Black flies aggressivity in Kafolo: influence of climatic and environmental factors

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Black flies aggressivity in Kafolo: influence of climatic and environmental factors
Coulibaly et al., J. Appl. Biosci. Vol: 174, 2022 Black flies aggressivity in Kafolo: influence of climatic and environmental
factors

 Journal of Applied Biosciences 174: 18031 – 18042
 ISSN 1997-5902

 Black flies aggressivity in Kafolo: influence of
 climatic and environmental factors
Fatoumata COULIBALY1, Grégoire YAPI YAPI1, Donatié Serge TOURE2,3, Kouamé
Alphonse KADJO1, Julien Marie-Christian DOANNIO 2
1
 Medical and Veterinary Entomology Centre, Alassane Ouattara University of Bouaké, Côte d’Ivoire, 27
BP 529 Abidjan 27, Côte d’Ivoire.
2
 Péléforo Gon Coulibaly University, BP 1328 Korhogo, Côte d’Ivoire.
3
 Suisse Centre for Scientific Researche in Côte d’Ivoire, 01 BP 1303 Abidjan, Côte d’Ivoire.
*
 Autor correspondant: touredonaties@gmail.com; Tel :( +225) 07 07 16 83 46

Submitted on 26th April 2022. Published online at www.m.elewa.org/journals/ on 30th June 2022
https://doi.org/10.35759/JABs.174.1

ABSTRACT
Objectives: The objective of this study is to investigate the influence of environmental factors on
aggressiveness rate of black flies, vector of Onchocerca volvius, the parasite that causes river
blindness in Kafolo, a village adjacent to the Comoé River located at the Ivoiro-Burkinabé border.
Methodology and results: The determination of temporal variations in black flies aggressivity was
done using standardised captures method on human bait according to protocol developed by
WHO/OCP. At the end of each hour of capture, the number of black flies collected was recorded
as well as the temperature and relative humidity. The results showed that except for the months of
March and April, the daily bite rates of the black flies were above the WHO tolerance level. The
highest daily bite rate (126 bpd) was recorded in September. The black flies aggressiveness was
highest in the late afternoon in all seasons, particularly in the rainy season, when fieldwork was
taking place. It changed constantly and inversely with ambient temperature and inconsistently with
relative humidity.
Conclusion and application of results: This study showed the importance of black flies
aggressiveness in Kafolo on the one hand, and the influence of climate and environment on this
aggressiveness on the other. The results of this study should guide the development of measures
to control the bites of black flies for the control of onchocerciasis in the region.
Keywords: Black fly, onchocerciasis, environmental factors, Ivoiro-Burkinabe border.

RÉSUMÉ
Objectifs: L'objectif général de cette étude est d'examiner l'influence des facteurs
environnementaux sur le taux d'agressivité des simulies (mouches noires), vecteur d'Onchocerca
volvius, le parasite qui cause la cécité des rivières à Kafolo, un village adjacent au fleuve Comoé
situé à la frontière Ivoiro-Burkinabé.
Méthodologie et résultats: La détermination des variations temporelles de l'agressivité des
mouches noires a été faite en utilisant une méthode de capture standardisée sur des appâts humains
selon le protocole développé par l'OMS/OCP. A la fin de chaque heure de capture, le nombre de

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mouches noires collectées a été enregistré ainsi que la température et l'humidité relative. Les
résultats ont montré qu'à l'exception des mois de mars et avril, les taux de piqûre quotidiens des
mouches noires étaient supérieurs au seuil de tolérance de l'OMS. Le taux de piqûre quotidien le
plus élevé (126 piqûres/homme/jour) a été enregistré en septembre. L'agressivité des mouches
noires était plus élevée en fin d'après-midi, quelle que soit la saison, en particulier pendant la saison
des pluies, au moment des travaux de terrain. Elle évoluait constamment et inversement avec la
température ambiante et de manière inconstante avec l'humidité relative.
Conclusion et applications des résultats: Cette étude a montré l’importance de l’agressivité
simulidiennne à Kafolo d’une part, et d’autre part, l’influence du climat et de l’environnement sur
cette agressivité. Les résultats de cette étude devraient guider à l’élaboration de mesures de lutte
contre les piqures des simulies pour le contrôle de l’onchocercose dans la région.
Mots clés : Simulie, Onchocercose, facteurs environnementaux, frontière ivoiro-burkinabé.

