Prevalence of Ectoparasitism on Small Ruminants in Kelantan, Malaysia

Kelantan is a chiefly agrarian state with abundant small-holder ruminant farms in the East Coast economic Region of Malaysia. Ectoparasitism affects small ruminant production in Malaysia. It often causes reduction in meat quality and milk production which affect the farmers’ income. To date, no report for the prevalence of ectoparasitism on small ruminant in Kelantan compared to other state in Malaysia. This study aims to determine the prevalence and associated risk factor of ruminant ectoparasitism in Kelantan. Ectoparasites were collected by manual picking and skin scrapping from 462 sheep and goats in Kelantan between April and September 2017 (during dry season). 60% of the sampled animals were infested with at least one species of the ectoparasites. In this study, lice and ticks were the most prevalent ectoparasites on small ruminant, which were 43.64% and 22.98%, respectively. The high biotic potential of lice population on host might be one of the factors they become the most prevalent species found on the animals. There was no significant relationship between ectoparasitism prevalence and species of small ruminants (χ2 = 1.12, p = 0.293). However, there was significant variations in prevalence between the regions where the animals were sampled from (χ2 = 30.25, p = 0.002) and farm management system for both species. This present study provides baseline epidemiological data on the prevalence of ectoparasitism in small ruminant. This information is useful for the formulation of prevention and control measures in order to enhance ruminant productivity in Kelantan.


INTRODUCTION
Kelantan is a chiefly agrarian state located in the northeast region of Peninsular Malaysia. It has ambient temperatures ranging from 24°C to 33°C (WorldData.info 2019) and a distinct October to March monsoon season. Small-scale backyard and small-holder ruminant production are common practices in Kelantan as are in other regions of Malaysia (Mohamed 2007). Farmers rear small ruminants, sheep and goats for their high fertility and short generation interval (in comparison to cattle). These traits are minimally affected by harsh environmental conditions and hence their production serve as source of secondary income and insurance for locals (Olafadehan et al. 2014).
Even though small ruminants accounts for 5% to 10% of Malaysian National Gross Domestic Products (GDP), their contribution to food production and national meat and milk self-sufficiency as well as supporting rural income are far below desired levels (Mohamed 2007). The major constraints to small ruminant production in Malaysia are diseases, limited feed resources and poor management systems. Ectoparasitism being a disease entity caused by parasitic infestation is able to cause overall deterioration of small ruminants' production and reproduction that eventually lead to serious economic losses to the small-holder farmers and the country as a whole (Shanmugavelu 2014).
Heavy infestation of ectoparasites such as lice, ticks, mites and fleas cause lower skin and hide quality, poor body condition along with reduction in milk and meat production (Abebe et al. 2011). Medical management of the diseases transmitted by these arthropods are accounted for economic losses to the farmers (Seyoum et al. 2015).
Despite of the economic and animal health importance of these ectoparasites, there is a lack of information on their prevalence and spatial distribution in small ruminants in the East Coast economic region of Malaysia.
47 Therefore, the objectives of this present study are to determine the prevalence of ectoparasites in small ruminants in Kelantan and identify the risk factors associated with the ectoparasitism.

Study Area
Field work was conducted in 10 districts of Kelantan, Malaysia within latitude 6°07'31.43" N and longitude 102°14'17.06" E. Sampling was conducted between April to September 2017 corresponding to the dry season. Farms were randomly selected from each of the 10 districts irrespective of their farm management systems viz. intensive, semi-intensive and extensive. Farms were identified and randomly selected from the Department of Veterinary Services, Kelantan database.

Sample Size Determination
Number of animals required to measure the prevalence of ectoparasites was calculated based on 50% expected prevalence (used to maximise sampling) at 95% confidence level and 5% desired absolute precision (Thrusfield 2005). Hence, the minimum number of animals utilised for the study was 384 (192 of sheep and 192 of goats).

Sampling Methods
Parameters such as age, gender, body score and farm management practices were recorded prior to the physical examination and sample collection. Survey forms (questionnaires) were distributed to farmers to obtain additional background information of the farm. The selected sheep and goats were physically examined for the presence of ectoparasites and lesions. Physical examination of the integumentary system was performed by multiple fleece parting in the direction opposite to hair normally rests as well as by visual inspection. Ectoparasites such as lice, ticks and fleas were collected manually (by hand or forceps) and preserved in separate vials containing 70% ethanol (Urquhart et al. 1996). Skin scrapings for mites were obtained from sheep and goats with mange-associated skin lesions (such as crustiness) and processed according to the method described by Cole (1986).

Ectoparasites Identification
Collected samples were examined under stereomicroscope for lice, tick and fleas through their morphological features. The identification up to genus level was performed by referring to the identification key in the guidelines given by Walker et al. (2003) for ticks and Wall and Shearer (2008) for lice, fleas and mites.

