Neglected and Underutilised Insects of Ghana: Identification, Spatial Distribution and Utilisation for Food, Feed and Nutrition

NEGLECTED AND UNDERUTILISED INSECTS OF GHANA: IDENTIFICATION, SPATIAL DISTRIBUTION AND UTILISATION FOR FOOD, FEED AND NUTRITION

A thesis submitted to the Department of Crop and Soil Sciences, Faculty of Agriculture, College of Agriculture and Natural Resources, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana, in partial fulfilment of the requirements for the award of the degree of

DOCTOR OF PHILOSOPHY IN ENTOMOLOGY

BY Jacob Paarechuga ANANKWARE BSc. Applied Biology (2009) M.Phil. Entomology (2012)

NOVEMBER, 2016

DECLARATION

I do hereby declare that, except for references to works of other researchers which have duly been cited, this thesis consists entirely of research conducted by me at the Kwame Nkrumah University of Science and Technology (KNUST), Kumasi, Ghana and at the entomology laboratories of the International Centre for Insect Physiology and Ecology (ICIPE), Nairobi, Kenya. I further declare that no part of this work has been presented for another degree elsewhere.

Jacob Paarechuga ANANKWARE …………………… …………………………

PG1189313 Signature Date

(Student Name and ID)

Certified by:

Dr. Enoch A. Osekre ………………………….. ……………………………

(Supervisor) Signature Date

Prof. D. Obeng-Ofori …………………………… …………………………….

(Co-Supervisor) Signature Date

Prof. Canute M. Khamala …………………………… …………………………….

(Co-Supervisor) Signature Date

Dr. Enoch A. Osekre …………………………… ………………………………

(Head of Department) Signature Date

ACKNOWLEDGEMENT

I thank the Almighty God for the gift of life and sound health that enabled me complete this work. My sincerest appreciation goes to my supervisors, Dr. Enoch A. Osekre,

Professor Daniel Obeng-Ofori and Professor Canute P. M. Khamala for their patience, relentless guidance, excellent suggestions, untiring assistance, critical reading of the manuscript and fatherly support throughout the project. I am greatly indebted to the following personalities: Dr. Jacob A. Hamidu, Dr. Kweku Adomako, Prof Comfort

Atuahene, Mr. Obed Opoku and Mr. Benjamin Adjei-Mensah of the Animal Science

Department, Kwame Nkrumah University of Science and Technology (KNUST) for their assistance with the experimental designs, logistics/space and data collection during the feeding-trial experiments. My thanks also go to Mr. Raphael A. Ayizanga of the

Department of Animal Science, University of Ghana, for advice on experimental designs and data analysis; Mr. Fauster Awepuga and the numerous volunteers who participated in the research project. My warmest appreciation goes to the staff, students and lecturers of the Department of Crop and Soil Sciences, KNUST. Finally, and most importantly, my heartfelt gratitude goes to Aspire Food Group, Ghana, Fish for Africa (FfA), Hon. Mark-

Owen Woyongo (Minister of Interior, former Defence Minister and MP for Navrongo

Central) and the Association of African Universities (AAU), for funding my Ph.D studies.

ABSTRACT

Even though animal meat plays a vital role in human diet, there are growing concerns about the supply gap and the ecological footprint resulting from high production and consumption of animal meat. These studies were conducted to identify the major edible insects of Ghana and encourage their cultivation and consumption in the country. The study was also aimed at developing an entomophagical map of Ghana and evaluate how insects could contribute to food, feed and nutrition security in Ghana. The studies also evaluated social and environmental factors that affect entomophagy in Ghana with a view to initiating programmes for their use for human and poultry nutrition in Africa. Two thousand questionnaires were administered to randomly selected respondents in all the ten regions of Ghana. Nine species of major edible insects belonging to five orders were identified. The nine edible insects in Ghana are: the larvae of the palm weevil

(Rhyncophorus phoenicis Fabricius), termites (Macrotermes bellicosus Smeathman), ground crickets (Scapteriscus vicinus Scudder), field crickets (Gryllus similis Chapman), house cricket (Acheta domesticus Linnaeus), grasshoppers (Zonocerus variegatus

Linnaeus), locusts (Locusta migratoria Linnaeus), the shea tree caterpillar (Cirina butyrospermi Vuillot) and larvae of the scarab beetle (Phyllophaga nebulosa Harris).

Proportionally, the scarab beetle (2%), field cricket (5%), shea tree caterpillar (8.7%), house cricket (9.5) and the locust (10%) were the least consumed insects whereas the palm weevil larvae (47.2%), termites (45.9%), ground cricket (33.3%) and grasshopper

(30.5%) were the most consumed insects in Ghana.With the exception of the palm weevil, all the other edible insects are only available from May to December.

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Entomophagy was found to be influenced by age, gender, education and occupation.

Also, entomophagy was more pronounced in rural areas than urban areas. The studies also revealed that entomophagy is practised across all age groups and gender.

Proportionally, 90%, 78% and 74% of the aged (60+), middle age (31-50) and the youth

(18-30) consume various edible insects, respectively. Over 87% of respondents who consume edible insects obtained them through hunting/trapping. An entomophagical map of Ghana was also developed to delineate the location and extent to which various edible insect species are utilized as food and feed. Proximate and comparative analyses of the nutritional chemistry of some identified entomophagical species were also done. The shea tree caterpillar (STC) C. butyrospermi contained the highest amount of crude protein of

63% while the Black Soldier Fly Larvae (BSFL) Hermetia illucens Linnaeus contained the highest percentage of ash (17%) with the Palm weevil larvae (PWL) recording the lowest percentage of ash (1.4%). The PWL had the highest fat content of 65.4%, followed by BSFL (18.0%). The predominant amino acid in house fly larvae (HSFL)

Musca domestica Linnaeus was phenylalanine (36.5 µg/g), followed by methionine (30.1

µg/g) whiles the limiting amino acid was arginine (7.5 µg/g). The highest amino acids in

PWL was phenylalanine (54.6 µg/g), followed by Isoleucine (53.0 µg/g) with the limiting amino acid being tyrosine (8.6 µg/g). Further experiments were conducted to develop a mass production system for BSFL, HSFL and PWL in the rural conditions of Ghana.

