- Email: [email protected]
Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta, Romania
Accepted Manuscript Title: Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta, Romania Author: Attila D. S´andor Mirabela O. Dumitrache Gianluca D’amico Botond J. Kiss Andrei D. Mihalca PII: DOI: Reference:
S0304-4017(14)00284-2 http://dx.doi.org/doi:10.1016/j.vetpar.2014.05.005 VETPAR 7241
To appear in:
Veterinary Parasitology
Received date: Revised date: Accepted date:
30-1-2014 7-5-2014 8-5-2014
Please cite this article as: S´andor, A.D., Dumitrache, M.O., D’amico, G., Kiss, B.J., Mihalca, A.D.,Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta, Romania, Veterinary Parasitology (2014), http://dx.doi.org/10.1016/j.vetpar.2014.05.005 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1 2
Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta, Romania
3 Attila D. SÁNDOR1, Mirabela O. DUMITRACHE1*, Gianluca D’AMICO1, Botond J. KISS2, Andrei D. MIHALCA1
6 7 8
1
cr
University of Agricultural Sciences and Veterinary Medicine, Faculty of Veterinary Medicine, Department of Parasitology and Parasitic Diseases, Calea Mănă tur 3-5, ClujNapoca 400372, Romania 2
Danube Delta National Institute for Research and Development, Str. Babadag 165, Tulcea 820112, Romania.
us
9 10
ip t
4 5
11
* Corresponding author: Mirabela O. DUMITRACHE, Address: Calea Mănăştur 3-5, ClujNapoca 400372, Romania; Tel: +40264596384; Fax: +40264593792; Email:[email protected])
an
12 13 14
M
15 Abstract
17 18 19 20 21 22 23 24 25 26 27 28 29 30
Changes in the distribution of tick species are among the major causes for the increase in prevalence of zoonotic diseases worldwide, with tick-borne diseases’ prevalence showing an emerging pattern. One of these ticks, Rhipicephalus 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. Here we report a case of dominant occurrence of Rhipicephalus 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. Rhipicephalus rossicus had a dominant occurrence in dogs in all but one location, accounting for 87.1% of all ticks (32.395.3% 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 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.
Ac ce p
te
d
16
31 32
Keywords: Rhipicephalus rossicus, Eastern Europe, tick, dog
33
1
Page 1 of 8
Main text
35
Ticks harbor more zoonotic pathogens than any other blood-feeding arthropod species
36
globally and they are the second most important vectors of epidemic importance after
37
mosquitoes. Ticks are known vectors for medically important viral diseases like tick-borne
38
encephalitis, louping ill, Crimean-Congo hemorrhagic fever (CCHF), Colorado tick fever,
39
and bacterial diseases, like Lyme disease, tick-borne relapsing fever, Mediterranean spotted
40
fever and Q-fever just to name a few (Dantas-Torres et al., 2012). Moreover, ticks transmit a
41
high number of pathogens affecting livestock and companion animals (Day, 2011; Smith and
42
Wall, 2013). Although most of these diseases have a long epidemiologic history and the
43
importance of ticks as vectors has been widely known, tick-borne diseases’ prevalence shows
44
an emerging pattern (Chomel, 2011; Salman et al., 2013). There are two main hypotheses
45
which explain this phenomenon: changes in geographical distribution of tick species and
46
increased contact of human population with ticks, caused by changes in human life-style
47
(Léger, 2013). Changes in the distribution of tick species are among the major causes for the
48
increase in prevalence of Lyme borreliosis, CCHF, tick-borne encephalitis or other vector-
49
borne infections of humans and domestic animals (Beugnet and Marie, 2009; Petney et al.,
50
2012). Most of the cases of tick species known to have recently increased their geographical
51
range are well documented in Western Europe and USA (Petney et al., 2012). However, there
52
is a lack of knowledge on the possible expansion of ticks with a more eastern distribution in
53
Europe. One of these ticks, Rhipicephalus rossicus, which is reported occasionally from
54
humans, seems to be particularly interesting because of its important demonstrated vectorial
55
role for zoonotic pathogens like Francisella tularensis, Coxiella burnetii, or CCHF and West
56
Nile viruses (Walker et al., 2000).
