Assessment of entomophagy in Abidjan ( Cote D ’ ivoire , West Africa )

In order to assess the contribution of edible insects to the efforts for combatting food insecurity and poverty in Côte d’Ivoire, a survey aimed at identifying edible insects in Côte d’Ivoire was conducted from August 2014 to August 2015 in three communes in the city of Abidjan (Abobo, Adjamé and Yopougon). Four hundred and seventy-two people were interviewed at random. The results revealed that 59.72% of the respondents consume insects against 40.27% who do not consume them. This study has helped to identify nine edible insect species belonging to eight families and five orders. The species Imbrasia oyemensis (Lepidoptera, Satunidae) and Macrotermes subhylinus (Isoptera, Macrotermitidae) are widely consumed due to their availability in markets. The species Rhyncophorus phoenicis (Coleoptera, Curculionidae) or palm tree caterpillar is one of the most prized by 40% of the surveyed population. The statistical analyses applied to the 365 people surveyed revealed that insect consumption is a function of the cultural area (X2=76.7; ddl= 4, p < 0.05) and the age ((X2=54.88, ddl=3; p < 0.05) of the consumers. In economic terms, insect trade remains a significant source of income in households having an average income estimated at 58,666.66±11216 FCFA per seller and per month. However, their availability in markets is seasonal. A mastery of the biology of these insects could ensure their permanent availability in markets.


INTRODUCTION
The global demand for food, especially animal protein, is continuously increasing due to population growth and urbanization (Lavalette, 2013).According to the studies of Durst et al. (2010) one billion people worldwide suffer from malnutrition and 98% of these people live in Asia and Africa (Lavalette, 2013).*Corresponding author.E-mail: ngoransw@yahoo.fr.
Author(s) agree that this article remains permanently open access under the terms of the Creative Commons Attribution License 4.0 International License  In response to these challenges, Food and Agriculture Organization (FAO) has opted for entomophagy or insect consumption as an alternative to the food and nutritional challenges of low-income populations (FAO, 2013).These animals are an important source of protein and energy for various populations (Chutima et al., 2015).
Insects are already consumed in several countries.In the Central African Republic, 85% of the population consume caterpillars (N'gasse et al., 2003).Moussa (2002) reported a consumption rate of 70% in the Democratic Republic of Congo.In Botswana, Van Huis et al. (2013) estimate the rate of insect consumption by the population at 91%.Although insect consumption is still common, the total number of species consumed tends to decline due to urbanization and wildlife extinction.In Côte d'Ivoire, more than 5% of the population is affected by difficulties in accessing traditional animal proteins such as meat and fish (INS, 2008) because of the often high prices.
Consumption of insects would be a way out of this situation.The collection and sale of insects not only generates substantial income for the vulnerable population but also provides a significant additional protein supply to women and children (Akpossan et al., 2009).The seasonality of these insects remains a challenge faced by the populations involved in this field.Indeed, the world of tomorrow is likely to be confronted with problems of food supply and durability of these insects.The shift from a gathering system to an organized mode of production through mass animal husbandry is therefore a path of the future.Studies on the nutritional value of certain edible insect species were made in Abidjan (Akpossan et al., 2009;Niaba et al., 2011;Gbogouri, 2013).A survey was conducted by Niaba et al (2012) on the consumption of winged termites in Côte d'Ivoire.However, few studies on the inventory and diversity of edible insects in Côte d'Ivoire have been carried out.The present study, which is part of the fight against food insecurity, has the long-term objective of promoting entomophagy in Côte d'Ivoire.Specifically, it is about inventorying the insect species consumed in Abidjan and assessing the factors related to their consumption.

Study environment
The study was carried out in the district of Abidjan, which covers an area of 57 735 ha inhabited by 4 707 000 inhabitants, that is, 20% of the country's total population (RGPH, 2014).The city of Abidjan has ten (10) communes, three of which have been selected for this study.These are the communes of Adjamé, Abobo, and Yopougon whose total population represents 3/4 of the total population of the city (RGPH, 2014).The common feature of these communes is the existence of the largest wholesale markets for food supplies in all the cities of the country and the subregions.In addition, these markets constitute sources of supply for other markets in the city (Figure 1).