Among the several organic wastes evaluated, the best yield for BSFL was from 3 kg moist spent grain (brewery waste) + 2 kg dry fish feed factory waste + 0.5 litre yeast

(liquid) + 4.5 litres of water. For the HSFL, two formulations (2 kg chicken manure + 2 kg fish feed waste + 3-5 L water or 3 kg brewery waste + 1 kg chicken manure + 1 kg

Yeast + 1 L water) proved very useful for mass rearing of the maggots. The potential of the BSFL meal as a replacement for fish/soyabean meal in the diets of broilers was also investigated. The crude protein of BSFL (44.8) was the highest and T1 (BSFL+Soy)

(20.8) recorded the lowest crude protein. The highest feed intake was recorded from T2

(BSFL+Fish) (5.7 kg) and the control T0 (Fish+Soy) registered the highest water intake

(12.15 l). In terms of total weight gain and final weight, T2 was superior to T1 but statistically (p > 0.05) similar to the control. Conversely, the differences between feed conversion ratio (FCR) and mortality rate were not significant (p > 0.05). The differences in all chicken carcass parameters measured except for empty intestine and abdominal fat weights were significant (p < 0.05). Again, T2 was better (p < 0.05) than T1 for heart weight and liver weight. Wings, breast and thigh weights were significantly (p < 0.05) influenced by BSFL but not for drumstick, and back weights. Birds fed with T1 had relatively lighter (p < 0.05) wings compared to those fed with T2. Haematological parameters were not significantly (p > 0.05) different among treatments except for white blood cell count and mean cell volume. The research has demonstrated that, edible insects especially the shea tree caterpillar (STC) is a good source of unsaturated fatty acids, particularly linolenic acid which is required in the diets of the aged. The oils in edible insects are rich in polyunsaturated fatty acids such as linoleic and α-linoleic acids which are essential for the development of children and infants. The high content of desirable unsaturated fatty acids in some edible insects makes them important food components in the diet of humans. The larvae of the black soldier fly can be used as a replacement for fish/soy meal in the diets of broiler chicks so as to reduce the cost of poultry production.

DEDICATION

I dedicate this work to my beloved parents Mr. and Mrs. George Bangase Anankware for giving me education and to my lovely wife Joyce Patience Anankware, my siblings;

Esther and Roger B. Anankware for their prayers and support. I also dedicate it to the numerous entomophagical entomologists and farmers who are toiling hard to feed this world. Finally, I dedicate this work to my mentor, Professor Daniel Obeng-Ofori, who has given me every cause to remain humble and keep working hard.

TABLE OF CONTENTS

DECLARATION ...... I

ACKNOWLEDGEMENT ...... II

ABSTRACT ...... III

TABLE OF CONTENTS ...... VII

LIST OF TABLES ...... XII

LIST OF FIGURES ...... XIV

LIST OF PLATES ...... XV

CHAPTER ONE: GENERAL INTRODUCTION ...... 1

1.1 Background of the study ...... 1

1.2 Problem statement ...... 2

1.3 Justification of the study ...... 3

1.4 Research Hypothesis ...... 4

1.5 Objectives ...... 4

CHAPTER TWO: LITERATURE REVIEW ...... 6

2.2 Evolution and frequency of entomophagy ...... 9

2.2.1 Entomophagy in Asia ...... 12

2.2.2 Entomophagy in Latin America ...... 15

2.2.3 Entomophagy in Africa ...... 18

2.2.4 Ghana ...... 20

2.3 Some important insect species consumed worldwide ...... 20

2.3.1 Caterpillars ...... 20

2.3.2 Palm weevil ...... 22

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2.3.3 Termites ...... 23

2.3.4 Stink bugs...... 23

2.3.5 The long-horned grasshopper, Ruspolia difference ...... 24

2.4 Factors determining entomophagy ...... 24

2.5 Edible insects as a natural resource ...... 27

2.6.1 Semi-cultivation of palm weevil larvae ...... 28

2.6.2 Caterpillars ...... 29

2.7 Domesticating edible insects: opportunities to the environment ...... 30

2.8 Advantages of rearing edible insects ...... 31

2.8.1 Feed conversion ...... 31

2.8.2 Organic waste products ...... 33

2.8.3 Greenhouse gas (GHG) and ammonia emissions ...... 34

2.8.4 Nutritional value of insects for human consumption ...... 36

2.9 Insects as animal feed ...... 43

CHAPTER THREE ...... 44

IDENTIFICATION AND CLASSIFICATION OF COMMON EDIBLE INSECTS AND FACTORS AFFECTING ENTOMOPHAGY IN GHANA ...... 44

3.1 INTRODUCTION ...... 44

3.2 MATERIALS AND METHODS ...... 45

3.2.1. Sampling sites and sample size ...... 46

3.2.3. Sources of data collected ...... 48

3.2.4 Insect collection, identification and classification ...... 50

3.2.5 Preparation of geographical map ...... 51

3.3 DATA ANALYSIS ...... 51

3.4 RESULTS ...... 53

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3.4.1 Socio-economic background of respondents ...... 53

