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\begin{document}

\title{Diversity of hard tick populations and their geographic variations in
northwestern Iran}



\author[1]{Eslam Moradi- Asl}%
\author[1]{Rohollah  Moradi}%
\author[1]{ Zakiah  Telmadarraiy}%
\author[1]{Sayena Rafizadeh}%
\author[2]{Yavar Rassi}%
\affil[1]{Affiliation not available}%
\affil[2]{2.	Department of Medical Entomology \& Vecotr Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran}%


\vspace{-1em}



  
  \date{May 28, 2024}


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\selectlanguage{english}
\begin{abstract}
Abstract Ticks are forced vertebrate ectoparasites, including humans,
and are vectors of serious diseases such as Crimean Congo Hemorrhagic
Fever, Relapsing Fever, and various forms of encephalitis. Spatial
assessment of the prevalence of ticks and detection of high risk areas
for tick-borne disease transmission and evaluation of ecological
measures are key aims of this research. Ticks were collected using
standard methods From 27 villages in the region of Sarab County in
north-eastern Iran during the four seasons of 2018-219 and identified
using valid keys. The calculation of indices for biodiversity were based
on the Margalf index, Shannon-Weiner index and Simpson index. R2.15
Statistical software was used for statistical analysis of indices of
biodiversity, and ArcMap10.4.1 software and IDW and GeneralG methods and
analysis were used to investigate spatial dispersion and to determine
important tick hotspots. Thirty-five percent of the 2,500 animals
surveyed were infected. A total of 1416 ticks were caught, 74.6 \% were
adult ticks, \% were nymph and 1.4 percent were larvae. Ninety four
percent of the ticks caught belonged to hard ticks relating to 4 genera
and 6 percent to soft ticks relating to 2 genera. The highest species
biodiversity was related to summer (1.4234), and the lowest was related
to winter (0.7379), according to the Margalef diversity index. In the
central part of the study region a large hotspot area was found. The
area of study was very prone to tick-borne disease transmission in terms
of tick diversity and tick species richness, and it was important to
inform people to monitor to avoid diseases. Keywords: Ticks, Species
biodiversity, GIS, Iran%
\end{abstract}%



\sloppy


\textbf{1.Introduction}

Ticks are the most important medical and veterinary ectoparasites and
are one of the most important arthropod groups (Lane and Crosskey 2012).
Ticks belong to the order of metastigmatia which feeds on animals and
humans and play an important role in the transmission of the disease.
This order is composed of two common argasidae and ixodidae
families(Goodman et al 2005). There are about 899 hard tick species, and
185 soft tick species (de la Fuente 2018). In Iran there've been
recorded of 14, ~5, 8, 11, 1 and 3 hard tick species of \emph{Hyalomma}
,\emph{Rhipicephalus, Ixodes, Haemaphysalis, Bophilus}
and\emph{Dermacentor} respectively. Ten percent of ticks feed on
domestic animals , particularly cattle, sheep and goats. These are of
major health significance due to the conditions that cause human and
animal diseases (Rahbari et al 2007, Masoumi Asl et al 2009, Davari et
al 2017 ).

Tick-borne diseases are among the most common emerging and re-emerging
diseases in recent years that have spread to different geographic areas
(de La Fuente et al 2017). Several diseases including tick-borne fever,
Rocky Mountain spotted fever, Q fever, Lyme disease, and Crimean-Congo
hemorrhagic fever (CCHF) are among the known tick-borne human diseases.
(Nava et al 2009,Otranto et al 2014,Moradi Asl et al 2018 ).

Regardless of the importance of ticks in spreading different pathogens,
its population structure, relative abundance and frequency, hosts type,
habitats, ecology and diversity of species must be regulated. The study
of tick biodiversity using various scientific indices seems to be very
helpful in this regard (Masoumi Asl et al 2009, Wood and Lafferty 2013).
The aims of this study was to determine the status of species diversity
and richness of hard and soft ticks and their geographical distribution
in the livestock of Sarab region in northwestern Iran using Simpson,
Shannon Weiner and GIS software indicators.

\textbf{2.Materials and methods} :

\textbf{2.1.Study area} : Sarab s a county in East Azerbaijan Province
in Iran. The capital of the county is Sarab. At the 2006 census, the
county's population was 132,094, in 31,977 families. The county is
subdivided into two districts: the Central District and Mehraban
District. The county has four cities: Sarab, Mehraban, Sharabian, and
Duzduzan. At the 2006 census, its population was 42,057, in 11,045
families. Livestock and animal husbandry have traditionally been common
in most rural households.

