# Effects of Climate Change on Ticks and Tick-Borne Diseases in Europe

Authors: J. S. Gray; H. Dautel; A. Estrada-Peña; O. Kahl; E. Lindgren
Journal: Interdisciplinary Perspectives on Infectious Diseases
 (2009)

---

## Abstract

Zoonotic tick-borne diseases are an increasing health burden in Europe and there is speculation that this is partly due to climate change affecting vector biology and disease transmission. Data on the vector tickIxodes ricinus suggest that an extension of its northern and altitude range has been accompanied by an increased prevalence of tick-borne encephalitis. Climate change may also be partly responsible for the change in distribution of Dermacentor reticulatus. Increased winter activity of  I. ricinus is probably due to warmer winters and a retrospective study suggests that hotter summers will change the dynamics and pattern of seasonal activity, resulting in the bulk of the tick population becoming active in the latter part of the year. Climate suitability models predict that eight important tick species are likely to establish more northern permanent populations in a climate-warming scenario. However, the complex ecology and epidemiology of such tick-borne diseases as Lyme borreliosis and tick-borne encephalitis make it difficult to implicate climate change as the main cause of their increasing prevalence. Climate change models are required that take account of the dynamic biological processes involved in vector abundance and pathogen transmission in order to predict future tick-borne disease scenarios.


---

## Body

## 1. Introduction

Zoonotic tick-borne  diseases in
Europe have  become increasingly prominent
since the emergence of Lyme borreliosis (LB)
in the early 1980s, and the incidence of this disease and that of tick-borne
encephalitis (TBE) have risen dramatically over the last two decades [1]. Both
diseases are transmitted by hard ticks of the Ixodes ricinus species complex (I.
ricinus and I. persulcatus) and since these ticks spend most of their time in the
environment, climate change is likely to affect their distribution and
abundance and, therefore, the incidence of disease. I. ricinus and I. persulcatus are particularly sensitive to
environmental conditions since in their prolonged nonparasitic phases they
require a microclimatic relative humidity of at least 80% to avoid fatal
desiccation. They are, therefore, restricted to areas of moderate-to-high
rainfall where there is a good cover of vegetation, so that the soil surface remains humid through the driest times of
the year [2]. The Fourth Assessment Report of the Intergovernmental Panel on
Climate Change [3] reported that in northern temperate Europe temperature increases of  1.5–2.5°C may occur
over the next few decades as a result of global warming. Such climate change
may extend or curtail host-seeking tick activity periods, potentially
increasing or decreasing tick abundance and distribution, and effects on tick
development rates can change seasonal activity patterns by altering the
proportion of the tick population that are exposed to regulatory mechanisms such
as diapause. In areas where lowered summer precipitation coincides with raised
summer temperatures, the survival, activity, and distribution of I. ricinus and I.persulcatus are likely to be reduced because of their
vulnerability to desiccation. These tick species acquire their hosts by ambushing them from the vegetation and a
significant number of large animals, such as deer, must be present in the
habitat in order to feed the adult females and thus maintain the tick
populations. The more catholic host preferences of the immature tick stages
(larvae and nymphs), which parasitize reptiles, small and medium-sized mammals
and birds, in addition to large mammals, contribute significantly to the
circulation of diverse pathogens between the tick and host populations. Climate
change may, therefore, exert a major influence on both tick abundance and
disease prevalence by affecting faunal diversity [4].Other important European tick species such asRhipicephalus sanguineus and Dermacentor reticulatus can be affected
by climate change through similar mechanisms, but anthropogenic factors also
have profound effects on disease incidence, and separating these from the
influence of climate change represents a major challenge. In this review
attention is mainly focused on evidence for the effects of climate change on
the distribution and abundance of European ticks. The potential impacts of
climate-change effects on the incidences of the diseases they transmit are
discussed.


## 2. Effects of Climate Change on Tick Distribution and Abundance

### 2.1.Ixodes ricinus

The
climate is regarded as the principal restricting factor at the northern limit
ofI. ricinus distribution [5]. Although I. ricinus is surprisingly cold-hardy
and when winter-acclimatized can survive 24-hour exposure to temperatures
ranging from −14.4°C to −18.9°C [6], the
detrimental effects of cold are accumulative and exposure for 30 days to only −10°C has been
shown to be lethal for a high proportion of unfed nymphs and diapausing
engorged larvae and nymphs [6]. Molting I.
ricinus ticks are even more vulnerable so that if summer temperatures are
not high enough to complete
development before the onset of winter (little or no development takes place
between 7  and 10°C [7, 8]), they are unlikely to survive even moderate frosts.
Degree-day models have been
developed which proved useful in elucidating the I.ricinus life cycle [9, 10], but more research on the winter biology
of this species would help further understand its northern distribution limit.In Sweden, the northern distribution limit ofI. ricinus, together with that of several other animal and plant species, has
shifted northwards since the climate started to noticeably change in the late
1980s [11]. The geographical distribution range of I. ricinus used to be located below 61°N [5], but ticks are now
established along the whole Baltic Sea coastline (up to 66°N) and along the river valleys and the larger lakes in the
northern regions. This shift in latitude distribution has been shown to be
related to changes over several seasons in the number of degree-days with
temperatures vital for tick survival, activity and development [12]. At the
highest latitudes fewer days with cold winter temperatures (well below  −12°C for longer
periods) had the clearest impact for new tick establishment (Figure 1).Changes in tick distribution in northern and central Sweden.
White dots illustrate
districts in Sweden
where ticks were reported to be present before 1980 (a) and in 1994-1995 (b).
The study region is within the black line (Lindgren et al. 2000,
[12] with
permission from Environmental Health
Perspectives).
(a)(b)In central Sweden (59°N to 61°N) in areas
with medium-high densities of ticks, increases in tick abundance were
correlated to a combination of mild winters (fewer days with temperatures below
7°C) and extended spring and autumn seasons (more days with minimum
temperatures not lower than 5 to 8°C). In south and central Sweden, the current climate only allows a tick
activity season of 6–8 months compared
to as much as 11 months in some parts of the British Isles, and further changes
in seasonal climate in Sweden
are likely to continue to have a major impact on the prevalence of ticks. The
combination of climate variables affecting ticks has also been shown to be
significantly correlated with increases in the incidence of TBE in Stockholm County  (59.2°N) during the period 1960–1998 [13]. The
risks of LB are likely to increase as well because Borrelia burgdorferi sensu lato (s.l.) spirochetes have been found
in I. ricinus throughout its range in
Sweden
[14].A comparable situation has been reported in changes to the
altitude distribution ofI. ricinus in the mountainous regions of the Czech Republic. Field studies
in 1957 and in 1979-80 showed that
ticks were prevalent up to 700 meters above sea level. Ticks were collected
from dogs or by drag-sampling in the same locations in 2001 and 2002 and were
then found as high as 1100 meters in areas where they had been absent from
small mammal samples [15–17] and where it has been shown that they could
not complete their life cycle over the period 1957–1983 [18].
Furthermore, the prevalence of ticks carrying the TBE virus or B. burgdorferi s. l. spirochetes also
seems to have increased at high altitude in the Czech Republic
[16, 19].


