Part I: Ectoparasite prevalences in sheep and in goats in and around Wolaita soddo, Southern Ethiopia

Part I: Ectoparasite prevalences in sheep and in goats in and around Wolaita soddo, Southern Ethiopia H. T. YACOB, T. A. YALEW, A. A. DINKA* Faculty of Veterinary Medicine, Addis Ababa University, P.O.Box 34, Debre Zeit, ETHIOPIA. *Corresponding author: dinka_ayana@yahoo.com SUMMARY The study was conducted during the period between November 2006 to May 2007 to identify ectoparasites and to determine their prevalence in small ruminants in and around Wolaita Soddo (Southern Ethiopia). A total of 214 sheep and 102 goats of both sexes (169 females and 147 males) divided in young and adult animals (72 and 244 respectively) were examined for the presence of ectoparasites or skin lesions. The overall ectoparasite prevalence was 55.7% (147 infested sheep and 29 infested goats) and sheep were significantly more often infected than goats. Within the sheep population, the ectoparasite frequency was significantly higher in females than in males. The main ectoparasites identified in this geographic area were ticks (Rhipicephalus, Boophilus and Amblyomma) and fleas (Ctenocephales felis and canis at a lesser extend). The tick infestation was significantly more frequently observed in sheep (31.78%) than in goats (18.63%) and was unaffected by the sex or the age. By contrast, the flea prevalence was similar in the 2 ruminant populations, the females (particularly in goats) or the young animals (particular in sheep) being significantly less resistant to the flea infestation. Only one case of mange (Demodex caprae) was diagnosed in a goat and pediculosis (Damalinia ovis) was only observed in sheep with a relative high frequency (25.70%). Although these results emphasize the relative higher resistance of goats compared to sheep towards ectoparasites and the low tick prevalence in Southern Ethiopia whereas the pediculosis infection rate would considerably vary according to the climatic conditions during the experimental period, this study demonstrates that ectoparasites greatly affect ruminant health and require an urgent control intervention. Keywords: Ectoparasites, prevalence, sheep, goat, Wolaita Soddo, Ethiopia. RÉSUMÉ Partie I : Fréquences des ectoparasitoses chez les moutons et les chèvres aux environs de Wolaita soddo au sud de l Ethiopie Cette étude conduite entre Novembre 2006 et Mai 2007 a pour objectifs d identifier les ectoparasites et de déterminer leur fréquence chez les petits ruminants de la région de Wolaita Soddo (sud de l Ethiopie). La présence d ectoparasites ou de lésions cutanées a été recherchée sur 214 moutons et 102 chèvres des 2 sexes (169 femelles et 147 mâles) divisés en jeunes et en adultes (72 et 244 animaux respectivement). La prévalence globale des ectoparasites a été de 55.7 % (147 moutons et 29 chèvres infestés), les moutons étant significativement plus souvent infestés que les chèvres. En outre, au sein de la population ovine, une plus forte prévalence a été observée chez les femelles (p < 0.05). Les principaux ectoparasites identifiées dans cette zone géographique ont été les tiques (Rhipicephalus, Boophilus et Amblyomma) et les puces (Ctenocephales felis et canis à un moindre degré). L infestation par les tiques s est avérée significativement plus fréquente chez les ovins (31.78 %) que chez les caprins (18.63 %) et serait indépendante de l âge ou du sexe. En revanche, les taux d infestation par les puces étaient équivalents dans les 2 populations de ruminants, les femelles (essentiellement chez les chèvres) ou les jeunes (surtout chez les ovins) étant infestés de façon privilégiée. Un seul cas de gale (Demodex caprae) a été diagnostiqué chez une chèvre et la pédiculose due à Damalinia ovis n a été observée que chez les ovins avec une fréquence relativement élevée (25.70 %). Bien que ces résultats soulignent une meilleure résistance des caprins aux ectoparasitoses et