Сезонная организация жизненного цикла иксодового клеща Dermacentor reticulatus в Центральной Европе. Роль данного клеща как переносчика возбудителей различных заболеваний Текст научной статьи по специальности « Биологические науки»

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Аннотация научной статьи по биологическим наукам, автор научной работы — Каль Олаф, Даутель Ханс

Иксодовые клещи являются важными переносчиками возбудителей различных заболеваний. Виды, живущие в северной климатической зоне, обычно характеризуются более продолжительными промежутками между кровососанием, и их жизненный цикл обычно занимает несколько лет. Наиболее важными клещами-переносчиками Центральной Европы являются Ixodes ricinus и Dermacentor reticulatus, жизненные циклы которых существенно отличаются, что имеет значение в их роли как переносчиков и для их пространственно-временного распределения. Каждая стадия жизненного цикла I. ricinus занимает длительное время. Смена стадий происходит ежесезонно, и периоды поиска хозяина и кровососания значительно перекрываются. Часто I. ricinus инфицируется от зараженного хозяина на стадии кровососущей личинки и, в свою очередь, служит переносчиком инфекции на последующих стадиях. Напротив, в случае с D. reticulatus ежесезонно сменяется лишь взрослая стадия клеща, продолжительность жизни которой составляет более года. Последовательность смены всех остальных стадий происходит всего лишь за один сезон. Поэтому сезонные температурные колебания являются важным сдерживающим фактором, и ожидается, что в будущем этот вид будет распространяться далее к северу Центральной Европы по мере потепления климата. Поскольку у D. reticulatus стадия кровососущей личинки сезонно предшествует стадии кровососущей нимфы, и нимфы никогда не питаются кровью тех же хозяев, что и незрелые особи, трансовариальный путь передачи является типичным для переносимых D. reticulatus возбудителей, таких, как Babesia canis.

SEASONAL LIFE CYCLE ORGANISATION OF THE IXODID TICK DERMACENTOR RETICULATUS IN CETNTRAL EUROPE IMPLICATIONS ON ITS VECTOR ROLE AND DISTRIBUTION

Ixodid ticks are important vectors disease. Species living in the northern temperate climate zone usually have extended offhost periods between their blood meals, and they usually need several years to complete their life cycle . The most important vector ticks in central Europe , Ixodes ricinus and Dermacentor reticulatus, distinctly vary in their seasonal life cycle organisation, which might be relevant for their individual vector roles and for their future distribution . Each life stage of I. ricinus is long-lived and occurs in every season with a large seasonal overlap in host-seeking and feeding. So it is common that I. ricinus becomes infected as a feeding larva on an infectious host and in turn passes on its infection to a host as a feeding nymph or adult. In contrast, in D. reticulatus, only the adult stage occurs in every season and may live for more than a year. The sequence from the egg stage to the resultant unfed adult has to be gone through within only one growing season. As a result, temperature during the growing season is an important limiting factor, so it is expected that this species will continue to expand its range further to the north in central Europe with a warmer climate in the future. Because, as a rule, the larval blood meal seasonally precedes the nymphal blood meal in D. reticulatus and feeding adults never use the same hosts as feeding immatures, transovarial transmission is a typical characteristic of D. reticulatus-borne agents, e.g. in Babesia canis.

Текст научной работы на тему «Сезонная организация жизненного цикла иксодового клеща Dermacentor reticulatus в Центральной Европе. Роль данного клеща как переносчика возбудителей различных заболеваний»

Kahl O., Dautel H.

tick-radar GmbH, Berlin

SEASONAL LIFE CYCLE ORGANISATION OF THE IXODID TICK DERMACENTOR RETICULATUS IN CETNTRAL EUROPE IMPLICATIONS ON ITS VECTOR ROLE AND DISTRIBUTION

Ixodid ticks are important vectors disease. Species living in the northern temperate climate zone usually have extended off-host periods between their blood meals, and they usually need several years to complete their life cycle. The most important vector ticks in central Europe, Ixodes ricinus and Dermacentor reticulatus, distinctly vary in their seasonal life cycle organisation, which might be relevant for their individual vector roles and for their future distribution.

