PhD THESIS
Contribution to the ecology and
taxonomy of ixodid ticks in Europe
and Africa
(SUMMARY OF THE Ph.D. THESIS)
Ph.D. Student Gianluca D’Amico
Scientific coordinators Associate Prof. Dipl. ECZM Dr.
Andrei D. Mihalca
Contribution to the ecology and taxonomy of ixodid ticks in Europe and Africa
SUMMARY
Ticks are obligate hematophagous parasites of the terrestrial vertebrates. Many
species are of major interest, their importance residing in their ability to act as vector
for numerous species of pathogens infecting animals and humans (Walker et al., 2000).
Ticks are part of phylum Arthropoda, class Arachnida. This class includes
spiders, scorpions, as well as the order Acari, which comprises several species of mites
and ticks. Within the Acari, the suborder Ixodida consists in three families of ticks:
Argasidae, Nuttalliellidae and Ixodidae (Walker et al., 2000).
Within the Ixodidae family, genus Rhipicephalus is one of the most well
represented, including 74 recognized species. Rhipicephalus is mainly an African origin
genus, with only ten species known exclusively outside the Afrotropical regions.
However, of all species, R. sanguineus is the most widely distributed (Walker et al.,
2000). The contemporary concept regarding the R. sanguineus group has been initiated
by Feldman-Muhsam (1952), Hoogstraal (1956), Morel and Vassiliades (1963) and
Filippova (1997), based on the pioneer ideas of Russian authors, such as Pomerantzev.
The taxonomic position of the R. sanguineus group of ticks is still under debate. The
biosystematics status of these species is difficult to determine, especially by
morphology, because the phenotypical methods are not sufficient to differentiate all
members of the group (Oliveira et al., 2005). The domestic dog is the typical host for R.
sanguineus, both in rural and urban areas (Szabó et al. 2001; Dantas-Torres et al.,
2004; Dantas-Torres et al. 2009). Occasionally, it may infest a large variety of domestic
or wild animals, such as cats, rodents, birds and humans. R. sanguineus ticks may act as
vectors and reservoirs for certain pathogens (e.g. Rickettsia conorii, Ehrlichia canis,
Babesia vogeli, Anaplasma platys, etc.) (Dantas-Torres, 2007). The role of R. sanguineus
ticks in transmission of pathogens to humans is well documented, despite their low
anthropophilia (Palmas et al., 2001). They are known vectors of Rickettsia rickettsii, the
agent of Rocky Mountains Spotted Fever in the USA (Demma et al., 2005). In the
Mediterranean regions, R. sanguineus are vectors and reservoirs of Rickettsia conorii,
agent of Mediterranean Spotted Fever (Matsumoto et al., 2005).
Rhipicephalus rossicus species is included in the R. sanguineus group. First
description was done after collection from hedgehogs and rats in the Russia. In 1928,
Olenev reported this species as similar to R. sanguineus. In 1939, Zumpt suggested that
it is a subspecies of R. sanguineus (R. sanguineus rossicus). In 1956, Shatas described
the immature stages (Mihalca et al., 2015). During 1920–1930, different Russian
authors divided R. sanguineus group into different branches: the ‘sanguineus branch’
and the ‘rossicus branch’ (Morel and Vassiliades, 1963; Saratsiotis, 1981). Nowadays,
R. rossicus is considered a valid tick species (Kolonin, 2009; Guglielmone et al., 2010;
Mihalca et al., 2015). However, in the last several past years, due to its close
morphological similarities, it is likely that R. rossicus has been misidentified as R.
I
Gianluca D’Amico
sanguineus, especially in areas where their distribution overlap (Kolomietz, 1936;
Dumitrache et al., 2014; Mihalca et al., 2015). R. rossicus was reported in Eurasian
steppe regions, (e.g. Armenia, Bulgaria, Romania, Ukraine, Uzbekistan, Azerbaijan,
China, Dagestan, Egypt, Georgia, Iran, Israel, Kazakhstan, Tajikistan, Moldavia, Poland,
Russia and Turkey) (Mihalca et al., 2015). The vectorial importance of R. rossicus may
be significantly higher than is currently recognized, and should be deeply investigated
(Mihalca et al., 2015).
