| Livestock Research for Rural Development 32 (1) 2020 | LRRD Search | LRRD Misssion | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
The study was carried out to evaluate the tick burden of cattle genotypes as an index of resistance to ticks of the family Ixodidae and Argasidae. Forty-two animals made up of Ndama, Gudali, White Fulani, Ndama x White Fulani (NF), Ndama x Gudali (NG), Gudali x White Fulani (GF), and Ndama x (Gudali x White Fulani) [N(GF)] classified as young (≤ 18 months of age) or adults (> 18 months of age) and of various coat colours were selected for the study. Ticks were collected from pre-selected body parts of the animals once a month during the dry season (February to April) and rainy season (May to July) and identified to the family Ixodidae (hard ticks) and Argasidae (soft ticks) while fifty ticks representing sub-samples of each family were identified to species level using morphological characteristics. Data revealed increasing trend in tick infestation from dry to rainy months with peak infestation in the months of June and July; significant breed, age class of animals, sex and age x sex interaction effects on tick infestation of cattle with purebred genotypes being more tick resistant than their crossbred counterparts. Young and male cattle were more resistant than adult and female cattle, respectively while coat colour did not significantly affect tick count. It was concluded that breed differences exist in tick resistance in the cattle herd and that further breeding and testing is required to establish the extent of tick resistance acquisition in the herd.
Keywords: cattle, crossbred, purebred, tick burden, tick resistance
Ticks are blood-sucking ectoparasites of domestic and wild animals. There are about 900 species of ticks that are endemic to most continents (Porto Neto et al 2011) especially the tropical and subtropical regions of the world (Jongejan and Uilenberg 2004; Mendes et al 2011). Ticks of the family Ixodidea (hard ticks) and Argasidae (soft ticks) are among the common ticks of cattle in Nigeria. The family Ixodidae contains about 684 species belonging to many genera including the genus Amblyomma (102 species), Aponomma (24 species), Dermacentor (30 species), Haemaphysalis (155 species), Hyalomma (30 species), Ixodes (235 species), and Rhipicephalus (Boophilus) (75 species) while the family Argasidae contains about 183 species classified to 4 genera namely Carios, Argas, Ornithodoros and Otobius (Jongejan and Uilenberg 2004).
The impact of ticks and tick-borne diseases on global livestock industries is of major concern (Piper et al 2009). Shyma et al (2015) reported that over 80 % of world’s cattle populations are affected by ticks and tick-borne diseases. Ticks and tick-borne diseases are responsible for huge losses in productivity and income of cattle farmers in Nigeria. Ticks cause anaemia, body weight loss, decreased milk production, loss of body condition, damage to hide and skin, udder and teats, and mortality in very severe cases (Biegelmeyer et al 2015). They act as vectors of numerous disease causing parasites of cattle (Tick-borne infections) including anaplasma, babesia and theileria responsible for anaplasmosis, babesiosis, and theileriosis, respectively. Ticks also act as reservoirs of other disease causing organisms like bacteria, rickettsia and viruses (Piper et al 2009).
Tick infestation is treated and controlled primarily through the use of acaricides however, resistance to acaricides: organophosphates, organochlorides, carbamates, amidines, and synthetic pyrenthroids as well as combinations of these agents have been reported globally (Piper et al 2009). Consequently, the cost of chemical treatment and control of ectoparasites continues to increase as a result of limited effectiveness (Piper et al 2009), the need for frequent or repeated application and the use of higher concentrations. Considering the trend in the development of acaricide resistance, scientists and practitioners believe that future brands of acaricides will encounter similar limited efficacy (Frisch 1999; Piper et al 2009) necessitating the call for a more sustainable solution to tick control in livestock populations (Piper et al 2009). Exploiting innate and acquired immunity as well as genetic attributes for resistance to tick infestation through selection and selective breeding has been advocated as a viable cattle tick control strategy because of the potential to reduce expenditure on acaricides and husbandary facilities associated with chemical control. Furthermore, control through genetic selection appears to be more environmentally friendly preventing among other things environmental pollution and toxicity to other biota.