Each life stage of I. ricinus is long-lived and occurs in every season with a large seasonal overlap in host-seeking and feeding. So it is common that I. ricinus becomes infected as a feeding larva on an infectious host and in turn passes on its infection to a host as a feeding nymph or adult. In contrast, in D. reticulatus, only the adult stage occurs in every season and may live for more than a year. The sequence from the egg stage to the resultant unfed adult has to be gone through within only one growing season. As a result, temperature during the growing season is an important limiting factor, so it is expected that this species will continue to expand its range further to the north in central Europe with a warmer climate in the future. Because, as a rule, the larval blood meal seasonally precedes the nymphal blood meal in D. reticulatus and feeding adults never use the same hosts as feeding immatures, transovarial transmission is a typical characteristic of D. reticulatus-borne agents, e.g. in Babesia canis.

Key words: Ixodes ricinus; Dermacentor reticulates; seasonal activity; life cycle; vector role; distribution; central Europe.

Каль О., Даутель Х.

tick-radar GmbH, Берлин

СЕЗОННАЯ ОРГАНИЗАЦИЯ ЖИЗНЕННОГО ЦИКЛА ИКСОДОВОГО КЛЕЩА

DERMACENTOR RETICULATUS В ЦЕНТРАЛЬНОЙ ЕВРОПЕ. РОЛЬ ДАННОГО КЛЕЩА

КАК ПЕРЕНОСЧИКА ВОЗБУДИТЕЛЕЙ РАЗЛИЧНЫХ ЗАБОЛЕВАНИЙ

Каждая стадия жизненного цикла I. ricinus занимает длительное время. Смена стадий происходит ежесезонно, и периоды поиска хозяина и кровососания значительно перекрываются. Часто I. ricinus инфицируется от зараженного хозяина на стадии кровососущей личинки и, в свою очередь, служит переносчиком инфекции на последующих стадиях. Напротив, в случае с D. reticulatus ежесезонно сменяется лишь взрослая стадия клеща, продолжительность жизни которой составляет более года. Последовательность смены всех остальных стадий происходит всего лишь за один сезон. Поэтому сезонные температурные колебания являются важным сдерживающим фактором, и ожидается, что в будущем этот вид будет распространяться далее к северу Центральной Европы по мере потепления климата. Поскольку у D. reticulatus стадия кровососущей личинки сезонно предшествует стадии кровососущей нимфы, и нимфы никогда не питаются кровью тех же хозяев, что и незрелые особи, трансовариальный путь передачи является типичным для переносимых D. reticulatus возбудителей, таких, как Babesia canis.

Ключевые слова: Ixodes ricinus; Dermacentor reticulates; сезонная активность; жизненный цикл;

переносчик возбудителей; распространенность; Центральная Европа.

Ticks are obligate blood-feeding arthropods of terrestrial vertebrates worldwide and as such transmit a large variety of pathogens of veterinary and medical significance [1]. In ixodid ticks (family Ixodidae), the egg stage is followed by 3 parasitic life stages, and it is not least the fact that each of them takes a huge blood meal in relation to their unfed body mass, over several days, that make them excellent vectors.

Ticks living in temperate climates often experience extended off-host periods between the blood meals

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during which the tick digests the taken blood, it then sooner or later moults to the next life stage (or in case of the adult female it oviposits) and becomes eventually again an unfed, host-seeking tick. There must be at least one life stage that is capable of overwintering. Thus, ticks have to cope with changing external conditions (weather, microclimate) for most of their lives. This includes hot, and sometimes dry, summers and cold winters. As a consequence, the tick life cycle, with its different stages, phases, and developmental events, needs to be seasonally synchronised in some manner with the seasons. Although Ixodes ricinus and Dermacentor reticulatus, the two most important vector tick species in central Europe, live in the same geographic area, the seasonal aspects of their life cycles differ distinctly.

This paper (i) briefly describes the organisation of the life cycle of D. reticulatus in central Europe in

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comparison to that of I. ricinus, (ii) outlines some implications of life cycle seasonality on vector efficiency, and (iii) points out how future conditions with higher average temperatures during the growing season may affect the distribution of D. reticulatus in central Europe.