une fréquence relativement faible des tiques dans le Sud de l Ethiopie alors que la prévalence de la pédiculose semble fortement soumise aux conditions climatiques durant la période d étude, cette étude montre que les ectoparasitoses affectent fréquemment les petits ruminants et doivent être urgemment contrôlées. Mots-clés : Ectoparasites, prévalence, mouton, chèvre, Wolaita Soddo, Ethiopie. Introduction It has been estimated that more than 38 millions cattle and 30 millions small ruminants, constitute the major portion of livestock resources in Ethiopia [8]. Meanwhile, small ruminants constitute about 30% of the total live stock population of the country [10] and are among important contributors to food production in Ethiopia, providing 35% of meat consumption and 14% of milk consumption [3]. In central highlands, where mixed crop livestock production system is practiced, small ruminants account for 40% of cash income and 19% of the household meat consumption [22]. Hides and skins account for 12-16% of the total value exports [3]. The current utilization of hides and skin is estimated to be 48% for cattle hide and 75% for goat skin [19]. Besides, wool and manure are also important products of small ruminants [15]. Even though small ruminants are important components of the Ethiopian farming system, their contribution to food consumption, rural income and export income are below the expected potential because small ruminant population in Ethiopia is constrained by the compound effect of diseases, poor feeding and poor managements [7]. Skin diseases caused by lice, sheep keds (Melophagus ovina), ticks and mange mites are among the major diseases of

ECTOPARASITES IN SMALL RUMINANTS FROM WOLAITA SODDO 451 small ruminants and cause serious economic loss to farmers through mortality, decreased production and reproduction, down grading and rejection of skins which also affect the tanning industries. According to tanneries report, skin diseases due to external parasites cause 35% sheep skin and 56% goat skin rejection [4]. In the study area (Southern Ethiopia), the population density of small ruminants is high and estimated to be 76 713 sheep and 98 493 goats [5]. However, because of various ectoparasites and skin diseases, small ruminant production and skin quality have been seriously affected and the situation is aggravated after nutritional and climatic stress following repeated drought [9]. Accordingly, the enormous economic losses induced by ectoparasites in small ruminants necessitate detailed investigation on their incidence in order to organize efforts to at least minimize these losses. This study is therefore aimed for assessing the prevalence of ectoparasites and determining the magnitude of these diseases in relation to age and sex of the animals. PROTOCOL DESIGN AND METHODS Animals were examined for presence of ectoparasites and skin lesions and after proper restraining some specimens were collected from diseased animals. Ectoparasites encountered either on the skin surface or attached to the hair were sampled and were collected in 70% alcohol. Further identification of the species was conducted in the laboratory according to methods described by SOULSBY [20]. Skin scrapping from suspected cases of mange were collected and preserved in 10% formalin. After addition of 10% KOH to the specimen, mites may be released from scabs and crusts before examination following procedures indicated by SOULSBY [20]. Multiple sites were scrapped to increase the likely hood of ectoparasite detection. Both superficial and deep skin scrapping were made to diagnose both burrowing and non burrowing mange [6]. Mange mites encountered were identified based on their morphological features [18]. Materials and Methods STUDY AREA The study was carried out in and around the Woliata Soddo region located between 6 36 N to 7 18 N latitude and 37 12 E up to 38 24 E longitude [5], in the Southern Ethiopia, at 383 km