It has been shown that differences in degree of resistance to tick infestation exist within and between cattle breeds (Tabor et al 2017). Also, host resistance to tick infestation is considered to be predominantly an acquired trait following a period of initial susceptibility as shown in Bos indicus cattle (Piper et al 2009). Numerous studies have also demonstrated that host resistance to tick infestation is heritable with heritability values of 0.39 to 0.49 in Bos taurus breeds and as high as 0.82 in Bos indicus breeds (Tabor et al 2017).
Resistance to tick infestation in cattle is commonly assessed by determining the tick burden of animals over a period of time (incidence of infestation) as well as by evaluating physiological parameters that indicate response to tick attacks (Tabor et al 2017). Tabor et al (2017) stated that the incidence of tick infestation on bovine hosts in divergent genetic backgrounds gives insight into the differences in resistance to tick infestation of different breeds. A number of studies have demonstrated differential expression of genes and a casket of physiological and biochemical parameters associated with response to tick infestation in resistant and susceptible cattle breeds (Franzin et al 2017; Tabor et al 2017). In the present study, we assessed the tick burden of seven cattle genotypes namely purebred N’dama, White Fulani, and Sokoto Gudali (Gudali); and crossbred N’dama x White Fulani (NF), N’dama x Gudali (NG), Gudali x White Fulani (GF), and N’dama x (Gudali x White Fulani) [N(GF)] to assess the tick resistance status of the genotypes and the potentials for within population selection for improved resistance to tick infestation in a closed breeding herd.
The study was carried out at the cattle breeding unit of the Teaching and Research Farm, Michael Okpara University of Agriculture Umudike (MOUAU), Abia State. Umudike lies on latitude 05o 29I North and longitude 07o 32I East in the rainforest zone of Southeastern Nigeria with ambient temperature range of 25 to 35o C and annual rainfall range of 1677.5 to 2200mm (N.R.C.R.I. 2016).
The cattle herd comprised of three indigenous breeds namely N’dama, Gudali and White Fulani and their crosses namely N’dama x Gudali (NG), Gudali x White Fulani (GF), N’dama x White Fulani (NF), and N’dama x (Gudali x White Fulani) [N(GF)]. The herd is managed semi-intensively. Husbandry practices include daily grazing of natural pasture from 07:00 to 13:00 h, and from 16:00 to 19:00 h. The animals return to the holding area for sheltering, watering and supplemental feeding after each period of grazing. Animals are strategically wormed at the beginning and end of rains and treated against blood parasites when necessary and following accurate diagnosis. Tick infestation was controlled by periodic administration of systemic acaricides.
The study considered the different cattle genotypes reared on the MOUAU Cattle Improvement Unit. A total of 42 animals made up of 12 N’dama cattle (6 cows, 3 cow calves, and 3 bull calves), three Gudali cows, six White Fulani (3 cows and 3 cow calves), three NF cows, six NG (3 cows and 3 cow calves), three GF cows, and nine N(GF) (6 cows and 3 bulls) were used for the study. Animals above 18 months of age were classified as adults while those 18 months or below were classified as young. The coat colours of the study animals were cream or white, light brown, brown, black, and black with white patches. The animals were properly identified using ear tags and were allowed to graze with the rest of the herd throughout the study period. Administration of acaricide to the herd was discontinued two months prior to selection of animals for the study and for the duration of the study, no acaricide was applied to the selected animals although they received other management practices as other animals in the herd.
Animals were evaluated for tick burden once every month from February to April (dry season) and from May to July (rainy season) of 2018. Animals were individually restrained in a crush and ticks collected with pincers from pre-selected regions of the body namely head, ears, neck, belly, back, udder, scrotum, legs and tail. Collected ticks were held in 70 % ethanol in universal bottles labeled with genotype, age class, sex, coat colour of animal and month of collection. Thereafter, they were taken to the laboratory for identification and enumeration. Ticks were identified and grouped to two families namely Ixodidae (hard ticks) and Argasidae (soft ticks). Fifty ticks representing a random sub-sample of each tick family were identified to species level with the aid of a stereomicroscope (Olympus) at 100x magnification using the key morphological characteristics of ticks as described by Walker et al (2003).