ECOLOGY OF D. RETJCULATUS AND J. RJCJNUS

In central Europe, I. ricinus, the castor bean tick, is essentially a forest tick, but it often occurs also in high numbers at the borders of forests and forest meadows (ecotones), on fallow land, in parks, and in gardens wherever the abiotic conditions meet its physiological requirements (table 1). Also, suitable hosts must be available. Especially the larval and the nymphal stages are catholic feeders, and the spectrum of terrestrial vertebrate species which are parasitized by them is large [5]. They include reptiles, birds, and smaller as well as larger species of mammals. In contrast, the adult female stage feeds only on medium-sized and large mammals, with the hedgehog probably the smallest animal on which adult I. ricinus can regularly be found. The males rarely attach and never take a large blood meal. So availability of suitable hosts is usually not a problem for I. ricinus im-matures, but can be for the adults in some locations.

There is convincing evidence from several recent studies that D. reticulatus, the meadow tick (a former synonym is Dermacen-tor pictus), has considerably enlarged its distribution area in Germany over the past 20 years [6].

This tick is the vector of Babesia canis, a protozoan intraerythroc-ytic parasite of dogs causing severe disease, and also of some other tick-borne pathogens. The apparent spread of canine babesiosis in Europe also indicates the changing range of D. reticulatus.

D. reticulatus is not a typical wood inhabitant, but prefers more open and sun-exposed areas like mixed landscapes with trees and bushes (forest steppes) and lowland forests, fallow land, also meadows. It occurs from France in the west through the middle parts

of Europe to Siberia in the east [7]. Whereas all pos-tembryonic stages of I. ricinus exhibit exophilic behaviour and quest for nearby passing hosts on exposed vantage points (e.g. at the tops of grass stems or herbal plants), D. reticulatus does so only in the adult stage. The larvae and nymphs of the latter are seemingly endophilic, inhabiting such microhabitats as rodent burrows or their entrances, and can therefore not be collected by flagging or dragging. The immature stages of D. reticulatus are found on small mammals, but the adults infest larger animals such as deer, wild boar, horses, cattle, sheep and also dogs. Human beings are rarely bitten by this tick in central Europe.

LJFE CYCLES OF J. RJCJNUS AND D. RETJCULATUS

All life stages of I. ricinus, including the egg stage, occur throughout the year. The postembryonic stages can hibernate both in the unfed and in the engorged state [8-10]. The seasonal periods of questing in the three postembryonic stages concur to a large extent, although larval activity in spring begins somewhat later than that of the nymphs and adults (table 2). In contrast to this, the egg, the larval, and the nymphal stages in D. reticulatus, they each live for only some

Some environmental factors and their significance for the occurrence of I. ricinus and D. reticulatus

Potentially critical factors I. ricinus D. reticulatus

Availability of suitable hosts In most habitats not a limiting factor for larvae and nymphs, but adults need medium-sized or large hosts

Humidity Distinctly less sensitive than Microclimatic relative I. ricinus to relative humidities humidity should not fall below r , Не можете найти то, что вам нужно? Попробуйте сервис подбора литературы.

Jnformation about authors:

KAHL Olaf, Chief executive officer, tick-radar GmbH, Berlin, Germany. E-mail: olaf.kahl@berlin.de DAUTEL Hans, Chief executive officer, tick-radar GmbH, Berlin, Germany. E-mail: dautel@insectservices.de

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Potential longevity and main seasonal activity/feeding of different life stages of the ticks D. reticulatus and I. ricinus in central Europe (in the case of the egg stage, seasonal occurrence is indicated). The egg and the larval and nymphal stages of D. reticulatus are short-lived, which correlates well with their seasonal activities. Adults of D. reticulatus, however, are long-lived and able to overwinter in the unfed, as well as in the engorged state, as are all life stages of I. ricinus including the eggs (Belozerov, 1982)

Life stage D. reticulatus I. ricinus

Egg Spring, short-lived Whole year, rather long-lived

Larva Mid-June to mid-August (mainly in July)a, short-lived May to October, long-lived

Nymph Mid-July to mid-September (mainly in August)a, short-lived March to November, long-lived

Adult February to May, August to November, long-lived March to November, long-lived

a Data from north-eastern Poland [11].

weeks, and they occur more or less consecutively during the growing season with the larva followed by the nymph.