### 2.2.Dermacentor reticulatus

Dermacentor reticulatus is a vector of
canine babesiosis, tularemia, Q-fever, and at least one zoonotic rickettsiosis
[20] and has
vector competence for Anaplasma marginale
[21]. Unlike I. ricinus, only the adults quest for hosts on surface
vegetation and they feed primarily on deer, frequently bite dogs, but only
occasionally humans, whereas the larvae and nymphs parasitize rodents. The life
cycle is much shorter than that of I. ricinus, with eggs deposited in the spring and
developing to adults within the same year [22]. The geographic range of the species extends from France and southwest England in the west to central Asia in the east. In
western and central Europe its northern limit is northern Germany, northern Poland,
and Lithuania, and its
southern limit is the
Mediterranean shore (restricted to humid mountainous areas), whereas it has a
more northern distribution in the east (St.
Petersburg). Within this area, its distribution is
highly focal, and within Germany
in 1976, it was only reported from four sites out of more than 3000 [23].In two recent studies, however, data were collected showing
that this tick species has since colonized many more sites in Germany
[19].
The first study (2003) consisted of the screening of 365 dogs from 171 sites.
Almost 10% of the ticks from 41 dogs were D.
reticulatus and the infested dogs came from 26 sites, all previously
unknown for the tick. Seven of the sites were subsequently confirmed by
flagging. In the second study (2004), 721 deer were shot at 201 sites from 161
districts and their heads examined for ticks. A total of 23 (3.2%) deer from 14
sites were infested and only two sites were already known for D. reticulatus. These results strongly
suggest that D. reticulatus has
expanded its range within the last three decades particularly in the eastern
and southwestern parts of Germany.
Further evidence for the changing distribution of D. reticulatus is provided by the occurrence of canine babesiosis
in new areas of Germany [24, 25], Hungary [26], Switzerland [27], and the Netherlands
[28].Several factors, perhaps acting synergistically, could be
responsible for this recent spread ofD.
reticulatus, including increased deer abundance and the availability of
more fallow land as a result of EU agricultural policies. However, there are
good reasons for implicating a warming climate as being at least partly
involved. Habitats with adult D.
reticulatus are all characterized by more or less intense solar radiation
and it is likely that the temperature sum (cumulative day-degrees above the developmental zero within one vegetation
period) at the soil surface is a
limiting factor for oviposition and embryonic development [20]. The fact that D. reticulatus occurs further north in
eastern Europe supports this view, since the continental climate there is
characterized by higher summer temperatures. Whereas adults are cold-hardy and
can survive continental winters [29], eggs and larvae that do not complete
development would not have survived the cold season of a few decades ago in
central Europe [30]. Further research to
clarify the situation could focus on suitable habitats in the north of Germany.


### 2.3.Hyalomma marginatum

H. marginatum is well known as a vector of the dangerous viral zoonosis
Crimean-Congo hemorrhagic fever (CCHF) [31]. Its possible northern spread and
establishment of permanent populations is thus of much significance, especially
since immature stages are frequently found on migratory birds flying to
temperate Europe [32]. The life cycle of this
tick is faster in southern parts of its distribution range (Northern
Africa) [32] with larvae active as early as February, but clearly
slower in northern, colder regions, with immatures active as late as June.
Analysis of the recorded distribution of the tick show that, according to
climate requirements, there are two clear clusters of populations [33]. One
cluster extends from the northern geographical limit of the species in the
Balkans (approx., latitude 44°N) and into Turkey and the Middle East. The second one is
restricted to Africa north of the Sahara and western parts of Spain. Analysis
of the climate niche of the first cluster clearly points to a
temperature-related limiting factor for these northern populations. Temperatures
between September and December are critical for the establishment of permanent
populations. Cumulative temperatures between September and December have an
average of 800°C in places where the tick has permanent populations, and below
400°C in sites not colonized by H.
marginatum. This finding seems to be related to the factors that affect
molting of immature stages and are not connected to the extremely cold winter
temperatures that prevent overwintering adults surviving into the next year, as
suggested by Hoogstraal et al.  [32]. If temperatures are high enough to allow molting
before the cold winters, unfed adults can survive the next active season. Field
observations (Z. Vatansever, personal comment) recorded the feeding of nymphs
in late summer in Turkey,
with the resulting unfed flat adults commonly overwintering in the first few
centimeters below the soil surface. Regulatory variables for these northern
populations appear to act on thermodependent phases of the tick life cycle. On
the other hand, climate niche analysis of the southern cluster of tick
communities points to a strict dependence on rainfall and potential
evaporation, but this may not be relevant if specimens from the southern range
can adapt to the colder conditions of the northern cluster.Although migratory birds are carriers of immatureHyalomma ticks and could potentially
introduce them into currently Hyalomma-free
areas in the spring, their climate requirements and current climate data do not
suggest that they can become established. Mid-March and early April are the
main periods of mass arrival of birds in Spain on their way to northern Europe. Data obtained
from the Climate Research Unit (UK) show that average temperature in that
period is 16-17°C in Morocco and Mauritania,
9–11°C in southern Spain, and 5-6°C in southern Germany.
According to data on molting of engorged nymphs under laboratory conditions,
about 300ºC cumulative degrees above the developmental zero (14–16°C) are
necessary to complete the molt [34]. Nymphs that engorge at the time of migratory
bird arrival in early spring would need much longer to molt in southern Germany, with a consequent increase in mortality, than in
north-western Africa, where only a few weeks
are required. In the current climatic
conditions, it is highly improbable that engorged nymphs can survive in
sufficient numbers to be founders of new permanent populations in Europe. Immature H.
marginatum are found on local (nonmigratory) birds in central Spain around
late May and early June, which is too late for northern African and southern
European populations of H. marginatum to mix because of the
current climate barriers imposed by their respective climate requirements at
the moment of bird migration. If
climate change includes the predicted temperature increases, H. marginatum ticks may become established in
northern latitudes but it is debatable whether initial introduction will occur
as a result of bird migration alone because very small numbers of ticks, all
immature stages, would be involved. It is more likely that, as autumn and
winter temperatures rise, establishment of H.
marginatum will mainly result
from the introduction of adult females feeding on wild and domestic ruminants
via the Middle East and the Balkans, where
there is much uncontrolled movement of livestock.


### 2.4.Rhipicephalus sanguineus

A special case of distribution and association to
environmental variables is that of the brown dog tick,Rhipicephalus sanguineus. It has a worldwide distribution mainly
because of introduction by dogs, but rarely occurs in temperate and cold
regions. However, R. sanguineus is an
endophilous tick (associated with shelters like kennels, private gardens, or
cracks in walls of human constructions), so may potentially cause temporary
infestations in heated accommodation anywhere in the world. Within its normal
range, R. sanguineus can reach huge
populations under adequate environmental conditions and continued presence of a
blood source. Currently, the brown dog tick is extremely common around the
Mediterranean region. In the coldest places of this region, the tick may
undergo a winter dormancy within the cracks of the walls, while in localities
with warmer winters continuing activity may take place. Only sporadic cases of
infestation by R. sanguineus have
been described in central and northern Europe.Studies on infestations in some Mediterranean
cities [35] showed that permanent populations of the tick are absent in
apartments where dogs are present, even without any kind of ixodicide
treatment. However, the tick is present and may occur in large numbers in small
private gardens and kennels of houses (or even within houses) in the outskirts.
These country-type houses are very common in the Mediterranean region. Hourly
climate data recorded by probes installed indoor and outdoor in these different
types of construction showed that adequate humidity is a critical factor for
successful establishment of indoor populations [35]. In central Europe, there are no humidity restrictions for the
development of the tick in the private gardens or kennels and spring and summer
temperatures are the only limitation. Recent studies on climate features [36]
have shown that particular events, such as the heat wave in Europe in 2003, can result in temporary conditions adequate for the development and
molting of immature stages. It is clear that despite the endophilous nature of
this tick species, climatic conditions in the outer environment are critical
for its long-term establishment in an area. An increase of about 2-3°C in the average
temperature from April–September could
result in the establishment of permanent populations of the tick in regions of
northern temperate Europe where it is
currently absent.