Ac ce p
te
d
M
an
us
cr
ip t
34
2
Page 2 of 8
Rhipicephalus rossicus is a tick with Eastern European and Western Asian distribution,
58
considered as being “rare”, with low prevalences in most studies reporting it (Walker et al.,
59
2000). Historically in Romania, it was recorded as an extremely rare tick, found only on
60
small mammals with only 4 known occurrences before 2012 (Feider, 1965; Mihalca et al.,
61
2012). Among domestic animals, dogs are probably the most important hosts, in general, for
62
ticks and tick-borne pathogens of human importance, due to their lifestyle and close contact
63
with people (Chomel, 2011). While R. sanguineus sensu lato (s.l.) is typically regarded as the
64
most common tick of dogs worldwide, the related species, R. rossicus is reported only
65
incidentally as a dog ectoparasite (Walker et al., 2000). We present here data which highlight
66
the dominance of R. rossicus in dogs from Romania, with importance to the possible
67
emergence of associated pathogens.
68
A total of 1068 ticks were collected from 84 household dogs between February 2012 and
69
November 2013. The collection occurred in five localities from the Danube Delta, SE
70
Romania (Figure 1), one of the largest wetland complexes of Europe. The region is primarily
71
of rural character, with important urban centers to the south (Constana) and north (Tulcea).
72
Dogs are commonly kept in households, with most individuals freely roaming around the
73
premises. Ticks were identified using morphological keys (Feider, 1965; Walker et al., 2000),
74
while identification was confirmed by molecular diagnostics based on 12S rDNA sequences
75
(Dumitrache et al., 2014). Six species of ticks were identified, with R. rossicus being found in
76
all five locations. Surprisingly, the dominant tick species was not R. sanguineus s.l., but R.
77
rossicus, accounting for 87.1% of all ticks (32.3-95.3% in different locations, see Table 1).
78
Rhipicephalus rossicus had the highest percent of occurrence in dogs in all but one location.
79
Rhipicephalus rossicus is a steppe and mountain steppe tick species, with a distribution from
80
Bulgaria and Romania to the east, occurring primarily in the Eurasian steppe zone to eastern
Ac ce p
te
d
M
an
us
cr
ip t
57
3
Page 3 of 8
Kazakhstan and western China. It is a three-host tick, with rodents, leporids and birds hosting
82
immature stages. Hedgehogs, hares, ungulates, horses and occasionally dogs and humans are
83
hosts of adults. All of these hosts are abundantly present in the area of the study. Although
84
previously recorded from dogs, it was primarily considered an important tick of wildlife and
85
domestic ungulates and its vectorial importance was treated as such (Walker et al., 2000). The
86
dominant presence in dogs from SE of Romania rises however a number of questions. Until
87
this study, R. sanguineus s.l. was considered as the only important tick species on dogs in
88
south-temperate regions of Europe (Walker et al., 2000), as well in Romania (Ioniă and
89
Mitrea, 2003). While R. sanguineus s.l. is a well-known vector for a great variety of
90
pathogens, its epidemiological importance for human pathogens is limited (Walker et al.,
91
2000). On the other hand, R. rossicus is a competent vector for CCHF, a disease only recently
92
reported from the study region (Ceianu et al., 2012). Moreover, R. rossicus seems to be more
93
common on humans than R. sanguineus s.l. (Walker et al., 2000), including in Romania
94
(Sándor, unpublished data).
te
d
M
an
us
cr
ip t
81
Ac ce p
95 96 97
Acknowledgements
98
For DMO this paper was supported by POSDRU/159/1.5/S/136893 project. For MAD, SAD
99
and GDA from grant PCE 236/2011. This study was conducted under the frame of the
100
EurNegVec COST Action TD1303. We would like to thank to C. Doma for the map in
101
Figure 1.
102 4
Page 4 of 8
103
References
104 Beugnet, F., Marie, J.L., 2009. Emerging arthropod-borne diseases of companion animals in
106
Europe. Vet. Parasitol. 163, 298–305.
107
Ceianu, C.S., Pănculescu-Gatej, R.I., Coudrier, D., Bouloy, M., 2012. First serologic
108
evidence for the circulation of Crimean-Congo hemorrhagic fever virus in Romania. Vector-
109
Borne Zoonotic. 12, 718–721.