The seasonal activity patterns of the different life stages are also relevant with respect to the vector roles of D. reticulatus and I. ricinus. It appears that it is mainly the immature stages of vector ticks that are involved in the perpetuation of tick-borne pathogens such as Borrelia burgdorferi s.l. and TBE virus in nature. The adult stage does usually not feed on reservoir host species (hedgehogs excluded), and, moreover, the number of adults is low when compared to the numbers of larvae and nymphs in a given 3-host tick species population. As a consequence, a given infection must be passed on from nymphs to larvae of the next generation to complete one infectious circle. This occurs via a reservoir host or a co-feeding transmission host [10]. Given the fact that I. ricinus larvae and nymphs are both numerous and have more or less the same host spectrum, the two life stages of this species might often feed on the same host individuals. A given infection can be passed on from nymphs to larvae by transmission via a reservoir host. A reservoir host becomes infected by a feeding nymph, subsequently the microorganism involved replicates in the reservoir host, and after a certain (sometimes rather short) period of time, this reservoir host becomes infectious, and larvae are infected when feeding on such a host. Another possibility of passing on a given infection from nymphs to larvae is by co-feeding transmission. In this case, the infection is transmitted from an infectious tick nymph to larval ticks feeding at the same time on the same host individual [11]. In both cases, infected engorged larvae give rise to infectious nymphs, and the infectious circle is completed. Depending on the microorganism involved, one or both modes of transmission may be important to keep the infectious circle going.

In the case of D. reticulatus in central Europe, there is only a small seasonal overlap between the feeding of larvae and that of nymphs [12, 13]. So even if they feed on the same host individuals, the larvae might usually be the first, a sequence that tends not to support the transmission of tick-borne pathogens from nymphs to larvae. Knowing that the immatures and the adults feed on different species of hosts and probably never meet on the same host individual, all this together suggests that D. reticulatus can only be a vector for those tick-borne pathogens that largely rely on transovarial transmission in the ticks, for example Babesia canis [14]. This also suggests that D. reticulatus, despite its proven capability of transmitting the TBE virus [15], is not able to act as the sole vector tick of the TBE virus (or other tick-borne pathogens that are not transovarially transmitted) in a given area. However, it can act as an auxiliary vector tick if its larval stage has the opportunity to feed on infectious hosts (infected by another vector) and may in turn transmit the infection to a host during the nymphal blood meal. This is a good example of how the seasonal pattern of host-seeking of different life stages of a given tick species (and also the presence of other vector tick species) may affect its ecological vector efficiency, irrespective of its physiological capability of transmitting the respective agent. The situation might be similar with D. marginatus, the only other Dermacentor species occurring in central Europe.

FUTURE DISTRIBUTIONS OF D. RETICULATUS IN GERMANY

I. ricinus currently occurs in all parts of Germany. A warmer climate in the future cannot further increase its distribution area in Germany with the exception of mountainous areas > 1000 m altitude.

The current northern boundary of distribution of D. reticulatus in Germany is not too far north of Berlin and north of Hannover [6]. In the 1990s and before, D. reticulatus was never collected by the authors of this paper in Berlin and its outskirts, and there are also no other such records from that time. This species might have reached Berlin in approximately 2000 (Dautel and Kahl, unpubl. results), and several other studies indicate that it increased its range in central Europe and also shifted its boundary of occurrence to the north in recent years [6]. This makes sense when looking at the life cycle of that tick species and its critical dependence on ambient temperature during the growing season. Whereas the adult stage of Eurasian Dermacentor species is long-lived, the egg, the larval and the nymphal stages are not. Oviposition, hatch of eggs, larval host finding and feeding, development from an engorged larva to an unfed nymph, nymphal host finding and feeding, development from

We thank Jeremy Gray (Dublin, Ireland) for critically reading a late draft of the paper.

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an engorged nymph to an unfed adult, are all highly dependent on ambient temperature and must occur within only one growing season. It is also highly questionable and still remains to be shown whether the engorged nymph or the moulting adult are able to hibernate under central European winter conditions.

It appears very probable that the microclimatic temperature sum during the growing season must be sufficiently high to allow the performance of the whole developmental chain from oviposition to the F1-generation unfed adult and that this might be a limiting factor at and beyond the northern boundary

of the D. reticulatus range. It is easy to conceive that under the conditions of increasing temperatures during the growing season, D. reticulatus may shift its northern border of occurrence further to the north, provided that suitable hosts are available. So we assume that this process is ongoing and might continue. This means that dog owners and veterinarians in northern Germany and in other areas north of the current northern boundary of the D. reticulatus range should be aware of the emerging risk of Babesia canis infections in dogs resulting from D. reticula-tus bites.

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