from Addis Ababa. Topographically, this region mainly consists in rugged and undulating mountains, rolling hills, plateaus and flat step slopes that extend to the Abaya Lake and to the Omo River [5]. The annual rainfall in the Woliata Soddo region ranges from 1 200-1 300 mm with a mean average temperature of 21 C [5]. ANIMALS From November 2006 to May 2007, 214 sheep and 102 goats of both sexes (147 males and 169 females) and of local breeds coming to the Soddo Veterinary clinic were included in the study. The age determination was made according to AIELLO and MAYS [2]. When lambs and kids were less than 6 month old, they were considered as young animals whereas when small ruminants were more than 6 month old they were included in the adult group. STATISTICAL ANALYSIS Proportions and the Pearson s chi-square test (X2) were used to analyze the data collected and differences were considered as significant when p-value was less than 0.05 [1]. Results The different ectoparasites identified were ticks (31.78% in sheep and 18.63% in goats), lice (25.70% in sheep and 0% in goats), flea (11.21% in sheep and 8.82% in goats) and mange (Demodex) (0% in sheep and 0.98% in goats) and the overall prevalence of ectoparasite was significantly higher in sheep (68.69%) than in goats (28.43%) (p < 0.001) (Table I). Moreover, considering the whole population of small ruminants, females (60.4%) tended to more often infested than males (49.7%) (p < 0.1) and the susceptibility of females to ectoparasites was confirmed in the sheep population (females: 75.45% and males: 61.54%, p < 0.05) but not in the goat population (Tables III and IV). No significant association between the ectoparasite prevalence and the age was evidenced in the whole population of small ruminants or in the sheep and goat specific populations. Ectoparasites Sheep (n = 214) Goats (n = 102) P Ticks 31.78 (68) 18.63 (19) < 0.05 Lice 25.70 (55) 0.00 (0) < 0.001 Flea Overall 11.21 (24) 8.82 (9) NS C. canis 3.74 (8) 1.96 (2) NS C. felis 7.48 (16) 6.86 (7) NS Mange 0.00 (0) 0.98 (1) - Total 68.69 (147) 28.43 (29) < 0.001 C. canis: Ctenocephales canis, C. felis: Ctenocephales felis, NS: not significant TABLE I : Prevalences in % (and number of cases) of ectoparasites observed in sheep (n = 214) and in goats (n = 102) in and around Wolaita soddo, Southern Ethiopia.

452 YACOB (H.) AND COLLABORATORS The proportion of sheep infected by ticks was significantly higher than that of goats (p < 0.05) (Table I) although the densities of ectoparasite by animal were similar (1.4 and 1.2 tick/animal in sheep and goat respectively) (Table II). The main tick species identified were Rhipicephalus (38.7% in sheep and 39.1% in goats), Boophilus (35.5% in sheep and 39.1% in goats) and Amblyomma (23.7% in sheep and 21.7% in goats). Only 2 ticks belonging to the Hyalomma genre were observed in sheep (Table II). No significant increase of the tick infestation risk was associated with the age or the sex in the 2 small ruminant species (Tables III and IV). The lice infestation was diagnosed only in sheep with a relative high prevalence (25.70%) whereas no case was observed in goats. Only the Damalinia genre was identified. Consequently, the difference for the pediculosis prevalences between the 2 small ruminant species was highly significant (p < 0.001) (Table I). The incidence of lice infestation was similar in both sexes, while the young sheep tended to be more resistant to this ectoparasite disease (p < 0.10) (Table III). In small ruminants, 2 flea species were identified: Ctenocephales canis and Ctenocephales felis, the last one being significantly more commonly detected in small ruminants with a frequency of 69.7% vs. 30.3% for C. canis (p < 0.05) (Table V). The prevalences of infestation induced by fleas whatever their genres or specifically by a given genre were similar in sheep and in goats. Moreover, males were significantly more resistant to the flea infestation