Prevalence of ecto- and haemo-parasites of free-range local ducks in Kenya

R M Waruiru¹, S K Mavuti², P G Mbuthia¹, L W Njagi¹, M N Mutune¹ and R O Otieno¹

¹ Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi, P.O. Box 29053-00625, Kangemi Nairobi, Kenya
² Directorate of Veterinary Services, Ministry of Agriculture, Livestock and Fisheries, Kenya
stekitong@yahoo.com

Abstract

A study was conducted between November 2008 and March 2009 to determine the prevalence of endo- and haemo-parasites in different age and sex groups of free range local ducks in Nairobi and its environs. The ducks were categorized into ducklings (<2 months), growers (2 to 6 months) and adults (>6 months). A total of 48 ducklings, 50 growers and 47 adults comprising 77 females and 68 males were sampled. Each duck was clinically examined with emphasis on the cutaneous system and observations recorded. Body, head and leg skins were examined and identified parasites quantified. Two thin blood smears were prepared from each bird, processed and examined for haemoparasites.
 

Echidnophaga gallinacea (sticktight flea of poultry) was the only ectoparasite observed in 35.2% of the ducks. Thika West sub-county in Kiambu County had a significantly higher prevalence (45.1%) of E. gallinacean compared to Embakasi (25.5%), Kasarani (15.7%) and Westlands (13.7%) sub-counties in Nairobi County (p<0.05). Growers had a significantly higher prevalence (47.1%) relative to ducklings (31.4%) and adult ducks (21.6%) (p<0.05). Female ducks had a significantly higher prevalence (58.8 %) of E. gallinacean than males (41.2%) (p<0.05). Heamoparasites were observed in 48.3% of the ducks. The prevalence recorded in the four study areas was not statistically significant (p>0.05). Grower ducks had a prevalence of 35.7%, adults, 34.3% and ducklings, 30.0 % (p>0.05) while, male and female ducks had an equal prevalence of 50.0 % (p>0.05). Four haemoparasites identified in decreasing order of prevalence were Aegyptinella spp. (40.7%), Leucocytozoon spp. (6.9%), Eperythrozoon spp. (3.5%) and Haemoproteus spp. (0.7%). The results of the present investigation reveal that ecto- and haemo-parasites are prevalent in local ducks in Nairobi and its environs.

Keywords: Aegyptinella, Eperythrozoon, fleas, Leucocytozoon, sex

Introduction

In view of the rapidly increasing human population (Anonymous 2009), food production and security will remain the priorities in the agricultural sector in Kenya (Anonymous 1997). Poultry production can assist in the improvement of food security in many countries. This is because they require less land than other animals and can be a source of income, besides providing a cheap source of protein in the form of meat and micro-nutrient rich eggs to the rural, urban and peri-urban poor human population (Permin et al 2002).

In Kenya, free range poultry production is mainly subsistence but it contributes close to 70% of the national egg and poultry meat output (Nzioka 2000). Domesticated ducks estimated to be 300,000, form part of the 37.5 million poultry in Kenya (Anonymous 2008). Their meat is red gamy and attractively marbled which makes for special delicacy and contains about 20% crude protein and 2% fat (Szasz and Bogenfurst 1998; Szasz 2003). Despite minimal inputs, ducks contribute to family food and income, and are reputable for being more resistant to diseases than chickens (Muhairwa et al 2007). As reported in research conducted in chickens, productivity of poultry is highly constrained by disease, parasitism and low level husbandry practices resulting in high mortality rates especially in the young birds (Kemboi et al 2013; Sabuni 2013; Chege 2014). However, little work has been reported on diseases and parasites of ducks in Africa in general and Kenya in particular (Cooper and Mellau 1992). The aim of this study was to determine the prevalence and species diversity of ecto- and haemo-parasites of ducks in Nairobi and its environs. In addition, information from this study may assist in developing control strategies of these parasites to improve the health and productivity of ducks and other poultry in Kenya.

Materials and Methods

Study area

Ducks were purchased from three Nairobi districts namely; Embakasi, Kasarani and Westlands and neighboring Thika central district. Embakasi and Kasarani districts are located on longitudes 36º 50´ and 37º 00´ east and latitudes 1º 15´ and 1º 10´ south and lie at an altitude of 1600-1850 meters above sea level. Temperatures are 16º C - 28º C with an annual average of 22º C. Westlands District is located on an upper midland topographical region whose landscape comprises volcanic foot bridges and mid level uplands. It lies on longitudes 36º 54´ and 36º 85´ east and latitudes 0º 75´ and 1º 20´ south of equator. Its altitude lies between 1555-2435 meters above sea level. Average temperatures range between 20.4º C - 34º C (Anonymous, 2008).

