Introduction

Trypanosomosis is a protozoan disease affecting livestock and humans in sub-Saharan Africa, causing serious economic and production losses in the livestock industry (Shaw 2004). Cattle production and practices began to evolve in Nigeria due to migration and environmental factors, and cattle owning pastoralists became settlers in the tropical rainforest, derived savannah and lowland rainforest. Bovine trypanosomosis caused by Trypanosoma vivax, T. congolense and T. brucei constitutes a threat to survival and productivity to the livestock industry (Oluwafemi et al. 2007). The influx of cattle in the study area has caused changes to the presence of various species of tsetse flies (G. palpalis, G. tachinoides, G. morsitans, G. longipalpis, G. fusca) and biting flies (Tabanus spp. and Stomoxys spp.), and these serve as setbacks to animal husbandry. The abundance of biting flies, communal clashes between pastoralists and farmers, and other social complexities are important issues on this sedentary activity (Odeniran et al. 2018). The distribution of fly vectors of trypanosomosis is closely related to environmental variables such as temperature, humidity, vegetational shelter and availability of hosts (Welburn and Maudlin 2012); subsequently, low to moderately high trypanosome infection has been reported in cattle from some parts of this region (Odeniran and Ademola 2018). The economic losses are closely associated with the extent to which the pathogenic effect of trypanosomes influences the production of the individual host. The economic losses affect mostly the poor resource farmers, Fulani pastoralists and public consumers. Understanding of farmers’ knowledge and perception on the impacts of trypanosomosis and occurring fly vectors and their participation in developing intervention strategies are prerequisites for effective implementation (Sindato et al. 2008). The study aimed at developing measures for reducing the impact of bovine trypanosomosis.

Methods

Study location

The study was conducted in areas located within the six southwestern states of Nigeria. These areas are within the tsetse fly belt of southwestern Nigeria and are in the tropical rainforest zone of Nigeria. The coordinates are within latitude 7° 13′ 57.66″ N–7° 57′ 54.14″ N and longitude 3° 18′ 24.18″ E–5° 29′ 46.13″ E. The rainy season is usually between April and October of every year, while the dry season with harmattan interlude starts November and ends in March. The study area is characterised by annual average temperature of 24–32 °C, humidity of 60–100% and high annual precipitation of 1500–2000 mm.

Study design

Standard questionnaire in a structured, semi-structured and unstructured manner, all incorporated into an overall questionnaire, was constructed to generate information on practices, knowledge and attitude of farmers on presence, impact, control and management of bovine trypanosomosis in southwestern Nigeria. Participatory rural appraisal (PRA) approach aims to incorporate the knowledge and opinions of rural people (livestock owners) in the planning and management of development projects (bovine trypanosomosis control) and programmes. PRA was employed to facilitate collection of this standardised field data. Qualitative and quantitative data of livestock management and trypanosomosis control was gathered and used for analyses with ecological, socioeconomic and political factors influencing livestock and disease control. Minimum and maximum focus group size obtainable were two and 20, respectively. In some areas where Hausa/Fulani language is predominantly spoken, an interpreter was used to apply the questionnaire in an unstructured manner.

Sampling strategy

Multistage random sampling to identify regions that cattle owners dominate was applied. Ten locations (Akinyele, Iddo, Eruwa, Igangan, Igboora, Ekiti, Lagos, Akure, Abeokuta and Osogbo) to include abattoir, farm settlements and cattle markets were involved in identifying practices and knowledge of bovine trypanosomosis. Questionnaire was administered to a total of 209 cattle owners (focus groups) in the study areas (Fig. 1). The focus group was important considering the number of workers that a keeper possess so that repetition would be ruled out and responses can be collective and more accurate.

Fig. 1
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Southwestern Nigeria states and numbers of livestock keepers (focus group) interviewed

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Statistical analysis

Differences in the annual cost parameters measured for treating trypanosomosis and other different diseases were tested for significance by the independent t test using GraphPad Prism version 5 for Windows (GraphPad, San Diego, CA, USA). Microsoft Excel spread sheet was used to manage the raw data, and Wilson confidence interval was used for descriptive analysis. The differences between analysed groups were considered significant when p value was less than 0.05. Poisson regression analysis was employed to compare the mortality rates of livestock.

