Hard Tick Species of Livestock and their Bioecology in Golestan Province, North of Iran.

BACKGROUND: A survey on tick species composition was carried out in Golestan Province Iran during year 2010-2011.The aim was to determine tick species parasitizing domestic ruminants and their seasonal population dynamics.
METHODS: A total of 124 sheep, 92 goats, 84 cattle, 74 camels and 12 horses in several villages were inspected for tick infestation. The collected ticks preserved in 70% alcohol and then were identified.
RESULTS: The overall 1059 ticks (453 female, 606 male) were collected. The ticks occur on sheep, goats, cattle, camels and horses as 72.1%, 77.3%, 75.8%, 69.3%, and 50% respectively. The frequency of ticks in spring was more than other seasons and the least was observed in winter. In the spring and summer, infestation rate in domestic ruminants were calculated as 100%. Six genus and fourteen hard and soft tick species were identified including Rhipicephalus sanguineus, R. bursa, Ixodes ricinus, Haemaphysalis punctata, H. sulcata, H. erinacei, H. inermis, Hyalomma marginatum, Hy. asiaticum, Hy. dromedarii, Hy. excavatum, Hy. anatolicum, Hy. detritum, Boophilus annulatus and Argas persicus. Rhipicephalus sanguineus was the most abundant species in the study area. The largest number of ticks was collected from animal ears and tails. Haemaphysalis, Hyalomma, Rhipicephalus and Boophilus occurred in mountainous, forest and plateau areas of Golestan Province but Ixodes occurred only in mountainous and forest areas, whereas Rhipicephalus and Hyalomma were present in coastal areas of Golestan Province.
CONCLUSION: The result of this study is a survey on tick species from domestic animals in Iran and implication of possible prevention measures for diseases transmitted by ticks.

Introduction

Medical and veterinary implications of ticks (Acari: Ixodidae) on human and animals life is very obvious question and proved from many years ago (Hoogstraal 1982). Annoyance and paralysis of livestock also transmission large number of pathogen agents is only some cosmopolitan associated tick problems (Sonenshine 1991, Service 2001). Approximately only 10% of the currently known 867 tick species are also responsible for damage directly due to their feeding behavior (Oliver 1989) and unavoidability act as vectors of a broad range of pathogens of those hosts. Ruminants are also affected by direct tick damage including tick bite abscesses, anemia, tick induced dermatophilosis. The pioneer work on tick fauna was Delpy L in Iran (Delpy 1936). Later continue by GS Pervomaisky, H Nemenz (Pervomaisky 1948, Nemenz 1953). Subsequently R Abbasian-Lintzen, Z Mazlum, G Maghami and A Rafyi et al. conducted some studies generally on domestic animals ticks in Iran (Abbasian-Lintzen 1960, Maghami 1968, Mazlum 1971). However certain studies also has been carried out on the ticks of wild animals by NA Filippova et al former presented data for 642 ixodid ticks taken from small-sized mammals mainly rodents in different zoogeographical zones of Iran and the latter studied ixodid ticks parasitizing wild sheep and goats in Iran focusing on maintaining natural foci of many hazardous diseases for human (Filippova et al. 1976). Recently Nabian et al and Rahbari et al published a list of adult ticks collected from domestic animals in North and whole Iran (Nabian et al. 2007, Rahbari et al. 2007a). Telmadarraiy et al. published a list of tick species and their prevalence in the Northwest and the Western part of Iran (Telmadarraiy et al. 2004, Telmadarraiy et al. 2008a, Telmadarraiy et al. 2010). Furthermore there are several reports on epidemiology, distribution, medically importance and acaricide susceptibility of different tick species through in this country (Telmadarraiy et al. 2007b, Vatandoost et al. 2010a). Since thus far only few studies were accomplished on tick fauna in different areas of Iran, it seems to be a gap in our knowledge about distribution of tick species in the Iran. In addition there is lack of finding about the frequency of ixodid tick species from domestic ruminants in Golestan Province. Therefore, this study is aimed to figure out the frequency of ticks on domestic ruminants likewise their seasonal and topological abundance and their host in the aforementioned part of Iran.