than females within the whole small ruminant population (p < 0.05) (Table V) and particularly in goats (p < 0.05) (Table IV). Besides, young ruminants appeared to be significantly more frequently infected than adults by fleas (p < 0.05) and particularly by C. felis (p < 0.01) (Table V). This preferential infestation of young animals by C. felis was specifically evidenced in sheep (p < 0.05) (Table III). Tick infestation Sheep (n = 214) Goats (n = 102) Prevalence 31.78% 18.63% Number of infected animals 68 19 Total number of ticks 93 23 Ambylomma 22 (23.7%) 5 (21.7%) Boophilus 33 (35.5%) 9 (39.1%) Hyalomma 2 (2.2%) 0 (0%) Rhipicephalus 36 (38.7%) 9 (39.1%) Tick density (/ animal) 1.4 1.2 TABLE II : Tick infestation in sheep (n = 214) and in goats (n = 102) in and around Wolaita soddo, Southern Ethiopia. Ectoparasites Prevalence Sex Age (and number) Males (n = 104) Females (n = 110) p Young (n = 51) Adult (n = 163) P Tick 31.78 (68) 28.85 (30) 34.55 (38) NS 29.41 (15) 32.52 (53) NS Lice 25.70 (55) 24.04 (25) 27.27 (30) NS 15.69 (8) 28.83 (47) < 0.10 Flea 11.21 (24) 8.65 (9) 13.64 (15) NS 17.65 (9) 9.20 (15) NS C. canis 3.74 (8) 2.88 (3) 4.55 (5) NS 1.96 (1) 4.29 (7) NS C. felis 7.48 (16) 5.77 (6) 9.09 (10) NS 15.69 (8) 4.91 (8) < 0.05 Total 68.69 (147) 61.54 (64) 75.45 (83) < 0.05 62.75 (32) 70.55 (115) NS TABLE III : Prevalences in % (and number of cases) of ectoparasites observed in sheep (n = 214) according to the age and sex in and around Wolaita soddo, Southern Ethiopia. Ectoparasites Prevalence Sex Age (and number) Males (n = 43) Females (n = 59) p Young (n = 21) Adult (n = 81) P Tick 18.63 (19) 18.60 (8) 18.64 (11) NS 19.05 (4) 18.52 (15) NS Lice 0.00 (0) 0.00 (0) 0.00 (0) - 0.00 (0) 0.00 (0) - Flea 8.82 (9) 2.33 (1) 13.56 (8) < 0.05 19.05 (4) 6.17 (5) < 0.10 C. canis 1.96 (2) 0.00 (0) 3.39 (2) - 4.76 (1) 1.23 (1) - C. felis 6.86 (7) 2.33 (1) 10.17 (6) NS 14.29 (3) 4.94 (4) NS Total 27.45 (28) 20.93 (9) 32.20 (19) NS 38.10 (8) 24.69 (20) NS TABLE IV : Prevalences in % (and number of cases) of ectoparasites observed in goats (n = 102) according to the age and sex in and around Wolaita soddo, Southern Ethiopia.

ECTOPARASITES IN SMALL RUMINANTS FROM WOLAITA SODDO 453 Flea Total Sex Age infestation Males (n = 147) Females (n = 169) p Young (n = 72) Adult (n = 244) P Overall 10.44 (33) 6.80 (10) 13.61 (23) < 0.05 18.06 (13) 8.20 (20) < 0.05 C. canis 3.16 (10) 2.04 (3) 4.14 (7) NS 2.78 (2) 3.28 (8) NS C. felis 7.28 (23) 4.76 (7) 9.47 (16) NS 15.28 (11) 4.92 (12) < 0.01 TABLE V : Flea infestation prevalence in % (and number) in the whole small ruminant population (n = 316, 214 sheep and 102 goats) in and around Wolaita soddo, Southern Ethiopia. Discussion In the small ruminants from the Wolaita soddo region investigated in the present study, a total ectoparasite prevalence of 55.7% was registered. The rate of infestation by ectoparasites was markedly elevated in sheep (68.7%) whereas goats appeared to be significantly more resistant (28.4% of infestation rate) probably because of their self grooming, licking, scratching, rubbing and grazing behaviours which would contribute to rapid ectoparasite elimination [17]. Within the sheep population, it was also noticed that females were significantly more frequently affected than males (75.45% vs. 61.54%): this result could be due to the weakness of pregnant and lactating females which could not efficiently get rid of ectoparasites, and particularly of ticks. A relative low prevalence of the tick infestation (31.8% in sheep and 18.6% in goats) was observed in the present study area. Comparable results (23.8% in sheep and 16% in goats) were reported from the Sidama Zone in Southern Ethiopia [21] whereas ZELALEM [22] observed very higher tick prevalences (65.6% in sheep and 33.0% in goats) in the Dire Dawa region (Eastern Ethiopia). Differences in the environmental conditions (study season and design) could have contributed for this