Results

Cattle owners in the study area

Population structure revealed 75.6% (95%CI 69.35–80.92%, SE 0.0297) of cattle owners in the study area were Hausa-Fulani tribe, 20.6% (95%CI 15.65–26.56%) were Yoruba and 3.8% (95%CI 1.95–7.37%) were from minority groups. Even though these livestock owners have different practices and profession (Fig. 2; Table 1), market statistics of cattle population in this study revealed 95.7% (95%CI 95.16–96.19%) of the cattle were purchased outside the study areas and transported by road, while approximately 1% (95%CI 0.79–1.30%) cattle censored were from transhumance and 3.3% (95%CI 2.86–3.76%, SE 0.0023) were from sedentary cattle owners. The sources of the animals and breed type showed that over 80% of purchases were from northern Nigeria (Fig. 3). Change in practices and its effect on bovine trypanosomosis was investigated in this study, with combined roles among livestock owners revealed the number of livestock keepers practicing zero grazing (66%, 95%CI 59.37–72.11%) is significantly higher than other practices (Table 1). There are no livestock keepers who solely engage on pastoralism alone in this study; however, 1.9% (95%CI 0.75–4.82%) combine zero grazing and nomadism (some animals were kept under zero grazing while others undertook migration), of which majority were both herders and traders. The traded animals were often kept under zero grazing. It is also interesting to discover that combined practices were observed in 21.1% (95%CI 16.07–27.08%, SE 0.0282) of the total respondents. The effect of environmental variables on cattle production was properly assessed, 89.5% (95%CI 84.58–92.92%) livestock owners indicated that extreme weather conditions affect their animals. A total of 76.1% (95%CI 96.86–81.36%) believed that both rain and dry seasons affect cattle productivity. Factors mentioned include scarcity of pasture, disease outbreaks and unthriftiness of animals. However, 10.5% (95%CI 7.52–14.54%) livestock owners reported that extreme weather conditions do not affect their animals. In this study, 85.6% (95%CI 80.25–89.76%) cattle owners do not have basic primary education; hence, livestock production is done by what they see others doing. Only 2.4% (95%CI 1.03–5.48%) understand the epidemiology of the trypanosomosis in this study area, stating categorically that tsetse flies and biting flies are the fly vectors of trypanosomes.

Fig. 2
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Proportions of practices by livestock owners in southwestern Nigeria. Combination of practices is indicated with plus (+) sign. Livestock owners with singular practice differ significantly from those with combined practices. Single practice [SD = 33.83, D = 0.290, P < 0.01] and combined practices [SD = 14.34, D = 0.166, P < 0.01], where SD represents standard deviation, D Kolmogorov-Smirnov one-sample test using Poisson distribution and P significant value

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Table 1 Practices among livestock owners in southwestern Nigeria
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Fig. 3
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Cattle sources and animal breed in relation to bovine trypanosomosis in southwestern Nigeria. A areas with no risk, B areas with less risk, C areas with high risk of bovine trypanosomosis

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Perceived constraints associated with livestock production

Diseases, seasonal changes, lack of adequate feed and water, transhumance, lack of government support, economic issues and expensive drugs were most frequently reported constraints that hinders the successful production of livestock in the study area. Trypanosomosis was the second most prevalent disease mentioned by the livestock owners (after foot and mouth disease (FMD)), with 70.8% (95%CI 64.32–76.56%) of total respondents acknowledging its presence in their herd; 16.2% (95%CI 11.15–23.00%) mentioned that they had lost livestock from the disease at one point or the other (Table 2). There is significant increase (P < 0.05) in the mortality rate associated to bovine trypanosomosis when compared with other livestock diseases. The frequently observed clinical signs noted by livestock owners from bovine trypanosomosis include lacrimation, salivation, pica (sand), weakness, alopecia, dehydration, anaemia, recumbence and death.