Ticks of the genus Ixodes are worldwide distributed and have a vectorial role for
several important zoonoses. The morphological characteristics used for identification
are often ambiguous, and they can only be used for determination of adults. Molecular
tools (DNA sequences) and morphological redescriptions offer an important insight for
better understanding the specific vectorial role of each species (Caporale et al., 1995).
There is a gap in information regarding the ticks of genus Ixodes in Africa. Other
than descriptions of some stages for most of the species, as available by Arthur (1965)
and additional records provided by Morel (1966), and Elbl and Anastos (1966), most
data regarding distribution, ecology, host preferences, medical implications and
molecular phylogenies, are missing. This is the case of I. aulacodi described originally
by Arthur (1956).
To date more than 700 different hard tick species have been described
worldwide (Guglielmone et al. 2014), and more than 60 Ixodid species can be found in
Europe.
Wild animals play a major role in the eco-epidemiology of tick-borne diseases,
as they may act as reservoir or amplifying host for different pathogens (Lorusso et al.,
2011). Different economic and ecological factors, as changing of the agricultural
practices or environmental changes, lead to a broader distribution area of the wild
hosts and vectors, facilitating the transfer of pathogens between wild and domestic
animals (Bengis et al., 2004). Among wildlife, the wild carnivores are difficult to
monitor and capture (Gese, 2001), reason why tick-host associations are hard to be
identified. In Romania studies regarding wildlife-ticks distribution are scarce and
dated.
The morphological identification of ticks is not a trivial issue as some species
form species-complexes with cryptic of sibling species, i.e. R. sanguineus group
(Dantas-Torres et al. 2013). Even in a thoroughly surveyed area like Europe, new
species have been recently described (i.e. I. inopinatus or I. ariadnae). Moreover,
morphological keys for ticks commonly cover only the species with medical interest,
not every stages being included. The use of adequate genetic markers will always be
based on the use of reference specimens for which morphological species-specific
identification have been correctly conducted (Nava et al., 2009; Araya-Ancheta et al.,
2015). Blind tests are often applied for the unbiased identification of organisms, in
order to compare the degree of similarity between the opinion of several specialists
about the morphology and classification of organisms, and to try to overcome
misidentifications.
II
Contribution to the ecology and taxonomy of ixodid ticks in Europe and Africa
The main objectives of this Phd thesis were:
 To evaluate the community structure of ticks in Africa (Lake Turkana region),
in order to provide an insight into the ecology and seasonality of ticks
collected in localities with an extreme range of ecological conditions.
 To identify the most dominant tick species in dogs in Romania (Danube Delta)
in order to assess the possible emergence of associated pathogens.
 To assess the tick communities parasitizing on dogs and to provide new data
regarding seasonal dynamics of a neglected, but widely distributed steppe tick,
Rhipicephalus rossicus in a locality of Danube Delta Biosphere Reserve.
 To identify tick species collected from hunted or road-killed wild carnivores in
order to complement and confirm the sparse information currently available
and to establish reliable data on tick-host associations.
 To identify the diversity of tick species found the subcutaneous tissues of red
foxes (Vulpes Vulpes), and to describe the lesions for understanding the
mechanism of subcutaneous localization.
 To describe the male and redescribe the female of Ixodes aulacodi tick species
and to provide the 16S rDNA sequence for this species.
 To test the reliability of a blind test of morphological identification of ticks
reported in Europe and Northern Africa, by several teams of European experts
and to compare their identification skills; to estimate the rate of confidence of
the participants with their identifications as compared with the rate of
mismatches, a ratio that express how efficiently the experts can manage the
threat derived by ticks; to evaluate the reliability and usability of a new
comprehensive key for all European ticks before its final publication as a book.