variation. Indeed, low tick prevalence may be related to an impaired tick development due to unfavourable climatic conditions (intermittent and weak rainfall in the Wolaita soddo area during the study period coupled to relative high temperatures). Three main tick genres were identified in the small ruminants in the present study: Boophilus spp, Rhipicephalus spp and Ambylomma spp. A similar frequency of the genre Ambylomma spp in sheep and goats has been reported in the Sidama zone (Southern Ethiopia) [21]. Furthermore, these 3 genres are known to be widely distributed in Ethiopia and to heavily parasitize live stock, the remaining species occurring in limited number and having little practical significance to livestock production [16]. In the present study, goats were significantly more resistant than sheep to the tick attacks. This result is in agreement with the admitted preference of ticks towards sheep [22]. On the other hand, LEHMAN [14] observed a greater susceptibility of young animals to ectoparasites and attributed it to a higher ratio of accessible surface to body volume and a poor grooming behaviour. But in the present study no significant difference for tick infestation between young and adult animals was evidenced in the sheep, goat or whole small ruminant populations. This discrepancy would be related to a poor access of young animals to pasture and to the climate unfavourable to tick development during the study period. No privileged tick infestation in females from sheep, goat or total small ruminant populations was encountered in this study contrary to HOSKINS et al. [12] which reported a particular susceptibility of females to tick attacks. According to the present study, only one genus of louse was identified in sheep (Damalina ovis) with a prevalence rate of 25.70%. This parasite has been considered as one of the major causes of rejection of skins at tanneries: it causes a defect known as Ekeke which is not a disease but a generic (Amharic) grading term used by tanneries in Ethiopia that means itching. It is an allergic hypersensitivity reaction to louse Damalina ovis and ked Melophagus ovnus in the local sheep breed. According to BAYOU [4], such a defect usually appears on the grain side of semi-processed skin but it is not normally observed in raw or unprocessed state. The Damalina ovis prevalence observed in the present study is by far higher than previous results obtained from central Ethiopia (0.8%) [11] and from Southern Ethiopia (Sidama region) (13%) [21]. These discrepancies could be explained by favourable climatic conditions of the study area for the biology of lice. Pediculosis was not observed in goats probably because of the particular goat behaviour that would reduce ectoparasite infestation rate. Only one case of mange (Demodex caprae) in goats was identified in this study the prevalence being 0.98% whereas no case was diagnosed in sheep. These results were comparable with previous studies conducted in the same study area (1.3% in goats and 0% in sheep) [7] and in the Sidama zone (Southern Ethiopia) (0.95% in goats and 0% in sheep) [21]. By contrast, KEDIR [13] obtained higher prevalences of mange mite infestation in small ruminants (26.1% in goats and 30% sheep) from the Tigray region in Northern Ethiopia. Nevertheless, this study was conducted on non-randomly selected sheep and goats showing visible skin lesions. Environmental factors might also have contributed to this great variation. In the same way a very elevated mange mite infestation prevalence (52.2%) was reported in goats from the Dire Dawa region whereas sheep were not contaminated [22]. There was no significant variation (P > 0.05) in the prevalence of flea infestation in male and female sheep but significant difference in flea infestation rate was observed between the two sexes in goats. Significant difference in the infestation by Ctenocephalides felis was noticed between young and adult sheep.