110
Chomel, B., 2011. Tick-borne infections in dogs - an emerging infectious threat. Vet.
111
Parasitol. 179, 294–301.
112
Dantas-Torres, F., Chomel, B.B., Otranto, D., 2012. Ticks and tick-borne diseases: a One
113
Health perspective. Trends Parasitol. 28, 437–446.
114
Day, M.J. 2011. One health: the importance of companion animal vector-borne diseases.
115
Parasit Vector. 4,49.
116
Dumitrache, M.O., Kiss, J.B., Dantas-Torres, F., Latrofa, M.S., D’Amico, G., Sándor, A.D.,
117
Mihalca, A.D. 2014. Seasonal dynamics of Rhipicephalus rossicus attacking domestic dogs
118
from the steppic region of southeastern Romania. Parasit Vector 7, 97.
119
Feider, Z., 1965. Fauna of the Popular Republic of Romania. Volume 5/2. Acaromorpha,
120
Suprafamily Ixodoidea [in Romanian]. Ed. Academiei RPR, Bucureşti.
121
Földvári, G., Márialigeti, M., Solymosi, N., Lukács, Z., Majoros, G., Kósa, J.P., Farkas, R.,
122
2007. Hard ticks infesting dogs in Hungary and their infection with Babesia and Borrelia
123
species. Parasitol. Res. 101, 25–34.
Ac ce p
te
d
M
an
us
cr
ip t
105
5
Page 5 of 8
Ioniă, M., Mitrea, I.L., 2003. [Observations regarding the biological cycle of the brown dog
125
tick (Rhipicephalus sanguineus Latreille 1806 – Acari: Ixodidae), in the environmental
126
conditions of Bucureti region]. Scientia Parasitol. 4, 167–171. [in Romanian]
127
Léger, E., Vourc’h, G., Vial, L., Chevillon, C., McCoy, K.D., 2013. Changing distributions of
128
ticks: causes and consequences. Exp. Appl. Acarol. 59, 219–244.
129
Mihalca, A.D., Dumitrache, M.O., Magdaş, C., Gherman, C.M., Domşa, C., Mircean, V.,
130
Ghira, I.V., Pocora, V., Cozma, V., Sándor, A.D., 2012. Synopsis of the hard ticks (Acari:
131
Ixodidae) of Romania with update on host associations and geographical distribution. Exp.
132
Appl. Acarol. 58, 183–206.
133
Petney, T.N., Skuballa, J., Muders, S., Pfäffle, M., Zetlmeisl, C., Oehme, R., 2012. The
134
changing distribution patterns of ticks (Ixodida) in Europe in relation to emerging tick-borne
135
diseases. In: Arthropods as Vectors of Emerging Diseases Springer Berlin Heidelberg; p. 151–
136
166.
137
Salman, M., Estrada-Peña, A., Tarrés-Call, J. 2013. Emerging (Re-emerging) tick-borne
138
infections and the dissemination of ticks. Ticks and Tick-Borne Diseases: Geographical
139
Distribution and Control Strategies in the Euro-Asia Region, p.1–5.
140
Smith, F.D., Wall, L.E.R., 2013. Prevalence of Babesia and Anaplasma in ticks infesting dogs
141
in Great Britain. Vet. Parasitol. 198, 18–23.
142
Walker, J.B., Keirans, J.E., Horak, I.G., 2000. The genus Rhipicephalus (Acari: Ixodidae). A
143
guide to the brown ticks of the world. Cambridge University Press, Cambridge
144
Figure 1. Map of the study region with the tick community structure in dogs.
145
Ac ce p
te
d
M
an
us
cr
ip t
124
6
Page 6 of 8
ip t
Table
1068
924
Ixodes ricinus
3 26
1
3 65 29
2 2
2 4
3
1
97
33
7
6
1
us
6 77 6 33 802
Rhipicephalus sanguineus
Hyalomma marginatum
Ixodes crenulatus
3
M
an
12 104 9 102 841
Dermacentor reticulatus
d
84
Rhipicephalus rossicus
ep te
Caraorman Chilia Veche Enisala Grindul Lupilor Iazurile
Total
Ac c
Collection site
Number of sampled dogs 2 64 3 7 8
cr
Table 1. Distribution and number of ticks collected from dogs in the Danube Delta, Romania.