The reaserch included in this PhD thesis was coordinated by the University of
Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Faculty of Veterinary
Medicine, Department on Parasitology and Parasitic Diseases, in collaboration with
other European Universities and different specialized laboratories, between 2012 and
2016.
This PhD thesis is structured in two main parts: literature review containing one
chapter and original reaserch containing seven chapters. The length of the thesis is 149
pages, including a number of 9 tables, 17 figures and 360 references.
The first part (literature review), includes Chapter I.1, describing the general
charateristics of ixodid ticks.
The second part (original research) includes the main objectives of the PhD
thesis, followed by chapters II.1-II.7 including the original research. The general
conclusions and recommendations are included in Chapter II.8 and the originality and
innovative contributions in Chapter II.9.
III
Gianluca D’Amico
In Chapter II.1, we evaluated the community structure of ticks in Africa (Lake
Turkana region); in addition, it was assessed the ecology and seasonality of ticks
collected in localities with an extreme range of ecological conditions: from hot desert
to mist afromontane forest. Our research was based on a long-term screening of ticks
parasitising the domestic dogs living with indigenous people around Lake Turkana, Mt.
Kulal and Mt. Nyiru areas, Northern Kenya. A total of 9977 ticks were collected from
1464 dogs of all ages and both sexes. Identification was performed using
morphological keys and data were analyzed using the Repeated Measures ANOVA,
post-hoc Scheffe test and F test, relating independent variables as seasons and regions.
Final results were translated to maps using GIS software (D’Amico et al., 2015). Five
species of ticks were identified: Rhipicephalus pulchellus, Rhipicephalus sanguineus
sensu lato (s.l.), Rhipicephalus armatus, Amblyomma gemma and Hyalomma truncatum.
Our results suggest a statistical difference of the tick community structure related to
seasonal and altitudinal distribution. Parasitism with R. armatus and R. pulchellus was
higher in September-October than in January, whereas, R. sanguineus s.l. was not
influenced by the season. Rhipicephalus armatus was present exclusively on dogs living
in semi-desert areas, while R. sanguineus s.l. was the dominant species present on the
shores of Lake Turkana. Although R. pulchellus was present in the all studied areas, this
species had a significantly higher abundance in the afromontane region of Mt. Kulal
and montane xeromorphic forest of Mt. Nyiru; these regions are characterized by
elevated humidity and cooler climate. Similar geo-climatic distribution is typical also
for A. gemma, which was found in dogs exclusively in Mt. Kulal afromontane area. The
current work represents the most extensive study performed on the tick community
structure of dogs in Eastern Africa. The results showed a relatively limited tick species
diversity, with clear seasonal differences and altitudinal distribution (D’Amico et al.,
2015).
Chapter II.2 presents data which highlight the dominance of Rhipicephalus
rossicus in dogs from Romania, with importance for the possible emergence of
associated pathogens. Changes in the distribution of tick species are among the major
causes for the increase in prevalence of zoonotic diseases worldwide, twith tick-borne
diseases’ prevalence showing an emerging pattern. One of these ticks, R. rossicus,
which is reported occasionally from humans, seems to be particularly interesting
because of its demonstrated vectorial role for zoonotic pathogens like Francisella
tularensis, Coxiella burnetii, or CCHF and West Nile viruses (Sándor et al., 2014). Here
we report a case of dominant occurrence of R. rossicus on household dogs in the
wetlands of Eastern Europe (Romania). Ticks were collected from dogs in 5 distinct
locations, with 1068 ticks of 6 species found. R. rossicus had a dominant occurrence in
dogs in all but one location, accounting for 87.1% of all ticks (32.3–95.3% in different
locations). Until this study, R. sanguineus was considered as the only important tick
species on dogs in south-temperate regions of Europe, as well in Romania. The
dominant presence of R. rossicus
IV
Contribution to the ecology and taxonomy of ixodid ticks in Europe and Africa
in dogs, its vectorial competence and broad host spectrum (including humans), make
this tick species an important candidate for further analysis and highlight the paucity
of our knowledge on disease vectors in this region of Europe (Sándor et al., 2014).