3.4.2 Taxonomic classification of the edible insects in Ghana ...... 54

3.4.3 Seasonality of edible insects ...... 56

3.4.4 Consumption of edible insects in Ghana ...... 59

3.4.5 Developmental stages consumed and purposes of consuming edible insects ...... 60

3.4.6 Factors that influence the practice of entomophagy in Ghana ...... 63

3.4.7 Insect consumption by locality in Ghana ...... 65

3.4.8 Zonal and seasonal variations in insect availability and consumption ...... 66

3.4.9 Acquiring edible insects ...... 67

3.5 DISCUSSION ...... 71

3.5.1 Socio-economic background of respondents ...... 71

3.5.2 Taxonomic classification, seasonality and consumption of edible insects in Ghana ...... 71

3.5.3 Harvesting of edible insects ...... 75

3.5.4 Developmental stages consumed and purposes of consuming edible insects in Ghana...... 76

3.5.4 Factors that influence the practice of entomophagy ...... 77

3.5.5 Insect consumption by locality in Ghana ...... 78

3.5.6 Determinants of insect availability and consumption ...... 79

3.6 Prospects and challenges to entomophagy in Ghana ...... 81

3.6.1 Prospects ...... 81

3.6.2 Challenges ...... 83

CHAPTER FOUR ...... 87

NUTRITIONAL CONTENT AND COMPARATIVE ANALYSIS OF VARIOUS EDIBLE INSECTS AND FEED FORMULATIONS ...... 87

4.1 INTRODUCTION ...... 87

4.2 MATERIALS AND METHODS ...... 88

4.2.1 Edible insecsts and analysis conducted...... 88

4.2.2 Amino acid profile ...... 89

4.2.3 Proximate analysis ...... 91

4.2.4 Total carbohydrate ...... 93

4.3 RESULTS ...... 93

4.3.1 Nutrient composition ...... 93

4.3.2 Composition of Amino Acids ...... 94

4.3.3 Composition of Fatty Acids ...... 95

Table 4.3 contd.: Average percentage fatty acid content of the selected insects ...... 98

Table 4.3 contd.: Average percentage fatty acid content of the selected insects ...... 99

4.4 DISCUSSION ...... 100

4.4.1 Proximate analysis of the selected insects ...... 100

4.4.2 Composition of Amino Acids ...... 103

4.4.3 Composition of Fatty Acid...... 104

CHAPTER FIVE ...... 111

MASS REARING PROTOCOLS FOR SOME EDIBLE INSECT SPECIES ...... 111

5.1 INTRODUCTION ...... 111

5.2 MATERIALS AND METHODS ...... 113

5.2.1 Production of larvae (maggots) of the black soldier fly, H. illucens ...... 113

5.2.3 Production of oil palm and raffia weevil ...... 118

5.2.4 Mass rearing of the house fly, M. domestica (Linnaeus) larvae (maggots) ...... 121

5.3 RESULTS ...... 124

5.4 DISCUSSION ...... 126

CHAPTER SIX ...... 129

POTENTIAL OF BLACK SOLDIER FLY, H. illuscens AS A REPLACEMENT FOR FISH/SOYBEAN MEAL IN THE DIET OF BROILERS ...... 129

6.1 INTRODUCTION ...... 129

6.2 MATERIALS AND METHODS ...... 131

6.2.1 Source (s) of black soldier fly larvae (BSFL) ...... 131

6.2.2 Experimental diets ...... 132

6.3 RESULTS ...... 135

6.3.1 Proximate composition of feed ...... 135

6.3.2 Effect of BSFL on growth performance of birds ...... 136

6.3.3 Effect of BSFL on carcass parameters of birds ...... 137

6.3.4 Effect of BSFL on primal cuts of birds ...... 139

6.3.5 Effect of BSFL on haematology of birds ...... 140

6.4 DISCUSSION ...... 142

CHAPTER SEVEN ...... 147

CONCLUSSIONS AND RECOMMENDATIONS ...... 147

7.1 CONCLUSSIONS ...... 147

7.2 RECOMMENDATIONS ...... 149

REFERENCES ...... 150

APPENDIX 1: QUESTIONNAIRE USED FOR THE SURVEY ...... 175

APENDIX 2: ANOVA TABLES ...... 178

LIST OF TABLES

Table 2.1: Some major edible insects of Asia...... 14

Table 2.1contd.: Some major edible insects of Asia ...... 15

Table 2.2: Some major edible insects of North and Latin America ...... 17

Table 2.3: Some major edible insects of Africa ...... 19

Table 2.4: Energy content of various insect species from various parts of the world...... 38

Table 2.5: Crude protein content of selected insect species by order...... 39

Table 2.6: Protein content variation at various metamorphosis stages of the raw variegated grasshopper (Zonocerus variegatus L.), Ogun State, Nigeria...... 40

Table 2.7: Fat content and major fatty acids in edible insects consumed in Cameroon. .. 41

Table 3.1: Regional, communal and gender distribution of respondents in the survey. ... 47

Table 3.2: Interpretation of the values of the level of association ...... 52

Table 3.3: Bio-data of respondents ...... 53

Table 3.4: Major edible insects in Ghana ...... 54

Table 3.5: Seasonality of the major edible insects in Ghana...... 58

Table 3.6a: Developmental stages of identified insects consumed by humans and means of acquiring them...... 61

Table 3.6b: Developmental stage of identified insects used as animal feed and means of acquiring them...... 62

Table 3.7: Correlation between entomophagy and some selected variables ...... 63

Table 3.8: Distribution of insect consumers by gender...... 63

Table 3.9: Distribution of insect consumers by age ...... 64

Table 3.10: Distribution of insect consumers by formal education...... 65

Table 3.11: Distribution of respondents on insect consumption by locality in Ghana. .... 65

