Research Article

Prevalence and Morphological Identification of Tick Infestation in Small Ruminants in Khyber Pakhtunkhwa, Pakistan

Zulfiqar Ali1, Asad Ullah2*, Shumaila Gul3, Maryam Begum4, Raheela Taj5, Tahira Tayyeb1, Maiz ur Rahman1, Muhammad Owais Khan1, Rafiq Ullah1, Imad Khan2, Ali Gohar2, Shakirullah Khan6, Khudija Ghani7 and Muneeb Islam8

1Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan; 2College of Veterinary Science and Animal Husbandry (CVS and AH), Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan; 3Department of Chemical and Life Sciences, Qurtuba University of Science and Information Technology Peshawar, Khyber Pakhtunkhwa, Pakistan; 4Department of Zoology, Women University Swabi, Swabi, Khyber Pakhtunkhwa, Pakistan; 5Institute of Chemical Sciences (ICS), University of Peshawar, Khyber Pakhtunkhwa, Pakistan; 6Veterinary Research and Disease Investigation Center (VR and DIC), Balogram Swat, Khyber Pakhtunkhwa, Pakistan; 7Sarhad Institute of Allied Health Sciences, Sarhad University of Science and Information Technology, Peshawar, Khyber Pakhtunkhwa, Pakistan; 8Department of Microbiology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.

Received | January 27, 2024; Accepted | August 06, 2024; Published | September 17, 2024

*Correspondence | Asad Ullah, College of Veterinary Science and Animal Husbandry (CVS and AH), Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan; Email: asadullah@awkum.edu.pk

Citation | Ali, Z., A. Ullah, S. Gul, M. Begum, R. Taj, T. Tayyeb, M. Rahman, M.O. Khan, R. Ullah, I. Khan, A. Gohar, S. Khan, K. Ghani and M. Islam. 2024. Prevalence and morphological identification of tick infestation in small ruminants in Khyber Pakhtunkhwa, Pakistan. Sarhad Journal of Agriculture, 40(3): 1056-1064.

DOI | https://dx.doi.org/10.17582/journal.sja/2024/40.3.1056.1064

Keywords | Prevalence, Identification, Small ruminants, Tick, Infestation, Pakistan

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Pakistan is an agricultural country and a large portion of Pakistani people work in animal husbandry. Especially in rural areas, 43% of workers are employed in the agriculture sector. Pakistan is home to 30.9 million sheep, 78.2 million goats, 41.2 million goats, 49.6 million cattle, and 41.2 million buffalo (Khan et al., 2022). After mosquitoes, ixodid ticks (Acari: Ixodidae) are the primary global carriers of infections with significant medicinal and veterinary value (Githeko et al., 2000). The backbone of Pakistan’s economy is domesticated animals, yet ectoparasites have prevented farm animal production from reaching its full potential (Sajid et al., 2008). Ticks are hematophagous parasites that harm people, domestic animals, and wild animals worldwide. Anemia, allergic responses, paralysis, and toxicoses are only a few examples of the direct harm that they inflict on their hosts (Cabezas-Cruz et al., 2014).

Ticks and the infections they spread directly harm animals by lowering the quality of their hides, their live weight, and their milk supply. Ticks can also result in anemia, toxemia, and paralysis, so they pose a significant barrier to producing a healthy livestock business. In tropical places of the whole world where farmers raise cattle, ticks cause substantial economic losses. For the proprietors of resource-constrained, small-holder dairy farms in subtropical nations like Pakistan, the livestock (Bubalus bubalis; population: 40 million) and cattle (Bos indicus and B. taurus; population: 47.8 million) are essential sources of revenue (Ghafar et al., 2020).