## 2.1.Ixodes ricinus

The
climate is regarded as the principal restricting factor at the northern limit
ofI. ricinus distribution [5]. Although I. ricinus is surprisingly cold-hardy
and when winter-acclimatized can survive 24-hour exposure to temperatures
ranging from −14.4°C to −18.9°C [6], the
detrimental effects of cold are accumulative and exposure for 30 days to only −10°C has been
shown to be lethal for a high proportion of unfed nymphs and diapausing
engorged larvae and nymphs [6]. Molting I.
ricinus ticks are even more vulnerable so that if summer temperatures are
not high enough to complete
development before the onset of winter (little or no development takes place
between 7  and 10°C [7, 8]), they are unlikely to survive even moderate frosts.
Degree-day models have been
developed which proved useful in elucidating the I.ricinus life cycle [9, 10], but more research on the winter biology
of this species would help further understand its northern distribution limit.In Sweden, the northern distribution limit ofI. ricinus, together with that of several other animal and plant species, has
shifted northwards since the climate started to noticeably change in the late
1980s [11]. The geographical distribution range of I. ricinus used to be located below 61°N [5], but ticks are now
established along the whole Baltic Sea coastline (up to 66°N) and along the river valleys and the larger lakes in the
northern regions. This shift in latitude distribution has been shown to be
related to changes over several seasons in the number of degree-days with
temperatures vital for tick survival, activity and development [12]. At the
highest latitudes fewer days with cold winter temperatures (well below  −12°C for longer
periods) had the clearest impact for new tick establishment (Figure 1).Changes in tick distribution in northern and central Sweden.
White dots illustrate
districts in Sweden
where ticks were reported to be present before 1980 (a) and in 1994-1995 (b).
The study region is within the black line (Lindgren et al. 2000,
[12] with
permission from Environmental Health
Perspectives).
(a)(b)In central Sweden (59°N to 61°N) in areas
with medium-high densities of ticks, increases in tick abundance were
correlated to a combination of mild winters (fewer days with temperatures below
7°C) and extended spring and autumn seasons (more days with minimum
temperatures not lower than 5 to 8°C). In south and central Sweden, the current climate only allows a tick
activity season of 6–8 months compared
to as much as 11 months in some parts of the British Isles, and further changes
in seasonal climate in Sweden
are likely to continue to have a major impact on the prevalence of ticks. The
combination of climate variables affecting ticks has also been shown to be
significantly correlated with increases in the incidence of TBE in Stockholm County  (59.2°N) during the period 1960–1998 [13]. The
risks of LB are likely to increase as well because Borrelia burgdorferi sensu lato (s.l.) spirochetes have been found
in I. ricinus throughout its range in
Sweden
[14].A comparable situation has been reported in changes to the
altitude distribution ofI. ricinus in the mountainous regions of the Czech Republic. Field studies
in 1957 and in 1979-80 showed that
ticks were prevalent up to 700 meters above sea level. Ticks were collected
from dogs or by drag-sampling in the same locations in 2001 and 2002 and were
then found as high as 1100 meters in areas where they had been absent from
small mammal samples [15–17] and where it has been shown that they could
not complete their life cycle over the period 1957–1983 [18].
Furthermore, the prevalence of ticks carrying the TBE virus or B. burgdorferi s. l. spirochetes also
seems to have increased at high altitude in the Czech Republic
[16, 19].


## 2.2.Dermacentor reticulatus

Dermacentor reticulatus is a vector of
canine babesiosis, tularemia, Q-fever, and at least one zoonotic rickettsiosis
[20] and has
vector competence for Anaplasma marginale
[21]. Unlike I. ricinus, only the adults quest for hosts on surface
vegetation and they feed primarily on deer, frequently bite dogs, but only
occasionally humans, whereas the larvae and nymphs parasitize rodents. The life
cycle is much shorter than that of I. ricinus, with eggs deposited in the spring and
developing to adults within the same year [22]. The geographic range of the species extends from France and southwest England in the west to central Asia in the east. In
western and central Europe its northern limit is northern Germany, northern Poland,
and Lithuania, and its
southern limit is the
Mediterranean shore (restricted to humid mountainous areas), whereas it has a
more northern distribution in the east (St.
Petersburg). Within this area, its distribution is
highly focal, and within Germany
in 1976, it was only reported from four sites out of more than 3000 [23].In two recent studies, however, data were collected showing
that this tick species has since colonized many more sites in Germany
[19].
The first study (2003) consisted of the screening of 365 dogs from 171 sites.
Almost 10% of the ticks from 41 dogs were D.
reticulatus and the infested dogs came from 26 sites, all previously
unknown for the tick. Seven of the sites were subsequently confirmed by
flagging. In the second study (2004), 721 deer were shot at 201 sites from 161
districts and their heads examined for ticks. A total of 23 (3.2%) deer from 14
sites were infested and only two sites were already known for D. reticulatus. These results strongly
suggest that D. reticulatus has
expanded its range within the last three decades particularly in the eastern
and southwestern parts of Germany.
Further evidence for the changing distribution of D. reticulatus is provided by the occurrence of canine babesiosis
in new areas of Germany [24, 25], Hungary [26], Switzerland [27], and the Netherlands
[28].Several factors, perhaps acting synergistically, could be
responsible for this recent spread ofD.
reticulatus, including increased deer abundance and the availability of
more fallow land as a result of EU agricultural policies. However, there are
good reasons for implicating a warming climate as being at least partly
involved. Habitats with adult D.
reticulatus are all characterized by more or less intense solar radiation
and it is likely that the temperature sum (cumulative day-degrees above the developmental zero within one vegetation
period) at the soil surface is a
limiting factor for oviposition and embryonic development [20]. The fact that D. reticulatus occurs further north in
eastern Europe supports this view, since the continental climate there is
characterized by higher summer temperatures. Whereas adults are cold-hardy and
can survive continental winters [29], eggs and larvae that do not complete
development would not have survived the cold season of a few decades ago in
central Europe [30]. Further research to
clarify the situation could focus on suitable habitats in the north of Germany.


## 2.3.Hyalomma marginatum

H. marginatum is well known as a vector of the dangerous viral zoonosis
Crimean-Congo hemorrhagic fever (CCHF) [31]. Its possible northern spread and
establishment of permanent populations is thus of much significance, especially
since immature stages are frequently found on migratory birds flying to
temperate Europe [32]. The life cycle of this
tick is faster in southern parts of its distribution range (Northern
Africa) [32] with larvae active as early as February, but clearly
slower in northern, colder regions, with immatures active as late as June.
Analysis of the recorded distribution of the tick show that, according to
climate requirements, there are two clear clusters of populations [33]. One
cluster extends from the northern geographical limit of the species in the
Balkans (approx., latitude 44°N) and into Turkey and the Middle East. The second one is
restricted to Africa north of the Sahara and western parts of Spain. Analysis
of the climate niche of the first cluster clearly points to a
temperature-related limiting factor for these northern populations. Temperatures
between September and December are critical for the establishment of permanent
populations. Cumulative temperatures between September and December have an
average of 800°C in places where the tick has permanent populations, and below
400°C in sites not colonized by H.
marginatum. This finding seems to be related to the factors that affect
molting of immature stages and are not connected to the extremely cold winter
temperatures that prevent overwintering adults surviving into the next year, as
suggested by Hoogstraal et al.  [32]. If temperatures are high enough to allow molting
before the cold winters, unfed adults can survive the next active season. Field
observations (Z. Vatansever, personal comment) recorded the feeding of nymphs
in late summer in Turkey,
with the resulting unfed flat adults commonly overwintering in the first few
centimeters below the soil surface. Regulatory variables for these northern
populations appear to act on thermodependent phases of the tick life cycle. On
the other hand, climate niche analysis of the southern cluster of tick
communities points to a strict dependence on rainfall and potential
evaporation, but this may not be relevant if specimens from the southern range
can adapt to the colder conditions of the northern cluster.Although migratory birds are carriers of immatureHyalomma ticks and could potentially
introduce them into currently Hyalomma-free
areas in the spring, their climate requirements and current climate data do not
suggest that they can become established. Mid-March and early April are the
main periods of mass arrival of birds in Spain on their way to northern Europe. Data obtained
from the Climate Research Unit (UK) show that average temperature in that
period is 16-17°C in Morocco and Mauritania,
9–11°C in southern Spain, and 5-6°C in southern Germany.
According to data on molting of engorged nymphs under laboratory conditions,
about 300ºC cumulative degrees above the developmental zero (14–16°C) are
necessary to complete the molt [34]. Nymphs that engorge at the time of migratory
bird arrival in early spring would need much longer to molt in southern Germany, with a consequent increase in mortality, than in
north-western Africa, where only a few weeks
are required. In the current climatic
conditions, it is highly improbable that engorged nymphs can survive in
sufficient numbers to be founders of new permanent populations in Europe. Immature H.
marginatum are found on local (nonmigratory) birds in central Spain around
late May and early June, which is too late for northern African and southern
European populations of H. marginatum to mix because of the
current climate barriers imposed by their respective climate requirements at
the moment of bird migration. If
climate change includes the predicted temperature increases, H. marginatum ticks may become established in
northern latitudes but it is debatable whether initial introduction will occur
as a result of bird migration alone because very small numbers of ticks, all
immature stages, would be involved. It is more likely that, as autumn and
winter temperatures rise, establishment of H.
marginatum will mainly result
from the introduction of adult females feeding on wild and domestic ruminants
via the Middle East and the Balkans, where
there is much uncontrolled movement of livestock.