Materials and Methods

Study area

The present study carried out in different zone of Golestan Province which is located in Northeastern of Iran and geographically located at 36°25´N and 53°51´E on the Southeastern coast of Caspian Sea, a region suitable for agriculture and animal husbandry. This province geographically divided into three parts: covered forest mountainous parts and plateau areas as well as the coastal plains.

Ticks

Tick sampling was carried out on all three part of the study area at different time intervals. A total of 124 sheep, 92 goats, 84 cattle, 74 camels and 12 horses in several villages in Golestan Province were examined for tick infestation on the whole body of each animal. The sites of tick attachment were recorded during collection, collected ticks were preserved in 70% alcohol, counted and tick identification done by using the suitable and comprehensive keys including Pomerantzev (1950) and Hoogstraal (1956) (Pomerantzev 1950, Hoogstraal 1956).

Results

During the study period among several villages the total number of 1009 ticks were collected and identified, the occurrence of ticks on sheep, goats, cattle, camels and horses were 72.1%, 77.3%, 75.8%, 69.3%, 50% respectively. Table 1 show the number of hard tick species in whole study area. The frequency of ticks in spring was more than other seasons and the least was observed in winter. In the spring and summer infestation rate of domestic ruminants was higher than 90% and in autumn and winter was lower than 25%. The mean number of ticks on each animal was high in spring and summer (40–50 ticks per animal) and was low in autumn and winter (3–5 ticks per animal), so the largest number of ticks were collected from animal ears and tails. Fifteen species of ticks were identified based on the morphological characteristics which comprise Rhipicephalus sanguineus, R. bursa, Ixodes ricinus, Haemaphysalis punctata, H. sulcata, H. erinacei, H. inermis, Hyalomma marginatum, Hy. asiaticum, Hy. excavatum, Hy. anatolicum, Hy. dromedarii, Hy. detritum, B. anulatus and Argas persicus was collected in nests of hen and domestic ruminants. Out of 1059 collected ticks from animal, a significant number of 593 R. sanguineus were identified. This species stands out as being the most prevalent tick species comprising 56% of the all ticks collected from domestic ruminants in Golestan Province. The tick species prevalence is shown in Table 1. Latter species was the most abundant tick in both mountainous areas and the coastal plains, as well as Hy. anatolicum in the plateau areas. Whereas I. ricinus, R. bursa, B. annulatus and H. inermis occurred in mountainous areas and Hy. dromedarii, Hy. asiaticum, Hy. excavatum and Hy. detritum occurred in plateau areas only. The species diversity of hard ticks in plateau areas was more than other areas (Fig. 1). The tick species diversity on sheep is highest from the other hosts (Table 2).

Table 1

Seasonal abundance of hard ticks in Golestan Province

Species	number (percent)	Season
		Spring		Summer		Autumn		Winter		Total
		♀	♂	♀	♂	♀	♂	♀	♂	♀	♂
Hy. anatolicum	148(14/7)	0	35	33	24	0	56	0	0	33	115
Hy. asiaticum	2(0/2)	0	2	0	0	0	0	0	0	0	2
Hy. detritum	2(0/2)	0	0	0	2	0	0	0	0	0	2
Hy. dromedarii	64(6/3)	26	24	0	11	0	1	1	1	27	37
Hy. excavatum	4(0/4)	0	2	0	0	0	2	0	0	0	4
Hy. marginatum	64(6/3)	8	21	2	27	0	6	0	0	10	54
H. erinacei	4(0/4)	0	0	0	0	3	0	1	0	4	0
H. inermis	24(2/4)	0	0	0	0	22	2	0	0	22	2
H. punctata	66(6/5)	0	0	0	0	52	11	0	3	52	14
H. sulcata	3(0/3)	0	0	0	0	1	0	1	1	2	1
I. ricinus	13(1/3)	6	0	1	0	6	0	0	0	13	0
R. (B.) annulatus	4(0/4)	0	0	0	0	4	0	0	0	4	0
R. bursa	18(1/8)	0	0	10	8	0	0	0	0	10	8
R. sanguineus	593(58/8)	163	250	88	92	0	0	0	0	251	342
Total	1009(100)	203	334	134	164	88	78	3	5	428	581