Table 2 Disease prevalence from livestock keepers report
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Transportation methods

Long articulated lorries were used to transport animals from far-north with 80–100 carrying capacity, while trucks with varying sizes were used for short distances. Cattle dealers spend as much as US$ 17.7–US$ 35.5 on each animal for transportation. It was reported that on few occasions, animal dies due to restlessness, poor ventilation, transport stress and diseases. Only a few traders that were interviewed (6.2%, 95%CI 3.67–10.35%, SE 0.0167) believed that animals can die of trypanosomosis due to stress from transportation. There is preference for animal breed as some traders do not purchase certain breeds mostly because of size (large animals are preferred) and susceptibility to trypanosomosis. The most commonly traded breeds were White Fulani, Sokoto Gudali and Red bororo, while the less traded were Kuri, Muturu and Ambala (Fig. 3). Other economic costs incurred include loading fee and off-loading fee, which costs between US$ 0.35 and US$ 0.70 per animal depending on relationship with the trader. Other transit payments like travel cost (toll fees, police fees etc.) are paid by the traders. However, on the arrival of the animals, some become recumbent because of the long distance they have travelled (1–3 days), while some are sold immediately at lower cost. These are called “wonle” in local language. Often, the animals are provided with drugs (including antibiotics, vitamins, and sometimes trypanocides) on arrival seeking to prevent them from dying of transport stress.

Transhumance and prevalence of trypanosomosis

The result from this study shows that 13.4% (95%CI 9.43–18.68%) of cattle owners practise transhumance, all during the wet season. A total of 82.1% (95%CI 64.41–92.21%) were both traders and herdsmen, while 17.9% (95%CI 7.79–35.59%) were herdsmen only (Fig. 2) that practiced transhumance. The reasons for transhumance were grazing problems that led to conflict on land use, abundance of flies during the wet season, avoidance of disease and to enhance the growth of their animals. The majority (85.6%, 95%CI 80.25–89.76%) reported that a minimum of 1 out of 100 cattle die per season during transhumance, while 14.4% (95%CI 10.24–19.75%) said they had no deaths associated with transhumance. They all reported to enjoy the migration practices as their animals were used to it. The seasonal factor of prevalence of trypanosomosis in various states of southwestern Nigeria also coincides with the migration plans (Fig. 4). More owners reported that the prevalence of trypanosomosis is highest in the month of April (beginning of rainy season), while it is lowest in the month of December (dry season). More than 150 livestock owners believed that the prevalence is high in the months of March, April, May and August (Fig. 4). This could influence the migration plans of transhumance in southwestern Nigeria. All the farmers interviewed, reported that migration begins in late February and early March to the guinea savanna areas of the country to avoid the wet seasons due to the factors mentioned. However, these pastoralists arrive at the tropical rainforest area in October (early dry) to provide better grazing lands for their livestock and explore the markets to sell some of their flocks. Results from the quantitative analysis show that 63.2% (95%CI 56.44–69.41) of livestock owners sell off cattle that refuse to respond to treatment of trypanosomosis.

Fig. 4
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Seasonal variation of bovine trypanosomosis reported by livestock keepers (n = 209). The peak periods P6…P2 was shown. Ratchet circular scan test for short seasonal peak P2 (2-month peak): March–April P < 0.05, P3: March–May P < 0.05, while Hewitt rank sum test for seasonal peak P4 (March–June): P = 0.089 and P5 (March–July): P = 0.094 shows no significance, while P6 (March–August): P = 0.013 with significance. Freedman’s test for any deviation from uniform incidence: V (N) = 0.344, while significant peak periods (P < 0.05) are shown for the monthly seasonal perception of cattle which occurred at P2, P3 and P6

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Quantification of socioeconomic losses to trypanosomosis in Nigeria

Vector threat

The three major transmitting vectors (Stomoxys, Tabanids and Glossina) of trypanosomosis in the study area were clearly identified as threats by livestock owners. Biting flies are mechanical vectors, and they are found throughout the year; 73.2% (95%CI 66.82–78.75%) perceived them as threat to livestock production due to disturbance and irritation they cause to the animals and keepers but only 1.4% (95%CI 0.49–4.13%) mentioned them as fly vectors of trypanosomosis. Although tsetse fly populations have reduced drastically, their distribution is found to be seasonal (Fig. 4). A total of 91% (95%CI 86.24–94.10%) considered tsetse flies as threat due to weakness and anaemia observed in cattle after heavy bites but only 1.9% (95%CI 0.75–4.82%) considered them agent of trypanosomosis. In total, 2.4% (95%CI 1.03–5.43%) of respondents recognised these fly vectors to transmit T. brucei, T. congolense and T. vivax. A total of 78.5% (95%CI 72.41–83.50%) livestock keepers believed that consumption of early rain lush and pica (sand) by cattle is the major cause of trypanosomosis while 19.1% (95%CI 14.38–25.01%) are indifferent about the major cause of the disease.