Ticks cause global output waste of between USD 22 billion and USD 30 billion annually, with the majority of these losses taking place in underdeveloped nations (Lew-Tabor and Valle, 2016). In livestock, ticks can result in economic losses due to tick burden, blood loss, injury to skin and mammary glands, tick poisons, or mortality or infirmity brought on tick born diseases (TBDs). Due to decreased milk production, decreased live weight gains in cattle, and damaged skins, these significant losses have a negative shock on the livelihood of farmers with limited resources (Dantas-Torres et al., 2008). Due to tick bites, tick infestations result in sores, infections, blood loss, and the possible spread of diseases. Tick-borne pathogens (TBPs) affect both human and animal health globally and include viruses, bacteria, protozoans, and helminths (Estrada-Peña et al., 2008). Diseases are caused by the former, whereas the latter are essential for keeping the vector healthy. Intracellular bacteria of the genus Rickettsia are responsible for tick-borne rickettsioses. A high temperature, rash, myalgia, headache, and lymphadenitis are some of the clinical symptoms (Onyiche et al., 2020). Animals and people can both contract infections from members of the genera Anaplasma and Ehrlichia (Family Anaplasmataceae) (Sharifiyazdi et al., 2017). Hard ticks of the genera Amblyomma, Haemaphysalis, Hyalomma, and Rhipicephalus are the primary local carriers of TBPs (Walker et al., 2003).

The province of Khyber Pakhtunkhwa, Pakistan is thought to be a hotspot for the development and reoccurrence of TBDs concern to both public health and veterinary medicine. Up to 75% of sheep, cattle, and goats in the area have been found to have tick infestations, compared to 58% of water buffalo. According to morphological identification, the tick species that were discovered to be infesting cattle the most commonly in Khyber Pakhtunkhwa Pakistan were R. annulatus, R. microplus, Hy. aciculifer, R. appendiculatus, and R. decoloratus (Farooqi et al., 2017; Nieto et al., 2012; Sajid et al., 2017).

Various risk factors have been linked to tick infection in livestock animals in past. For instance, various regions of the world have investigated how environment and host characteristics affect the dispersion of cow ticks. Only a few studies in Pakistan have identified the risk factors for tick infestation on livestock farms; therefore, examining these risk factors at the level of small-scale farmers may be crucial for developing a program for tick management that is both successful and affordable (Estrada-Pena, 2009; Sajid et al., 2009; Iqbal et al., 2013).

Nevertheless, accurate morphological identification of ticks takes knowledge, and it may be difficult with engorged or physically harmed specimens. As a result, other approaches, like the use of mitochondrial markers, cox1, and 16S rRNA, are suitable for molecular identification and inferring phylogenies of the tick species, which has resulted in the creation of the DNA barcoding system for ticks (Lv et al., 2014; Duron et al., 2015; Kasi et al., 2020). There hasn’t been any research done in Pakistan yet that looks at the molecular traits, genetic diversity, and epidemiology of hard ticks that infest dogs, except one morphological study that listed the three main genera of ixodid ticks (Haemaphysalis, Hyalomma, and Rhipicephalus) (Kasi et al., 2020; Zeb et al., 2019). The current study was designed to identify ticks morpho-molecularly in a randomized sample of livestock to evaluate their prevalence, spatiotemporal distribution patterns, associated risk factors, and molecular phylogenies in District Mardan, Buner, and Dir Lower, Khyber Pakhtunkhwa Pakistan.

Materials and Methods

Study area

The current study was in District Mardan, Buner, and Dir Lower, Khyber Pakhtunkhwa Pakistan from January 2022 to January 2023 (Figure 1). Mardan is located at an elevation of 310.42 meters (1018.44 feet) above sea level, Mardan has a Humid subtropical, no dry season climate. The district’s yearly temperature is 18.94ºC (66.09ºF) and it is -1.95% lower than Pakistan’s averages. Mardan typically receives about 127.16 millimeters (5.01 inches) of precipitation and has 140.52 rainy days (38.5% of the time) annually. District Buner is located on elevation of 944 meters (varies from 200 ft to 9550 ft) above sea level. The highest maximum temperature ranges from 40ºC to 44ºC during May to July. Annual rainfall ranges between 672mm to 1198mm. The elevation of Dir Lower ranges from 1200m to 2800m above sea level. The highest temperature ranges from 30ºC to 35. Annual rainfall at Dir averages 58 inches, of which 400mm falls during the summer and twice that amount during the winter. High temperature and humidity throughout the summer time create ideal circumstances for tick development and infestation in this area.

