Overview of haematophagous flies involved in the transmission of vector-borne diseases in cattle

doi:10.21203/rs.3.rs-4831525/v1

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Overview of haematophagous flies involved in the transmission of vector-borne diseases in cattle

https://doi.org/10.21203/rs.3.rs-4831525/v1

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The aim of this study is to identify the hematophagous flies that contribute to disease transmission in cattle. This work took place in the department of Kounahiri (Côte d'Ivoire), 520 km from the city of Abidjan in December 2022. It took place over 08 days. Tabanidae and Stomoxyinae were caught using Vavoua traps. The insects collected were then placed in a freezer for twenty minutes to kill any insects that were still alive before being stored in a vial containing 70° ethanol. The identification of the different Stomoxyinae species was then developed using the determination keys of Zumpt and the additional morphological character to better separate S. calcitrans and S. niger niger. The Tabanidae were identified using the identification keys published by Oldroyd. The Tabanidae were divided into two genera: three (03) Philipotabanus elviae and thirty-one (31) Tabanus taeniola. On the other hand, among the Stomoxyinae, we identified 18 Stomoxys indicus and 25 Stomoxys calcitrans. The apparent density (AD) was 3.208 flies per day. As for the assessment of specific densities as a function of species composition, Tabanus taeniola had a higher specific density, at 40.26%, with 31 individuals out of a total of 77 flies. In addition, the diversity of haematophagous flies in relation to the biotope gave Margalef’s diversity indices of 0.612 for Stomoxes and 0.652 for Tabanidae. We can conclude from this research that, the inclusion of mechanical vectors in vector control strategies should help to minimise the impact of biting flies on livestock.

Tabanus taeniola

diversity

Stomoxys calcitrans

Philipotabanus elviae

Flies

Côte d’Ivoire

Meat is the most valuable livestock product and, for many people, serves as a prime source of animal protein. It is either consumed as a component of kitchen-style food preparations or as processed meat products (Godfray et al. 2018). It constitutes a very favorable ground for parasitic diseases, such as fasciolosis and hydatidosis, infections, such as tuberculosis and abscesses, and physical issues, such as traumatic meats, which are zoonotic or non-zoonotic pathological findings with the mode of transmission either direct or indirect and causing serious economic losses (Mimoune et al. 2022). Muscoid flies are among the most important pests in livestock and poultry production. Stable flies (Stomoxys spp.) recently surpassed horn flies (Haematobia spp.) as the most important arthropod pest of cattle production (Baldacchino et al. 2013; Lendzele et al. 2023). Indeed, they are involved in many processes and mechanisms essential for the functioning of ecosystems (Basset et al. 2004; Prisca et al. 2021). However, there are also insect species, particularly haematophagous diptera such as the Tabanidae, which play a role in the transmission of several pathogens responsible for numerous diseases (Krinsky 1976). In fact, tabanids are known to be mechanical vectors of trypanosomes, notably Trypanosoma vivax, responsible for African animal trypanosomiasis (Acapovi-Yao et al. 2016). Apart from the direct effects caused by Stomoxys on livestock such as nuisance and blood sucking behaviours, Stomoxys can indirectly serve as mechanical vectors of several pathogens (Baldacchino et al. 2013; Lendzele et al. 2023). An investigation regarding the preferred breeding substrates for S. calcitrans showed a high propensity for egg-laying in vertebrate-herbivore dung, caused by signature odours emanating from the dung (Baleba et al. 2019). However, Stomoxys have a broad range of habitats and are continuously adapting to exploit new breeding substrates in forest, livestock, and human settlement areas (Lendzele et al. 2019). The aim of this study is to identify the hematophagous flies that contribute to disease transmission in cattle, in order to develop vector control and disease management strategies for cattle herds.

Study site

This work took place from December 2022 in the department of Kounahiri in the Béré region. The chief town of the Béré region is 520 Km from the city of Abidjan. It is located in the North Center of Côte d'Ivoire and this department lies precisely between latitudes 7°30' and 8°10' N then longitudes 5°40' and 6°20'W and covers an area of 2110 km², its population is estimated at 101111 in habitants (National Institute of Statistics 2021). Its population is predominantly rural and agricultural. The department lies between the medium and low forest agro-climatic zones (Fig. 1). The medium forest zone has an equatorial climate with two rainy and two dry seasons. The climate has only two seasons (wet and dry). Average rainfall is 899.6 mm. The area available for development is 50,000 hectares. There are two types of vegetation: sub-Sudanese savannah in the northern part of the region, and Sudanese savannah in the extreme south. Livestock farming is one of the region's most important activities.