Fig. 1

Topological preference of hard ticks collected in Golestan Province (the number of specimens presented between two parenthesis)

Table 2

The host diversity of hard tick species in Golestan Province

Species number (percent)	Host
	Cattle	Sheep	Goat	Camel	Horse
Hy. anatolicum	108	0	0	25	15
Hy. asiaticum	1	0	0	1	0
Hy. detritum	0	0	0	2	0
Hy. dromedarii	0	0	0	64	0
Hy. excavatum	4	0	0	0	0
Hy. marginatum	40	0	0	13	11
H. erinacei	3	1	0	0	0
H. inermis	24	0	0	0	0
H. punctata	63	3	0	0	0
H. sulcata	1	2	0	0	0
I. ricinus	7	0	6	0	0
R. (B.) annulatus	4	0	0	0	0
R. bursa	10	5	0	0	3
R. sanguineus	15	359	202	4	13
Total	280	370	208	109	42

Discussion

In the present study 206 (53.3%) out of 386 livestock was infested with tick. The number of ticks was high in spring and summer (40–50 tick per animal) but low in autumn and winter (3–5 tick per animal, average 21.5–25). Hosseini vasoukolaei et al. (2010) in Ghaemshahr recorded that tick infestation rate of animal and the number of ticks per animal was 24% and 3–5 respectively (Hosseini vasoukolaei et al. 2010). In the study conducted by Rahbari et al. (2007) in four different zoogeographical areas in Iran where the majority of the domestic ruminants in Iran exist the number of ticks per animal (10–20) was low (Rahbari et al. 2007a). In respect of this result to result of the present investigation tick infestation rate of animals was high in our studied area. Through viewpoint of tick infestation of livestock the percentage of tick per sheep, goat, cattle, camel and horse were equal 45.1%, 47.8%, 64.2%, 62.1%, and 50.0% respectively. Tick infestation of cattle, sheep and goat in the study of Rahbari et al. (2007) was equal 62%, 55% and 57% respectively (Rahbari et al. 2007a). In the other study carry out by Davoudi et al. (2008) in Northwestern parts of Iran 10.16% of cattle and 1.07% of buffaloes were infested by ticks. Thus tick infestation of animals in our studied areas than Ghaemshahr and Northwestern parts of Iran was higher but coincided with the result of Rahbari et al. (2007). These results reveal significant differences concerning tick abundance on different hosts in different geographical areas. In a survey conducted from April 2001 to January 2003 in Tamil Nadu of India from 600 sheep and goat was selected randomly 64.6% sheep and 97.66% goat were infested by ticks (Vathsala et al. 2008) and therefore tick infestation rate of animals in Indian study is higher from tick infestation rate of animals in our country. We observed that infestation rate may be maximized in the spring and summer seasons. This result is in agreement with study of Davoudi et al. (2008) he also sees the highest rate of infestation occur in spring (Davoudi et al. 2008). However Telmadarraiy et al. (2004) and Salari Lak et al. (2008) in the Northwestern Iran most of tick collected in the summer and spring respectively (Telmadarraiy et al. 2004, Salari Lak et al. 2008). It may be as a result of that climate condition and flora of Northwestern Iran in summer is similar to climate condition of our studied area in spring. In the studies conducted in Iran and also in our study, the lowest number of ticks were collected during winter, whereas interestingly in Tamil Nadu of India seasonal tick infestation rate of sheep and goat in winter (January to March) was 61% and 97.66% respectively (Vathsala et al. 2008). This could be due to Indian climate conditions in winter agree with climate condition of Northwestern Iran in same season. In the present study, the ticks were obtained in more number from animal ears and tails. The possible factors effect question include temperature and humidity of skin also delicateness of it that cause tick attached and engorged on this sites. Whereas in winter which is colder than