Using tick enumeration data, the following tick infestation parameters were determined
(a) Tick percentage abundance (A): This was calculated across herd and month of tick collection for each genotype using a modified expression by Yessinou et al (2018):
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(b) Mean parasitic intensity (I): This was calculated for each month of tick collection across genotypes using the expression:
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Classification of the mean parasitic intensity followed the scheme suggested by Bilong-Bilong and Njine (1998) as reported by Yessinou et al (2018) viz:
a. I < 10: Very low parasitic intensity,
b. 10 < I < 50: low parasitic intensity,
c. 50 < I < 100: average parasitic intensity,
d. I > 100: high parasitic intensity.
Data on tick count were subjected to repeated measures analysis of variance in SPSS version 2.0 to compare between genotypes, month of study, and coat colour of animals and to independent samples t-test to compare between sexes and ages of animals. Different means were separated using the Duncan New Multiple Range Test in SPSS.
A total of 6854 ticks were collected across genotypes and over the six months of study. Argasid ticks were the most abundant accounting for 4512 or 69 % of all ticks collected while Ixodid ticks were 2072 or 31.0 %. Fifty ticks sampled from the Ixodid and Argacid ticks yielded two species, respectively namely Amblyoma variegatum and Rhipicephalus annulatus for ixodid ticks, and Ornithodoros moubata and Allectrobius capensis for Argacid ticks. Amblyoma variegatum was the more prevalent Ixodid tick (69.1 %) while Ornithodoyos moubata was the more prevalent Argacid tick species (62.9 %). Figure 1 shows increasing trends of tick infestation (panel A) and mean parasitic intensity (panel B) of Ixodid and Argasid ticks across the study period. At each month, the mean parasitic intensity of Argacid ticks was more than that of Ixodid ticks corresponding to higher infestation of the cattle genotypes by Argasid ticks.
 |
| Figure 1. Month-wise tick count (panel A) and mean parasitic intensity (panel B) |
The effect of breed of cattle on tick infestation (Figure 2) indicate that crossbred genotypes (GF, NF, and NG) were the most infested with Ixodid ticks (11.41 ± 1.17, 11.11 ± 1.17 and 8.97 ± 0.83 Ixodid ticks, respectively) while purebred N’dama was the least infested with tick burden of 6.32 ± 0.57 ticks. For Argacid ticks, GF cattle were the most infested (33.39 ± 1.68 ticks) followed by NF genotype (24.89 ± 1.68 ticks). Again, the N’dama breed had the least tick burden of 13.46 ± 0.84 Argacid ticks. The crossbred genotypes hence had the highest overall tick count of 44.83 ± 2.73, 36.56 ± 2.73 and 27.28 ± 1.93 ticks for GF, NF, and NG, respectively.
Highest infestation by Ixodid ticks was observed during the rainy season (May to July) in all cattle genotypes however peak infestation was observed in N’dama and GF in June (12.33 ± 1.01 and 18.00 ± 2.02 ticks, respectively) and in Gudali in May (12.33 ± 2.02 ticks) while in White Fulani, NF, NG, and N(GF) peak infestation was observed in July (14.00 ± 1.43, 16.33 ± 2.02, 16.33 ± 1.43 and 14.33 ± 1.17 ticks, respectively). The least tick burdens were observed in the dry season months of February in all cattle genotypes except in Gudali and GF which had least Ixodid tick counts in March (Figure 3). For Argasid ticks, peak infestations were observed in N’dama and GF in June and February, respectively but in Gudali, White Fulani, NF, NG and N(GF) in April, while least argacid tick burden was observed in N’dama, White Fulani, NF, and N(GF) in February but in NG in March, and in Gudali and GF in July. When the total tick burden of the animals was considered, all genotypes had highest tick burden during the peak of rains (June and July) except NF which had highest total tick infestation in July followed by April.
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| Figure 2.
Effect of breed of cattle on tick infestation. NF:
N’dama x White Fulani, NG: N’dama x Gudali, GF: Gudali x White Fulani, N(GF): N’dama (GF), a,b,c,d: significantly different means (p<0.05) |
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| Figure 3. Interaction effect of cattle genotype x month of study on tick infestation | |
Tick burden did not differ significantly between animals of different coat colours (Table 1). Animals with white or cream coat however, had numerically higher tick counts for the two tick families followed by those of light brown while animals with darker coat colours (brown and black) had lower parasite counts.