\textbf{2.2.Tick collection} :

Twenty-seven villages were selected from a total of nine districts. Ten
Locations were selected in each village (human, animal and livestock
storage areas, traditional and modern grain deposits, farmland attached
to the village and preferably attached to active livestock sables ,
estimated at 300 places in total.

During the study, 441000 cattle (331000 sheep and goats) and (95000 cows
and oxen) (8000 horses) and (7000 donkeys) were in the Sarab county.
Therefore, ticks from a total of 2,500 livestock were collected in this
study, of which 75\% of the sample size were sheep and goats, 23\% were
cows and oxen, and 2\% were horses and donkeys. Valid keys were used to
identify species of the ticks (Keirans and Litwak 1989, Gregory et al
1998). This experiment was carried out under the guidance of the Ethics
Committee of the Tehran University of Medical Sciences
(IR.TUMS.SPH.REC.1398.058).

\textbf{2.3.Biodiversity Indices}

Different indices of biodiversity were used in this study including
species richness (Margalef's richness index), species diversity
(Simpson's and Shannon Weiner's index).

\textbf{2.4.Calculation of tick dispersion}

Arcmap 10.4.1 software and interpolation with Inverse Distance Weighted
(IDW) were used to analyze tick dispersion and to assess the
distribution of disease vectors hot spots. The General G formula was
used to determine the pattern of distribution of all Crimean Congo
disease species and main vectors including \emph{Hyalomma marginatum}and
\emph{H.anatolicum} in the study region.

\begin{equation}
G=\ \frac{\sum_{i}^{N}{=1\ \sum_{j}^{N}{=1}}\text{Wij\ xi\ xj}}{\sum_{i}^{N}{=1\ \sum_{j}^{N}{=1\ xi\ xj}}},j\neq i\nonumber \\
 \end{equation}

\textbf{3.Results}

For a total of 2,500 animals examined, ticks infested 763 animals (30.5
\%). A total of 300 stalls and stables were checked in 27 villages, 75
of which were infested with ticks ~(25\%). A total of 1,416 ticks have
been collected, of which 30\% were male, 44.6\% were female, 22\% were
nymphs and 1.4\% were also tick larvae. Of the 94\% of the ticks
collected, 11 species have been classified as hard ticks, belonging to 4
genera: Hyalomma (65\%), Heamiphysalis (11\%), Rhipicephalus (6\%), and
Dermacenter (12\%). Three species of soft ticks from two genera of
Ornithodorus and Argas were identified. (Table 1).\selectlanguage{english}
\begin{longtable}[]{@{}llllllllllll@{}}
\toprule
\textbf{Total} & \textbf{Larva} & \textbf{Nymph} & \textbf{Adult ticks}
& \textbf{Adult ticks} & \textbf{Hosts} & \textbf{Hosts} &
\textbf{Hosts} & \textbf{Hosts} & \textbf{Species} & \textbf{Genus} &
\textbf{Family}\tabularnewline
\midrule
\endhead
& & & \textbf{Female} & \textbf{Male} & \textbf{Shelters} &
\textbf{Donkey \& Horse} & \textbf{Sheep \&Got} & \textbf{Cow \&Ox} & &
&\tabularnewline
46 & 0 & 0 & 33 & 13 & 0 & 0 & 17 & 11 & \emph{H.anatolicum} &
\emph{Hyalomma} & Ixodidae\tabularnewline
319 & 0 & 2 & 111 & 206 & 0 & 12 & 69 & 52 & \emph{H.marginatum} &
\emph{Hyalomma} &\tabularnewline
60 & 0 & 0 & 25 & 35 & 0 & 0 & 22 & 12 & \emph{H.scupense} &
\emph{Hyalomma} &\tabularnewline
143 & 0 & 0 & 141 & 2 & 0 & 2 & 67 & 39 & \emph{H.sp} & \emph{Hyalomma}
&\tabularnewline
55 & 0 & 0 & 17 & 38 & 0 & 2 & 18 & 8 & \emph{H.asiaticum} &
\emph{Hyalomma} &\tabularnewline
18 & 18 & 0 & 0 & 0 & 0 & 0 & 2 & 0 & \emph{larva} & \emph{Hyalomma}
&\tabularnewline
279 & 0 & 279 & 0 & 0 & 0 & 7 & 70 & 32 & nymph & \emph{Hyalomma}
&\tabularnewline
104 & 0 & 0 & 87 & 17 & 0 & 0 & 65 & 4 & \emph{He.sulcata} &
\emph{Haemaphysalis} &\tabularnewline
31 & 0 & 0 & 18 & 13 & 0 & 0 & 14 & 4 & \emph{He.numidiana (erinacei)} &
\emph{Haemaphysalis} &\tabularnewline
23 & 0 & 0 & 23 & 0 & 0 & 0 & 19 & 0 & \emph{He.concinna} &
\emph{Haemaphysalis} &\tabularnewline
76 & 0 & 0 & 54 & 22 & 3 & 4 & 21 & 8 & \emph{R.sanguineus} &
\emph{Rhipicephalus} &\tabularnewline
20 & 0 & 0 & 10 & 10 & 0 & 0 & 6 & 8 & \emph{R.bursa} &
\emph{Rhipicephalus} &\tabularnewline
169 & 0 & 0 & 105 & 64 & 0 & 2 & 76 & 42 & \emph{marginatus} &
\emph{Dermasentor} &\tabularnewline
520 & 0 & 434 & 65 & 21 & 63 & 0 & 42 & 0 & \emph{O.lahorensis} &
\emph{Ornithodoros} & Argasidae\tabularnewline
7 & 0 & 0 & 3 & 4 & 2 & 0 & 2 & 4 & \emph{A.reflexus} & \emph{Argas}
&\tabularnewline
42 & 0 & 29 & 13 & 0 & 7 & 0 & 0 & 0 & \emph{persicus} & \emph{Argas} &
Soft tick\tabularnewline
1912 & 18 & 744 & 705 & 445 & 75 & 29 & 510 & 224 & & &\tabularnewline
\bottomrule
\end{longtable}