454 YACOB (H.) AND COLLABORATORS As a conclusion, this study demonstrates that ectoparasites mainly ticks (Boophilus, Rhipicephalus and Ambylomma), fleas (Ctenocephalides felis and C. canis at a lesser extend) and lice (Damalina ovis) infested small ruminants, particularly the sheep population, with a high global prevalence (55.7%) in the Wolaita Soddo region and lead to severe economic losses. References 1. - AGRAWA B.L.: Basic Statistics, 3 rd Ed., B.L. AGRAWAL (ed.), 215-232 pages, New age Int 1 (P) limited publishers, New Delhi, India, 1996. 2. - AIELLO S.E., MAYS A: The Merck Veterinary Manual, 8 th Ed, 131-140 pages, Merck and Co (eds). Inc., White House Station, N.J. USA, 1998. 3. - ASFAW A.: The Tanning Industry, In: Ian, B.C. and Bayou, B.(eds.) proceedings of control of sheep and goat skin disease to improve quality of hides and skin, 13-14 Feb. 1998, FAO, Addis Ababa, Ethiopia, 1998. 4. - BAYOU K.: Overview of sheep and goat skin diseases, treatment trial for improved quality of hides and skins (phase II).13-20 pages, Proceeding, FALO MOA, Addis Ababa, Ethiopia, 1998. 5. - BOPED: Bureau of Plan and Economic Department, Wolaita Soddo, Ethiopia, 2000. 6. - CARLTON W.W., Mc GAVIN M.D.: Special Veterinary Pathology, 2 nd Ed,, 476-502 pages, Mosby year book Inc., St. Louis. Missouri, USA, 1995. 7. - CHALACHEW N.: Study on skin diseases of cattle, sheep and goats in Wolaita Soddo, Southern Ethiopia, DVM thesis, Faculty of Veterinary Medicine, Addis Ababa University, 2001. 8. - CSA: Ethiopian Agricultural Sample Enumeration, 2001/2002, Central Statistic Authority; Federal Democratic Republic of Ethiopia, 2004. 9. - GETACHEW T.: Parasites of small ruminants. In: Gray G.D., and Uilenberg G, (eds.) parasitological Research in Africa, 1995. 10. - GRYSCELS G., ANDERSON F.M.: Studies on traditional agricultural systems, initial result, 1977-1980 In: research on farm and livestock productivity in Central Ethiopian Highlands International live stock research center for Africa, 1983. 11. - HAFFIZE M.: Study on skin diseases of small ruminants in Central Ethiopia, DVM thesis, Faculty of Veterinary Medicine, Addis Ababa University, 2001. 12. - HOSKINS I.D., CUPP E.W.: Ticks and veterinary importance part I. The ixodidae family, identification, behavior and associated disease, Compend. Contin., ESUC, 1991. 2, 16-37. 13. - KEDIR M.: Study on mange mite infestation in small ruminants and camels in two selected agro-climatic zones in Tigray, Northern Ethiopia, DVM thesis, Faculty of Veterinary Medicine, Addis Ababa University, 2002. 14. - LEHMAN J.: Ectoparasite: Direct impact on host fitness. Vet. Parasitol., 1993, 9 (1), 8-12. 15. - MAHMUD M.: Raw hides and skin improvement in Ethiopia, status and challenges. In: proceedings of the opportunities and Challenges of Goat Production in East Africa, a conference Held 10-12 Nov. 2000 at Debub University, Awassa, G.D. and Uilenberg, G, (eds.) parasitological research in Africa, 2000. 16. - MEKONNEN S.: Ticks, tick-borne diseases and control strategies in Ethiopia. In: tick-borne pathogens at the host vector interface: 441-446 pages, A Global Prospective. August 28 - September 1, 1995, Kruger National Park, South Africa. 1995. 17. - PEGRAM R.G., TATCHELL R.J., CASTRO J.J., CHIZYUKA M.G.B., GREEK M.J., Mc COSKER P.G., MORAN M.C., NIGA- RURA G.: Tick control, new concepts. www.fao. orglag/aga/agap/frg/ feed back. htm. 2004. 18. - RICHARD W., DAVID S.: Veterinary entomology; Arthropod ectoparasites of veterinary importance, 292-310 pages, CHAPMAN and HALL (eds), London, UK., 1997. 19. - STOIC P.J.: National leather and footwear industry scheme proposal. Development Project / Ethiopia / 93 / 005. United Nations International Development Organization, Veinna, Austria. 1997, 93-95. 20. - SOULSBY E.J.L.: Helminthes, arthropods and protozoa of domestic animals, 357-507 pages, 7 th Ed. LEA and FEBIGER (eds), Philadelphia, USA, pp. 1992. 21. - TESHOME W.: Study on small ruminant skin disease in Sidama Zone, Southern Ethiopia. DVM thesis. Faculty of Veterinary Medicine, Addis Ababa University, 2002. 22. - ZELALEM T.: Survey of mange mites of small Ruminants in Dire Dawa Region, DVM thesis, Faculty of Veterinary Medicine, Addis Ababa University, 1994.