Table 3.12: Respondents’ View on Insects Serving as a Source of Income in Ghana. .... 66

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Table 3.13: Distribution of respondents on difficulty of hunting insects ...... 68

Table 3.14: Distance travelled in hunting/trapping edible insects ...... 68

Table 3.15: Response on health risk posed by eating insects...... 70

Table 3.16: Purposes for rearing/harvesting insects in the various regions of Ghana...... 70

Table 4. 1 Nutrient content of selected edible insects ...... 94

Table 4.2. Amino acid content of selected insects ...... 95

Table 4.3: Average percentage fatty acid content of the selected insects ...... 97

Table 5.1: Performance of BSF larvae reared on different substrates...... 126

Table 6.1: Per cent ingredients in starter diet used to raise broiler birds ...... 132

Table 6.2: Per cent ingredients in grower-finisher diet used to raise broiler birds ...... 133

Table 6.3: Chemical composition of BSF, fish meal and soybean meal ...... 136

Table 6.4: Growth of broiler chicken fed on diets containing different oncentrations of black soldier fly larvae...... 137

Table 6.5a: Carcass parameters of broiler chicken fed on diets containing different concentrations of black soldier fly larvae...... 138

Table 6.5b: Carcass parameters of broiler chicken fed diets containing different concentrations of black soldier fly larvae...... 139

Table 6.6: Primal cuts of broiler chicken fed diets containing different concentrations of black soldier fly larvae ...... 140

Table 6.7a: Haematology of broiler chicken fed diets containing different concentrations of black soldier fly larvae ...... 141

Table 6.7b: Haematology of broiler chicken fed diets containing different concentrations of black soldier fly larvae...... 142

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LIST OF FIGURES

Figure 2.1: Entomophagical map of the world...... 11

Figure 2.2: Worldwide percentage distribution of entomophagical insects by order ...... 12

Figure 2.3: Feed conversion efficiencies of crickets versus conventional meats...... 33

Figure 2.4a: GHG’s emission of three insect species versus pig and beef cattle...... 35

Figure 2.4b: Ammonia emission of three insect species versus pig and beef cattle ...... 36

Figure 3.1: Availability and Human Consumption of Insects as Food in Ghana ...... 59

Figure 3.2: Availability and Use of Insects as Feed for Animals in Ghana ...... 60

Figure 3.3: Percentage distribution of reasons for eating insects in Ghana ...... 62

Figure 3.4: Species of insects consumed in the various ecological zones of Ghana ...... 67

Figure 5.1: A sketch of the cage used in rearing the adult BSF...... 115

Figure 5.2: A flow chart showing house fly maggot production...... 123

Figure 5.3: Steps involved in rearing the adult BSF, larvae and pupae ...... 125

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LIST OF PLATES

Plate 2.1: Illustration of insect use in the animal feed chain…………………………….33

Plate 3.1a: Scarab beetle larva……………………..……………………………………54

Plate 3.1b: Shea tree caterpillar…...………...………………………………………...…54

Plate 3.1c: Grasshopper……………...………...………………………………………...54

Plate 3.1d: House cricket………………………...………………………………………54

Plate 3.1e: Palm weevil larva……………………..……………………………………..54

Plate 3.1f: Locust…………………………………..……………………………………54

Plate 3.1g: Ground cricket…………………………..…………………………………..55

Plate 3.1h: Termite………………………………….…………………………………..55

Plate 3.1i: Field cricket……………………………….………………………………....55

Plate 3.2: Trapping palm weevil larvae using innovative strategies in the Ashanti Region of Ghana…………………………………………………………………………………82

Plate 4.1: vortexer and sonicator bath…………………………………………………...93

Plate 5.1: Sample of containers used for rearing PWL.………….…………………….120

Plate 5.2: Adult Palm Weevils………………………….……….……………………..120

Plate 5.3: Palm yolk soaked in a container……………….…….……………………...120

Plate 5.4: Palm yolk in container ready for adult inoculation…..………………….…..120

Plate 5.5: Container showing larvae on feed………………………………………...…121

Plate 5.6: Container showing long palm fibres…………………………………………121

Plate 6.1: Rearing cage for black soldier fly……………………………………………131

CHAPTER ONE: GENERAL INTRODUCTION

1.0 INRODUCTION

1.1 Background of the study

Food security and malnutrition are major areas of concern to human development and poverty reduction globally. While significant gains are being made in reducing poverty, rising food prices continue to push more people, especially in developing countries, into food poverty (Asian Development Bank, 2012). The Human Development Report in

2014 attributed the rising food prices to decrease in agricultural investment and research coupled with climate change as well as the high food demand due to rapid population growth globally (UNDP, 2014). The demand for meat is experiencing exponential growth globally due mainly to the demand in vital macronutrients and micronutrients available in meat that are essential for proper growth and development in children and adults (van

Huis et al., 2013). Despite the vital role that animal meat plays in human diet, there are growing concerns about the supply gap and the ecological footprint resulting from high production and consumption of animal meat (The Organic Centre, 2010; International

Food Policy Research Institute, 2003).

The high demand for meat has consequently resulted in intensive industrial production of animal meat from cattle, pig, poultry and fish. Producing animal meat, however, requires large quantities of vegetation and water thereby imposing a major toll on the environment

(Heinrich, 2014). Moreover, a significant proportion of the feed for these animals is often imported. In 2008 for instance, globally, 46% of all fish feed was imported to support aquaculture. While more feed is needed to support the industry, acquiring this feed was

much cumbersome due to the ever-expanding aquaculture industry coupled with high competition from other industries (such as poultry, pig and ruminants) for similar feed resources including soya, fishmeal and fish oil (FAO, 2011a).