Thika central district lies between latitudes 3º 53´ and 1º 45´ south of equator and longitudes 36º 35´ and 37º 25´ east and has a topography of about 1060 meters above sea level. Rainfall ranges from 965mm to 2130 mm. Temperatures range between 8º C - 30º C with an annual average of 20º C (Anonymous, 2006). The study areas were purposively chosen based on the availability of different age groups and sexes of ducks in the slum areas of Nairobi and its environs and the willingness of the owners to sell some of the birds in their flocks.

Study ducks

Ducks were obtained from various localities within the slums using random purposive sampling method between November 2008 and March 2009. A list of farmers who kept ducks was obtained from the County Livestock Production Officers from the two Counties. The list of duck farmers formed the sampling frame. The ducks were categorized into ducklings (<2 months), growers (2 to 6 months) and adults (>6 months) according to Magwisha et al (2002). From each farmer, 1 to 5 ducks were purchased. A total of 47 adults, 50 growers and 48 ducklings comprising 77 females and 68 males were sampled. All ducks were transported alive in cages to the Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi where laboratory examination was conducted.

Examination of ducks for ectoparasites

All the ducks were transported alive in cages immediately after purchase to the Department of Veterinary Pathology, Microbiology and Parasitology where laboratory examination was conducted. The ducks were thoroughly examined before being necroptized. They were skinned with all the feathers intact. Half of the body skin was examined according to MAFF (1986) and Sabuni et al (2010) and the total number of parasites multiplied by two to give the overall parasite intensity.

Identification of ectoparasites

The ectoparasites were processed as described by MAFF (1986) and identified according to their morphological characteristics using entomological keys (Soulsby 1982; Wall and Shearer 1997).

Identification of haemoparasites

The ducks were killed by cervical dislocation, followed by severing of the carotid arteries and jugular veins using a scalpel blade (Charlton et al 2006). Two fresh thin blood smears were prepared using microscope slides and blood from the severed jugular veins. The smears were processed and examined as described by Nemi (1986) and, the haemoparasites morphologically identified as described by other workers (Soulsby1982; Permin and Hansen (1998).

Data analysis

Data was entered in Ms-Excel (Microsoft corporation 2003), and later exported to Genstat® Discovery edition 3 for descriptive statistical analysis. To test differences in parasite prevalence between age, sex groups and study areas, the two sample binomial test (Genstat® Discovery Edition 3) was used. The prevalence of the parasites was defined as the total number of ducks infected with the parasites divided by the number of ducks examined (Margolis et al 1982). A critical probability of 0.05 was adopted throughout as a cut-off point for statistical significance between groups.

Results

Ectoparasites

Echidnophaga gallinacea (sticktight flea of poultry) was the only ectoparasite observed in 51 (35.2%) local ducks. The flea occurred around the eyelids, the head and necks of ducks (Figure 1). Grossly, lesions observed on the skin were feather loss around the head and neck regions, hyperemia and thickened skin especially around the eyelids (Figure 2).

Figure 1: A duck infested with Echidinophaga gallinacea (Arrows)

Figure 2: A duck showing feather loss around the head and neck regions (arrows)

The adult flea was small, measuring about 2 mm in length and black to brown in color. The head was sharply angled at the front (frons) with no genal or pronotal ctenidia (Figure 3).

Figure 3: Echidinophaga gallinacea from a duck showing head sharply angled at the frons (Arrow)

The total flea count ranged from 0 to 163, with an average of 31.7 fleas per duck. Ducks from Thika West sub-county had the highest prevalence of E. gallinacea of 45.1% (23/51), Embakasi sub-county 25.5% (13/51), Kasarani sub-county 15.7% (8/51) and Westlands sub-county 13.7% (7/51) (Table 1).There was a significant difference (p<0.05) in E. gallinacea infestation between Thika West sub-county and the three Nairobi sub-counties. Growers had a prevalence of 47.1% (24/51) which was higher than ducklings 31.4% (16/51) and adult ducks 21.6% (11/51). Female ducks had a higher prevalence 58.8% (30/51) than male ducks 41.2% (21/51) (Table 1). There was a significant difference in occurrence of E. gallinacea among age groups and sexes of ducks (p < 0.05).