DATA MANAGEMENT AND ANALYSIS
Data management was conducted by using Microsoft Excel ® and all recorded data were analysed using Statistical Package for Social Science (SPSS ® ) version 20. Descriptive statistics, percentages and 95% confidence interval were used to summarise the proportion of infested and non-infested animals. The association with different risk factors on the prevalence and distribution of ectoparasites were analysed using Chi-square test. The differences were considered as significant when at 95% confidence intervals while statistical significance was set at p < 0.05.

RESULTS AND DISCUSSION
The prevalence of ectoparasitism in small ruminants was significantly associated with the region where the animals were sampled from (χ 2 = 30.25, p = 0.002158). In the coastal region of Kelantan, the prevalence of ectoparasitism was 50.71%; while in the inland region the prevalence of ectoparasitism was 73.71% (Table 1). This study observed a statistically significant relationship in prevalence between different regions of the state (p < 0.05). Ectoparasitism in sheep and goats was higher in the inland areas of Kelantan with a prevalence of 73.71% in comparison to coastal areas (50.71%). The high prevalence of ectoparasitism in the inland regions of Kelantan is associated with the presence of conserved forested areas which provides favourable climatic and environmental conditions for the thriving of ectoparasites. Geographical factors are known to affect the distribution of many animal species and thus ectoparasites (Watanabe et al. 2016). Other researchers have also presented similar results for inland and coastal regions in different countries (Ghosh et al. 2007;Bermudez & Miranda 2011;Tamerat et al. 2016). There was a statistically significant association between the prevalence of caprine ectoparasitism and farm management system (χ 2 = 6.06, p = 0.048). Higher prevalence caprine ectoparasitism was observed in farms practicing semiintensive management system (73.33%) followed by extensive (67.39%) and intensive (59.69%) management systems (Table 2). There was also a statistically significant association between prevalence of ovine ectoparasitism and farm management system (χ 2 = 51.12, p < 0.0001). Higher prevalence of ectoparasitism in sheep was observed in farms practicing semi-intensive management system (78.42%) while farms practicing the intensive system had 30.68% prevalence ( Table 2). Extensive farm management was not practiced for sheep in the farms studied in Kelantan. The current study revealed that farm management practices has statistically significant relationship with the prevalence of ectoparasitism in small ruminants (p < 0.05) in Kelantan. Extensive and semi-intensive management has high prevalence of ectoparasites due to higher risk of exposure to ectoparasites during grazing (Wall & Shearer 2008). In semi-intensive management practices exposed animals easily spread the ectoparasites to other animals in the farm on return via contact (Diaz 2006). In this study, the overall prevalence of small ruminant ectoparasitism was 63.20% (292/462). The highest ectoparasite was lice, which were 43.64% discovered in the small ruminant. The optimum temperature and humidity in the study area attributed to the reproduction of lice on these small ruminants. This study conducted on a tropical environment. Tropical climates promote a higher number of parasitic load in small ruminants (Azfan 2018). Subsequently, with tick, which was 22.98% found in this study. Ectoparasitism prevalence in sheep was found to be 59.91% (136/227) while in goats 64.68% (156/235). There was a statistically significant difference in ectoparasite prevalence between sheep and goats (χ 2 = 4.36, p = 0.038). The prevalence of ectoparasites identified on goats were lice (48.94%) followed by ticks (20.85%), fleas (1.70%) and mites (1.28%). Similar findings were observed for sheep with lice being the dominant ectoparasite (38.33%), followed by ticks (25.11%) and fleas (0.88%) (Fig. 1). The prevalence of caprine ectoparasitism of the present study differs from what had been reported by Khadijah et al. (2014), where 80% of caprine ectoparasitism were reported in Kuala Terengganu, Peninsular Malaysia. The prevalence of ectoparasites infestation were higher in Terengganu because the smaller number of animals was sampled and the area that had been covered also limited. The variation of ectoparasitism prevalence in different study areas also could be due to differences in the management, agro-climate, seasons, health care and ectoparasite control practices in the respective study areas (Tamerat et al. 2016). It is evident that the prevalence of small ruminant ectoparasitism in this study is high in Kelantan, thus indicating a chronic underreporting of the condition in the state. This study identified an overall 62.99% prevalence of ectoparasites infestation; out of which 59.91% was the prevalence of ovine ectoparasitism and 64.68% for caprine ectoparasitism. This finding is in line with that of Jarso et al. (2014) who reported ectoparasitism prevalence of 10.3% for sheep and 16.5% and goats in the Kombolcha region of North East Ethiopia. In a similar study in Ethiopia reported an ectoparasitism prevalence of 42.2% and 51.4% for sheep and goats, respectively (Tamerat & Zeryehun 2015). Bovicola caprae and Linognathus africanus were found on the goat meanwhile only Bovicola ovis was found on the sheep (Fig. 2). Lice species that were found on individual animals studied, where chewing lice (Bovicola sp.) were widely distributed on the