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Table 1. Effect of cattle coat colour on tick infestation |
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Coat colour |
Ixodid tick |
Argacid tick |
Total tick |
|
Black |
7.42 ± 0.52 |
15.38 ± 0.75 |
22.89 ± 1.22 |
|
Black with white patches |
6.47 ± 0.83 |
13.89 ± 1.19 |
20.08 ± 1.93 |
|
Brown |
8.00 ± 1.17 |
18.06 ± 1.68 |
26.06 ± 2.73 |
|
Light brown |
8.97 ± 0.83 |
18.31 ± 1.19 |
27.28 ± 1.93 |
|
White/cream |
8.97 ± 0.59 |
22.83 ± 0.84 |
32.76 ± 1.37 |
|
p value |
0.62 |
0.82 |
0.83 |
Young cattle had lower tick infestation compared to adult cattle (Figure 4).
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| Figure 4. Effect of age of cattle on tick infestation; a,b: significantly different means (p<0.05) |
Young cattle had mean Ixodid tick count of 6.44 ± 0.52 and Argacid tick count of 12.04 ± 0.75 which were lower (p < 0.004) compared to the values for adult cattle (9.21 ± 0.39 and 21.16 ± 0.56 ticks, respectively). The total tick burden for young cattle was hence lower at 18.49 ± 1.22 ticks compared to 30.38 ± 0.91 ticks for adults (p < 0.000).
Irrespective of age of cattle, gender had significant effect on the distribution of ticks among cattle genotypes. Females were more infested by Ixodid (p<0.018) and Argasid ticks (p<0.020) and had higher total tick burden than males (p<0.015) (Figure 5).
 |
| Figure 5. Effect of sex on tick burden; a, b: significantly different means (p<0.05) |
When age of cattle was considered, cows were more infested with Argasid ticks than bulls (p<0.02) and total tick count was higher in cows than in bulls (p<0.002) (Figure 6 panel A). No significant differences in tick burden were observed between young cows and young bulls but young cows tended to be more heavily infested than young bulls (p<0.065) (Figure 6 panel B).
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| Figure 6. Interaction effect of age x sex of cattle on tick infestation: Panel A: adult cattle, panel B: young cattle |
A total of 6854 ticks were collected from seven cattle genotypes over the six months of study with argasid ticks being the more prevalent tick on all cattle genotypes. Infestation of cattle in the tropics with different species of ticks has been widely reported. In Benin, Yessinou et al (2018) reported tick load of 9049 ticks on four cattle genotypes over a period of 20 weeks while in Ethiopia, Tafesse and Amante (2019) observed tick count of 2255 ticks from 274 animals over a period of 8 months. These studies considered only tick genera belonging to the family Ixodidae indicating that this tick family could be the most economically important in their environment or studied population. The present study recorded high prevalence of argasid and ixodid ticks indicating that both tick families are economically important ectoparasites of cattle in the humid rainforest environment of Southeastern Nigeria. The observed multi species tick infestation agrees with Tafesse and Amante (2019) who reported that 78 % of all animals examined had multi species tick infestation. Multi species tick infestation of cattle breeds was also reported by Yessinou et al (2018) and Jawale et al (2012). Of the two species identified in the family Ixodidae, Rhipicephalus annulatus was less important than Amblyoma variegatum contrary to Yessinou et al (2018) who reported higher prevalence of Rhipicephalus microplus compared to other Ixodid tick spp. Our results are however, in agreement with numerous other reports (Farougou et al 2007; Clercq et al 2012; Kwak et al 2014) which showed higher prevalence of Amblyoma variegatum in cattle populations. The finding of high prevalence of Ornithodorus moubata in the present study is significant as it suggests greater attention to tick genera/spp which hitherto was believed to be of less economic importance in cattle populations. In the present study, the mean parasitic intensity (I) for argasid ticks were generally higher than those of ixodid ticks across the period of study corresponding to the higher abundance of ticks of this family in the studied population. The mean parasitic intensities for both tick families were however, low (I < 50) indicating low ectoparasite burden in the studied herd probably on account of routine ectoparasite control programme employed by the farm. Yessinou et al (2018) reported mean parasitic intensity (I) of less than 50 for Amblyoma variegatus and I < 10 for Hyaloma species.