## 2.4.Rhipicephalus sanguineus

A special case of distribution and association to
environmental variables is that of the brown dog tick,Rhipicephalus sanguineus. It has a worldwide distribution mainly
because of introduction by dogs, but rarely occurs in temperate and cold
regions. However, R. sanguineus is an
endophilous tick (associated with shelters like kennels, private gardens, or
cracks in walls of human constructions), so may potentially cause temporary
infestations in heated accommodation anywhere in the world. Within its normal
range, R. sanguineus can reach huge
populations under adequate environmental conditions and continued presence of a
blood source. Currently, the brown dog tick is extremely common around the
Mediterranean region. In the coldest places of this region, the tick may
undergo a winter dormancy within the cracks of the walls, while in localities
with warmer winters continuing activity may take place. Only sporadic cases of
infestation by R. sanguineus have
been described in central and northern Europe.Studies on infestations in some Mediterranean
cities [35] showed that permanent populations of the tick are absent in
apartments where dogs are present, even without any kind of ixodicide
treatment. However, the tick is present and may occur in large numbers in small
private gardens and kennels of houses (or even within houses) in the outskirts.
These country-type houses are very common in the Mediterranean region. Hourly
climate data recorded by probes installed indoor and outdoor in these different
types of construction showed that adequate humidity is a critical factor for
successful establishment of indoor populations [35]. In central Europe, there are no humidity restrictions for the
development of the tick in the private gardens or kennels and spring and summer
temperatures are the only limitation. Recent studies on climate features [36]
have shown that particular events, such as the heat wave in Europe in 2003, can result in temporary conditions adequate for the development and
molting of immature stages. It is clear that despite the endophilous nature of
this tick species, climatic conditions in the outer environment are critical
for its long-term establishment in an area. An increase of about 2-3°C in the average
temperature from April–September could
result in the establishment of permanent populations of the tick in regions of
northern temperate Europe where it is
currently absent.


## 3. Effects of Climate Change on the Seasonal Aactivity of Ticks

### 3.1. Winter Activity ofIxodes ricinus

It is
common knowledge that the seasonal activity ofI. ricinus nymphs and adults extends from March to October in most
parts of central Europe, whereas the larval stage begins questing only in May,
at least in Berlin
forests (Kahl and Dautel, unpublished). In contrast to parts of the British Isles, any tick activity from mid-November to
mid-February is unusual in that region. The strong influence that
temperature can exert on tick activity patterns, even in the cold season, was
demonstrated in eastern Germany
in the extraordinarily mild winter of 2006/7. The
continuously warm-to-mild autumn in 2006 (1st September to 30th November),
which was 3.4°C warmer than the long-term mean for 1961–90, was followed
by a winter (1st December to 28th February) 4.6°C milder than the
long-term mean (http://www.dwd.de, data from Potsdam) with only two days with a
maximum temperature <0°C. On prepared field plots in a Berlin forest,
questing adult I. ricinus (Figure 2)
were found on every observation date throughout the winter (early November to
early March) and questing nymphal ticks were absent on only two out of 19
occasions [36]. Moreover, Dautel and colleagues collected 88 nymphs and seven
adult I.ricinus in two man-hours by flagging
1000m2 in a nearby forest in mid-January 2007. At the same locality
on another occasion in mid-February, nymphal and adult questing tick abundance
was still higher (temperature maximum on both days approximately 7°C).Figure 2
Dorsally marked adult femaleIxodes ricinus questing on a wooden rod
placed in a field plot for observation of I.
ricinus questing activity in a Germany (Berlin) forest (Dautel et al. 2008
[37], with permission from International
Journal of Medical Microbiology).This is a
good example of how flexible the seasonal questing activity of this widespread
vector tick can be if the temperature conditions change from the local norm.
The unusual registration of four cases of human TBE (a notifiable disease in Germany) in early 2007 (early January to late
February) shows that there was some tick questing activity in other parts of Germany
as well
during that winter. If winter
temperatures generally increase in the future, it can be assumed that seasonal
periods with no questingI. ricinus will become shorter in central Europe. It is
evident that winter activity of vector ticks distinctly increases the risk for
forest visitors of an infectious tick bite, especially if they do not expect
ticks to be active at that time of the year. It is unclear, however, what the chances
are for a winter-active tick to find a host at that time (because of reduced
host abundance in winter though this may also change with the advent of warmer
winters). It is also unclear how winter activity may affect the remaining
seasonal activity pattern (winter-active ticks spend precious energy) or
whether any changes in the seasonal activity of I. ricinus nymphs and adults are beneficial or detrimental for the
perpetuation of tick-borne pathogens. The infection of I. ricinus larvae during feeding is a crucial step in the circulation
of many tick-borne pathogens and the effects of higher ambient temperatures on
the seasonal activity of larvae and its chances to find a suitable host may be
of great significance in determining the prevalence of some tick-borne
diseases.


### 3.2. Summer Activity ofIxodes ricinus

In 1976 the early summer weather in County Wicklow, Ireland, included maximum air temperatures of29–31°C recorded on
sheep pastures where Ixodes ricinus activity was being studied. Such monthly maxima in early summer may be the rule
rather than the exception in this region in the coming decades [3].
Retrospective use was made of 1976 summer temperature and tick data in an
examination of the effects of high temperatures on tick development and activity
in relation to the predicted global warming [38]. In most parts of its range, I.ricinus shows some degree of bimodal
seasonal activity and in 1975, more ticks were collected in autumn than in
spring/summer, which may be attributed to the presence of hosts on these
particular sheep pastures in late summer and autumn but not in spring or early
summer for several years. However, by 1977, the pattern of tick activity had
changed dramatically and more than 90% nymphal activity occurred from March to
June. It was postulated that the elevated early and mid-summer temperatures of
1976 were the primary cause of the change from autumn to
spring/summer-dominated nymphal activity.This possibility was investigated by studies on tick
development under quasi-natural conditions. The threshold period for deposited
engorged larvae to enter a developmental diapause was identified as the first
two weeks of August, after which time larvae overwintered in an engorged state
and did not reappear as nymphs until the following autumn. The tick abundance
data suggested that the 1975 autumn-feeding adults gave rise to larvae that fed
predominantly in the prediapause period, so that they had the opportunity to
overwinter as unfed nymphs and thus join the spring-active ticks in 1977. This
interpretation was supported by a degree-day development model forI.ricinus originally described by
Gardiner et al. [9], that predicted the appearance of larvae from autumn-laid
eggs a month earlier when exposed to 1976 temperatures than when exposed to
more normal temperatures [10]. The high summer temperatures of 1976 had
apparently transferred ticks from an autumn-active cohort to a spring-active
one. The process revealed by this study suggests that after hotter summers much
of the host-seeking activity of I.ricinus will occur in late autumn, to a lesser extent in the winter months, and with
strong activity again in early spring. Larval activity is likely to be mainly
restricted to mid-summer (as long as humidity requirements are satisfied) with
the majority of larvae avoiding developmental diapause and becoming active as
nymphs in late autumn or early spring of the following year. Interestingly,
this pattern of activity is very similar to that of the American
I.scapularis in New
Jersey, USA
[39, 40], where air temperatures exceed  26°C for 50–60 days of the
year. Suitable studies in southern Europe have not been undertaken, but a
similar phenology to the predicted scenario for I. ricinus in hot summers was described in a recent comprehensive
study in central Spain
where maximum summer air temperatures generally reach 26°C [41]. It might be
expected that with low precipitation in hot summers, survival and activity of
ticks such as I.ricinus, which is very susceptible to
desiccation, would be reduced. Indeed, it has been reported that in Switzerland saturation deficits depressed
nymphal and adult I.ricinus activity [42]. However, Irish
data [38] showed that all active stages of I.ricinus will quest throughout hot dry weather as long as
appropriate vegetation cover is present to provide opportunities for
rehydration. The same  situation appears to obtain for I. scapularis immature stages in the USA
[40].It seems likely that with increased global warming,I.ricinus activity will occur more in the
autumn and winter months in many areas and, furthermore, a greater proportion
of the tick population may be active at this time than at present, with a
consequent temporal change in the risk of tick-borne diseases.