“Neglected” or “underutilised” insect species may be defined as those insects that are important for the sustainance of local human communities but remain poorly documented, ignored and underexploited by mainstream researchers and development partners. Briefly stated, they are species whose potential has not been fully realized. They are often ignored by society due to their less economic, cultural, genetic and environmental factors, particularly in the agrobiodiversity-rich tropics (IPGRI, 2002).

Insects are often considered a nuisance to human beings and mere pests of crops and animals. However, insects offer ecological services that are fundamental to the survival of humankind. They pollinate pants, improve soil fertility through waste bioconversion, serve as natural biocontrol for harmful pest species, and they provide valuable products for humans such as honey, silk and medical applications such as maggot therapy (van

Huis et al., 2013). An estimated 100 000 pollinator species have been identified and almost all of these (98 percent) are insects (Ingram et al., 1996). Over 90 percent of the

250 000 flowering plant species depend on pollinators.

1.2 Problem statement

Food security is a global challenge. Meat consumption has dramatically increased in recent years, over five times globally since 1945 and more than 20 times in China alone since 1970 (Kenis et al., 2006.). Animal feed needs a substantial amount of proteins- soy

and fish meal. Owing to rising demand for food, especially meat, there is a pressing need to increase the supply of protein from viable sources (Anankware et al., 2015).

While the consumption of edible insects is gaining currency in countries like Mexico

(Ramos-Elorduy et al., 2011), their use as part of traditional diet has been observed to continually decrease in many communities in Africa, specifically in Ghana, where these edible insects originally formed a vital source of food and nutrition of the local people

(Anankware et al., 2015). This situation has generally been attributed to limited knowledge on the dietary value of edible insects coupled with urbanisation and modernisation. Promoting sustainable meat supply to support the world’s population and biodiversity therefore requires a diversification in food production which has less ecological footprint (Gerbens-Leenes et al., 2013). Insects offer a suitable compliment to meat protein.

1.3 Justification of the study

Increased demand and the resultant hike in prices of fishmeal and soy as well as rising fish production, are pushing new frointiers in research into the development of insect- based protein for fish and poultry. Insect-based feed merchandise could have a comparable market as soy and fishmeal, which are currently the main constituents used in formulating feed for livestock and aquaculture (Anankware et al., 2015).

Ghana imports over 90% of the protein required for fish and poultry rearing (Anankware et al., 2015). Due to increased demand for food, particularly meat, there is an urgent need to increase the supply of protein from sustainable sources, including edible insects. For

sustainable utilisation of edible insects as source of protein, it is important to identify and map out the various insect species consumed by various ethnic groups, record the seasonality, accessibility and challenges, as well as develope a spatial map of the location of these insects. Additionally, the viability of cultivating and using various edible insect species to support the dietary system of people as well as serve as feed for farmed animals and fish must be established impirically.

1.4 Research Hypothesis

Insects are a viable source of food for man and poultry in smallholder farm environments of Ghana.

1.5 Objectives

The main objective of this research was to identify and map out the various insect species consumed by various tribes, develop a spatial map of the locations of these insects and investigate the factors that affect and promote entomophagy in Ghana. The specific objectives were to:

i. Identify, classify and establish a geographical distribution of common edible

insects in Ghana and to catalogue consumer-related factors that affect

entomophagy.

ii. Conduct proximate analysis of some entomophagical species.

iii. Establish mass rearing protocols for selected potential entomophagical species.

iv. Explore the potential of black soldier fly larvae (BSFL) as a replacement for

fish/soybean meal in the diet for rearing chicken broilers.

CHAPTER TWO: LITERATURE REVIEW

2.1 Economic importance of insects

Evolution in the last 40 million years has resulted in different adaptations by various arthropod species to different environments. Approximately, a million of the 1.4 million identified species of animals on earth are insects, with several millions yet to be identified (van Huis et al., 2013). Insects are often considered a nuisance to human beings and mere pests of crops and animals. However, insects offer ecological services that are fundamental to the survival of humankind. They pollinate pants, improve soil fertility through waste bioconversion, serve as natural biocontrol for harmful pest species, and they provide valuable products for humans such as honey, silk (van Huis et al.,

2013). An estimated 100 000 pollinator species have been identified and almost all of these (98 percent) are insects (Ingram et al., 1996). Over 90 percent of the 250 000 flowering plant species depend on pollinators.

Many insects are rich in protein and good fats and high in calcium, iron and zinc (van

Huis et al., 2013). Apart from human consumption, insects have been used as feed for poultry and pigs. Contrary to popular belief, of the 1 million described insect species, only 5000 can be considered harmful to crops, livestock or human beings (Van Lenteren,

2006). In addition, insects have assumed their place in human cultures as collection items and ornaments and in movies, visual arts and literature (Ingram et al., 1996). Other medical applications include maggot therapy and the use of bee products – such as honey, propolis, royal jelly and venom – in treating traumatic and infected wounds and burns

(van Huis, 2003a).

Due to their high fecundity, ease of access, nutritional composition and simple rearing techniques, insects offer a cheap and sustainable opportunity to curtail malnutrition by providing emergency food and improving livelihoods of the vulnerable in society. The most frequently consumed insects include: beetles (Coleoptera) (31%), caterpillars

(Lepidoptera) (18%) and bees, wasps and ants (Hymenoptera) (14%). The rest are grasshoppers, locusts and crickets (Orthoptera) (13%), cicadas, planthoppers, scale insects, true bugs and leafhoppers (Hemiptera) (10%), termites (Isoptera) (3%), dragonflies (Odonata) (3%), true flies (Diptera) (2%) and other orders (5%) (van Huis et al., 2013).