Table1. The total number of ticks collected from hosts and residential
places in Sarab county,2018-19

Sheep and goats with 58.68\%, cows and ox with 13.23\% and horses and
donkeys with 2.14\% respectively were the most infested animals with
ticks. In terms of age, ticks were observed more in animals under 3
years of age (49 \%) and the lowest infection (10 \%) was observed in
animals over 7 years of age, and the most infested section of the
animals were sub-tail (29.89 \%) and animal ears (25.69 \%).

\textbf{3.1.Biodiversity and species richness}

Tick diversity and species richness~were calculated on the basis of two
factors: seasonal activity and host, the Margalf species richness index
showed that the highest richness was related to summer (1.4234), and the
lowest richness was related to winter (0.7379). The species diversity of
ticks collected at different seasons in the research region was also
significantly different (P\textless{}0.05).

The highest species diversity was related to summer (2.1709), and the
lowest species diversity was related to winter (0.781), according to the
Shannon-Wiener index measurements. The index of evennes of ticks
collected during different seasons in the research region was
significantly different (P\textless{}0.05). The evennes index analysis
found that the highest uniformity was in relation to the summer season
(0.9428) and the lowest uniformity was in relation to the autumn season
(0.4428). The Simpson species diversity index also showed that the
highest diversity was correlated with summer (0.8622), and the lowest
diversity was associated with autumn (0.3549). The results of this study
found that the species richness of ticks collected in the Sarab region
during the first and second six months of the year had a significant
difference (P\textless{}0.05), and the first six months of the year had
higher and more diversity and richness~of species than the second six
months of the year (Table 2).

Table 2. Biodiversity and species richness of ticks captured in the
studied areas of Sarab county, based on seasonal activity, 2018-2019\selectlanguage{english}
\begin{longtable}[]{@{}lllll@{}}
\toprule
& Spring & Summer & Fall & Winter\tabularnewline
\midrule
\endhead
Shannon-Wiener index & 2.1267 & 2.1709 & 0.7934 & 0.781\tabularnewline
Simpson's index)D( & 0.1449 & 0.1378 & 0.6451 & 0.6385\tabularnewline
Simpson's index(D-1) & 0.8551 & 0.8622 & 0.3549 & 0.3615\tabularnewline
Evennes Index & 0.9236161 & 0.942812 & 0.4428048 &
0.485265\tabularnewline
Margalef diversity index & 1.3702635 & 1.423474 & 0.8287641 &
0.7379352\tabularnewline
\bottomrule
\end{longtable}

According to the Simpson Species Diversity Index, the findings of
species diversity and richess based on different hosts showed that the
highest species diversity among the studied hosts was correlated to
sheep and goats (0.881), and the lowest species diversity was found in
horses and donkeys (0.715). The highest species diversity was found in
~sheep and goats~(2.333) and the lowest species diversity in horse and
donkey ~hosts (1.399) according to the Shannon-Wiener index. There was a
significant difference in the evenness index for livestock hosts that
ranged from the highest for sheep and goats (0.9096) to the lowest for
cows and ox (0.7945).(Table 3).