 

Sample size, collection, and preservation

A total of 114 villages were chosen depending on the availability of permits. Using a prescribed methodology, they were screened for ticks (Ica et al., 2007). Ticks were collected from different parts of the body and examined for species identification. The mouthparts of any ticks found were carefully removed with forceps to preserve their integrity (Soulsby Hilminthes, 1982). All parts of the host body (ear, mammary gland, genital organ, tail, and body) were deeply examined for the presence of the tick. After being separated from the body of the host, ticks were preserved in 70% ethanol. The collected ticks were kept in a safe tube in a refrigerator. Ticks have been collected in a cryogenic tube. Irrespective of the gender of animal ticks’ collection has been done. A maximum of 10 and a minimum of 5 ticks were collected per host from different parts of the body.

Morphological identification

Samples are properly identified and sealed for storage in refrigerators. Using a stereomicroscope and a species-specific identification key, the morphological characteristics such as scutum pattern, spiracle plate, coxa structure, adanal plates and capitulum shape were determined.

First, a gross identification of the ticks was performed. As a final step, the ticks were classified into different species depending on their morphology and basic structural characteristics. Such as the shape of the scutum, and its ventral structure. After genera identification of collected ticks, female adult ticks of each genus were separated by observing small areas of scutum on the anterior dorsum. All Ticks Identification whether male or female has been done by using a stereomicroscope and identified using different taxonomic keys like ticks of domestic animals in Africa: A guide to identification of species (Walker et al., 2003; Kaiser et al., 1963). The collected data were analyzed, and the abundance of each tick species was determined on the geological chart. Seasonal-wise prevalence variation of ticks has been shown.

Results and Discussion

The present results discover the prevalence of three tick genera and the ten species that are Haemaphysalis punctata, Haemaphysalis sulcata, Rhipicephalus senegalensis, Rhiphicephalus lunulatus, Rhiphicephalus turanicus, Rhiphicephalus microlus, Hyalomma excavatum and hyalomma dromedarrii, Hyalomma anatolicum, Rhipicephalus sanguineus. A total of 5000 goats and sheep of various ages, breeds, sexes, and locations were inspected and examined for tick infestation. A total of 1774 goats and 1044 sheep were found to be tick infested, and the percentage prevalence was 59.37 for goats and 51.45 for sheep were recorded as shown in Table 1. The unidentified and immature ticks on both hosts were neglected from discussion and analysis due to the difficult identification. The tick infestation rate was recorded in three different districts of Khyber Pakhtunkhwa with significant variation. For Goats the highest prevalence of tick infestation was recorded in Mardan while for sheep, the highest prevalence was observed in District Dir Lower (Figure 2).

 

Table 1: Percent prevalence of tick infestation in goats and sheep population in the study area.

Hosts	Non-infested population	Tick-infested population	Total population	Prevalence (%)
Goats	1214	1774	2988	59.37
Sheep	985	1044	2029	51.45

 

 

District-wise tick prevalence

The results of tick species collected and identified from districts Mardan, Buner, and Dir Lower, Khyber Pakhtunkhwa confirmed the distinct distribution patterns. Rhiphicephalus microplus, Haemaphysalis sulcata, Rhiphicephalus senegalensis, Rhipicephalus lunulatus, and hyalomma excavatum were reported from the goats of district Mardan (Table 2, Figure 3). Haemaphysalis punctata, Haemaphysalis sulcate, and Hyalomma dromedarri were found in sheep of district Mardan (Table 3, Figure 4). Rhiphicephalus microplus, Rhiphicephalus senegalensis, and Haemaphysalis suclcata were reported in goats of district Buner (Table 2). Haemaphysalis sulcate, and Haemaphysalis punctata were present on sheep of district Buner (Table 3). Haemaphysalis sulcata and Haemaphysalis punctata were present in the sheep as well as in goats of district Dir Lower.

