦ 44 57 N, 20◦ 51 01 E) located in ˙ foothills. It is a small wooden church located the Roznowskie on the hill. The attic of this church provides shelter for a nursery colony of Rh. hipposideros numbering ca. 100 adult bats. The church is situated in close vicinity (ca. 0.8 km) of the great hibernaculum of the lesser horseshoe bat known as the Diabla Dziura cave, which houses up to 130 individuals. The cave also provides shelter for a large population of I. vespertilionis (Piksa et al., 2013a). (ii) The Cistercian Abbey in Szczyrzyc (49◦ 47 03 N, 20◦ 11 17 E) is located in the Beskid Wyspowy Mountains. The attics of the monastery and other buildings comprising this abbey provide shelter for maternity colonies of Rh. hipposideros and Myotis emarginatus, comprising a maximum of 230 and approximately 200 adult bats, respectively. There are no caves in the vicinity of the monastery within a radius of 11 km. The Zbójecka Cave in Łopien´ is the nearest site where a large population of I. vespertilionis has been observed (Piksa et al., 2013a). Both of these sites are situated in southern Poland in the Carpathians (Fig. 1).

54 N

N

Poland Cistercian Abbey in Szczyrzyc Zbójecka Cave in Łopień

Diabla Dziura Cave Church in Bukowiec

50 N

16 E

20 E

50 km Fig. 1. Map showing the study sites located in southern Poland.

week of April), when the colonies were fully formed (last week of May), after the young bats were raised (mid-July), in the second week of August (during a period of intensive feeding), in September and October (period of successive dispersion of nursery colonies). From June until mid-July, the studies were suspended (this covered the period of advanced pregnancy, delivery, and the first phase of nursing the young bats). In order to minimize the disturbance to bats, the number of visits in the attics of the church and abbey was limited to one a month or in some cases once every 2 months. During the surveys, bats were taken by hand from the roof or caught using a hand net and identified to species and sex. In searching for any ticks parasitizing on the host bat, its whole body was carefully examined, and any ticks found were removed using forceps before being placed in identifiable tubes with 70% ethyl alcohol. Fieldwork was carried out under licenses issued by the Ministry of Environment and General Directorate for Environmental Protection. Statistical analysis Sterne’s exact 95% confidence intervals (CI) and 95% bootstrap confidence intervals (with 2000 replications) were calculated for prevalences and mean intensities, respectively (Reiczigel, 2003). Chi-square test was used to check the significance of differences in the prevalence of ticks between different months and between sites. The Kruskal–Wallis test with post hoc Dunna and the Mann–Whitney U-test was also used to compare the mean intensities of ticks over time (different months) and between sites. A P value of 0.05 was considered statistically significant. Statistical analyses were performed using Quantitative Parasitology version 3.0 (Reiczigel and Rózsa, 2005) and R version 2.14 (R Development Core Team R, 2012). For the calculation of the monthly dynamic of infestation intensity, only those bats that were infested with at least one tick of a given developmental stage were considered. Results During field surveys, a total of 810 Rh. hipposideros was examined, and 464 long-legged bat ticks were found on 217 individual bats. Most frequently collected were immature stages; adult female ticks were found in much small numbers (Table 1). The church in Bukowiec

Tick and bat surveys Ticks were collected from lesser horseshoe bats roosting in their nursery colonies (attics of a church and abbey). The studies were conducted from April to October, i.e. throughout the period when bats had congregated in their nursery colonies from 2010 to 2012. Sampling was carried out when the colonies were first formed (last

Ixodes vespertilionis was detected on Rh. hipposideros throughout the whole experimental period. In total, 311 bats were examined 135 of which were infested with a total of 329 ticks (Table 1). Considerable differences in the prevalence and infestation intensity of immature stages of I. vespertilionis parasitizing on bats between different months were observed (Figs. 2a and 3a, Table 2). Females

K. Piksa et al. / Ticks and Tick-borne Diseases 5 (2014) 69–74 Table 1 Number, prevalence, and intensity of infestation of Ixodes vespertilionis parasitizing on Rhinolophus hipposideros recorded in nursery colonies (in brackets the number of examined bats). Prevalence (%)

Intensity (mean)

Cistercian Abbey in Szczyrzyc (499) Larvae 49 68 Nymphs 18 Females 135 All stages

Abundance (n)

8.8 9.8 3.0 16.4

1.1 1.4 1.2 1.7

Church in Bukowiec (311) Larvae 176 Nymphs 129 24 Females 329 All stages

31.5 20.6 6.1 43.4

1.8 2.0 1.3 2.4

1 0 Apr 4

May

Jun

Jul

Aug

Sep

Oct

May

Jun

Jul Month

Aug

Sep

Oct

3b

3 2

2a

larvae nymph female

0.6

1 0

0.4

Proportion of bats infested

larvae nymph female

2

0.8

Apr

0.2

Fig. 3. Monthly infestation intensity (mean intensity) of larvae, nymphs, and females of Ixodes vespertilionis on Rhinolophus hipposideros in the church in Bukowiec (3a) and the Cistercian Abbey in Szczyrzyc (3b) (with 95% confidence intervals). In June, controls were omitted (asterisk mark).

0.0 Apr

May

Jun

Jul

Aug

Sep

Oct

0.8

and May; thereafter, their prevalence rapidly decreased (Fig. 2a). The highest intensity of infestation was recorded in April and the lowest in July and August (Fig. 3a). In September and October, the frequency of immature stages (particularly larvae) on bats clearly increased (Fig. 2a), although the increase in intensity of infestation was not so obvious (Fig. 3a). Over 31% of the infested lesser horseshoe bats were infested with different developmental stages of ticks at the same time, and one mixed species infestation was found: one nymph and one larva of I. vespertilionis and a partially engorged I. ricinus female.

2b 0.6

0.4

0.2

0.0 Apr

May

Jun

Jul Month

Aug

Sep

Oct

Cistercian Abbey in Szczyrzyc

Fig. 2. Monthly infestation rates (prevalence) of larvae, nymphs, and females of Ixodes vespertilionis on Rhinolophus hipposideros in the church in Bukowiec (2a) and the Cistercian Abbey in Szczyrzyc (2b) (with 95% confidence intervals). In June, controls were omitted (asterisk mark).

occurred on bats only during spring, and their prevalence and infestation intensity were low (Figs. 2a and 3a, Table 1). Larvae and nymphs infested bats significantly more frequently during April

Table 2 Summary of the chi-square test and Kruskal–Wallis test comparing the prevalence and infestation intensity of particular developmental stages of Ixodes vespertilionis parasitizing on Rhinolophus hipposideros in different months. Tick stage

3a

3

Mean intensity

Tick stage

4

71

Prevalence 2 value

Infestation intensity (df)

P value

H value

P value

Church in Bukowiec 33.83 Larvae 58.19 Nymphs 1.72 Females 76.28 All stages

5 5 1 5

The patterns of seasonal activity of Ixodes vespertilionis (Acari: Ixodidae) on Rhinolophus hipposideros in nursery colonies.

The aim of this study was to describe the dynamics of the long-legged bat tick Ixodes vespertilionis infestation on the lesser horseshoe bat Rhinoloph...
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