Insects are a healthy and highly nutritious source of food with high protein, vitamin, fat, minerals and fibre content (Van Itterbeeck and van Huis, 2012). The nutritional composition of edible insects is exceedingly variable owing to the wide range of edible insect species. Within the same group of species, nutritional composition may vary with the metamorphic stage of the insect, its habitat and diet. For instance, the composition of unsaturated omega-3 and 6 fatty acids in mealworms is analogous to that in fish and higher than in cattle and pigs. Furthermore, the protein, mineral and vitamin content of mealworms is comparable to that in fish and meat (van Huis et al., 2013).

In the past, edible insects were ostensibly an unlimited resource derived from nature (van

Huis et al., 2013). Nevertheless, most edible insect species are currently in jeopardy due to pollution, overharvesting and habitat degradation. The distribution, ecology and availability of edible insects will likely be affected by climate change in ways that are still relatively unknown (van Huis et al., 2013).

The high feed conversion efficiency of insects makes their rearing harmless to the environment. For example, crickets gain 1 kilogram of bodyweight from 2 kilograms of feed. Moreover, organic side-streams like human and animal waste can be used to effectively rear insects and this can greatly reduce environmental contamination (van

Huis et al., 2013). Available evidence suggests that insects emit fewer greenhouse gases and less ammonia than cattle or pigs and require considerably less land and water than cattle rearing. Unlike mammals and birds, insects may pose less risk of transmitting zoonotic diseases to man, fauna and flora (van Huis et al., 2013). Finally, insect farming may require minimal land or market introduction efforts, as insects already form an integral part of some local food cuisines.

For decades if not centuries, a multiplicity of insects have been a cherished source of protein for both food and feed across continents other than Europe. With consumption habits shifting to pork, chicken, beef and fish, insects have the prospect to be effectively utilised as a natural ingredient in high-protein feed. Jobs and improved livelihoods can be achieved by insect gathering and farming as mini-livestock at the household level or industrial scale. In developing countries, some of the poorest members of society, such as women and landless dwellers can easily become involved in the gathering, rearing, processing and sale of insects. This can directly improve their diets and create cash income through the sale of surplus products as street foods.

2.2 Evolution and frequency of entomophagy

The interaction between humans and edible insects dates back to the eighth century BCE.

This has been captured in a host of literature that gives evidence of the practice of entomophagy (consumption of insects) in ancient times (van Huis et al., 2013). Despite some limitations to the growth of entomophagy mainly due to urbanisation and modenisation, the practice of entomophagy continues to gain more popularity and it is recommended as vital for promoting sustainable development especially in the areas of food security (van Huis et al., 2013).

Entomophagy has been identified with various tribes including the Romans and the

Greeks back in the eighth century BCE. In his work, Bodenheimer (1951) reported on the consumption of edible insects such as locusts as a vital delicacy during important occasions and among royals such as the palace of Asurbanipal. In an earlier work,

Aristotle (384-322 BCE) narrated the use of various edible insects including the cicadas which were a popular delicacy in ancient Greece. These insects are consumed at various developmental stages; from larval through to the adult stages. Adding to the stock of literature on the practice of entomophagy, Pliny the Elder; a renowned philosopher and author of the encyclopedia Historia Naturalis, mentioned the cossus (the larva of the

Cerambyx cerdo L. (longhorn beetle)) as cherished delicacy among the Romans.

The consumption of edible insects is engraved in various religious literature, beliefs and practices among various faith groups. Religious writings of Christian and Islamic literature cite the consumption of insects as an acceptable practice. Evidence from the

Holy Bible is found in the book of Leviticus where specific reference is made on the

consumption of insects such as the beetles and locusts (Leviticus XI: 21, 22). El-Mallakh and El-Mallakh (1994) also provided evidence of entomophagy in Islamic belief. They name the ants, bees, lice, locusts and termites as examples of edible insects.

The number of edible insect species in the world is unknown and several reasons may account for this. By using only Latin names and correcting for synonyms, Jongema

(2015) of the Wageningen University (WUR) compiled a worldwide inventory that listed

1,900 edible insect species worldwide (Figure 2.1). Lower estimates do exist. DeFoliart

(1997) counted only 1,000 species, while Ramos Elorduy (2006) identified 1,681 species.

Regional and national estimates have also been made. For example, van Huis (2005) identified 250 edible species in Africa; Ramos Elorduy et al. (2011) listed 549 species in

Mexico. In China, Chen et al. (2009) documented 170 species; Young-Aree and

Viwatpanich (2005) reported 164 species in the Laos People’s Democratic Republic,

Myanmar, Thailand and Viet Nam. Paoletti and Dufour (2005) also estimated that 428 species were consumed as food in the Amazon.

Figure 2.1: Entomophagical map of the world.

Fgure 2.1 shows the entomophagical map of the world. Unfortunately, information from and on Ghana is conspicuously missing due to the absence of data.

Figure 2.2 gives the details in terms of percentages of the most commonly consumed insects worldwide. Lepidoptera are consumed almost entirely as caterpillars and

Hymenoptera are consumed mostly in their larval or pupal stages. Both adults and larvae of the Coleopterans are eaten, while the Orthoptera, Isoptera and Hemiptera orders are mostly eaten as mature adults (Cerritos, 2009).

3% 3% 2%

11% 33%

14%

15% 19%

Coleoptera Lepidoptera Hymenopteara Orthoptera Hemiptera Isoptera Odonata Diptera

Figure 2.2: Worldwide percentage distribution of entomophagical insects by order

The frequency of insect consumption around the world is poorly documented. The few examples found in literature are from Asia, Latin America and Africa. However,

Jongema (2015) successfully compiled a list of the world’s edible insects. The major ones are summarised in Tables 2.1, 2.2 and 2.3 for Asia, North and Latin America and Africa, respectively.