 

Table 2: Prevalence of tick infestation in goat population in district Mardan, Buner and Dir Lower.

District	Identified tick species
	Rhiphice-phalus microplus	Haema-physalis punctata	Haema-physalis sulcata	Hyalomma excavatum	Rhiphice-phalus turanicus	Rhiphice-phalus sene-galensis	Rhiphice-phalus lunulatus	Hyalo-mma drome-darri	Hyalo-mma anato-licum
Mardan	178	92	189	134	49	120	78	97	122
Buner	132	101	244	44	32	92	56	22	40
Dir Lower	102	244	332	0	0	27	17	0	0

 

Table 3: Prevalence of tick infestation in sheep population in district Mardan, Buner and Dir Lowe.

District	Identified tick species
	Rhiphice-phalus microplus	Haema-physalis punctata	Haema-physalis sulcata	Hyalomma excavatum	Rhiphice-phalus turanicus	Rhiphice-phalus senegalensis	Rhiphice-phalus sanguineus	Hyalo-mma drome-darri	Hyalo-mma anato-licum
Mardan	72	101	98	47	86	120	39	42	92
Buner	61	201	144	20	67	52	0	0	0
Dir Lower	93	344	232	11	0	27	0	0	0

 

 

 

 

Seasonal prevalence of ticks

Tick prevalence showed different variations in the four seasons. Summer was the most prevalent and maximum number of ticks has been collected in the summer which was about 2527 ticks followed by spring in which 1273 ticks were collected. In autumn season which was less prevalent, the collected ticks count was 702. Winter was the less prevalent season and hardly 339 ticks were collected throughout the winter (Figure 5).

Genera-based prevalence of tick infestation

The high infestation rate of Haemaphysalis punctata, and Haemaphysalis sulcata was recorded in district Dir (lower) in sheep. The dominant tick genera of Dir Lower was Haemaphysalis. Rhiphicephalus and Hyalomma were the dominant species identified in district Mardan. District Buner dominant tick species was also Haemaphysalis.

In the research investigation, distinct tick species were recorded amongst different host animals. Hard tick’s higher prevalence in goats and sheep has several contributing factors such as climate conditions, average temperature, relative humidity, vegetation type, and landscape which provide favorable environments for the development of many tick’s species (Bacon et al., 2022). Various conditions which may affect the reproduction and development of ticks in a specified locality include humidity, temperature, and precipitation (Greenfield, 2011).

Among the ticks collected and identified from goats and sheep ten tick species were identified from three different districts of Khyber Pakhtunkhwa, Mardan, Buner, Dir Lower. These ten tick species have belonged to three genera Hylomma, Haemaphysalis, and Rhiphicephalus. In our findings, the prevalence of Haemaphysalis and Rhiphicephalus were recorded higher. A similar study was conducted by Farooqi et al. (2017) in which the occurrence of hard tick species was investigated in different ecological zones of Khyber Pakhtunkhwa and documented Haemaphysalis and Rhiphicephalus as the abundant genera while the least abundant tick genus was Hyalomma (Farooqi et al., 2017).

These ticks species belonged to the above genera Rhiphicephalus, Haemaphysalis, and Hyalomma are known to be facilitators of several tick-borne infections and have been reported previously (Telmadarraiy et al., 2015; Mans et al., 2015; Ghafar et al., 2020; Estrada-Peña et al., 2008). Tick fauna associated with the study has previously been described in South Africa (Jongejan et al., 2020); Lebanon (Dabaja et al., 2017) and Pakistan (Muhammad et al., 2008).