## 3.1. Winter Activity ofIxodes ricinus

It is
common knowledge that the seasonal activity ofI. ricinus nymphs and adults extends from March to October in most
parts of central Europe, whereas the larval stage begins questing only in May,
at least in Berlin
forests (Kahl and Dautel, unpublished). In contrast to parts of the British Isles, any tick activity from mid-November to
mid-February is unusual in that region. The strong influence that
temperature can exert on tick activity patterns, even in the cold season, was
demonstrated in eastern Germany
in the extraordinarily mild winter of 2006/7. The
continuously warm-to-mild autumn in 2006 (1st September to 30th November),
which was 3.4°C warmer than the long-term mean for 1961–90, was followed
by a winter (1st December to 28th February) 4.6°C milder than the
long-term mean (http://www.dwd.de, data from Potsdam) with only two days with a
maximum temperature <0°C. On prepared field plots in a Berlin forest,
questing adult I. ricinus (Figure 2)
were found on every observation date throughout the winter (early November to
early March) and questing nymphal ticks were absent on only two out of 19
occasions [36]. Moreover, Dautel and colleagues collected 88 nymphs and seven
adult I.ricinus in two man-hours by flagging
1000m2 in a nearby forest in mid-January 2007. At the same locality
on another occasion in mid-February, nymphal and adult questing tick abundance
was still higher (temperature maximum on both days approximately 7°C).Figure 2
Dorsally marked adult femaleIxodes ricinus questing on a wooden rod
placed in a field plot for observation of I.
ricinus questing activity in a Germany (Berlin) forest (Dautel et al. 2008
[37], with permission from International
Journal of Medical Microbiology).This is a
good example of how flexible the seasonal questing activity of this widespread
vector tick can be if the temperature conditions change from the local norm.
The unusual registration of four cases of human TBE (a notifiable disease in Germany) in early 2007 (early January to late
February) shows that there was some tick questing activity in other parts of Germany
as well
during that winter. If winter
temperatures generally increase in the future, it can be assumed that seasonal
periods with no questingI. ricinus will become shorter in central Europe. It is
evident that winter activity of vector ticks distinctly increases the risk for
forest visitors of an infectious tick bite, especially if they do not expect
ticks to be active at that time of the year. It is unclear, however, what the chances
are for a winter-active tick to find a host at that time (because of reduced
host abundance in winter though this may also change with the advent of warmer
winters). It is also unclear how winter activity may affect the remaining
seasonal activity pattern (winter-active ticks spend precious energy) or
whether any changes in the seasonal activity of I. ricinus nymphs and adults are beneficial or detrimental for the
perpetuation of tick-borne pathogens. The infection of I. ricinus larvae during feeding is a crucial step in the circulation
of many tick-borne pathogens and the effects of higher ambient temperatures on
the seasonal activity of larvae and its chances to find a suitable host may be
of great significance in determining the prevalence of some tick-borne
diseases.


## 3.2. Summer Activity ofIxodes ricinus

In 1976 the early summer weather in County Wicklow, Ireland, included maximum air temperatures of29–31°C recorded on
sheep pastures where Ixodes ricinus activity was being studied. Such monthly maxima in early summer may be the rule
rather than the exception in this region in the coming decades [3].
Retrospective use was made of 1976 summer temperature and tick data in an
examination of the effects of high temperatures on tick development and activity
in relation to the predicted global warming [38]. In most parts of its range, I.ricinus shows some degree of bimodal
seasonal activity and in 1975, more ticks were collected in autumn than in
spring/summer, which may be attributed to the presence of hosts on these
particular sheep pastures in late summer and autumn but not in spring or early
summer for several years. However, by 1977, the pattern of tick activity had
changed dramatically and more than 90% nymphal activity occurred from March to
June. It was postulated that the elevated early and mid-summer temperatures of
1976 were the primary cause of the change from autumn to
spring/summer-dominated nymphal activity.This possibility was investigated by studies on tick
development under quasi-natural conditions. The threshold period for deposited
engorged larvae to enter a developmental diapause was identified as the first
two weeks of August, after which time larvae overwintered in an engorged state
and did not reappear as nymphs until the following autumn. The tick abundance
data suggested that the 1975 autumn-feeding adults gave rise to larvae that fed
predominantly in the prediapause period, so that they had the opportunity to
overwinter as unfed nymphs and thus join the spring-active ticks in 1977. This
interpretation was supported by a degree-day development model forI.ricinus originally described by
Gardiner et al. [9], that predicted the appearance of larvae from autumn-laid
eggs a month earlier when exposed to 1976 temperatures than when exposed to
more normal temperatures [10]. The high summer temperatures of 1976 had
apparently transferred ticks from an autumn-active cohort to a spring-active
one. The process revealed by this study suggests that after hotter summers much
of the host-seeking activity of I.ricinus will occur in late autumn, to a lesser extent in the winter months, and with
strong activity again in early spring. Larval activity is likely to be mainly
restricted to mid-summer (as long as humidity requirements are satisfied) with
the majority of larvae avoiding developmental diapause and becoming active as
nymphs in late autumn or early spring of the following year. Interestingly,
this pattern of activity is very similar to that of the American
I.scapularis in New
Jersey, USA
[39, 40], where air temperatures exceed  26°C for 50–60 days of the
year. Suitable studies in southern Europe have not been undertaken, but a
similar phenology to the predicted scenario for I. ricinus in hot summers was described in a recent comprehensive
study in central Spain
where maximum summer air temperatures generally reach 26°C [41]. It might be
expected that with low precipitation in hot summers, survival and activity of
ticks such as I.ricinus, which is very susceptible to
desiccation, would be reduced. Indeed, it has been reported that in Switzerland saturation deficits depressed
nymphal and adult I.ricinus activity [42]. However, Irish
data [38] showed that all active stages of I.ricinus will quest throughout hot dry weather as long as
appropriate vegetation cover is present to provide opportunities for
rehydration. The same  situation appears to obtain for I. scapularis immature stages in the USA
[40].It seems likely that with increased global warming,I.ricinus activity will occur more in the
autumn and winter months in many areas and, furthermore, a greater proportion
of the tick population may be active at this time than at present, with a
consequent temporal change in the risk of tick-borne diseases.


## 4. The Role of Modeling in Analysis of Climate Change Effects on Ticks

### 4.1. Climate Suitability Modeling

Climate suitability for a tick population can be defined as
the fitness of a set of climatic conditions for the existence of that
population in a given region. However, many other factors operating at different
levels restrict the effective dispersal and establishment of potential
invaders. Thus, while the climate in a particular location may be suitable for
a given tick species, the potential for dispersal there and the ability to
establish a new viable population may be very low. Furthermore, microclimatic
variables such as soil surface temperature and relative humidity (which are
affected by such things as slope and aspect, snow cover, vegetation, litter
layer, humus and underlying soils) may be crucial in determining the
distribution pattern of specific niches for tick survival within an area. Most
data on climate preferences of ticks have been empirically derived from
descriptions of the abiotic components of the environmental niche, as defined
by the climate-supported native populations, and based on the assumption that
they are homogeneously distributed in the native area.The basic concept underlying species occurrence
modeling is the definition of the ecological niche: each species is found
within specific ranges for environmental variables that support individual
survival and reproduction [43]. We refer here to climate instead of
environmental or ecological space because these studies are aimed at
understanding the relationship of ticks to climate, and ignore other basic
aspects, such as vegetation patterns or host abundance, that are also involved
in delineation of the “ecological” preferences of a tick species or population.
Species occurrence can be predicted by inclusion of appropriate climate variables
in what are commonly referred to as climate suitability models (CSMs): the
relationships are generalized from a sample of correlations of species presence
with specific values of environmental variables. While it is well recognized
that the climate niche space occupied by a species across its geographic range
may vary, this is rarely considered in current modeling approaches despite its
obvious importance. When regional climate niche variations occur, a CSM derived
for a particular area may not apply to other areas, and a model derived from a
large area may have comparatively weak local predictive power. A widely held
assumption in traditional models of tick distribution is that responses of
species to environmental gradients are unimodal and symmetrical. Thus, climate
suitability is predicted to decline from central (and ecologically optimal)
areas of a species’ range towards the periphery. In suboptimal conditions, a
species may compensate for physiological stress by a shift in niche position.
For wide-ranging species, suitable ecological conditions may vary considerably
between different regions within the range.However, these CSM are unsuitable if an
adequate understanding of the factors operating over the transmission of a
disease is necessary. The many variables involved in such processes, like
hosts, densities of questing infected ticks, and a perception of the small
scale of foci, are only adequately addressed with models designed to describe
seasonal dynamics. While some models with biological content have been produced
for tick species such asBoophilus
microplus [44], Amblyomma americanum [45], and Ixodes scapularis [46],
none are currently available for European ticks. Such models are a priority to
adequately understand the impact of climate change on tick populations,
provided that adequate data are used for important components such as host
densities and microhabitat suitability. However, despite the absence of such
data in climate suitability models, these models have proved useful in the
elucidation of tick-borne disease foci for the recent outbreak of CCHF in Turkey  [47].