INTRODUCTION
Onchocerciasis or river blindness is a parasitic case of Kafolo, located in the North-East of
dermal endemic caused by a nematode worm, Côte d'Ivoire close to the border with Burkina
Onchocerca volvulus, which occurs in Africa, Faso. Indeed, during a pilot study on the
Latin America and the Arabian Peninsula. Comoé River, in this area, numerous
Approximately 123 million people are at risk. complaints were recorded from various
The fragmented and heterogeneous area of communities living or working near the river,
endemicity in Africa lies between the 15th relating to this increasingly increasing black
parallel north and the 14th parallel south fly aggressivity in the village of Kafalo. Much
(Koala, 2019). The parasite is transmitted to research had been undertaken to understand
humans infected black flies. The larvae of the the biology and ecology of the black fly. Some
insect is aquatic and needs fast-flowing of this research has focused on their activities
waterways for its development. This explains and more specifically on their aggressivity.
why the disease outbreaks are found along Indeed, the topic of black fly aggression had
rivers. Adult female of black flies can also be been the subject of many studies. Some of
found at varying distances from the these studies were devoted to the search for
watercourses due to their ability to travel factors that could influence the dynamics of
several tens of kilometres (within 24 hours). their population, and hence the aggressiveness
Female hoverflies, bite outside homes from the adults of black fly (imagos). From this
dawn to dusk. The control of onchocerciasis research, two main groups of factors have been
carried out by the WHO/OCP programme has identified: the first is linked to the simuliidae,
eliminated the risk of transmission of the particularly its intrinsic state, and the second,
disease and has significantly reduced black fly known as extrinsic factors, including
aggressivity in all the countries that benefited environmental and climatic factors. This
from the programme. However, since the article focuses on the second group, with a
programme was terminated in 2002, there has focus on climatic factors. This study was
been a massive return of black flies in areas carried out in 2019 in Kafolo. Close to Comoé
near rivers where these vectors have their rivers aiming to (i) determine the dynamics of
breeding grounds (Pitroipa X. et al., 2002; black fly aggressivity on humans during all
Sylla M. et al., 2002). In Côte d'Ivoire, black season and (ii) determine the effect of
fly aggression occurs in many areas along temperature and relative humidity on this
waterways (Pitroipa et al, 2002; Sylla M. 2002; aggressivity in the course of a day.
Coulibaly. 2007 and Yapi. 2014). This is the

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MATERIALS AND METHODS
Study area: Côte d'Ivoire and Burkina Faso season, which runs from November to April,
are two border countries in West Africa with precedes the rainy season marked by two
an area of 322,462 and 274,200 km² rainfall maxima, one in August and September.
respectively. They share a 584 km border. The daily and annual thermal amplitudes are
These two countries share a watercourse, the relatively large; the humidity rate is lower than
Comoé River. The River has its source in Péni, in the south of the country. This area is
a town located between Bobo-Dioulasso and characterised by the intermittent presence of a
Banfora in Burkina Faso. It crosses Côte cool, dry wind, the harmattan, between
d'Ivoire from north to south and flows into the December and February. Annual rainfall varies
Atlantic Ocean near the town of Grand- between 1000 mm and 1400 mm. The average
Bassam, some 40 km east of Abidjan; its rainfall recorded is 1203 mm
mouth is located east of the Ebrié Lagoon. It is (Ferkessédougou). The region's vegetation is
813 kilometres long. The village of Kafolo is composed of a mosaic of shrubby or wooded
located in the Tchologo region, more precisely savannah and open forest. The agroforestry
in the department of Kong in the North-East of parks are composed of fruit trees that are
Côte d'Ivoire and on the Ivorian-Burkinabe naturally present but have been modified by
border. It used to belong to the Health District human activities, such as baobab, néré, shea,
of Ferkessédougou. But since the end of 2019 mango and cashew. Agriculture is the main
it has been attached to the health district of activity in Kafolo, followed by fishing and
Kong. The village of Kafolo is about 700 km ecotourism. Kafolo is bordered by the Comoé
from Abidjan and more than 300 km from River. The Comoé enters Côte d'Ivoire at
Bouaké. It is located between 09° 35' 01''.9 N Kafolo and drains the Comoé National Park.
and 04° 18' 59''.3 W. In this region, the climate This river is a suitable place for the
is Sudanese with two main seasons. The dry development of black flies (Figure 1).