Processes

Tabanidae and Stomoxyinae were caught using Vavoua traps (Laveissière et al. 1990). The insects collected were first stored in labelled bottles and then in a refrigerator. They were then preserved in 70° ethanol and identified using a binocular magnifying glass.

Capture of Stomoxes and Tabanidae

For the capture of insects, the traps were set up taking into account the two sample collection areas. This was done in order to assess the specific diversity of haematophagous fly species depending on the biotope. The Vavoua trap was chosen because of its effectiveness, which has been approved in several countries for capturing horseflies and stomoxes, and also because of cost constraints. A total of three (3) traps were placed in the previously identified areas. That is, 01 in farms located near watercourses and 2 in farms near forest areas. The traps were at least 300 metres apart in the forest zone. The various captures took place between November and December 2022. The traps were set at 7 a.m. and retrieved at 6 p.m. for 08 days. While the traps were being retrieved, the capture cages were labelled with the trap number and brought back to the laboratory.

Conservation and identification of Tabanidae and Stomoxes

The insects collected were then placed in a freezer for twenty minutes to kill any insects that were still alive before being stored in a vial containing 70° ethanol. They were then sorted in the laboratory under a binocular magnifying glass to separate the Stomoxes from the tabanids. The identification of the different Stomoxyinae species was then developed using the determination keys of Zumpt (1973) and the additional morphological character described by Garros et al. (2004) to better separate S. calcitrans (Linnaeus, 1758) and S. niger niger (Macquart, 1851). The Tabanidae were identified using the identification keys published by Oldroyd (1973).

Data analysis

➣ Margalef's diversity

Margalef's diversity index was calculated to assess the diversity of tabanids in the biosphere reserve. This is calculated using the following formula: the ratio of the number of species (S) minus one (1) to the log of the total number of individuals collected (N).

$$\:\:\varvec{D}=\frac{(\mathbf{S}-1)}{\mathbf{l}\mathbf{n}\:\left(\mathbf{N}\right)\:}$$

➣ Density

This corresponds to the abundance of the different species of tabanids caught and is expressed by calculating their apparent density per trap per day.

➣ Apparent density

$$\:\varvec{D}\varvec{A}=\frac{\:\text{N}\text{u}\text{m}\text{b}\text{e}\text{r}\:\text{o}\text{f}\:\text{i}\text{n}\text{s}\text{e}\text{c}\text{t}\text{s}\:\text{c}\text{a}\text{u}\text{g}\text{h}\text{t}\:(\text{m}\text{a}\text{l}\text{e}+\text{f}\text{e}\text{m}\text{a}\text{l}\text{e})}{\text{N}\text{u}\text{m}\text{b}\text{e}\text{r}\:\text{o}\text{f}\:\text{t}\text{r}\text{a}\text{p}\text{s}\:\text{x}\:\text{n}\text{u}\text{m}\text{b}\text{e}\text{r}\:\text{o}\text{f}\:\text{t}\text{r}\text{a}\text{p}\:\text{d}\text{a}\text{y}\text{s}}$$

➣ Specific density

$$\:\:\varvec{D}\varvec{S}=\left[\frac{\:\text{N}\text{u}\text{m}\text{b}\text{e}\text{r}\:\text{o}\text{f}\:\text{i}\text{n}\text{d}\text{i}\text{v}\text{i}\text{d}\text{u}\text{a}\text{l}\text{s}\:\text{b}\text{e}\text{l}\text{o}\text{n}\text{g}\text{i}\text{n}\text{g}\:\text{t}\text{o}\:\text{a}\:\text{g}\text{i}\text{v}\text{e}\text{n}\:\text{s}\text{p}\text{e}\text{c}\text{i}\text{e}\text{s}}{\text{T}\text{o}\text{t}\text{a}\text{l}\:\text{n}\text{u}\text{m}\text{b}\text{e}\text{r}\:\text{o}\text{f}\:\text{i}\text{n}\text{d}\text{i}\text{v}\text{i}\text{d}\text{u}\text{a}\text{l}\text{s}\:\text{o}\text{f}\:\text{a}\text{l}\text{l}\:\text{s}\text{p}\text{e}\text{c}\text{i}\text{e}\text{s}\:\text{c}\text{a}\text{u}\text{g}\text{h}\text{t}}\right]100$$