Chapter II.3 shows the seasonal dynamics of Rhipicephalus rossicus attacking
domestic dogs from the steppic region of southeastern Romania. Danube Delta
Biosphere Reserve is one of the most interesting regions in Europe from an
epidemiological point of view due to its great biodiversity, local climatic conditions and
various types of habitats. Moreover, there is no data regarding the ectoparasite
communities of dogs from this area. In this frame, the aims of our study were to
establish the tick communities parasitizing dogs and to provide new data regarding
seasonal dynamics of a neglected tick species, R. rossicus (Dumitrache et al., 2014). A
survey was carried out in order to gather information regarding tick species attaching
to domestic dogs from a steppic region of southeastern Romania and to establish their
seasonal dynamics. The research was conducted from 1 December 2012 to 30
November 2013, on 8 dogs from Iazurile, a locality from the west-central part of the
Danube Delta Biosphere Reserve. In total, 384 examinations were made, each dog
being checked for tick infestation 4 times per month, for one year. The 893 ticks found
belonged to six species: R. rossicus (95.6%), Dermacentor reticulatus (3.2%), Ixodes
ricinus (0.5%), Hyalomma marginatum (0.3%), R. sanguineus sensu lato (s.l.) (0.2%)
and I. crenulatus (0.1%). From the 91 positive examinations, R. rossicus was found in
80 (87.9%). Single species infestation occurred in 84 examinations. In 7 out of 91
positive examinations mixed infestation were found. No ticks were found in December,
January and September. For R. rossicus, high frequency and intensity were observed in
May, June and July. The activity peaks for D. reticulatus were in spring and autumn. Our
results highlight that within the range of R. sanguineus s.l., the most common dog tick
worldwide, selected dog populations may be predominantly infested by closely related
species, like in our case, R. rossicus (Dumitrache et al., 2014).
Chapter II.4 provides new data regarding hard-tick diversity and tick-host
associations in wildlife in Romania. This study aim was to identify tick species in wild
carnivores and to establish reliable data on tick-host association The study was
conducted in different Romanian localities from all 5 ecoregions found in the country.
Fourteen species of wild carnivores were examined. Immature and adult ticks were
collected and identified using the morphological keys. The frequency and mean
intensity of ticks, overall and differentiated by species, developmental stage and hosts
were calculated. Of 202 wild carnivores, 68 were parasitized by ticks. The mean
intensity of tick infestation was similar in males (6.97, BCa 95% CI: 5.15-9.88) and
females (5.76, BCa 95% CI: 4.15-9.17). The highest prevalence of infested animals was
recorded in panonian and steppic ecoregions, 66.7% and 52.7%, respectively. In
continental regions the prevalence was 26.7%, while in pontic ecoregion was 28%. The
lowest value, 16.7% was recorded in the alpine biogeographical region.
V
Gianluca D’Amico
A total number of 430 ticks were collected, and 24.8% of the animals were infested
with more than one tick species. 14 new tick-host association were recorded. Our
results suggest that antrophogenic changes of the environment lead to the diminishing
of the boundaries, between wild and domestic animals, increasing the exposure for
both animals and humans, to infective agents, including tick-borne pathogens.
Chapter II.5 describes unsual findings observed during an extensive survey of
parasites in red foxes (Vulpes vulpes) that was conducted in the Czech Republic.
Carcasses were examined by necropsy, and occasionally small, dark nodules
apparently containing ticks were observed in the subcutaneous tissue of several foxes.