Table 3. Determining the diversity and species richness of ticks caught
separately by the host in the study areas in Sarab county, 2018-2019\selectlanguage{english}
\begin{longtable}[]{@{}lllll@{}}
\toprule
& Cow \& Ox & Goat \&sheep & Donkey \&Horse & Stables\tabularnewline
\midrule
\endhead
Shannon-Wiener index & 1.905 & 2.333 & 1.399 & 0.447\tabularnewline
Simpson's index)D( & 0.198 & 0.119 & 0.285 & 0.787\tabularnewline
Simpson's index(D-1) & 0.802 & 0.881 & 0.715 & 0.213\tabularnewline
Evennes Index & 0.7945 & 0.9096 & 0.8693 & 0.3224\tabularnewline
Margalef diversity index & 1.807 & 1.708 & 1.077 & 0.483\tabularnewline
\bottomrule
\end{longtable}

\textbf{3.2.Spatial distribution}

The most ticks were collected in the villages of Dozduzan 123 (6.43\%),
Sharbian 120 (6.28\%), Mehraban 117 (6.12\%), Kelian 107 (5.6\%), Ardha
106 (5.54\%) and Mahin Bijand 101 (5.3\%) and the lowest in Dichan
village 47 (2.45\%). In Mehraban district the highest spatial dispersion
as well as the highest density of hard and soft tick species were found.

The findings of the interpolation study (IDW) revealed that there was a
large hotspot area in the central part and a small hotspot in the
northwestern part of the county of Sarab in terms of tick abundance,
both of which were high-risk areas in the Mehraban region with 4596 and
1150 households in population. (Figure 1).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

Figure 1. General distribution of ticks caught in the study areas of
Sarab county,2018-2019

The results of the analysis of spatial distribution patterns for all
species and for two species of \emph{H.marginatum}
and\emph{H.anatolicum} using the General G index showed that all species
were distributed randomly in all areas of study and did not have a
specific pattern such as cluster or regular (Figure 2 and Table 4).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

Figure 2. Results of scattering pattern analysis of ticks caught in
Sarab county, East Azerbaijan, northwest of Iran, 2018-19\selectlanguage{english}
\begin{longtable}[]{@{}llllll@{}}
\toprule
General G Summary & General G Summary & General G Summary & Global
Moran's I Summary & Global Moran's I Summary & Global Moran's I
Summary\tabularnewline
\midrule
\endhead
Species & Observed General G & Expected General G & Variance & z-score &
p-value\tabularnewline
All species & 0.000015 & 0.000016 & 0.000000 & -0.357036 &
0.721065\tabularnewline
\emph{Hyalomma marginatum} & 0.000014 & 0.000016 & 0.000000 & -1.464457
& 0.143069\tabularnewline
\emph{Hyalomma antalicum} & 0.000013 & 0.000016 & 0.000000 & -0.911540 &
0.362011\tabularnewline
\bottomrule
\end{longtable}

Table 4. The results of hot-spot and autocorrelation analysis of tick
species in Sarab county, East Azerbaijan, northwest of Iran, 2018-19

\textbf{4.Discussion}

In this study, 2,500 different livestock were studied and 30.5\% of
livestock and 25\% of stalls and stables were infested with different
ticks, this is one of the first studies to include more samples and tick
populations were also studied in Iran. In related surveys, the infection
rate of ticks was 11\%, 9.37\%, 43\% and 24\% in northwest, west and
north Iran (Salim Abadi et al 2011, Hashemi-Fesharaki et al 2011,
Telmadarreyi 2010, Bakhshai et al 2012).

The highest frequency of captured ticks was related to spring (37.24\%)
and the lowest frequency is related to winter (11.83\%) and this
indicates the seasonal behavior of ticks in the mountainous and
northwestern regions of Iran, mainly in spring, which can be attributed
to the Nasiri study in Abdanan County, Ilam Province (Nasiri et al
2010). Nonetheless, more seasonal tick activity was recorded in summer
and autumn in areas such as Golestan province northern Iran, which have
ecologically different climates and have lower altitudes and higher
temperatures than the mountainous areas (Sarani et al 2014).

The highest tick infection was observed in sheep and goats in this
research (79.23 \%) and it was consistent with another study in the
province of Ardabil, northwest Iran (Telmadarreyi 2010).