Inventory of species and calculation of overall prevalence

Over a period of eight days, seventy-seven specimens were captured using three Vavoua traps. These vectors were classified into two distinct families, namely the Tabanidae and the Stomoxyinae. With regard to the Tabanidae, we recorded a total of 34 flies, divided between two genera: three Philipotabanus elviae and thirty-one Tabanus taeniola. In the Stomoxyinae family, we identified 18 Stomoxys indicus and 25 Stomoxys calcitrans (Fig. 2). Identification of horseflies and Stomoxys

Calculation of apparent density

All 77 haematophagous flies were collected over a period of eight days, which is equivalent to an apparent density (AD) of 3.208 flies per day. Of these flies, 37.66% or 29 individuals were caught in zone 1, characterised by the proximity of farms to watercourses, with an apparent density per trap and per day of 3.625 flies per trap per day. In zone 2, where the farms are close to forested areas, 48 specimens (62.34% of the total) were collected, with an apparent density of 3 flies per trap per day (Table 1).

Table 1

Apparent density of biting flies
Areas	Numbers of Traps	Numbers of Flies	Apparent density (Flies/trap/day)
Area 1	01	29	3.625
Area 2	02	48	3
Total	03	77	3.208

Distribution of genera by biotope

In the two environments used to place the traps, three genera of flies were identified. In the area close to the watercourses (Area 1), the apparent density of Stomoxys was 1.125 flies per trap per day, which is equivalent to a total of 9 flies caught per trap in eight days. For the genus Tabanus, the apparent density was estimated at 2.125 flies per trap per day, either a total of 17 flies caught over the same period. For the Philipotabanus genus, the apparent density was lower, with 0.375 flies per trap per day, representing a total of 03 flies caught. No Philipotabanus specimens were caught during the entire sampling period in traps placed on farms close to forested areas (Area 2). The apparent density for the genus Stomoxys in this same biotope was 2.125 flies per trap per day, iether a total of 34 flies caught. For the genus Tabanus, the apparent density was 0.875 flies per trap per day, equivalent to a total of 14 flies per trap per day (Fig. 3).

Assessment of specific densities according to species composition

The composition of the haematophagous flies caught during this study enabled them to be classified into four distinct species: Stomoxys calcitrans, Stomoxys indicus, Tabanus taeniola and Philipotabanus elviae. The Stomoxys calcitrans species accounted for 32.46% of the total, iether a total of 25 flies out of the 77 caught. For the species Stomoxys indicus, the specific density was 23.37%, equivalent to 18 flies. Next, the species Tabanus taeniola had a higher specific density, at 40.26%, with 31 individuals out of a total of 77 flies. Finally, Philipotabanus elviae was less represented, with only 3 individuals out of 77, corresponding to a specific density of 3.90% (Fig. 4).

Diversity of haematophagous flies in relation to the biotope

Index, which reflects the variety of tabanids and Stomoxes, revealed that the majority of flies were caught in the forest zone (48 specimens) using the Vavoua trap, compared with 29 caught in the area near watercourses. The biodiversity observed was not dominated by tabanids or Stomoxes, and only two tabanid species (Philipotabanus elviae and Tabanus taeniola) and two Stomoxes species (Stomoxys indicus and Stomoxys calcitrans) were collected. Margalef's diversity indices were 0,265 for Stomoxes and 0,283 for Tabanidae (Fig. 5).

The data collected from this study revealed the presence of four (04) species of biting flies: Philipotabanus elviae, Tabanus taeniola, Stomoxys indicus and Stomoxys calcitrans, all belonging to two families: Stomoxyinae and Tabanidae. The size of the samples obtained during the capture would seem to be linked to the period (November) of capture and above all to the use of certain repellents against these biting insects. Furthermore, the low captures during this study could be explained by the use of a single type of trap (Ange et al. 2016). Entomological findings in this study revealed 43 (55.84%) Stomoxys, 03 (3.89%) Philipotabanus and 31 (23.87%) Tabnus were captured during this work. This variability of species could be linked to the presence of the watercourses that drain this department and, above all, the edges and forests that constitute a favourable habitat for their development. Other findings revealed the presence of 18%.58 (704/3085) of Tabanus and Stomoxys (Seyoun et al. 2022).