2.2.1 Entomophagy in Asia

About 150 to 200 edible insects’ species are consumed in Southeast Asia alone. Red stripe weevils (Rhynchophorus ferrugineus Fabricius) from the Sago palm (Metroxylon sagu Rottb) are particulaly popular in Asia and are a serious delicacy in several regions

(Johnson, 2010). Certain insect species are available all year-round; these include several aquatic species, whilst others are seasonal. In Viet Nam, Myanmar and Thailand, several insect species are harvested all year-round from various habitats thereby ensuring a

continuous supply of edible insects (Yhoung-Aree and Viwatpanich, 2005; Yhoung-Aree,

2010).

Presently, entomophagy in most Asian countries is attributable to migration patterns. For example, northeastern Thailand was renowed for eating insects but labour-migration to tourist areas in the south, including Bangkok, has resulted in a well established practice throughout the country (Yen, 2009). An estimated 81 insect species are eaten in Thailand, over 50 insect species in South Asia (Pakistan, Sri Lanka and India), 39 species in the

Pacific Islands and Papua New Guinea, and between 150 to 200 species in Southeast Asia

(Johnson, 2010). Table 2.1 shows some of the major edible insects in Asia.

Table 2.1: Some major edible insects of Asia

Common Stage Genus Species Family Order names consumed Sitophilus oryzae (L.) Curculionidae Col. Rice weevil All stages ferrugineus Red stripe Larva, Rhynchophorus schah (F.) Dryophthoridae Col. weevil adult Water picicornis scavenger Hydrophilus (Chevr.) Hydrophilidae Col. Beetles Adult dominus Heliocopris (Bates) Scarabaeidae Col. Dung beetle Larva Mealworm Tenebrio molitor (L.) Tenebrionidae Col. beetle Larva Larva, Apis mellifera (L.) Apidae Hym. Honey bee pupa smaragdina Green tree Oecophylla (F.) Formicidae Hym. ant, redant All stages Macrotermes Winged spp. Termitidae Isopt. Termite adult Bombyx mori (L.) Bombycidae Lep. Silk worm Pupa guttatus Hairy Anax (Burm.) Aeschnidae Odonata emperor Adult Pantala flavscens (L.) Libellulidae Odonata Adult gigantea Acrida (Herbst) Acrididae Orth. Adult Migratory Locusta migratoria (L.) Acrididae Orth. locust Adult chinensis Oxya (Thunberg) Acrididae Orth. Adult Domesticus Acheta (L.) Gryllidae Orth. Adult bimaculatus Two spotted Gryllus (De Geer) Gryllidae Orth. cricket Adult Gryllotalpa sp. Gryllotalpidae Orth. Mole cricket Adult Conocephalus sp. Tettigoniidae Orth. Katydid Adult gregaria Schistocerca (Forskal) Acrididae Orth. Desert locust Adult echinata Haaniella (Redtenbacher) Heteropterygidae Phasmida Stick insect Adult

Table 2.1 contd.: Some major edible insects of Asia

Common Stage Genus Species Family Order names consumed Asian glabripennis longhorn Anoplophora (Motsch.) Cerambycidae Col. beetle ferrugineus Curculionidae Red palm Rhynchophorus (Oliv.) Dryophthorinae Col. weevil Larva longimanus Curculionidae Bamboo Cyrtotrachelus (F.) Dryophthorinae Col. weevil Larva deyrollei Hem. Giant water Lethocerus (Vuillefroy) Belostomatidae Het. bug Adult Hem. Cicada flammata Dist. Cicadidae Hom. Cicadas Apis mellifera (L.) Apidae Hym. Honey bee Pupa smaragdina Oecophylla (F.) Formicidae Hym. Green tree ant velutina Asian auraria predatory Larva, Vespa (Smith) Vespidae Hym. wasp pupa Nymph, Odonata gen. Odonata Dragonfly adult

Source: Y. Jongema (2015).

Legend: Col = Coleoptera, Hym = Hymenoptera, Orth = Orthoptera, Isopt = Isoptera, Lep = Lepidoptera, Phasmida = Phasmidae, Hem = Hemiptera, Het = Heteroptera, Dictyo = Dictyoptera.

2.2.2 Entomophagy in Latin America

Indigenous Mexicans possess a deep understanding of the traditional animal and plant species in their diets, as well as the life cycles of insects (Ramos-Elorduy, 1997; Ramos-

Elorduy et al., 1997). Insects are believed to operate in tandem with nature such as plant life cycles, moon cycles, rainy seasons and thunder (van Huis et al., 2013). For instance, the escamoles (larvae of the ants of the Liometopum sp.) are collected when the jarilla plant (Senecio salignus DC) is flowering. The harvesting of chapulines (Sphenarium

purpurascens Charpentier) coincides with the onset of the rainy season (van Huis et al.,

2013).

Insect collection is a seasonal affair in the Amazon. The Maku Indians; indigenous hunter-gatherers in the tropical forest of northwestern Amazonia in Brazil, harvest insects during the rainy season (from July to September) when game and fish hunting is difficult

(Milton, 1984). Smith and Paucar (2000) suggested that vibrations caused by rain and the sound of thunder trigger their emergence. Not all insects, however, are harvested during the rainy season. The larvae of the red palm weevil (R. palmarum L) and bearded weevil

(Rhinostomus barbirostris F.) are harvested by the Joïti people in Venezuela, from

September to January (at the end of the rainy season). Rain, in fact, keeps adult beetles away and tends to increase fungal attack (Choo et al., 2009). Table 2.2 shows some of the major edible insects in North and Latin America.