In the sample area, the tick biodiversity, according to the
Shannon-Wiener index, was found to be moderate to high (2.432) and the
biodiversity index of Simpson (D-1) was also determined to be 0,856. The
dominant species in the area therefore had a great diversity. We found
the highest richness~of ticks captured from cows and ox and the lowest
~~from horses and donkeys, according to the Margalef species
richness~index. The findings of this research did not confirm previous
studies in the province of Golestan (Sarani et al 2014) that found more
sheep species compared to cows. The diversity of the species was highest
in autumn, and lowest in winter. The findings of this research were
consistent with study for seasonal ticks activities in northwestern Iran
(Vatandoost et al 2012).

Six genera and 14 species of hard and soft ticks were collected in this
research, of which the dominant genus was Hyalomma (48.12 \%). The
findings of this research revealed that the region was prone to diseases
like Crimean Congo hemorrhagic fever.~ According to the study (2004) in
the eastern province of Azarbaijan, northwestern Iran, the Hyalomma
genus was confirmed to have the highest abundance~(52.81 \%) which was
consistent with recent study(unpublished data). Interestingly, in a
survey conducted in West Azerbaijan province, 7 tick species with more
abundant in the Hyalomma genus (unpublished data) were reported to have
the highest abundance and distribution, as our recent research did.
Based on the findings of this study and the above research, it can be
inferred that the provinces located in northwestern Iran including East
Azerbaijan, West Azerbaijan and Ardabil had a high abundance of Hyalomma
species and were ecologically suitable habitat for this tick.

Identifying high-risk and low-risk disease and vector areas allows to
make better decisions on the management of the vectors and diseases
transmitted by them, and to arrange for the control and preventive
management of the region. Throughout this research, the spreading of
ticks as the vectors was found randomly around the region, but internal
analysis revealed that the high-risk area of ticks was very high in the
west of the study area as well as being a large hotspot. The high
population of livestock and livestock occupation which have been the key
hosts of ticks were some of the factors involved in this region.
Therefore, in terms of tick-borne diseases, this area is indeed one of
the high-risk areas and control measures should be taken to prevent
bites of ticks and diseases that they transmit.

\textbf{5.Conclusion}

The findings of the recent study indicate that the number of tick
species caught in this region is varied due to the large abundance of
livestock in Sarab county and the wealth of animal and livestock
husbandry practices and the production of dairy products. Because of the
small scale of the county it reveals the richness of different species
of ticks in this region. In the study of tick diversity in the research
region among different hosts, it was observed that all the indices
observed on sheep and goats have a comparatively higher value that the
ticks are more associated with long hair hosts, so periodically picking
the wool and hair of these hosts may be a way to reduce tick activity.
Throughout this research, the spreading of ticks as the vectors was
found randomly around the region, but internal analysis revealed that
the high-risk area of ticks was very high in the west of the study area
as well as being a large hotspot.

A\textbf{cknowledgements}

This study was financially supported by the Deputy of Research, Tehran
University of Medical Sciences, Grant No. 40919.

\textbf{Conflict of interest}

There is no conflict of interest.

\textbf{Ethics statement}

This experiment was carried out under the guidance of the Ethics
Committee of the Tehran University of Medical Sciences
(IR.TUMS.SPH.REC.1398.058).

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Trends in ecology \& evolution,28,239-47. doi:
10.1016/j.tree.2012.10.011.\selectlanguage{english}
\begin{figure}[H]
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\includegraphics[width=0.70\columnwidth]{figures/Fig-1-Sarab/Fig-1-Sarab}

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\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Fig-2-sarab-county/Fig-2-sarab-county}

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\textbf{Hosted file}

\verb`Table 1 Sarab.docx`  available at \url{https://authorea.com/users/357558/articles/480059-diversity-of-hard-tick-populations-and-their-geographic-variations-in-northwestern-iran}

\textbf{Hosted file}

\verb`Table 2 Sarab.docx`  available at \url{https://authorea.com/users/357558/articles/480059-diversity-of-hard-tick-populations-and-their-geographic-variations-in-northwestern-iran}

\textbf{Hosted file}

\verb`Table 3 Sarab.docx`  available at \url{https://authorea.com/users/357558/articles/480059-diversity-of-hard-tick-populations-and-their-geographic-variations-in-northwestern-iran}

\textbf{Hosted file}

\verb`Table 4 Sarab.docx`  available at \url{https://authorea.com/users/357558/articles/480059-diversity-of-hard-tick-populations-and-their-geographic-variations-in-northwestern-iran}

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