A similar finding was observed in a red fox in Romania. Histopathological examination
was performed using hematoxylin and eosin staining. Of the 91 foxes examined from
the Czech Republic, 14 (15.4 %) were harboring ticks in the subcutaneous tissue. In the
majority of these cases, 1 to 3 nodules/fox were found, with a maximum of 31
nodules/fox. In the Romanian fox were also identified subcutaneous ticks. All ticks
collected from subcutaneous tissue were partially engorged adults. Based on
morphological features, Ixodes ricinus, I. hexagonus, I. crenulatus and Dermacentor
reticulatus were identified. The histopathological examination revealed chronic
granulomatous panniculitis with peripheral fibrosis and intralesional presence of the
ticks. Only few data are available regarding ticks localized in the subcutaneous tissue
of any host. All the ticks were dead or already decomposed and it is evident that
subcutaneous location does not represent an evolutionary advantage, as the
detachment and finishing the life cycle is impossible.
Chapter II.6 reports the description of the male, redescription of the female
and 16S rDNA sequence of Ixodes aulacodi Arthur, 1956 (Ixodidae). This tick species is
a poorly known species that has been recorded predominantly in the wet countries of
western and central Africa, mainly associated to the greater cane rat Thryonomys
swinderianus (Temmink). We redescribed the female, described the male (ascribed to
the species from specimens found in copula) and provide the 16S rDNA sequence. We
also provide complete illustrations of the adults based on specimens found on greater
cane rats in Ivory Coast. I. aulacodi is included in the group of species of the subgenus
Afrixodes that have horseshoe shaped anal groove, and which lack auriculae and
cornua. The female is easily separated when compared with other species because of a
unique combination of characters: All the coxae have internal spurs, coxa II has two
external
spurs, syncoxae are absent, and trochanters I-III have one spur each. The male has a
notched hypostome and lacks syncoxae, auriculae and cornua (Chiţimia-Dobler et al.,
2016).
Given the importance of tick identification for public health, the last chapter
(II.7) reports the results of a blind test of ixodid tick identification by European
experts. The most prevalent tick species in Western Europe and Northern Africa were
included in the study. A total of 15 laboratories were voluntarily enrolled in the test.
Each
VI
Contribution to the ecology and taxonomy of ixodid ticks in Europe and Africa
participant received between 22 and 25 specimens of adult ticks of the species
Dermacentor marginatus, D. reticulatus, Haemaphysalis punctata, Ixodes ricinus, I.
hexagonus, Hyalomma lusitanicum, H. marginatum, Rhipicephalus annulatus, R. bursa, R.
sanguineus s.l., and/or R. rossicus, which were randomly selected and blindly
distributed among the participants together with a questionnaire. Only specimens
collected while questing and, if possible, in the same survey, were circulated. Because
of the random nature of the test, a participant could receive several specimens of the
same species. Ticks were morphologically identified by three of the co-authors and
identification confirmed by a fourth co-author who used molecular methods based on
several genes. Species in the different genera had variable misidentification rates (MR)
of 7% (Dermacentor), 19% (Haemaphysalis), 36% (Hyalomma) 14% (Ixodes), and 54%
(Rhipicephalus). Within genera, the MR was also variable ranging from 5.4% for I.
ricinus or 7.4% for D. marginatus or D. reticulatus to 100% for R. rossicus. The test
provided a total misidentification rate of 29% of the species of ticks. There are no
significant differences in MR according to the sex of the tick. Participants were
requested to perform a second round of identifications on the same set of ticks, using
only purposely prepared keys (without illustrations), circulated to the enrolled
participants, with details on 2 species of the genus Dermacentor, 8 of Haemaphysalis,
10 of Hyalomma, 23 of Ixodes, and 6 of Rhipicephalus. The average MR in the second
round was 28%: 0% (Dermacentor), 33% (Haemaphysalis), 30% (Hyalomma) 18%
(Ixodes), and 50% (Rhipicephalus). Species which are non-endemic in the countries of
the participating laboratories had always highest MR, i.e. purely Mediterranean species
had highest MR by laboratories in Central and Northern Europe. Participants
expressed their concerns about a correct identification for almost the 50% of the ticks
of the genera Hyalomma and Rhipicephalus. Interestingly, participants expressed a
total confidence in the identification of the 100% of erroneously identified Ixodes spp.