Cost of trypanocides

It was discovered from this study that 97.0% (95%CI 92.52–98.82%) livestock owners make use of at least one synthetic drug to combat trypanosomosis. However, of this number 3.1% (95%CI 1.21–7.70%) make use of antibiotics only (Table 3). Hence, it was observed that only 93.9% (95%CI 88.58–96.92%) make use of trypanocides with or without other drug combinations. The current annual cost of trypanocides is estimated at approximately US$ 8.4 million, assuming the use of trypanocides in the study area is like other areas, since all the areas are under the risk of trypanosomosis (Table 4). There were 3.0% (95%CI 1.18–7.48%, SE 0.0148) cattle owners who make use of traditional drugs and all refused to disclose the content of the locally made drug.

Table 3 Proportions of trypanocide use/strategy among livestock owners
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Table 4 Estimated annual cost of trypanocides in southwest Nigeria: a postulate from this study
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Use of insecticides by livestock owners

During early-wet and wet seasons, the population dynamics of transmitting vectors increase and livestock owners utilise insecticides. From this study, about 60.5% (95%CI 51.84–68.48%, SE 0.0432) respondents make use of insecticides. Some livestock owners use it monthly, while some use it weekly or even daily. Cypermethrin could cost as much as $US 15 per litre bottle, and the 3% concentration often encountered on the field should treat 50 animals weighing 200 kg each at 10 kg/ml. It was observed that some owners could use it for weeks or months depending on the abundance of flies in that season. It was reported that butchers do not use insecticides for their animals because they only have them within 24–48 h. Hence, the quantitative figures here will exclude the butchers only (80) as indicated in Fig. 2; however, dual or multiple livestock practitioners make use of insecticides. Results from this study shows that 78/129 (60.5%, 95%CI 51.84–68.48%) make use of insecticides, 25/129 (19.4%, 95%CI 13.49–27.05%) depend on smoke generated from the plant (Senna occidentalis) called “Bangaru angasa” in Fulani language, 7/129 (5.4%, 95%CI 2.65–10.78%) use concoction that include herbicides and 19/129 (14.7%, 95%CI 9.64–21.86%) do not control flies at all. From those that use insecticides, 66/78 (84.6%, 95%CI 75.01–90.97%) depend on cypermethrin, 8/78 (10.2%, 95%CI 5.29–18.95%) use permethrin, 2/78 (2.6%, 95%CI 0.71–8.88%) use ivermectin and chrysanthemum each. It was also reported that Fulanis that stay in camps, referred to as “Gaa”, prefer to use smoke (from the plant mentioned) overnight to prevent night bites from tsetse flies and biting flies throughout the dry season. However, at the beginning of rain, they reported the use of both smoke and insecticides (majorly cypermethrin).

Economic losses of cattle to trypanosomosis in Nigeria

Trypanosomosis has caused several losses in the livestock industry (Table 5). However, indirect losses are often unaccounted due to the complexities in livestock production in Nigeria. Direct losses from trypanosomosis have been reported from this study (Table 4). Direct loss of ≥ US$ 426 can be incurred from mortality of a single animal due to the ravaging of trypanosomosis. Most farmers could give concise information on losses during the early and late stages with the latter leading to ≥ 80% economic loss or more per animal. Culling of irresponsive livestock to trypanocides because of trypanosomosis was observed by 77.5% (95%CI 71.38–82.65%) of respondents.

Table 5 Losses to trypanosomosis on bovine economic scale
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Treatment of trypanosomosis by livestock owners

The request of veterinary services among livestock owners from this study is very low. The result shows that 82.3% (95%CI 76.55–86.87%, SE 0.0264) do not request veterinary services. They attend to the animals on their own by injecting them with drugs or local remedies, and the few that do request a veterinarian (17.7%, 95%CI 13.13–23.45%, SE 0.0264) only do so when the veterinary doctor is around. Despite owners accepting recorded deaths from trypanosomosis (Table 2), they still feel reluctant requesting the services of the veterinary doctor. This is due to the fear that they could be government agents, and hence, their animals may be totally condemned for sale. Another reason given was that they can do what the veterinarian does and there is no need to paying for veterinary services. The result also shows that different livestock owners have different approach for treating their animals against trypanosomosis, some of which include combination of antibiotics and or vitamins (Table 3).