MATERIALS AND METHODS
The biological material consisted of edible insect species identified during the survey.The technical material consisted of a survey form, a digital camera, a notebook and plastic boxes for collecting the insects encountered.The catalog of Delvare and Aberlenc (1989) has helped make the laboratory identification.

Inventory of edible insects
A survey was carried out from August 2014 to August 2015.The sample was composed of 472 respondents consisting of consumers and insect traders.Two questionnaires with open and closed questions adapted according to the model of Balinga et al. (2004) were submitted to the respondents.The first was addressed to insect consumers and the second to wholesalers and retailers.They were distributed to households and markets with a view of assessing the edible insect marketing chain in Côte d'Ivoire.The questionnaires were sent to both men and women aged between 15 and 90 years divided into four age groups (15 to 17 years, 18 to 35 years, 36 to 50 years, 51 years and over) according to the National Institute of Statistics (INS, 2016).In total, samples of 30 fresh insect specimens and 30 dried specimens were collected as part of the survey.As for the larvae, they were reared in the laboratory until the emergence of the adult.The adults were identified in the Laboratory of Zoology and Animal Biology of the University Félix Houphouët-Boigny using a BMK 31 162 binocular magnifier and the catalog of Delvare and Aberlenc (1989).

Consumer survey
The information was gathered from 365 households in the three communes, including 125 in Adjamé, 161 in Abobo and 79 in Yopougon according to random sampling.The number of respondents per commune was related to their availability.The people interviewed in a household should answer questions during an interview.The language used for the survey was French.For the respondents who did not understand this language, translators were requested.Information was given on the vernacular names of the edible insects as well as the reasons for their consumption.The different ethnic groups encountered were grouped in the five cultural areas called Akan, Mandé nord, Mandé sud, Krou and Voltaic in Côte d'Ivoire (INS, 2016).

Trader survey on insect marketing
The marketing survey took place in 3 markets of the three communes visited, namely the Gouro market of Adjamé, the main market of Abobo Gare and the one of Yopougon Gesco.It concerned 107 sellers chosen at random from the 3 markets, including 41 in Adjamé 35 in Abobo and 31 in Yopougon.The number of respondents in each market was related to the

Statistical analyses
The different parameters were studied using STATISTICA version 16 software.The level of significance was set at 5%.A Pearson chi² test followed by correspondence analysis tests was used to determine the different relationships between insect consumption, education attainment, cultural area and age of consumers.

Demographic characteristics of the surveyed population
The 365 respondents were split into four age groups of15 to 17 years, representing children (30.68%), from 18 and from 36 to 50 years of age representing adults (28.76%).People aged 51 or over (old people) accounted for 12.60% of the respondents.For the entire sample, the male subjects accounted for 52.87% and the female subjects for 47.12%.In terms of educational attainment, 23% were school drop outs, 25.20% had primary education, 30.13% had secondary education and 21.64% had higher education.As for the ethnic group, 18.35% were from the Akan group, 21.64% from the Mandé nord group, 21.09% from the Mandé sud group, 20.54% from the Krou group and 18.36% from the voltaic group.

Consumption of insects by age, sex, educational attainment and cultural area
The statistical analyses applied to the 365 respondents revealed that 59.72% of the respondents consume caterpillars against 40.27% who do not consume them.This consumption of insects is linked to several factors including age, educational attainment and cultural area.Among the consumers, children were the majority (44.95%) and elderly people were the minority (8.25%) (X²=54.88,ddl=3, p < 0.05) (Figure 3).Concerning educational attainment, people out of school (33.48%)  consume the most insects and those having higher education consume less (16.97%) (Figure 4).Concerning cultural area, the Krou (76%) were the ones who consume the most insects (Figure 5).They were followed by the Mandé nord (30.05%), the Mandé sud (24.88%), the Voltaic (11.27%) and the Akan (7.05%) (X²=76.7;ddl=4; p < 0.05) (Table 1).The Pearson chi² test applied to the population sample revealed that insect consumption was not a function of gender (X² = 4.32; ddl = 1; p = 0.37526).The results of the survey showed that the proportion of men who consume insects (57.33%) is higher than that of women (42.66%).