Page 7 of 8
Ac
ce
pt
ed
M
an
us
cr
i
Figure
Page 8 of 8
S0304-4017(14)00284-2 http://dx.doi.org/doi:10.1016/j.vetpar.2014.05.005 VETPAR 7241
To appear in:
Veterinary Parasitology
Received date: Revised date: Accepted date:
30-1-2014 7-5-2014 8-5-2014
Please cite this article as: S´andor, A.D., Dumitrache, M.O., D’amico, G., Kiss, B.J., Mihalca, A.D.,Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta, Romania, Veterinary Parasitology (2014), http://dx.doi.org/10.1016/j.vetpar.2014.05.005 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1 2
Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta, Romania
3 Attila D. SÁNDOR1, Mirabela O. DUMITRACHE1*, Gianluca D’AMICO1, Botond J. KISS2, Andrei D. MIHALCA1
6 7 8
1
cr
University of Agricultural Sciences and Veterinary Medicine, Faculty of Veterinary Medicine, Department of Parasitology and Parasitic Diseases, Calea Mănă tur 3-5, ClujNapoca 400372, Romania 2
Danube Delta National Institute for Research and Development, Str. Babadag 165, Tulcea 820112, Romania.
us
9 10
ip t
4 5
11
* Corresponding author: Mirabela O. DUMITRACHE, Address: Calea Mănăştur 3-5, ClujNapoca 400372, Romania; Tel: +40264596384; Fax: +40264593792; Email:[email protected])
an
12 13 14
M
15 Abstract
17 18 19 20 21 22 23 24 25 26 27 28 29 30
Changes in the distribution of tick species are among the major causes for the increase in prevalence of zoonotic diseases worldwide, with tick-borne diseases’ prevalence showing an emerging pattern. One of these ticks, Rhipicephalus 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. Here we report a case of dominant occurrence of Rhipicephalus 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. Rhipicephalus rossicus had a dominant occurrence in dogs in all but one location, accounting for 87.1% of all ticks (32.395.3% 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 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.
Ac ce p
te
d
16
31 32
Keywords: Rhipicephalus rossicus, Eastern Europe, tick, dog
33
1
Page 1 of 8
Main text
35
Ticks harbor more zoonotic pathogens than any other blood-feeding arthropod species
36
globally and they are the second most important vectors of epidemic importance after
37
mosquitoes. Ticks are known vectors for medically important viral diseases like tick-borne
38
encephalitis, louping ill, Crimean-Congo hemorrhagic fever (CCHF), Colorado tick fever,
39
and bacterial diseases, like Lyme disease, tick-borne relapsing fever, Mediterranean spotted
40
fever and Q-fever just to name a few (Dantas-Torres et al., 2012). Moreover, ticks transmit a
41
high number of pathogens affecting livestock and companion animals (Day, 2011; Smith and
42
Wall, 2013). Although most of these diseases have a long epidemiologic history and the
43
importance of ticks as vectors has been widely known, tick-borne diseases’ prevalence shows
44
an emerging pattern (Chomel, 2011; Salman et al., 2013). There are two main hypotheses
45
which explain this phenomenon: changes in geographical distribution of tick species and
46
increased contact of human population with ticks, caused by changes in human life-style
47
(Léger, 2013). Changes in the distribution of tick species are among the major causes for the
48
increase in prevalence of Lyme borreliosis, CCHF, tick-borne encephalitis or other vector-
49
borne infections of humans and domestic animals (Beugnet and Marie, 2009; Petney et al.,
50
2012). Most of the cases of tick species known to have recently increased their geographical
51
range are well documented in Western Europe and USA (Petney et al., 2012). However, there
52
is a lack of knowledge on the possible expansion of ticks with a more eastern distribution in
53
Europe. One of these ticks, Rhipicephalus rossicus, which is reported occasionally from
54
humans, seems to be particularly interesting because of its important demonstrated vectorial
55
role for zoonotic pathogens like Francisella tularensis, Coxiella burnetii, or CCHF and West
56
Nile viruses (Walker et al., 2000).