The results show a lack of adequate knowledge of the identity of the most prominent
species of ticks in the Western Palearctic, and underpin the need of adequate reference
libraries for specialists involved in the identification of ticks. Results also showed that
an adequate combination of several genes may adequately identify the target species of
ticks.
The general conclusions were:
 Analysis of the tick community structure of dogs in Eastern Africa showed a
relatively limited tick species diversity, with a clear seasonal and altitudinal
distribution. The dominant species in the afromontane region was R.
pulchellus, while in the desert areas, the dominant species was R. sanguineus
s.l..
 Analysis of tick community structure in dogs in the Eurasian steppic region of
Danube Delta showed that the ticks collected from different dog populations
VII
Gianluca D’Amico
were predominately R. rossicus, a tick species closely related to R. sanguineus
s.l.. As the vectorial role of R. rossicus for important canine pathogens has not
been evaluated yet, our results highlight the importance of a correct
identification in order to overcome possible emergence diseases.
 The dominant presence of R. rossicus in dogs in Danube Delta, its vectorial
competence and broad host spectrum (including humans), make this tick
species an important candidate for further analysis and highlight the paucity
of our knowledge on disease vectors in this region of Europe.
 Our study of ticks species parasitizing wild carnivores in Romania suggest that
biotic homogenization leads to different changes on pathogens ecology and
distribution, and to an increased exposure of both animals and humans, to
infective agents, including tick-borne pathogens. These findings highlight the
imperative need of surveillance of disease that may be transmitted by wild
carnivores, especially in areas where they are limited or absent.
 Occurrence of subcutaneous ticks in red foxes (Vulpes vulpes) may be the
result of different factors contribution (deep embedment, long feeding time
and increased reactivity of fox skin). It is hard to assume that this location
represents an evolutionary advantage as their detachment and finishing the
life cycle is impossible.
 Description of the male, re-description of the female, and providing the 16S
rDNA sequence of Ixodes aulacodi complete the existing information of this
representative tick species of the subgenus Afrixodes. Given the paucity of
molecular data for this branch of the genus Ixodes, the 16S sequence we
provided should be considered as a first approach to the molecular
characterization of the African Ixodes.
 While the awareness about ticks and tick-borne pathogens increases
worldwide, there is a lack of adequate knowledge about the identity of the
most prominent species. Although some tick species may lack interest in
circulating pathogens, they must be considered confusing entities when
compared with the focal species, introducing noise in reporting. Our results of
the blind test performed by experts are claiming about the need of adequate
training ticks identification, a step necessary either to address epidemiological
studies or to cope with the risk by invasive species.
VIII
Contribution to the ecology and taxonomy of ixodid ticks in Europe and Africa
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
ARAYA-ANCHETTA. A., BUSCH, J. D., SCOLES, G. A., WAGNER, D. M. 2015, Thirty years of
tick population genetics: A comprehensive review. Inf Gen Evol, 29, 164-179.
BENGIS R. G., LEIGHTON F. A., FISCHER J. R., ARTOIS M., MÖRNER T., TATE C. M. 2004, The
role of wildlife in emerging and re-emerging zoonoses. Revue scientifique et technique de
l’Office International des Epizooties, 23(2), 497-511.
CAPORALE, D. A., RICH, S. M., SPIELMAN, A., TELFORD, S. R., KOCHER, T. D. 1995.
Discriminating between Ixodes ticks by means of mitochondrial DNA sequences. Mol
Phylogenet Evol, 4(4), 361-365.
CHIŢIMIA-DOBLER, L., D'AMICO, G., YAO, P. K., KALMÁR, Z., GHERMAN, C. M., MIHALCA, A.
D., ESTRADA-PEÑA, A. 2016, Description of the male, redescription of the female and 16S
rDNA sequence of Ixodes aulacodi (Ixodidae). Ticks Tick Borne Dis, 7(3), 433-8.