### 4.2. Recent (100 Years) Changes in Climate Suitability forIxodes ricinus

Both regional climatic
requirement variations and the existence of  “demes” (defined as populations of
closely related interbreeding organisms of the same species with differing
responses to the wide array of climate factors occurring across the
geographical range of the species) have been demonstrated forI. ricinus
[47]
(Figure 3).Figure 3
The vegetation-derived
clusters as recognized over the western Palaearctic. The image was obtained
from a yearly series of monthly satellite images, capturing the Normalized
Difference Vegetation Index (NDVI): a measure of the photosynthetic activity of
the vegetation. These images were subjected to a cluster analysis according to
the monthly NDVI features to obtain 10 categories (category 1 is water and not
displayed in the picture). (Estrada-Peña et al. 2006 [48], with permission from Medical and Veterinary Entomology).The study revealed at least 10
distinctI. ricinus groups with a
pattern of distribution closely overlapping with the presence of previously
reported phenotypic forms of the species, and is in general agreement with a
16S mitochondrial rDNA study of genetic variation in I.ricinus [49]. The importance of these findings is that the climate
and vegetation features correlated with the genetic groups in the whole tick
metapopulation, with different populations having specific climatic
requirements and unique genetic fingerprints. A study on the changes in climate
suitability for I.ricinus in the western Palearctic has
been carried out using deme-derived models based on the different populations
recognized in the Palaearctic [50]. The distribution records available for the
different demes were used to build partial models (i.e., applied to regions of
the whole distribution range) from which a complete map for the whole region
was produced. The study used a long (1900–1999) series of
climate data at coarse resolution (10 minutes of arc) to examine the trends in
climate and to estimate sustained variations in climate suitability for I.ricinus. While some areas showed a
deterministic (i.e., continuous) tendency towards increasing or decreasing
suitability for the tick, others showed unambiguous cycles of climate
suitability, termed areas of random walk. In these, populations of the tick may
undergo periodical variations in their geographical range as a consequence of
cyclic changes in climate.This analysis suggests that while climate
suitability forI. ricinus did not
change in a large area of Europe during the
100-year study period, it increased in specific geographically limited
locations and decreased in  others (Figure 4).An analysis
of the long-term changes in climate suitability for the tickIxodes ricinus in Europe (1900–1999). A
temporally extensively gridded dataset was subjected to a temporal analysis to
understand how climate has changed in 100 years and how this trend affected the
climate suitability for the tick. Areas are divided into suitable and
unsuitable (the last, without colors in the figure). In the panel “A,” the area
marked as suitable and stable means no changes in suitability for the tick.
Deterministic increase or decrease means a continued trend towards increasing
or decreasing climate suitability. Panel B shows the areas where random walk
trend has been observed. These areas are subjected to periodic cycles of
climate, thus allowing cycles of increasing or decreasing climate suitability
for the tick. (Estrada-Peña and Venzal 2006 [50], with permission from Ecohealth).These changes are not recent and are associated with yearly
and summer rainfall patterns rather than with temperature. The reported
increased abundance ofI. ricinus in
parts of Europe (e.g., Sweden
[11]) coincides geographically with the regions where a recent increase in
climate suitability has been detected, within zones having a marked random walk
tendency. Thus, the observation of higher tick abundance in recent years may
not be due to a permanent shift in tick populations, but rather because the
long-term climate cycle, which varies on a wide timescale, has been in a phase
that is favorable to tick survival. No single variable was consistently associated
in the study period with changes in climate suitability across sites where
random walk was detected. The absence of a single regulatory variable seems to
be connected with the different climate niche experienced by the tick
populations in their distribution area. Thus, rainfall and temperature have
different regulatory abilities according to the portion of the tick’s climate
envelope represented in a given area.


### 4.3. An Overview of the Climate Suitability for Ticks in the Mediterranean Region

The Mediterranean region is expected to experience profound
changes in climate [51], and furthermore, its close proximity to the African
continent makes it a particularly sensitive area to invasion by ticks currently
restricted to northern Africa. It is,
therefore, of interest to explore the predicted impact of climate changes on
the suitability for ticks. The ticks involved (genera Boophilus, Dermacentor, Rhipicephalus, and Hyalomma) find their maximum suitability in Mediterranean type
vegetation, including areas with cold winters and dry summers, and are
prevalent in wide areas of that region, extending well into the Middle East. Most of them are vectors of pathogens of
animals and humans. Predicted changes in climate are also expected to have a
serious impact on the vegetation structure, driving the area toward a more
open, brush-like vegetation, where these ticks find their ecological optima.An
estimation of the climate niches for each of these ticks has already been published [52].
Global climate models remain relatively coarse in terms of spatial resolution;
this compromised the desired resolution of that analysis. To address this
problem, new climate layers were created with monthly increases and decreases
in temperature of 1 and 2°C, and monthly variations in rainfall of 60, 80, 120,
and 140% of actual values. For each combination of temperature and rainfall,
the climate suitability for each species in the region was evaluated. The
baseline climate suitability was used as a framework to compute the impact of
the different changes of climate over the expansion or retraction of the
geographical range for each species. The expected impact is displayed in
Figure 5.Predicted geographic impact
(habitat suitability turnover) of different climate change scenarios. The maps
shows the forecasted changes in habitat suitability for different tick species,
with changes in temperature (left column) or rainfall (right column) analyzed
by consensus analysis (a statistical method of classification using multiple
input variables) to show the most coherent response to a range of changes in
predictor variables. Dark shades of grey indicate increased climate suitability
following a decrease in the predictor variable scenario (temperature or
rainfall). Light shades of grey indicate increased climate suitability
following an increase in the predictor variable. A and B:B. annulatus; C and D: D.
marginatus; E and F: H. excavatum;
G and H: H. marginatum; I and
J: R. bursa; K and L: R. turanicus.
(Estrada-Peña and Venzal 2007 [52], with permission
from Journal of Medical Entomology).ForB. annulatus and H. excavatum, an increase in temperature would lead to an increase
in suitability within regions of northern Africa and limited parts of southern Europe. Changes in rainfall are predicted to have little
geographic impact on B. annulatus (which in any case is a one-host-tick that is much less exposed to ambient
conditions than three-host-ticks), but they show a clear effect on H. excavatum.In the case ofD. marginatus, a decrease in temperature
results in an increase in the extent of adequate suitability in northern
Africa, most of coastal southern Europe, and wide areas of southern Spain,
whereas an increase in temperature would result in a northward expansion of the
suitable habitat for this species. Changes in rainfall result in similar
effects to those described for the above-mentioned changes in temperature.
Large areas of Europe would potentially be
affected by an increase in the climate suitability for Rhipicephalus spp. and H.
marginatum after an increase in temperature and decrease in rainfall.
Decreasing temperatures in Europe are
predicted to result in habitat loss for B.
annulatus, R. bursa, and H.
marginatum. Again, we must stress that this is an evaluation of the climate
suitability for these tick species, since changes in vegetation, host
availability, and animal movements were not included in the models.