Consumption of insects depending on sources of motivation
The reasons for the consumption of insects were multiple Thus, 49.39% of consumers said that the insects taste good; 12.20% mentioned that they contain proteins, vitamins and minerals such as calcium and iron; 20.62% consumed them by eating habit and finally 17.43% out of curiosity (Figure 6).As for non-consumers of insects, 64.42% did not do so in disgust; 16.56% for fear and 19.02% due to customary considerations.

Status of traders
The census conducted revealed that 27% of traders in the markets sold insects.Women accounted for 74.4% of these traders.However, the 7 wholesalers encountered in the different markets were men.Ethnically speaking, populations from the West (Gouro, Yacouba Guéré) and  the north (Senoufo, Tagbanan, Malinké etc.) of Côte d'Ivoire were the most involved in insect sale.These two ethnic groups are also major consumers of insects.The average age of traders was between 30.90±10.84 years.

Methods of insect supply
The most common supply method practiced by traders was direct purchase of insects in a wholesale market in Abidjan (54.5%).The second method consisted in moving to insect collection sites (45.5%).The distribution chain from harvest to marketing could be summarized in four steps (Figure 7).In 92% of cases, collectors were usually women (51%) and children (34%).Their first clients were small local traders who, in turn sold the products to wholesalers.The latter supplied the markets of large cities.The supply of the cities with edible insects is therefore carried out by wholesalers.According to the results of the survey, Abidjan receives insects from different cities in Côte d'Ivoire and some neighboring countries such as Ghana, Burkina Faso and Mali during periods of shortages (Figure 8).

Profitability of insect trade
From the beginning to the end of the marketing channel, that is to say from the collector to the retailer in Abidjan, prices were multiplied by coefficients ranging from 5 to 10 depending on the places of provenance of insects.According to the traders surveyed, the selling prices in the market vary from one species to another and depending on the harvest period.The best-selling species were R. phoenicis which is a species more prized by collectors themselves and I. oyemensis whose prices at the wholesalers were respectively 5000 and 4000 FCFA per kg of larvae.They were followed by termites that cost 1100 FCFA per kilogram (Table 2).Unfortunately, the species R. phoenicis was less present in the markets because of the rapid decomposition of its larvae according to the traders.The majority of retailers surveyed reported that insect trade is profitable and mentioned profit margins estimated at 69.33±11.30%.The average monthly income was estimated at 58.666.66 ±11216 FCFA in that period of the year.The measuring instruments for sale varied according to the species and its condition (fresh or dried) (Figure 9).Some traders  (61.2%) said that income from the sale of insects makes it possible to cover household expenses (food, clothing and child health care), and part of this money was used to support their savings account.However, 38.8% argue that this trade is less profitable due to fluctuations in the price of insects with wholesalers but also the seasonality of the activity.For this group of traders, outside the period of abundance, other products such as cassava, vegetables, fruits, and fishes are marketed to cover daily expenses.