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Figure 1: Map of the study area

Methodology: The capture of black flies was between 09 ° 35 ' 18 '' N and 04 ° 18 ' 25''. 9 W.
done on human bait according to the The catches were made according to the
WHO/OCP capture technique (Berre. 1966; standard capture mode. This consisted of
Philippon, 1977). The catchers were catching the flies by two catchers on an hourly
previously trained in this technique, treated rotation system. At the end of each hour, the
with ivermectin, and vaccinated against yellow batches were labelled; the date, time, name of
fever according to the recommendations of the the catching point and that of the catcher were
National Ethics Committee; some of them specified. The catchers then recorded the
received anti-malaria treatment. Within the number of females caught per hour on a
village, two (02) capture points were chosen capture sheet, as well as information on
according to the selection criteria listed by Le meteorological parameters such as ambient air
Berre (Le Berre R., 1966) and Philippon (1977 temperature and relative humidity (recorded
and 1978). The first point is located upstream every hour). The catch was carried out between
of the larval site and is called "Kafolo Amont" 7 a.m. and 6 p.m. (i.e. 11 hours); on two
(09 ° 35 ' 27 ''. 9 N and 04 ° 18 ' 36''.7 W). The consecutive days each month for one year;
second point named “Kafolo Aval " is located from January to December 2019. At the end of

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this study we determined the following -the average monthly temperatures and relative
parameters: humidity rates by adding up
-the daily aggressiveness rate or daily bite rate
 on the one hand, the sum of the hourly
(DBR) or average aggressive density for each
 temperatures recorded during the 2 days of
month using the following formula monthly capture divided by 22
 and the sum of the hourly relative humidity
Daily Bite Rate DBR= rates recorded during the 2 days of monthly
 ℎ capture divided by 22. NB: 22 represents the
 ℎ ℎ total number of hours of capture, i.e., 11 hours
 of capture in one day during the 2 days in the
 month.

RESULTS
Seasonal variations in simulidean aggressive density recorded was 84.50
aggression in Kafolo bites/person/day with a pick of 126
Simulidean densities: Table 1 show the bites/person/day in September. In the dry
number of black flies collected and their season, the average aggressive density was
aggressivity. A total of 3038 black flies were 63.29 bites/person/day, and the lowest were
collected, 1010 in the dry season and 2028 in recorded in March and April with a density of
the rainy season, from January to December 4.5 and 1.5 bites/person/day, respectively.
2019. In the rainy season, the average

Table 1: Number of black flies collected and their aggressive densities, data collected from
January to December 2019
 Number of black flies Aggressivity
 Seasons Months days caught (bites/person/day)
 January 2 281 70,25
 February 2 239 59,75
 March 2 18 4,5
 Dry season April 2 6 1,5
 November 2 196 49
 December 2 270 67,5
 Total 1 1010 42,08
 May 2 131 32,75
 June 2 219 54,75
 July 2 318 79,5
 Rainy
 season August 2 395 98,75
 September 2 504 126
 October 2 461 115,25
 Total 2 2028 84,5
 TOTAL 3038 63,29

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Pace of aggression of black flies in Kafolo: constant throughout the day. There were time
The analysis of the hourly aggressiveness of slots where it was zero. Two periods of intense
the black flies allows us to note the following aggression were observed: the first between 9
points: to 11 am and the second much more important
During the dry season: A low aggressiveness, at the end of the day, between 4 and 5 pm,
very low or even non-existent was recorded (Figure 2).
during the first hour of catch (7 - 8 hours) from During the rainy season: In the rainy season,
January to March. Thereafter, the black flies aggressiveness was earlier, i.e., it
aggressiveness of black flies increased started earlier in the morning (07:00). The
progressively during the day, reaching its evolution was irregular but important during
maximum at the end of the day. However, in the day to reach its peak at the last hour of
March and April, this aggressiveness was not catch (17:00 to 18:00) (Figure 3).