animal's body than the sucking lice (Lignonathus sp.). This study revealed that lice and ticks are common ectoparasites on small ruminants in Kelantan. Yakhchali and Hosseine (2006) reported that lice and ticks are common ectoparasites on small ruminant in Urmia suburb, Iran. Moreover, Mbuh et al. (2008) also reported only tick and lice that were common ectoparasites on small ruminants in Bokova, a rural area of Buea Sub Division, Cameroon. Among the ectoparasites detected, lice were found as the most prevalent in both sheep and goat, which comprised 43.72% of the total prevalence. This result in concordance with previous studies that reported lice as the most prevalent ectoparasite species in small ruminants (Eticha et al. 2017;Getaneh et al. 2016;Seyoum et al. 2015). The high prevalence of lice might due to the high biotic potential of lice population in the host (Bates 2012). As the entire lifecycle of lice is completed within one host, population of lice can be rapidly established once they come into contact with a suitable host. Spreading of lice to other animals within same herd is not uncommon as the transmission of lice can be achieved through close proximity contact (Hart 1994). Result from this study revealed that tick's prevalence was higher in sheep compared to goat. This was in agreement with Fentahun et al. (2012) and Yacob et al. (2008), who also reported a high prevalence of ticks in sheep than in goats. The variation in tick prevalence on different species is be attributed to a variety of factors such as behavioural characteristics of different species of animals, awareness/education of the farmers and farm management practices (Ghosh et al. 2007). Tick collected from sheep and goats in this study belonged to four genera which are Haemaphysalis, Boophilus, Rhipicephalus and Amblyomma. Three tick genera, Haemaphysalis, Boophilus and Rhipicephalus were found to be common on both sheep and goats while the genus Amblyomma was only present on sheep (Fig. 3). The study by Irshad et al. (2010) revealed that Rhipicephalus, Haemaphysalis, Ixodes and Ambylomma were found in sheep and goats at two different livestock farms located in the Potohar region, namely Barani Livestock Production Research Institute (BLPRI) Kherimurat, District Attock and National Agricultural Research centre (NARC), Islamabad, Pakistan. Another study by Jafer et al. (2017) reported that Boophilus, Rhipicephalus, Amblyomma and Hyalomma were found on small ruminants in and around Dire Dawa, eastern Ethiopia. On the other hand, three genera of ticks viz. Boophilus, Amblyomma and Rhipicephalus were identified both on sheep and goats by Sertse and Wossene (2007) in eastern part of Amhara region, northeast Ethiopia and by Adang et al. (2015) in the northeast of Nigeria. The flea, Ctenocephalides sp. was found on both sheep and goats reared in farms with poor management practice (Fig. 4). The prevalence rate for flea infestation in this study area -Kelantan, was 1.30%. This study showed lower prevalence compared to the study done by other researchers in Nigeria, northwest Ethiopia, southern Ethiopia, northeast Ethiopia and in Tanzania (Kusiluka et al. 1995;Sertse & Wossene 2007;Yacob et al. 2008;Fentahun et al. 2012;Adang et al. 2015;Seyoum et al. 2015). This is probably associated with the lower humidity on the study area during the dry season with the average of relative humidity of 60%, when > 70% of relative humidity is usually required for survival at the high temperature (Soulsby 1968).
Mange mites, Sarcoptes sp. were found only on goats in few farms (Fig. 4). The mange mite Sarcoptes was found to be of lesser prevalence (1.28%) than other ectoparasites in goats in Kelantan. This result is lower compared to Dorny et al. (1994) who reported a prevalence of mites (88%) on goats in Selangor and Perak. Kelantan also has a lower prevalence of mange mites compared to reports from other countries, 20% (UK) by Lusat et al. (2009), 52% (north-western Kenya) by Wafula et al. (2008) and 100% of caprine flock (north-eastern Italy) by Menzano et al. (2007). These differences in prevalence might be due to difference in animal population which causes unfavourable condition for the transmission of mites between animal and result in lower level of mite infestation (Tesfaheywet & Simeon 2016). Besides, Sarcoptes sp. was the only one genus that found in this study. This is similar findings from the previous study done by León-Vizcaíno et al. (1999) and Gabaj et al. (1992), who reported that Sarcoptes was the common mites found on goats.

CONCLUSION
In conclusion, this present study revealed that high prevalence of small ruminant ectoparasitism could be the major causes of sheep and goat production constraints and quality deterioration. Ectoparasitism in sheep and goats was higher in the inland areas compared to the coastal area. Our result also showed that semiintensive and extensive management system have the highest ectoparasitism rate. Hence, it would be valuable to implement effective extension system for the management and more programs that could lift up community awareness based on the risk factors as mentioned in this study. This particularly dedicated on farm management, effect of ectoparasites, and strategic practice of control measures with full cooperation from farmers and authorities (Veterinary department) in the districts area. More studies on ectoparasitism needs to be conducted in this region and Peninsular Malaysia to provide information on prevention and control measure in order to farmers' income and improve agriculture industry.