## 4.1. Climate Suitability Modeling

Climate suitability for a tick population can be defined as
the fitness of a set of climatic conditions for the existence of that
population in a given region. However, many other factors operating at different
levels restrict the effective dispersal and establishment of potential
invaders. Thus, while the climate in a particular location may be suitable for
a given tick species, the potential for dispersal there and the ability to
establish a new viable population may be very low. Furthermore, microclimatic
variables such as soil surface temperature and relative humidity (which are
affected by such things as slope and aspect, snow cover, vegetation, litter
layer, humus and underlying soils) may be crucial in determining the
distribution pattern of specific niches for tick survival within an area. Most
data on climate preferences of ticks have been empirically derived from
descriptions of the abiotic components of the environmental niche, as defined
by the climate-supported native populations, and based on the assumption that
they are homogeneously distributed in the native area.The basic concept underlying species occurrence
modeling is the definition of the ecological niche: each species is found
within specific ranges for environmental variables that support individual
survival and reproduction [43]. We refer here to climate instead of
environmental or ecological space because these studies are aimed at
understanding the relationship of ticks to climate, and ignore other basic
aspects, such as vegetation patterns or host abundance, that are also involved
in delineation of the “ecological” preferences of a tick species or population.
Species occurrence can be predicted by inclusion of appropriate climate variables
in what are commonly referred to as climate suitability models (CSMs): the
relationships are generalized from a sample of correlations of species presence
with specific values of environmental variables. While it is well recognized
that the climate niche space occupied by a species across its geographic range
may vary, this is rarely considered in current modeling approaches despite its
obvious importance. When regional climate niche variations occur, a CSM derived
for a particular area may not apply to other areas, and a model derived from a
large area may have comparatively weak local predictive power. A widely held
assumption in traditional models of tick distribution is that responses of
species to environmental gradients are unimodal and symmetrical. Thus, climate
suitability is predicted to decline from central (and ecologically optimal)
areas of a species’ range towards the periphery. In suboptimal conditions, a
species may compensate for physiological stress by a shift in niche position.
For wide-ranging species, suitable ecological conditions may vary considerably
between different regions within the range.However, these CSM are unsuitable if an
adequate understanding of the factors operating over the transmission of a
disease is necessary. The many variables involved in such processes, like
hosts, densities of questing infected ticks, and a perception of the small
scale of foci, are only adequately addressed with models designed to describe
seasonal dynamics. While some models with biological content have been produced
for tick species such asBoophilus
microplus [44], Amblyomma americanum [45], and Ixodes scapularis [46],
none are currently available for European ticks. Such models are a priority to
adequately understand the impact of climate change on tick populations,
provided that adequate data are used for important components such as host
densities and microhabitat suitability. However, despite the absence of such
data in climate suitability models, these models have proved useful in the
elucidation of tick-borne disease foci for the recent outbreak of CCHF in Turkey  [47].


## 4.2. Recent (100 Years) Changes in Climate Suitability forIxodes ricinus

Both regional climatic
requirement variations and the existence of  “demes” (defined as populations of
closely related interbreeding organisms of the same species with differing
responses to the wide array of climate factors occurring across the
geographical range of the species) have been demonstrated forI. ricinus
[47]
(Figure 3).Figure 3
The vegetation-derived
clusters as recognized over the western Palaearctic. The image was obtained
from a yearly series of monthly satellite images, capturing the Normalized
Difference Vegetation Index (NDVI): a measure of the photosynthetic activity of
the vegetation. These images were subjected to a cluster analysis according to
the monthly NDVI features to obtain 10 categories (category 1 is water and not
displayed in the picture). (Estrada-Peña et al. 2006 [48], with permission from Medical and Veterinary Entomology).The study revealed at least 10
distinctI. ricinus groups with a
pattern of distribution closely overlapping with the presence of previously
reported phenotypic forms of the species, and is in general agreement with a
16S mitochondrial rDNA study of genetic variation in I.ricinus [49]. The importance of these findings is that the climate
and vegetation features correlated with the genetic groups in the whole tick
metapopulation, with different populations having specific climatic
requirements and unique genetic fingerprints. A study on the changes in climate
suitability for I.ricinus in the western Palearctic has
been carried out using deme-derived models based on the different populations
recognized in the Palaearctic [50]. The distribution records available for the
different demes were used to build partial models (i.e., applied to regions of
the whole distribution range) from which a complete map for the whole region
was produced. The study used a long (1900–1999) series of
climate data at coarse resolution (10 minutes of arc) to examine the trends in
climate and to estimate sustained variations in climate suitability for I.ricinus. While some areas showed a
deterministic (i.e., continuous) tendency towards increasing or decreasing
suitability for the tick, others showed unambiguous cycles of climate
suitability, termed areas of random walk. In these, populations of the tick may
undergo periodical variations in their geographical range as a consequence of
cyclic changes in climate.This analysis suggests that while climate
suitability forI. ricinus did not
change in a large area of Europe during the
100-year study period, it increased in specific geographically limited
locations and decreased in  others (Figure 4).An analysis
of the long-term changes in climate suitability for the tickIxodes ricinus in Europe (1900–1999). A
temporally extensively gridded dataset was subjected to a temporal analysis to
understand how climate has changed in 100 years and how this trend affected the
climate suitability for the tick. Areas are divided into suitable and
unsuitable (the last, without colors in the figure). In the panel “A,” the area
marked as suitable and stable means no changes in suitability for the tick.
Deterministic increase or decrease means a continued trend towards increasing
or decreasing climate suitability. Panel B shows the areas where random walk
trend has been observed. These areas are subjected to periodic cycles of
climate, thus allowing cycles of increasing or decreasing climate suitability
for the tick. (Estrada-Peña and Venzal 2006 [50], with permission from Ecohealth).These changes are not recent and are associated with yearly
and summer rainfall patterns rather than with temperature. The reported
increased abundance ofI. ricinus in
parts of Europe (e.g., Sweden
[11]) coincides geographically with the regions where a recent increase in
climate suitability has been detected, within zones having a marked random walk
tendency. Thus, the observation of higher tick abundance in recent years may
not be due to a permanent shift in tick populations, but rather because the
long-term climate cycle, which varies on a wide timescale, has been in a phase
that is favorable to tick survival. No single variable was consistently associated
in the study period with changes in climate suitability across sites where
random walk was detected. The absence of a single regulatory variable seems to
be connected with the different climate niche experienced by the tick
populations in their distribution area. Thus, rainfall and temperature have
different regulatory abilities according to the portion of the tick’s climate
envelope represented in a given area.


## 4.3. An Overview of the Climate Suitability for Ticks in the Mediterranean Region

The Mediterranean region is expected to experience profound
changes in climate [51], and furthermore, its close proximity to the African
continent makes it a particularly sensitive area to invasion by ticks currently
restricted to northern Africa. It is,
therefore, of interest to explore the predicted impact of climate changes on
the suitability for ticks. The ticks involved (genera Boophilus, Dermacentor, Rhipicephalus, and Hyalomma) find their maximum suitability in Mediterranean type
vegetation, including areas with cold winters and dry summers, and are
prevalent in wide areas of that region, extending well into the Middle East. Most of them are vectors of pathogens of
animals and humans. Predicted changes in climate are also expected to have a
serious impact on the vegetation structure, driving the area toward a more
open, brush-like vegetation, where these ticks find their ecological optima.An
estimation of the climate niches for each of these ticks has already been published [52].
Global climate models remain relatively coarse in terms of spatial resolution;
this compromised the desired resolution of that analysis. To address this
problem, new climate layers were created with monthly increases and decreases
in temperature of 1 and 2°C, and monthly variations in rainfall of 60, 80, 120,
and 140% of actual values. For each combination of temperature and rainfall,
the climate suitability for each species in the region was evaluated. The
baseline climate suitability was used as a framework to compute the impact of
the different changes of climate over the expansion or retraction of the
geographical range for each species. The expected impact is displayed in
Figure 5.Predicted geographic impact
(habitat suitability turnover) of different climate change scenarios. The maps
shows the forecasted changes in habitat suitability for different tick species,
with changes in temperature (left column) or rainfall (right column) analyzed
by consensus analysis (a statistical method of classification using multiple
input variables) to show the most coherent response to a range of changes in
predictor variables. Dark shades of grey indicate increased climate suitability
following a decrease in the predictor variable scenario (temperature or
rainfall). Light shades of grey indicate increased climate suitability
following an increase in the predictor variable. A and B:B. annulatus; C and D: D.
marginatus; E and F: H. excavatum;
G and H: H. marginatum; I and
J: R. bursa; K and L: R. turanicus.
(Estrada-Peña and Venzal 2007 [52], with permission
from Journal of Medical Entomology).ForB. annulatus and H. excavatum, an increase in temperature would lead to an increase
in suitability within regions of northern Africa and limited parts of southern Europe. Changes in rainfall are predicted to have little
geographic impact on B. annulatus (which in any case is a one-host-tick that is much less exposed to ambient
conditions than three-host-ticks), but they show a clear effect on H. excavatum.In the case ofD. marginatus, a decrease in temperature
results in an increase in the extent of adequate suitability in northern
Africa, most of coastal southern Europe, and wide areas of southern Spain,
whereas an increase in temperature would result in a northward expansion of the
suitable habitat for this species. Changes in rainfall result in similar
effects to those described for the above-mentioned changes in temperature.
Large areas of Europe would potentially be
affected by an increase in the climate suitability for Rhipicephalus spp. and H.
marginatum after an increase in temperature and decrease in rainfall.
Decreasing temperatures in Europe are
predicted to result in habitat loss for B.
annulatus, R. bursa, and H.
marginatum. Again, we must stress that this is an evaluation of the climate
suitability for these tick species, since changes in vegetation, host
availability, and animal movements were not included in the models.