Among the pure breeds, Ndama was least infested with both ixodid and argasid ticks indicating that this genotype is the most resistant of the three pure breeds studied. The pure breeds were also more resistant to tick infestation compared to the crossbred genotypes. This could be attributed to the repeated infestation of the pure breeds following their longer stay in the herd compared to the crossbreds which were produced by mating the pure breeds and which had experienced fewer repeated tick infestations compared to their purebred parents. Host resistance to tick infestation is believed to be an acquired trait following repeated infestation and an initial period of susceptibility (Piper et al 2009). Ibelli et al (2012) reported significantly higher tick counts in crossbred Angus x Nelore cattle compare to Senepol x Nelore and purebred Nelore cattle while Jawale et al (2012) reported higher prevalence of tick infestation in crossbred cattle compared to purebred Gir, Holstein Friesian and Jersey. The result of the present study was however in disagreement with that of Yessinou et al (2018) that reported similar tick infestation in crossbred cattle and purebred Borou, and Azawak but higher infestation in purebred Girolando which was a later introduction in the studied herd.
Although ticks were found on all cattle genotypes over the months of study, the observed highest tick burdens during June to July in all genotypes indicate higher prevalence of ticks of all families during these months which correspond to peak of rainy season characterized by high ambient temperature and moisture content of the environment and which favour tick multiplication and spread. Significant seasonal variation in tick infestation of cattle had been reported by other studies. For instance, Mohamed et al (2014) reported higher tick counts in wet than dry season. Mekonnen et al (2007) also reported higher tick counts during rainy than dry season even though ticks were found on the cattle throughout the period of study as was observed in the present study. On the other hand, Kemal et al (2016) did not observe considerable differences in tick burden of cattle during wet and dry seasons contrary to the findings of the present study.
In the present study, cattle coat colour did not significantly influence distribution of ticks even though light coat coloured genotypes tended to be more heavily infested with ticks. There is dearth of information on the effect of coat colour characteristics on tick resistance however, it is believed that skin and coat traits, along with hide colour, can be related to maintenance of ticks on the host (O’Kelly and Spier 1983; Ibelli et al 2012). It does appear also that light coat colour could enhance identification of hosts by ticks.
Young cattle (cattle 18 months of age or below) were less infested by ticks compared to adults indicating that immunity against tick infestation could be age dependent as alluded to by Kemal et al (2016) who reported higher tick burden in old than young cattle. Rocho et al (2019) also observed significant age effect on infestation of ixodid ticks in Columbian cattle. Reasons for lower tick count in young cattle compared to adult/old animals include higher immunity against ticks in young than in old animals, and the usual preferential husbandry attention given to young animals. Furthermore, calves emit lesser quantities of carbon dioxide than adult/old animals. High carbon dioxide (CO2) production is believed to enhance the location of a host animal by ticks (Yessinou et al 2018). In contrast to the findings of the present study, Abdella et al (2017) did not observe significant effect of age of animals on tick infestation.
Comparison between sexes across ages for tick resistance showed that female cattle were less resistant to ticks (had higher tick burden) compared to males and this agrees with Rocha et al (2019) that reported higher tick load on Columbian female cattle compared to males. Rehman et al (2017) observed higher tick infestation in Pakistani and Egyptian female cattle compared to males while Tafesse and Amante (2019) reported higher tick infestation in Ethiopian cows compared to bulls. Our result is however in contrast to that of Yessinou et al (2018) that reported higher tick counts from male compared to female cattle. The authors attributed the result to higher CO2 emission by heavier males compared to lighter females. It is believed that CO2 emission is a primary determining factor in the detection of animal location or presence by ticks (Yessinou et al 2018). When the age of animals was considered, cows were still less resistant to ticks than bulls, and young cows also tended to have higher tick counts than young bulls indicating that female cattle could be innately less resistant to ticks. We speculate that pregnant cows apart from being heavier (and hence emit higher CO2) than bulls are also more sedentary and therefore more limited in the exercise of self grooming and these could contribute to the higher tick burden observed in cows compared to bulls.
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Received 12 October 2019; Accepted 7 November 2019; Published 2 January 2020