other seasons ticks attached the trunk between wool’s host which is warmer than ears and tail thus become their preference site in the winter season. In our study, five genera of ixodid ticks including Rhipicephalus (60.5%), Hyalomma (27.1%), Haemaphysalis (10.6%), Ixodes (1.3%), and Boophilus (0.4%) were collected and Rhipicephalus ticks were dominant in the investigated area. In a survey on ticks collected from sheep, in Bahar township of Hamadan Province in the Western part of Iran, the ixodid ticks found were Hyalomma, Rhipicephalus and Haemaphysalis and Hyalomma ticks were predominant ticks (Telmadarraiy et al. 2008a). The frequency of Hyalomma and Rhipicephalus species in a study conducted in Ardabil Province located in the Northwest of Iran, comprising 43.6% and 41.7% of all collected ticks respectively (Telmadarraiy et al. 2010). In the studies performed in West Azerbaijan Province Hyalomma ticks were dominant as 63.2% and 61.3% respectively (Davoudi et al. 2008, Salari Lak et al. 2008). In the other study in West Azerbijan Rhipicephalus (42%), Hyalomma (41%), Boophilus (7%), Dermacentor (7%), and Haemaphysalis (3%) were found where Rhipicephalus as well as Hyalomma were the most prevalent tick species (Telmadarraiy et al. 2004). Thus could not be understand that in the most aforesaid studies Hyalomma ticks were the most abundant ticks, but the largest number of ticks that in Northwest of Iran were found belonging Rhipicephalus genus and the most abundant species in the study area was Rhipicephalus sanguineus which is in agreement with study of Hosseini vasoukolaei et al. (2010). Along with our findings, Nabian et al. (2007) found that R. sanguineus is the major species in Mazandaran Province and did not find R. bursa (Nabian et al. 2007), but result of our study show eight male and ten female R. bursa in contrast with only one female R. bursa (Hosseini vasoukolaei et al. 2010). In the study conducted by Rahbari et al. (2007) R. sanguineus was the main species in the North of Iran (Rahbari et al. 2007a). From the studies accomplished by Telmadarriy et al. (2004, 2008) and Davoudi et al. (2008) two species R sanguineus and R bursa were collected from different animals including sheep, goats, cattle, buffaloes and camels (Telmadarraiy et al. 2004, Telmadarraiy et al. 2008a), showing Rhipicephalus are concerned to blood of different hosts. According to these studies, it can be concluded that R. sanguineus is the tick species with great significance for domestic ruminants in the North of Iran. Razmi et al. (2007) found that Boophilus comprising the majority (51.3%) of ticks collected in a study conducted in Mazandaran Province following Hyalomma (18.5 %), Rhipicephalus (16.8%), Haemaphysalis (6.3%), Ixodes (6.3%) and Dermacentor (0.1%) were also present in the study area (Razmi et al. 2007), but in our study Boophilus collected with low frequency and never we collected Dermacentor species. The ticks of the genus Ixodes are the important vectors of Lyme borreliosis in Europe and America commonly collected in Iran with species I. ricinus only in the Caspian Sea littoral area (Nabian et al. 2007 Rahbari et al. 2007a, Razmi et al. 2007). In our study Ixodes tick were found with low frequency (1.3%). The most common ixodid tick vector of Human Granulocytic Ehrlichiosis (HGE) in Europe is I. ricinus (Rymaszewska and Grenda 2008). In a study by Bashiribod et al. (2004) in Ghaemshahr, 5.1% of all I ricinus ticks examined by molecular methods was shown to be infected with Anaplasma phagocotophilum (Bashiribod et al. 2004). In a study by Hosseini Vasoukolaei et al. (2010) 49 out of 323 collected ticks were identified as I ricinus, which is an important vector of tick-borne disease aforesaid and may be considered in the study