D'AMICO, G., DUMITRACHE, M. O., ŠIROKÝ, P., ALBRECHTOVÁ, K., SLOBODA, M., DOMŞA, C.,
SÁNDOR, A. D., BALÁZSI, R., KANYARI, P. W., MODRÝ, D., MIHALCA, A. D. 2015, Altitudinal
and seasonal differences of tick communities in dogs from pastoralist tribes of Northern
Kenya. Vet Parasitol, 212(3-4), 318-23.
DANTAS-TORRES, F. 2007, Rocky Mountain spotted fever. Lancet Infect Dis, 7, 724-732.
DANTAS-TORRES, F., FIGUEREDO, L. A., FAUSTINO, M. A. G. 2004, Ectoparasitos de cães
provenientes de alguns municípios da Região Metropolitana do Recife, Pernambuco, Brasil.
Rev Bras Parasitol Vet, 13, 151-154.
DANTAS-TORRES, F., LATROFA, M.S., ANNOSCIA, G., GIANNELLI, A., PARISI, A., OTRANTO,
D. 2013, Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from
the New and Old Worlds. Parasit Vector, 6, 213.
DANTAS-TORRES, F., MELO, M. F., FIGUEREDO, L. A., BRANDÃO-FILHO, S. P. 2009,
Ectoparasite infestation on rural dogs in the municipality of São Vicente Férrer,
Pernambuco, Northeastern Brazil. Rev Bras Parasitol Vet, 18, 75-77.
DEMMA, L. J., TRAEGER, M. S., NICHOLSON, W. L., PADDOCK, C. D., BLAU, D. M., EREMEEVA,
M. E., DASCH, G. A., LEVIN, M. L., SINGLETON, JR., J., ZAKI, S. R., CHEEK, J. E., SWERDLOW, D.
L., MCQUISTON, J. H. 2005, Rocky Mountain spotted fever from an unexpected tick vector
in Arizona. N Engl J Med, 353, 587-594.
DUMITRACHE, M. O., KISS, J. B., DANTAS-TORRES, F., LATROFA, M. S., D’AMICO, G.,
SÁNDOR, A. D., MIHALCA, A. D. 2014, Seasonal dynamics of ky attacking domestic dogs
from the steppic region of southeastern Romania. Parasit Vector, 7, 97.
FELDMAN-MUHSAM, B. 1952, On the identity of Rhipicephalus sanguineus. Lat Bull Res
Counc Israel, 2, 187-194.
FILIPPOVA, N. A. 1997, Fauna of Russia and neighbouring countries. Arachnoidea, Ixodid
ticks of subfamily Amblyomminae. Russian Academy of Sciences, Zoological Institute,
Nauka Publishing House, St Petersburg, New Series 145, IV(5).
GESE, E. M. 2001, Monitoring of terrestrial carnivore populations. USDA National Wildlife
Research Center-Staff Publications, 576.
IX
Gianluca D’Amico
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
GUGLIELMONE, A. A., ROBBINS, G. R., APANASKEVICH A. D., PETNEY, N. T., ESTRADAPEÑA, A., HORAK, G. I., RENFU, S., BARKER, C. S. 2010, The Argasidae, Ixodidae and
Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa, 2528, 128.
GUGLIELMONE, A.A., ROBBINS, R.G., APANASKEVICH, D.A., PETNEY, T.N., ESTRADA-PEÑA,
A., HORAK, I.G. 2014, The Hard Ticks of the World. Ed. Springer, pp. 738.
HOOGSTRAAL, H. 1956, African Ixodoidea. I. Ticks of the Sudan (with Special Reference to
Equatoria Province and with Preliminary Reviews of the Genera Boophilus,
KOLOMIETZ, J. S. 1936, Zur Frage der Verbreitung und Lebensweise der Zecke
Rhipicephalus rossicus Yak. Und Koh.-Yak. in der Ukraine. Zeitschrift für Parasitenkunde, 8,
538-541.