Haemoparasites

Out of the 145 birds examined, 70 (48.9%) ducks of different age groups and sex were infected with haemoparasites. Those from Embakasi sub-county had the highest prevalence of 38.6% followed by Westlands (24.3%), Kasarani (20.0%) and Thika West (17.1%) (Table 2). Grower ducks had a prevalence of 35.7% (25/70), adults (34.3%) and ducklings (30.0%) (Table 2). Males had a prevalence of 50.0% equal to that of female ducks. The prevalence recorded among duck age groups, sexes and study areas was not statistically significant (p > 0.05).

Four haemoparasite genera identified were Aegyptinella spp. (40.7%), Leucocytozoon spp. (6.9%), Eperythrozoon spp. (3.6%) and Haemoproteus spp. (0.7%). Sixty five out of 70 infected ducks (92.9%) were infected by a single species while, 5/70 (7.1 %) were infected by 2 haemoparasite species in various combinations (Table 3).

Aegyptinella spp.

Aegyptinella spp. were found as round to oval bodies with chromatin displaced to the periphery occurring in the cytoplasm of erythrocytes as trophozoites (Figures 4 and 5).

Figure 4: Duck blood smear showing a red blood cell infected with Aegyptinella spp. (x1000)	Figure 5: Duck blood smear showing normal red blood cells (x 1000)

Of the 59 ducks that were infected with Aegyptinella spp. either singly or mixed infection, 24 (40.7%) were from Embakasi sub-county, 12 (20.3%) each from Kasarani and Westlands sub-counties and 11 (18.6 %) were from Thika West sub-county (Table 4).

The prevalence rate of this parasite (single or mixed infection) was 30.5% (18/59) in ducklings, 37.3% (22/59) in growers and 32.2% (19/59) in adult ducks. Male ducks had a prevalence of 45.8% (27/59) slightly lower than female birds at 54.2% (32/59). There was a significant difference in the prevalence of Aegyptinella spp. between the sub-counties (p<0.05) but not between the sexes and age groups of ducks (p>0.05).

Leucocytozoon spp.

Ten out of 145 (6.9%) ducks examined were infected with Leucocytozoon spp.

These were round and intra-cellular causing marked enlargement and distortion of the infected erythrocytes. The nucleus of the host cell was elongate and formed a long thin dark crescent along one side of the parasitized cell (Figure 6). The distribution of the 10 ducks infected with Leucocytozoon spp. between sub-counties was: Embakasi (4), Kasarani (3), Thika West (2) and Westlands (1), respectively. The prevalence of this parasite was 40.0% in ducklings, 20.0% in growers and 40.0% in adult ducks. Male ducks had a prevalence of 70.0% relative to 30.0% in females. Prevalence was statistically significant between sexes (p<0.05) but not among age groups of ducks and sub-counties sampled (p>0.05).

Figure 6: A blood smear from a duck showing a distorted red blood cell (D) and nucleus (N) at one side of the cell that is infected by leucocytozoon caulleryi (x1000)

Eperythrozoon species

Five (5) out of 145 (3.5%) ducks examined were infected with Eperythrozoon spp. These were minute ring shaped granular bodies occurring on the surface of erythrocytes and extracellularly on the blood smear (Figure 7). The prevalence between sub-counties was: Embakasi (40%), Kasarani (40%), Westlands (20%) and Thika West (0%), respectively. Prevalence in growers and adult ducks was each 40.0% relative to ducklings (20.0%). The prevalence in males was 60.0% compared to females at 40.0%. The prevalence of Eperythrozoon between sub-counties, age groups and sexes was not statistically significant (p>0.05).

Figure 7: A blood smear from a duck showing eperythrozoon spp. occurring on the surface of red blood cells (white arrow) and extracellularly (black arrow)

Haemoproteus spp.

Out of 145 ducks examined, 0.7% (1/145) had Haemoproteus spp. In Giemsa stained blood smears, the parasite appeared elongate, sometimes as horseshoe shaped cells embracing the erythrocyte nucleus. Only one male grower from Westlands sub-county was infected by this parasite.

Discussion

Echidnophaga gallinacea (sticktight flea) was the only ectoparasite found in the present study with a prevalence of 35.2%. The prevalence was in contrast to previous findings recorded in Kenyan chicken by Sabuni et al (2010) of 29.2% but lower than 47.1% reported by Chege et al (2014). Sticktight fleas were generally found in clusters around the eyes, on the head and on the neck preferring the more feathered areas. This was in contrast to the observation by Gustafson et al (1997) where the fleas preferred the non-feathered areas in chicken. Macroscopic study of head skin with E. gallinacea infestation showed, edema and hyperemia around the eye (on the eye lids) and there was de-feathering on the neck where the fleas had attached.