The overall apparent density of biting flies (Tabanus and Stomoxys) was 3.208 flies/day. This low apparent density is probably due to the period (early dry season) of capture (November-December). Similar results of a low apparent density (2.93 flies/trap/day) of biting flies have been obtained (Seyoun et al. 2022). Moreover, these low apparent densities of Tabanus and Stomoxys have already been revealed by several authors (Eyasu et al. 2022).

The apparent densities of haematophagous flies in relation to the type of biotope revealed that in farms located near watercourses (Zone 1) the apparent density was 3.625 compared with 3 farms near forested areas. These high numbers of biting flies in the two habitats could be due to the increased humidity in these areas during the drought, which would be conducive to their activity. The variation observed is in agreement with that of Desta et al. (2013) and Seyoun et al. (2022) who showed a high apparent density of tsetse flies in the riverine vegetation type followed by savannah, forest, bush and cultivated areas. In addition, the density according to the genus of flies recorded an identical apparent density of 2.125 for Tabanus and Stomoxys. The diversity of hosts available would appear to contribute to their distribution in this locality. Our results are at odds with other studies that confirm the predominance of the Tabanus genus in Côte d'Ivoire (Acapovi et al. 2013) and Cameroon (Eteme et al. 2023).

Finally, Tabnus taeniola was the fly represented (40.26%) in the specific distribution of haematophagous flies. This zone being the ecological transition zone, it would be better suited to this species. The species T. par and T. taeniola were observed in all biotopes with a high abundance in forest galleries (Eteme et al. 2023). Acapovi (2005) showed that T. taeniola and T. par are abundant in all biotopes and collections of swampy water, which represent breeding sites for the latter.

This study reports that only four species of haematophagous flies were captured, including Philipotabanus elviae, Tabanus taeniola, Stomoxys indicus and Stomoxys calcitrans. This low diversity could be explained by the capture period and, above all, by the duration of the study. These opposite results were reported in studies conducted by researchers in Makokou, Gabon, which revealed the presence of seven Stomoxys species (Mavoungou et al. 2013). On the other hand, another study in Gabon, focusing on the inventory of haematophagous flies, revealed that the stomox family was the only group of haematophagous flies captured during our study (Kutomy et al. 2014).

This study provided an overview of the diversity of vectors of bovine anaplasmosis in the department of Kounahiri. It revealed the presence of Stomoxyinae and Tabanidae in the different sites studied. Consequently, the distribution of the diversity of species of haematophagous flies (Stomoxys, Philipotabanus and Tabanus) captured was almost balanced. We caught a total of 03 Philipotabanus elviae and thirty-one Tabanus taeniola, 18 Stomoxys indicus and 25 Stomoxys calcitrans. In addition, a high specific density (40.26%) was obtained for the Tabanus taeniola species, either 31 out of 77 flies. Appropriate control and monitoring methods will need to be implemented in each case. The inclusion of mechanical vectors in vector control strategies should help to minimise the impact of biting flies on livestock.

Ethical approval

The experiment was non-invasive and complied with Ivorian legislation. At the end of the study, the specimens were deposited in the entomological collection of the Korhogo Regional Laboratory (LRK), Côte d'Ivoire.

Conflicts of Interest

Competing interests on behalf of all the authors, I hereby state that there is no conflict of interest, including any financial, personal or other relationships with other people or organizations, which could inappropriately influence this work. The participating authors grant their authorization for the publication of this study in International Journal of Tropical Insect Science. This work has not been published previously, and it is not under consideration for publication elsewhere.

Acknowledgment:

Our thanks go to the head and senior research technicians of the Regional Laboratory of Korhogo (LRK) of the National Laboratory for Agricultural Development Support (LANADA) in the parasitology department.

Data Availability

The data used to support the findings of this study are available from the corresponding author on request.

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You are reading this latest preprint version

Overview of haematophagous flies involved in the transmission of vector-borne diseases in cattle

Status:

Version 1

Abstract

Figures

Introduction

Materials and Methods

Study site

Processes

Capture of Stomoxes and Tabanidae

Conservation and identification of Tabanidae and Stomoxes

Data analysis

➣ Margalef's diversity

➣ Density

➣ Apparent density

➣ Specific density

Results

Inventory of species and calculation of overall prevalence

Calculation of apparent density

Distribution of genera by biotope

Assessment of specific densities according to species composition

Diversity of haematophagous flies in relation to the biotope

Discussion

Conclusion

Declarations

Conflicts of Interest

Acknowledgment:

Data Availability

References

Status:

Version 1