Figure 2: Evolution of the hourly aggressiveness rate of black flies in the dry season

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Figure 3: Evolution of the hourly aggression rate of black flies in the rainy season

Effect of temperature and relative humidity gradually increased. The highest rates of
on the aggressiveness of black flies: Average aggression in the dry season were observed in
temperatures ranged from 26.64°C in January December, January and February. Black flies
(Harmattan period) to 35.09°C in April. aggressiveness evolved inversely with
Average relative humidity ranged from temperature and also inversely with relative
10.09% in April (driest month) to 74.50% in humidity during these 3 months. During the
August. During the dry season in March, April rainy season (May, June, July, August,
and November, the aggressiveness of the black September and October), black flies
flies evolved in the same direction as the aggressiveness evolved in the same direction
relative humidity and in the opposite direction as relative humidity, in the opposite direction
to the temperature. In fact, during these three of temperature. Indeed, an increase in black
months, a decrease in black flies flies um aggressiveness, an increase in relative
aggressiveness, a decrease in relative humidity humidity and a decrease in temperature were
and an increase in temperature were noted. In noted during the whole rainy season (Figure 4).
December, black flies aggressiveness

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 140

 120

 100

 80

 60

 40

 20

 0

 average temperature average relative humidity daily bite rate

Figure 4: Effect of temperature and relative humidity on the aggressiveness of simuliidae

DISCUSSION
The Comoé River is known to be favourable flies in March at Badara Karaboro and Badara
for the development of black flies. It is a Dogossè because the Comoé had dried up
permanent river, whose rugged course offers completely in these locations (Koala et al.,
many possibilities for the installation of 2015). Black flies densities were higher in the
preimaginal breeding sites for S. damnosum rainy season than in the dry season. Indeed,
(Le Berre 1966). The Comoé River has an their densities increased from May onwards,
important influence on the transmission of with the arrival of the first rains. There was a
onchocerciasis in this region. Indeed, the resumption of the flow and a rise in the level
seasonal variation in river levels influences the of the river. The rains reached their peak in
seasonal density of preimaginal populations of August and September. The floods led to an
S. damnosum. The results of the captures increase in the amount of support, which
indicated that the lowest black flies densities consisted mainly of branches and leaves of the
were observed during the months of March and (submerged) vegetation along the riverbed.
April in all our catch points. These low The large amount of submerged vegetation
aggressive densities are thought to be due to combined with the rapid flow of the river
the total drying up of the Comoé River at the provides ideal conditions for the establishment
larval site in Kafolo. This drying up of the river of the pre-imaginal stages of the black flies,
constituted an unfavourable condition for the resulting in an increase in the imaginal
development of the pre-imaginal stages and population. Indeed, during the second half of
consequently of the adults. This finding the rainy season, i.e., from August to October,
resulted in a partial or total interruption of the the black flies densities were very high, i.e., 3
population from this breeding site. These times the tolerable threshold of 30
results were similar to those of Koala and his bites/person/day (Quillévéré 1979); with a
collaborators who did not collect any black peak in September. These rates reflected the