KOLONIN, G. V. 2009, Fauna of ixodid ticks of the world (Acari, Ixodidae).
http://www.kolonin.org. Accessed 5 December 2013.
LORUSSO, V., LIA, R. P., DANTAS-TORRES, F., MALLIA, E., RAVAGNAN, S., CAPELLI, G.,
OTRANTO D. 2011, Ixodid ticks of road-killed wildlife species in southern Italy: new tickhost associations and locality records. Exp Appl Acarol, 55, 293-300.
MATSUMOTO, K., BROUQUI, P., RAOULT, D., PAROLA, P. 2005, Experimental infection
models of ticks of the Rhipicephalus sanguineus group with Rickettsia conorii. Vect Borne
Zoonotic Dis, 5, 363-372.
MIHALCA, A. D., KALMÁR, Z., DUMITRACHE, M. O., 2015, Rhipicephalus rossicus, a neglected
tick at the margin of Europe: a review of its distribution, ecology and medical importance.
Med Vet Entomol, doi: 10.1111/mve.12112.
MOREL, P.C., VASSILIADES, G. 1963, Les Rhipicephalus du groupe sanguineus: espéces
Africaines (Acariens: Ixodoidea). Rev Elev Med Vet Pay, 15, 343-386.
NAVA, S., GUGLIELMONE, A. A., MANGOLD, A. J. 2009, An overview of systematics and
evolution of ticks. Frontiers Biosci, 14, 2857-2877.
OLENEV, N.O. 1928, Determination of ticks of the family Ixodidae Murray of the U.S.S.R.
Doklady Akademii Nauk SSSR, 16, 84-96.
OLIVEIRA, P. R., BECHARA, G. H., DENARDI, S. E., SAITO, K. C., NUNES, E. T., SZABÓ, M. P.,
MATHIAS, M. I., 2005, Comparison of the external morphology of Rhipicephalus sanguineus
(Latreille, 1806) (Acari: Ixodidae) ticks from Brazil and Argentina. Vet Parasitol, 129, 139147.
PALMAS, C., BORTOLETTI, G., CONCHEDDA, M., CONTINI, C., GABRIELE, F., ECCA, A. R.
2001, Study on immunobiology in ectoparasites of public health interest: Rhipicephalus
sanguineus. Parassitologia, 43, 29.
SÁNDOR, A. D., DUMITRACHE, D. O., D’AMICO, G., KISS, B. J., MIHALCA, A. D. 2014,
Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the
wetlands of the Danube Delta, Romania. Vet Parasitol, 204(3-4), 430-432.
SARATSIOTIS, A. G. 1981, Étude morphologique et biologique de Rhipicephalus moucheti
Morel, 1964, groupe de Rh. sanguineus (Acariens: Ixodoidea), espèce africaine. Acarologia,
12, 15-24.
SHATAS, Y. F. 1956, Larvae and nymphs of some species of the genus Rhipicephalus Koch
(Acarina, Ixodidae). Entomological Review, 35, 944-955.
SZABÓ, M. P., CUNHA, T. M., PINTER, A., VICENTINI, F. 2001, Ticks (Acari: Ixodidae)
associated with domestic dogs in Franca region, São Paulo, Brazil. Exp Appl Acarol, 25, 909916.
X
Contribution to the ecology and taxonomy of ixodid ticks in Europe and Africa
32.
33.
WALKER, J.B., KEIRANS, J.E., HORAK, I.G. 2000, The Genus Rhipicephalus (Acari, Ixodidae):
A Guide to the Brown Ticks of the World. Ed. Cambridge University Press, pp. 1-643.
ZUMPT, F. 1939, Die Rhipicephalus-Arten der USSR, ein Beitrag zur Variabilitat in der
Sanguineus-Gruppe. I. Vorstudie zu einer Revision der Gattung Rhipicephalus Koch. Z
Parasitenkd, 11, 400-409.
XI
Gianluca D’Amico
XII