area, need for further investigation (Hosseini vasoukolaei et al. 2010). In the study undertaken by Nabian et al. (2007) genus Ixodes was found with frequency 2.32% (Nabian et al. 2007). Several Haemaphysalis species were found in Iran. In the present study, H. erinacei, H. sulcata, H. punctata and H. inermis were collected from farm animals, in spite of only H. erinacei was reported in study of Hosseini Vasoukolaei et al. (2010) from North of Iran (Hosseini vasoukolaei et al. 2010). Rahbari et al. (2007) in a study completed in three geographical zone of Iran reported 6 species H. punctata (3.4%), H. parva (0.5%), H. sulcata (0.6%), H. choldokovskyi (1.7%) (now synonymized as H. sulcata), H. concinna (0.06%) and Haemaphysalis sp. (0.6%) but never reported H. erinacei and H. inermis (Rahbari et al. 2007b). Interestingly the latter species recorded by Telmadarraiy (2008) in South of Sari in Mazandaran Province (Telmadarraiy et al. 2008b). In respect of much Haemaphysalis are three host ticks thus they may be serve as competent vectors of different domestic ruminant thereupon human diseases. In the present work several Hyalomma including Hy. dromedarii, Hy. marginatum, Hy. asiaticum, Hy. excavatum, Hy. anatolicum, Hy. detritum were collected at least in all studied geographical areas. Whereas in a series studies conducted by one of authors (ZT) from year 2004 to year 2010 in Yazd, Ilam, East and West Azerbaijan, Ardabil, Hamadan, Khorasan Jonoobi Provinces as well as South of Sari in Mazandaran Province (Telmadarraiy et al. 2004, Telmadarraiy et al. 2006, Telmadarraiy et al. 2008a, Telmadarraiy et al. 2008b, Nasiri et al. 2010, Salim abadi et al. 2010, Telmadarraiy et al. 2010) various Hyalomma species were recognized like present study. Also author with cooperation other (2007, 2009, 2010) studied ectoparasite of rodents including ticks as well as lesser mouse eared bat, Myotis blyti (Telmadarraiy et al. 2007a, Kia et al. 2009, Vatandoost et al. 2010b). It is necessary indicate which Hyalomma species has critical role for transmission of Crimean Congo Hemorrhagic Fever. With respect to which is three geographic continents including mountainous, littoral and plateau possess Golestan Province species diversity and the number of species found in mountainous, littoral and plateau area comprising 6, 2 and 10 species respectively. Otherwise following ticks genera and species collected respect to three aforesaid situation constitute R. sanguineus (69%) in mountainous and (93.5%) in littoral area which is more incident from other species. Beside Hy. anatolicum (47.9%) and Hy. dromedarii (29%) in plateau area were dominant species. Whereas in a study conducted in plateau area of Yazd Province Hy. dromedarii was more prevalent species (55.92 %) while D. marginatus, Hy. marginatum and Hy. anatolicum ticks were collected with very slightly frequency (Salim abadi et al. 2010). In another study directed in Esfahan Province R. sanguinus in mountainous and Hy. anatolicum in plateau areas were the most abundant ticks respectively (Noaman et al. 2008). It may be concluded that genera of Rhipicephalus and Hyalomma are as principal genera in mountainous and plateau area respectively. In the present study most of tick species were collected from cattle, only Hy. dromedarii and Hy. detritum were found on camel. In addition Hy. anatolicum was predominant Hyalomma species obtained from cattle and the other tick genera and species including H. sulcata, H. erinacei (Haemaphysalis), Hy. asiaticum, Hy. excavatum (Hyalomma) and Boophilus (Rhipicephalus) annulatus only with low frequency collected from cattle host. Likewise the most number of species collected from two hosts camel and horse including Hy. dromedarii and Hy. anatolicum respectively.