Government intervention programmes

From this study, only 1.9% (95%CI 0.75–4.82%) of respondents had ever heard of any government intervention programme. They could only recall free treatment of animals against trypanosomosis especially in the northern part of the country (guinea savannah). However, in recent times and especially in the southwestern Nigeria, there are no current governmental or non-governmental intervention programmes targeted at trypanosomosis. Respondents were willing to join, assist and participate in the intervention programme; however, 0.96% (95%CI 0.26–3.42%) of respondents representing two groups/households had negative attitudes to be part of any government or non-government programmes.

Discussion

Livestock production is a major factor in agricultural development in Africa (Vreysen 2006). Most sub-Saharan African countries have neglected the factors responsible for viable livestock industry. Livestock producer’s perception evaluation has been done in some African countries (Seyoum et al. 2013; Bouyer et al. 2015). The increasing sedentariness of livestock keepers, zero-grazing, mixed farming system and pastoralism with reduction of nomadism was also noticed in this study. This corresponds to an earlier report of 37% rural households across Nigeria involved in mixed farming (FAO 2011). The reason for combined roles is to maximise individual profits on livestock production (Table 1), but the concept has yielded little or no increase due to the thriving of trypanosomosis. Most of the animals traded in the study areas are from northern Nigeria and neighbouring states and countries; hence, the occurrences of bovine trypanosomosis often reported in herds on arrival could be transported. The present study revealed that livestock producers could determine seasonal variations and peak levels of bovine trypanosomosis and its fly vector populations which was in line with studies done in Ethiopia (Seyoum et al. 2013), Kenya (Catley et al. 2002) and West Africa (Grace et al. 2009). This indicate that livestock owners’ perspectives could be important in designing control strategies. The change in fly habitat due to the management practices which poses both positive and negative impacts on livestock production. The pattern of transhumance has made it difficult to design an effective control approach for trypanosomosis (Babalobi et al. 2000). The reduced transhumance activities practiced only during wet season in this study area contrast the large number of cattle owners who practiced transhumance in northern Nigeria (Majekodunmi et al. 2013). The death associated with bovine trypanosomosis was highest on the account of the cattle owners. This could be due to lack of quality diagnostic techniques, poor engagement of veterinarians, inconsistent fly vector control approaches and, possibly, the ineffectiveness of trypanocides in the market (Kingsley 2015). Treatment regimen revealed self-treatment by livestock owners, and antibiotics with other supplements are often included in the treatment plan (Table 3). Although, anthelminthic and strategic feeding supplements have been mentioned along trypanocides in integrated trypanosomosis control measures (Holmes 2004) due to trypanosome and helminth pathologic synergy (Kaufmann et al. 1992), yet treatment strategies observed in study areas could lead to increased drug resistance. The popularity of tsetse flies among livestock owners compared to biting flies could be due to the long-age awareness on the impact of the fly on humans and animals. The common species of parasites (Trypanosoma congolense, Trypanosoma brucei and Trypanosoma vivax) causing the disease is known among livestock owners because of their relationship with veterinarians on the field. The use of trypanocides is common among the livestock owners because of its availability in the market. Less attention is paid on the dosage of drug recommended, and hence, this could further increase the resistant strains of trypanosomes in the bloodstream. Besides, drug residues in meat products could be above threshold levels and these could be very detrimental to animal and human health. Drug resistant strains of major trypanosome species (T. vivax and T. congolense) have been encountered in the field throughout Nigeria; this could have been because of drug misuse (Ilemobade 1988). The number of livestock owners who use insecticides suggests that crude methods of fly control is also employed. However, the effectiveness of the substances used need to be quantified. The problems of resistance and cross-resistance to insecticides, environmental damage, and high cost of insecticides have been reported (Chater 2002). The incidence of disease was higher mostly in wet season as observed in the study. This could be attributed to the influx of the vectors during this period and rapid completion of the life cycle of tsetse. The high incidence of biting flies especially Stomoxys spp. is also of great concern as they were reported to be present all year round. Due to the self-approach on control methods against bovine trypanosomosis often used by the livestock owners, the level of control success could be affected. In conclusion, drug resistance coupled with trypanosome risk and fly abundance threatens cattle-based livelihoods (Geerts et al. 2001), and Nigeria may experience reduced productivity for many more years. The strategic use of trypanocide and insecticides combined with disease monitoring, evaluation and routine management practices can be helpful to reduce or eradicate the losses on bovine trypanosomosis in the livestock industry.