Our results showed that goats were infested with ticks at 59.37% while sheep were infested with ticks at 51.45%. The highest tick infestation was observed in the sheep than in goats of district Dir Lower. This pattern has been also recorded in some studies of tick infestation of animals in Pakistan (Rashid et al., 2018; Ramzan et al., 2019). The highest tick infestation was observed in the goats than in the sheep of district Mardan which was by the results of Rehman et al. (2017). But this report was opposite in Dir Lower case as there were higher tick infestations in sheep than goats. The relatively high infestation of ticks may be due to their skin as they have thin skin as compared to other animals. This may be due to hilly and semi-hilly areas while plain areas have the highest infestation recorded in goats. The highest distribution of hard ticks in our study could be due to prevailing rainfall, relative humidity, host availability, condition of host body, acaricides application, breed, age, sex, average temperature, altitude, vegetation type, landscape of area animal husbandry practices (Estrada‐Peña, 2003; Burri et al., 2007; Gray, 2008; Rony et al., 2010; Sajid et al., 2011).

In the current study sheep and goats in the 1-2 years age group were more infected than those older than 2 or more-year age group. Our finding results agree with previous findings that the younger animals shows more vulnerability to tick infestation than the adult hosts (Abera et al., 2010). The possible justified answer to this might be that after continuous exposure to tick infestation, the adult host has developed resistance also because of the soft skin of younger animals. The younger animals were also directly connected with their parents and other animals through which the tick transfer occurred.

The high prevalence rates of tick infestation in all three districts were recorded throughout the summer which are likely due to the humidity, moisture, and high temperature. It was according to the previous studies which also shown peak infestation rates in summer (Gul et al., 2021; Ullah et al., 2018).

Furthermore, the current results showed that the female tick’s prevalence was more as compared to the prevalence of male ticks previously reported by Mustafa et al. (2014). Tick prevalence was somewhat higher in female sheep and goats than in males. This was against some previous studies (Shoaib et al., 2021).

Conclusions and Recommendations

The present study showed the prevalence of ticks and identified ten (10) tick species that belonged to three main genera Haemaphysalis, Rhipicephalus, and Hyalomma were the predominant tick species in small ruminant populations in district Mardan, Buner, and Dir Lower, Khyber Pakhtunkhwa, Pakistan. These ticks feed on blood and transmit various diseases affecting both domestic animals and humans directly or indirectly. It is evident from our study that tick infestation has an existing animal population and is a major threat to both the human and animal population in the area. It is recommended that necessary control measures and awareness campaigns should be adopted and implemented at the government level to control the problem of tick infestation in both small and large ruminant populations in the province of Khyber Pakhtunkhwa, Pakistan.

Acknowledgments

The authors are thankful to the supporting staff of both the College of Veterinary Science and Animal Husbandry (CVS and AH) and Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan for their assistance during this research study.

Novelty Statement

This research and experimental work on “Prevalence and Morphological Identification of Tick Infestation in Small Ruminants in Khyber Pakhtunkhwa, Pakistan” is original and new in the field of zoology in Khyber Pakhtunkhwa, Pakistan.

Author’s Contribution

Zulfiqar Ali: Investigation, writing-original draft preparation.

Asad Ullah: Supervision.

Shumaila Gul: Project administration.

Maryam Begum: Resources.

Raheela Taj: Formal analysis.

Tahira Tayyeb: Methodology.

Maiz ur Rahman: Visualization.

Muhammad Owais Khan: Data curation.

Rafiq Ullah: Conceptualization.

Imad Khan and Ali Gohar: Writing-review and editing.

Shakirullah Khan and Khudija Ghani: Softwar.

Muneeb Islam: Validation.

Statement of conflict of interest

The authors declared no potential conflicts of interest with respect to research, authorship, and/or publication with the work submitted.

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