Echidnophaga gallinacea is found in many tropical and subtropical regions of the world, including Africa and is not host specific. Its host range includes: poultry, rodents, wild birds, humans, cats and dogs (Cooper and Mellau 1992; Permin et al 2002; Arends 2003; Mungube et al 2008). All birds are susceptible and heavy infestations cause irritation, stunted growth, reduced egg production, anemia, and mortality in young birds (Cooper and Mellau 1992; Arends 2003). In addition, E. gallinacea transmit several infectious agents like the pox virus of poultry (Gustafson et al 1997; Arends 2003). Histopatholological studies by Mavuti (2010) on ducks showed that E. gallinacea was associated with lesions including: necrosis, congestion of dermal blood vessels, petechial hemorrhages hyperkeratinization, parakeratosis, epidermal breakages and inflammatory changes involving deeper layers of the skin. These findings were similar to those described by Sabuni et al (2010) who studied histopatholological lesions of the skin in chickens.

Thika West sub-county had a higher prevalence of E. gallinacea compared to Embakasi, Kasarani and Westlands sub-counties of Nairobi County. The reason for the variation in prevalence between sub-counties was not clear but may be associated with the poor hygienic practices in the study sites. These created a favorable environment for the fleas and the free-range system, which provided a more sustainable environment for the ecto-parasites (Sabuni et al 2010; Tolossa et al 2013).

In this study, there were significant differences between prevalence in the different age groups with growers having the highest prevalence (47.1%) relative to ducklings (31.4%) and adult ducks (21.6%). This was as recently reported in chicken by Mirzaei et al (2016) where immature birds were more susceptible to ectoparasitic infestation relative to adults. However, this was in variance with other findings of Biu et al (2008) in Nigeria and Permin et al (2002) in Zimbabwe who reported that old indigenous chickens were more infested compared to younger ones. This disparity of research findings might be due to the variations in geo-climatic condition of the study areas and immune response of the different age groups to ectoparasitism among others (Permin et al 2002; Sabuni et al 2010).

Females had a significantly higher prevalence (58.8%) compared to male ducks (41.2%). This was in variance with the findings of other workers, who reported a higher occurrence of ectoparasites infestation in male chickens (Mungube et al 2008).One of the reasons could be the stationary state of hens during incubation of their eggs, which makes them more susceptible to parasitic infestations (Mirzaei et al 2016). However, further investigations on these findings are indicated.

Examination of blood smear revealed the presence of four haemoparasites of ducks with an overall prevalence of 48.3%. This prevalence is comparable to that reported in southeastern Nigeria by Opara et al (2016) of 40% in naturally infected adult scavenging ducks. However, the present prevalence in ducks was lower than that reported in chickens in Uganda (61.9 %) by Valkiûnas (2005) and Kenya (79.2 %) by Sabuni et al (2011).The two studies in ducks suggest that these hosts may be more resistant than chickens to haemoparasitic infections; however, studies in chickens and ducks with similar exposure to infection are required to add strength to these observations.

Aegyptinella, Leucocytozoon, Eperythrozoon and Haemoproteus species were found in the present study in ducks while, Leucocytozoon (83.3%) and Trypanosoma (16.7%) were the only species recorded in the Nigerian study (Opara et al 2016). The latter study also reported that the two haemoparasites could cause microcytic normochromic anaemia and leucocytosis which may adversely affect their productivity (Opara et al 2016). Mixed infections with two of these haemoparasites (Aegyptinella/Leucocytozoon or Aegyptinella/Eperythrozoon) were encountered in the present study. A recent study in Kenya recorded Plasmodium (53.5%) followed by Leucocytozoon (52.1%) and Hemoproteus (3.5%) in chickens (Sabuni et al 2011).

There were no significant differences in occurrences among duck age groups and across sexes for haemoparasites observed in the present study. However, Haemoproteus was only found in grower ducks and has not been previously reported in other African countries.

Conclusions

• The present study has demonstrated that E. gallinacea and haemoparasites are prevalent among different sexes and age groups of free-range local ducks in Nairobi and its environs.

Acknowledgements

The authors thank Prof Carol J Cardona for availing material support through Avian Flu School, Poultry Health Development Project, University of California, Davis and Global Livestock Collaborative Research Support Programme, USAID, for funding this study.  We acknowledge the the University of Nairobi for providing the work space and facilities and the duck owners for their cooperation.

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Received 17 February 2017; Accepted 9 May 2017; Published 2 July 2017

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