Ac ce p
te
d
M
an
us
cr
ip t
34
2
Page 2 of 8
Rhipicephalus rossicus is a tick with Eastern European and Western Asian distribution,
58
considered as being “rare”, with low prevalences in most studies reporting it (Walker et al.,
59
2000). Historically in Romania, it was recorded as an extremely rare tick, found only on
60
small mammals with only 4 known occurrences before 2012 (Feider, 1965; Mihalca et al.,
61
2012). Among domestic animals, dogs are probably the most important hosts, in general, for
62
ticks and tick-borne pathogens of human importance, due to their lifestyle and close contact
63
with people (Chomel, 2011). While R. sanguineus sensu lato (s.l.) is typically regarded as the
64
most common tick of dogs worldwide, the related species, R. rossicus is reported only
65
incidentally as a dog ectoparasite (Walker et al., 2000). We present here data which highlight
66
the dominance of R. rossicus in dogs from Romania, with importance to the possible
67
emergence of associated pathogens.
68
A total of 1068 ticks were collected from 84 household dogs between February 2012 and
69
November 2013. The collection occurred in five localities from the Danube Delta, SE
70
Romania (Figure 1), one of the largest wetland complexes of Europe. The region is primarily
71
of rural character, with important urban centers to the south (Constana) and north (Tulcea).
72
Dogs are commonly kept in households, with most individuals freely roaming around the
73
premises. Ticks were identified using morphological keys (Feider, 1965; Walker et al., 2000),
74
while identification was confirmed by molecular diagnostics based on 12S rDNA sequences
75
(Dumitrache et al., 2014). Six species of ticks were identified, with R. rossicus being found in
76
all five locations. Surprisingly, the dominant tick species was not R. sanguineus s.l., but R.
77
rossicus, accounting for 87.1% of all ticks (32.3-95.3% in different locations, see Table 1).
78
Rhipicephalus rossicus had the highest percent of occurrence in dogs in all but one location.
79
Rhipicephalus rossicus is a steppe and mountain steppe tick species, with a distribution from
80
Bulgaria and Romania to the east, occurring primarily in the Eurasian steppe zone to eastern
Ac ce p
te
d
M
an
us
cr
ip t
57
3
Page 3 of 8
Kazakhstan and western China. It is a three-host tick, with rodents, leporids and birds hosting
82
immature stages. Hedgehogs, hares, ungulates, horses and occasionally dogs and humans are
83
hosts of adults. All of these hosts are abundantly present in the area of the study. Although
84
previously recorded from dogs, it was primarily considered an important tick of wildlife and
85
domestic ungulates and its vectorial importance was treated as such (Walker et al., 2000). The
86
dominant presence in dogs from SE of Romania rises however a number of questions. Until
87
this study, R. sanguineus s.l. was considered as the only important tick species on dogs in
88
south-temperate regions of Europe (Walker et al., 2000), as well in Romania (Ioniă and
89
Mitrea, 2003). While R. sanguineus s.l. is a well-known vector for a great variety of
90
pathogens, its epidemiological importance for human pathogens is limited (Walker et al.,
91
2000). On the other hand, R. rossicus is a competent vector for CCHF, a disease only recently
92
reported from the study region (Ceianu et al., 2012). Moreover, R. rossicus seems to be more
93
common on humans than R. sanguineus s.l. (Walker et al., 2000), including in Romania
94
(Sándor, unpublished data).
te
d
M
an
us
cr
ip t
81
Ac ce p
95 96 97
Acknowledgements
98
For DMO this paper was supported by POSDRU/159/1.5/S/136893 project. For MAD, SAD
99
and GDA from grant PCE 236/2011. This study was conducted under the frame of the
100
EurNegVec COST Action TD1303. We would like to thank to C. Doma for the map in
101
Figure 1.
102 4
Page 4 of 8
103
References
104 Beugnet, F., Marie, J.L., 2009. Emerging arthropod-borne diseases of companion animals in
106
Europe. Vet. Parasitol. 163, 298–305.
107
Ceianu, C.S., Pănculescu-Gatej, R.I., Coudrier, D., Bouloy, M., 2012. First serologic
108
evidence for the circulation of Crimean-Congo hemorrhagic fever virus in Romania. Vector-
109
Borne Zoonotic. 12, 718–721.
110
Chomel, B., 2011. Tick-borne infections in dogs - an emerging infectious threat. Vet.
111
Parasitol. 179, 294–301.