## 5. Effects on Tick-Borne Diseases in Europe

All the
tick species considered in the earlier sections are important vectors of
disease and an increasing incidence of these diseases is the most significant
potential outcome of climate changes that affect ticks, directly or indirectly.
As described above, there is little doubt thatDermacentor reticulatus is currently extending its range and this
is reflected in the occurrence of canine babesiosis (caused by Babesia canis canis) in new areas (24,
25, 26, 27, 28). Hyalomma marginatum is
one of the vectors of Crimean-Congo hemorrhagic fever (CCHF), which occurs in
parts of Africa, Asia, the Middle East, and south-east Europe.
The largest epidemic on-record occurred in Turkey, which started in 2002 and
is still ongoing [47], and further north, a recent outbreak was reported in the
Balkans, another known endemic area [53], but there is no evidence as yet that
this disease is spreading further northwards. However, as discussed above, the
potential for the introduction and establishment of vector populations in areas
of predicted climate suitability is increasing.Rhipicephalus sanguineus is the primary vector of Mediterranean-spotted
fever (a rickettsial zoonosis caused by Rickettsia
conorii), and also Ehrlichia canis and Babesiacanis vogeli (causing, resp., rickettsial and protozoal diseases of
dogs). Although R. sanguineus can establish
in kennels in central and northern European latitudes, thus potentially causing
short-lived localized disease outbreaks, sufficient survival in the external
environment does not seem to occur for significant disease transmission in
northern temperate Europe. Nevertheless,
concerns about its possible introduction and establishment have prompted the authorities in some countries, such as the United Kingdom and Ireland, to make treatment against
ticks a component of the pet-passport scheme.Ixodes ricinus is the most abundant and widespread tick in Europe and
together with the Eurasian species, I.persulcatus,
transmits Lyme borreliosis (LB) and tick-borne encephalitis (TBE). LB occurs at
a relatively high incidence for a zoonotic disease, ranging from 155 per
100,000 in Slovenia to 0.6
per 100,000 in Ireland
[54]. However, it is difficult to statistically relate LB incidence to climate
change because the reliability of incidence data is uncertain due to diagnostic problems and
limited or absent reporting in most countries. Nevertheless, in some regions,
it has proved possible to relate disease incidence to climate, and a positive
association of incidence with mild winters and warm, humid summers was reported
in southern Sweden
[55]. The suggested effect of mild winters is possibly due to an extension of
the tick activity season, resulting in increased numbers of infected ticks
becoming available in the following year. Warm humid summers might result in a more
efficient transmission by the vector, but there is limited evidence for this
and the authors suggest that the observed increased LB incidence may be due to
increased human exposure in these conditions.Since TBE is notifiable in most countries where it occurs,
current incidence data are more reliable than those for LB, even though
reporting standards differ between countries and there are increasing
differences in TBE vaccination rates between countries. Increases in Swedish
cases since the mid-80s were associated with two consecutive years with milder
winters, earlier arrival of spring and prolonged autumn periods with
temperatures above5–8°C [13]. The
possibility that this is caused by climate effects on ticks is suggested by the
northward extension of I.ricinus distribution [11, 12].
Similarly, an upward movement of the TBE prevalence altitude ceiling
correlating with increasing temperatures has been reported [15, 56], which
accords with reports of increasing numbers of active ticks at higher altitudes
[15].Detecting climatic effects
on the incidence of LB and TBE in areas close to the latitude and altitude
distribution limits of the vector is less complex than in other parts of Europe where the direct and indirect impacts of climate
change on disease incidence are often confounded by other factors. Such studies
should either be based on reliable long-term historical datasets in an area
(e.g., the 40 year surveillance program for TBE in Stockholm County, Sweden
[13]) or based on data from different regions or countries, collected with
similar methodologies (e.g., vector sampling and analysis) and subject to
similar variations (e.g., TBE vaccination rates and reporting criteria). There
is a need for a pan-European surveillance network, for example based on the
abundance of infected vectors, as suggested by WHO [57].Randolph et al. [58] correlated the occurrence of
synchronous activity of I. ricinus larvae
and nymphs (resulting in cofeeding transmission) with that of TBE cases, and
also reported a relationship between these two variables and the rate of
decline of autumn temperatures. It, therefore, seems likely that climate change
will affect the dynamics of TBE transmission, thus altering the distribution of the disease [59], but the exact mechanisms of this interaction remain
to be elucidated.Despite the ready availability of data on TBE incidence, a firm causal
relationship with climate change remains elusive. A detailed study of the
records of TBE incidence over the last 2-3 decades in
Estonia, Latvia, and Lithuania showed that although TBE incidence rose
dramatically in some areas, there was so much heterogeneity in the data that it
was impossible to identify climate change as the main factor driving increased
disease incidence. It was concluded that the many socioeconomic changes arising
from the end of Soviet rule probably acted synergistically with climate factors
to increase TBE incidence [60].


## 6. Conclusions

Transmission
of infection occurs when thereis an overlap of activities between
reservoir, vector, and humans, and differs according to the pathogens and the
location. Climate change may impact all of these stages and their
interactions.
Although changes in climate and in the length
of the different seasons will directly affect tick survival, activity, and
development, there is no good evidence that rising temperatures will result in
a greater abundance of ticks by simply increasing rates of development; rather
changes in development rates will make tick cohorts available to different
diapause windows (largely determined by day length), thus changing patterns of
seasonal activity [38]. Indirect effects of climate change will impact the
number of infected ticks by affecting vegetation. For example, a warming
climate in central Europe is likely to result in a decrease of Norway spruce (Picea abies) and the areas involved will
probably be colonized by beech (Fagus
sylvatica) [61], the fallen leaves of which provide a favorable
microclimate for survival of the free-living tick stages. Additionally, climate
change will also have indirect effects on tick-borne pathogen transmission by
affecting the survival and abundance of tick maintenance hosts, such as deer,
and pathogen-reservoir hosts such as rodents and birds. Climate change may also
influence disease risk by affecting the long-term use of land (e.g., farming,
tourism, etc.), and weather patterns have an effect by influencing short-term
human behavior such as picnics and mushroom picking. Climate effects are more
easily noticeable close to the geographical distribution limits of both vector
and disease. The magnitude of the effects of climate change in an endemic area
depends on local conditions and vulnerability, and is determined not only by
ecological conditions but may be influenced by socioeconomic factors, human
migration and settlement, ecosystems and biodiversity, migrating patterns of
birds, land-use and land cover changes, human cultural and behavioral patterns,
and immunity in the population. Since some of these conditions are in turn
influenced by climate change, a complex chain of processes exists that makes
the precise factors responsible for changes in disease incidence often
difficult to determine [54]. A further difficulty in determining future
scenarios is presented by the fact that the predominant tick species in Europe, Ixodes ricinus is extremely flexible
and adaptable and can exhibit rather different seasonal activity even in
adjacent parts of its geographical range. Much current research effort attempts
to match datasets collected for different purposes and in order to reduce
confounding variables, it is evident that data from long-term studies on
disease incidence, tick biology, tick distribution and tick abundance, host
abundance and distribution, and relevant vegetation biology, specifically in
relation to climate change, are required [62]. Such data will permit the
development of models to predict future tick-borne disease scenarios, which
take account of dynamic biological processes instead of simply the likelihood
of occurrence of climate suitability for particular tick species.



---

*Source: 593232-2009-01-04.xml*