DISCUSSION
This study shows that nine insect species, namely R phoenicis, O. rhinoceros, I. oyemensis, C. butyrospermi, A. melifera, C. cossus, L. migratoria, A. domesticus, M. subhyalinus split into seven families and five orders are consumed in Abidjan..In Ghana, Anankwa et al. (2016) identified the same number of insect species.Payne et al. (2016) identified ten species of edible insects in the Democratic Republic of Congo.
In Southwestern Nigeria, the number of insectsconsumed is estimated to be seventeen according to the works of Banjo et al. (2006).Indeed, the different species identified in Côte d'Ivoire are also consumed in some countries such as Ghana where species such as R. phoenicis, C. butyrospermi, L. migratoria, A. domesticus and M. Subhyalinus are part of the daily diet of the population (Anankwa et al., 2016).
M. subhyalinus is a species of termite whose consumption extends over several African countries including Angola, Zambia, Togo, and Burundi (Jongema, 2015).Like termites, R. phoenicis is a species consumed in several western and central African countries (Jongema, 2015).In other countries such as Burkina Faso, the C. butyrospermi caterpillar is an important source of food for the local population (Anvo et al., 2016).The consumption of I. oyemensis caterpillar is less diversified, according to the list of Jongema (2015) this species has been reported as edible in Congo and Côte d'Ivoire.
The fact that I. oyemensis and M. subhyalinus were the most sold in the markets could be linked to their availability and good preservation.These results corroborate those of Tamesse et al. ( 2015) who showed that larvae of Lepidoptera (34.36%) and Isoptera (42.94%) are the most widely marketed insects in Yaoundé (Cameroon) markets.Larvae of R. phoenicis were less represented in the markets visited.This might be due to the fact that the collectors themselves are heavy consumers thereof and also to the rapid decomposition of these larvae because of their high fat content.Lenga et al. (2012) reported a lipid content of 65.70% of the total weight in R. phoenicis.In terms of insect consumption, the results showed that 59.72% of the respondents consume insects against 40.27% who donot consume them.These results are close to those of Balinga et al. (2004) who reported that 65.8% of Cameroonians consume caterpillars against 31.3%who are indifferent.However, 85% of populations in the Central African Republic are fond of caterpillars (Mabossy et al., 2013).
Children are generally out of school in rural areas, making them the main source of collectors and consumers of insects.The low insect consumption among those with higher education could be explained by the change in eating habits resulting from the culture shock due to urbanization, and greater availability of alternative sources of protein in urban areas, which tends to depreciate consumer interest in large cities for insects that are more attracted by elaborate and imported foods (Mabossy et al., 2013;Le Gall, 2015).
The high consumption of insects by the Krou and Mandé is explained by their eating habit.This observation is confirmed by Moussa (2002) who reported that insect consumption in the Republic of Congo is an eating habit.According to our investigations, the trade is carried out only by women and young girls aged between 18 and 50 years.Balinga et al. (2004) point out that in Central African markets, insect sellers are mainly women and children.Insect trade is a seasonal activity but generates average incomes estimated at 59000 CFAF per seller and per month.These figures may vary from one country to another depending on the period and availability of insects in the markets.Dounias (2003) noted an amount of 50 000 FCFA per seller and per month in southern Cameroon.

Conclusion
This study on edible insects in the city of Abidjan has helped identify nine edible insect species belonging to five orders and seven families.Of the surveyed people, 59.72% consume thereof.This consumption is related to age and cultural area.Children and the people school drop outs, are the biggest consumers, as are the Krou and Mandé.These two ethnic groups are the most involved in edible insect trade.Profit margins related to this activity are estimated at 59000 FCFA/month/merchant during the periods of insect availability.It also contributes to economic equilibrium and poverty reduction in households.

Figure 1 .
Figure 1.Location of the study area.

Figure 2 .
Figure 2. Proportion of respondents who reported having consumed each of these species.

Figure 3 .
Figure 3. Insect consumption rate depending on the age groups.

Figure 4 .
Figure 4. Insect consumption rate depending on educational attainment.

Figure 5 .
Figure 5. Insect consumption rate depending on cultural area.

Figure 6 .
Figure 6.Sources of motivation for insec consumption mntioned by the respondents.

Figure 8 .
Figure 8. Edible insect supply area to the city of Abidjan.

Table 1 .
Data on the different insect species sold and consumed in the three sampled communes.

Table 2 .
Estimate of profit margin related to insect sale.