112
Dantas-Torres, F., Chomel, B.B., Otranto, D., 2012. Ticks and tick-borne diseases: a One
113
Health perspective. Trends Parasitol. 28, 437–446.
114
Day, M.J. 2011. One health: the importance of companion animal vector-borne diseases.
115
Parasit Vector. 4,49.
116
Dumitrache, M.O., Kiss, J.B., Dantas-Torres, F., Latrofa, M.S., D’Amico, G., Sándor, A.D.,
117
Mihalca, A.D. 2014. Seasonal dynamics of Rhipicephalus rossicus attacking domestic dogs
118
from the steppic region of southeastern Romania. Parasit Vector 7, 97.
119
Feider, Z., 1965. Fauna of the Popular Republic of Romania. Volume 5/2. Acaromorpha,
120
Suprafamily Ixodoidea [in Romanian]. Ed. Academiei RPR, Bucureşti.
121
Földvári, G., Márialigeti, M., Solymosi, N., Lukács, Z., Majoros, G., Kósa, J.P., Farkas, R.,
122
2007. Hard ticks infesting dogs in Hungary and their infection with Babesia and Borrelia
123
species. Parasitol. Res. 101, 25–34.
Ac ce p
te
d
M
an
us
cr
ip t
105
5
Page 5 of 8
Ioniă, M., Mitrea, I.L., 2003. [Observations regarding the biological cycle of the brown dog
125
tick (Rhipicephalus sanguineus Latreille 1806 – Acari: Ixodidae), in the environmental
126
conditions of Bucureti region]. Scientia Parasitol. 4, 167–171. [in Romanian]
127
Léger, E., Vourc’h, G., Vial, L., Chevillon, C., McCoy, K.D., 2013. Changing distributions of
128
ticks: causes and consequences. Exp. Appl. Acarol. 59, 219–244.
129
Mihalca, A.D., Dumitrache, M.O., Magdaş, C., Gherman, C.M., Domşa, C., Mircean, V.,
130
Ghira, I.V., Pocora, V., Cozma, V., Sándor, A.D., 2012. Synopsis of the hard ticks (Acari:
131
Ixodidae) of Romania with update on host associations and geographical distribution. Exp.
132
Appl. Acarol. 58, 183–206.
133
Petney, T.N., Skuballa, J., Muders, S., Pfäffle, M., Zetlmeisl, C., Oehme, R., 2012. The
134
changing distribution patterns of ticks (Ixodida) in Europe in relation to emerging tick-borne
135
diseases. In: Arthropods as Vectors of Emerging Diseases Springer Berlin Heidelberg; p. 151–
136
166.
137
Salman, M., Estrada-Peña, A., Tarrés-Call, J. 2013. Emerging (Re-emerging) tick-borne
138
infections and the dissemination of ticks. Ticks and Tick-Borne Diseases: Geographical
139
Distribution and Control Strategies in the Euro-Asia Region, p.1–5.
140
Smith, F.D., Wall, L.E.R., 2013. Prevalence of Babesia and Anaplasma in ticks infesting dogs
141
in Great Britain. Vet. Parasitol. 198, 18–23.
142
Walker, J.B., Keirans, J.E., Horak, I.G., 2000. The genus Rhipicephalus (Acari: Ixodidae). A
143
guide to the brown ticks of the world. Cambridge University Press, Cambridge
144
Figure 1. Map of the study region with the tick community structure in dogs.
145
Ac ce p
te
d
M
an
us
cr
ip t
124
6
Page 6 of 8
ip t
Table
1068
924
Ixodes ricinus
3 26
1
3 65 29
2 2
2 4
3
1
97
33
7
6
1
us
6 77 6 33 802
Rhipicephalus sanguineus
Hyalomma marginatum
Ixodes crenulatus
3
M
an
12 104 9 102 841
Dermacentor reticulatus
d
84
Rhipicephalus rossicus
ep te
Caraorman Chilia Veche Enisala Grindul Lupilor Iazurile
Total
Ac c
Collection site
Number of sampled dogs 2 64 3 7 8
cr
Table 1. Distribution and number of ticks collected from dogs in the Danube Delta, Romania.
Page 7 of 8
Ac
ce
pt
ed
M
an
us
cr
i
Figure
Page 8 of 8