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nuisance and probably the risk of late afternoon. The rainy season was
onchocerciasis transmission to which the accompanied by a drop in temperature that
populations are exposed. Koala et al. also predominates most of the time during the day.
observed in their study in the upper Comoé This atmospheric condition was favourable to
River, that black flies aggression was highest black flies activity and was reflected in the
in September (Koala et al., 2019). The importance of black flies aggressiveness,
situation in the deposit near Kafolo is that which was not only early (early morning) but
described by Le Berre (1966) and Philippon was spread over all the time slots of the day.
(1978) as a variation, of the synchronous type. As a result, there was no drop in black flies
This type of variation has also been observed aggressiveness in the middle of the day as was
by many authors ((Barbazan et al. 1998), the case in the dry season. In the last hour of
(Coulibaly F., 2007), (Eisenbarth, 2016), (Yapi catch (17:00-18:00), the decline in temperature
Y. G., 2014) and (Koala et al., 2019)) in their and rise in relative humidity further intensified
study. The activity of an Insect, in whatever black flies aggression to a maximum;
form it occurs, is never constant and varies achieving a single peak in the evening.
according to the different hours of the day and Crosskey (1955) also noted in his study that in
night (LE Berre, 1966). Regarding black flies the rainy season, during which the maximum
aggressiveness, the first observations on the temperature did not exceed 32°C, there was no
stinging times made by Dry, as early as 1921 noticeable decrease in catches in the middle of
(Dry, 1921) and then by Blaclock in 1926 the day. He described a daily catch curve with
(Blaclock (1926)) made it possible to specify a single peak at the end of the day. The
the period of daily aggressiveness, which was aggressiveness of female black flies was
from 7 to 18 hours. Hourly variations in their closely related to variations in meteorological
aggression were subsequently the subject of parameters, including temperature, humidity,
numerous studies (Crosskey, 1955); (Crisp, air pressure and light (Rubtzov 1936, Harker,
1956) and (L. Davies, 1957)). In this study, 1961). It was observed in this study that, in
during the dry season, two periods of intense general, black flies aggressiveness evolved in
aggression were observed: the first between 9 the opposite direction to temperature
and 11 am and the second much more throughout the year. It evolved in the same
important at the end of the day (between 4 and direction as relative humidity during most of
6 pm). However, in March and April, this the year except during the months of January,
aggressiveness was not constant throughout February, and December during the harmattan,
the day. There were time slots where it was in dry season. Indeed, it appeared from these
zero. This variation in the daily aggressiveness observations that the highest rates of
rate would be due to the variations in aggressiveness in the dry season were recorded
temperature and relative humidity during the during the months of January, February, and
day. From 11 o'clock onwards, the aggressive December. During these three months, the
density dropped due to the rise in temperature, harmattan wind prevailed. This wind
which resulted in a drop in black flies (harmattan) with low monthly average
aggressiveness. At the end of the day, the temperatures of 26.64°C and 28.18°C (varying
temperatures became low again, resulting in an between 16 and 34°C) and low monthly
increase in black flies aggression. These results relative humidity of 17.09 and 16.45%
were similar to those described by Lewis (varying between 7 and 29%) favoured
(1961) and Le Berre (1966). These two authors relatively high black flies aggressivity. The
observed a curve with two peaks in the dry aggressiveness of the black flies thus evolved
season: the first in the morning, the other in the in the opposite direction to the relative

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humidity and in the opposite direction to the rise in the water level of the river to create
temperature. In March-April, with the end of favourable conditions for the development of
the harmattan, there was a rise in temperatures the preimaginal stages, resulting in an increase
with very high monthly averages of 31.81° in the imaginal population. This suggested that
(March) and 35.09° (April) and low monthly black flies aggressiveness evolved with
averages of 12.73% and 10.09% of relative relative humidity and inversely with ambient
humidity. These extreme atmospheric temperature throughout the rainy season. Most
conditions led to a drying up of the river at the authors recognised the predominant role of
level of the larval site, the breeding ground of temperature in the daily attack frequency of
the black flies. The conditions necessary for female black flies (Underhill, 1940); (Davies,
the development of the black flies did not exist, 1957a); (Usova and Kulikova, 1958).
and the population from the breeding site was However, for these authors, hygrometry plays
completely interrupted. Hence the low black only a secondary role in the aggressiveness of
flies densities observed, 4.5 and 1.5 simulids (Le Berre, 1966). For Crisp (1956),
bites/person/day. The aggressiveness of the humidity influences the stinging rate, but he
black flies thus evolved in the same direction observed a certain amount of activity when
as the relative humidity and in the opposite humidity is very low. Other authors even
direction to the temperature. During the rainy consider that "relative humidity has no
season, the increase in relative humidity and influence on the stinging activity of black
the decrease in temperature combined with the flies" (Detinova and Beltukova, 1958).

CONCLUSION AND APPLICATION OF RESULTS
This study showed, on the one hand, the the environment. It varies with the seasons and
importance of the aggressiveness of black flies with the water levels in the river. The
in Kafolo. Indeed, outside the months of March aggressiveness of the fish is not always in the
and April, the number of bites/man/day same direction as the relative humidity and is
recorded is generally higher than the tolerable always in the opposite direction to the
threshold (30); it reached 126 bites/man/day in temperature. These results could help in the
September. The aggressiveness of the development of control measures against black
hatchlings is highest in the late afternoon. flies bites responsible for skin lesions and
Furthermore, the study showed that this allergies, but also and above all responsible for
aggressiveness is influenced by the climate and the transmission of human onchocerciasis.

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