Table 2.2: Some major edible insects of North and Latin America

Common Stage Genus Species Family Order names consumed reticularis Prionoplus (White) Cerambycidae Col. Huhu beetle Larva ferrugineus Asian palm Larva, pupa, Rhynchophorus (Oliv.) Dryophthorinae Col. weevil adult rhinoceros Oryctes (L.) Scarabaeidae Col. Larva Cosmozosteria sp. Blattidae Dictyo. Cockroach Nymph, adult smaragdina Oecophylla (F.) Formicidae Hym. Green tree ant Pupa humectus hidalgoensis Canthon (Bates) Scarabaeidae Col. Tobacco Manduca sexta (L.) Sphingidae Lep. hornworm Larva tinctus Larva, pupa, Tropisternus (Sharp) Hydrophilidae Col. adult mexicana Phyllophaga (Blanch.) Scarabaeidae Col. Larva Tenebrio molitor L. Tenebrionidae Col. Larva confusum (Du Confused flour Tribolium Val) Tenebrionidae Col. beetle americana (L.)/ germanica Periplaneta (L.) Blattidae Dictyo. Cockroaches Nymph, adult Apis mellifera (L.) Apidae Hym. Larva, pupa mexicana Reproductive Atta (Smith) Formicidae Hym. adult Bombyx mori (L.) Bombycidae Lep. Silkworm moth Larva, pupa cancellata cancellata Schistocerca (Serv.) Acrididae Orth. Nymph, adult domesticus European house Acheta (L.) Gryllidae Orth. Cricket mexicanum histrio Sphenarium (Gerst.) Pyrgomorphidae Orth. Nymph, adult

Source: Y. Jongema (2015).

Legend: Col = Coleoptera, Hym = Hymenoptera, Orth = Orthoptera, Isopt = Isoptera, Lep = Lepidoptera, Phasmida = Phasmidae, Hem = Hemiptera, Het = Heteroptera, Dictyo = Dictyoptera.

2.2.3 Entomophagy in Africa

The African continent abound in insects, and so become an important food source when food staples are scarce. When hunting game/fish becomes difficult in the rainy season, insects play a pivotal role in food security in some African countries (van Huis et al.,

2013). Caterpillars are especially popular during the rainy season, although their availability can vary even within the same country depending on climatic conditions

(Vantomme et al., 2004).

According to Bahuchet (1975) and Bahuchet and Garine (1990), caterpillars provide an important source of protein during the rainy season (July to October) especially for pygmies in the Central African Republic. In the rainy season, average consumption is estimated at 42 freshly harvested caterpillars per person per day. Although, availabilty and consumption is much lower in certain parts of the year, the insects are available year- round, either dried or smoked. The indigenous Gbaya of Central Africa consume about

96 different insect species; this amounts to about 15% of their protein intake (Roulon-

Doko, 1998). Table 2.3 shows some of the major edible insects in Africa.

Table 2.3: Some major edible insects of Africa

Common Stage Genus Species Family Order names consumed wellmani Lampetis (Kerremans) Buprestidae Col Jewel beetle Larva Longhorned Analeptes trifasciata (F.) Cerambycidae Col beetle Larva plumbeus Polyclaeis (Guérin) Curculionidae Col Weevil Adult African palm Rhynchophorus phoenicis (F.) Dryophthoridae Col weevil Larva Water senegalensis scavenger Hydrophilus (Percheron) Hydrophilidae Col beetle Scarabaeidae Rhinoceros Augosoma centaurus (F.) Dynastinae Col beetles Larva abbreviate Scarabaeidae Chondrorrhina (F.) Cetoniinae Col Flower beetle pallidipes Chaoborus (Theob.) Chaoboridae Dip Lake fly midges Sudan millet Agonoscelis versicolor (F.) Pentatomidae Hem bug mellifera Apis mellifera (L.) Apidae Hym Honey bee Larva longinoda Oecophylla (Latr.) Formicidae Hym Weaver ants bellicosus Macrotermes (Smeathman) Termitidae Isopt Termites All stages forda Pallid emperor Cirina (Westwood) Saturniidae Lep moth Larva butyrospermi Cirina syn (Vuillot) Saturniidae Lep Larva Imbrasia belina (Gonimbrasia) (Westwood) Saturniidae Lep migratoria African migratorioides migratory Locusta (R.& F.) Acrididae Orth locust Adult gregaria Schistocerca (Forskål) Acrididae Orth Desert locust Adult

Source: Y. Jongema (2015). Legend: Col = Coleoptera, Hym = Hymenoptera, Orth = Orthoptera, Isopt = Isoptera, Lep = Lepidoptera, Phasmida = Phasmidae, Hem = Hemiptera, Het = Heteroptera, Dip = Diptera.

2.2.4 Ghana

Traditionally, Ghanaians eat insects. Insects have been consumed in Ghana probably since the first inhabitants settled there. Entomophagy is so widespread in Ghana that it can be witnessed in every indigenous community of the country (Anankware et al.,

2015). It is widely practiced in the various regions of the country. Different insect species are consumed in different regions ostensibly due to the distribution disparities of vegetation and insect species. For example, fried termites, Macrotermes bellicosus

(Smeathman) and dried shea defoliator, Cirini butyrospermi (Vuillot) are common in the markets of the three Northern regions especially Wa, the Upper West regional capital

(Anankware et al., 2013, 2015).

2.3 Some important insect species consumed worldwide

2.3.1 Caterpillars

Caterpillars remain one of the world’s most varied collections of edible insects. Not only are they valuable sources of protein and other micronutrients; they also make valuable contributions to livelihoods in many parts of the world. Caterpillars are collected by hand primarily by women and children and then degutted, boiled in salted water and sun-dried as a way of preservation. This form of preserved caterpillars could last for months and thus serve as a valuable source of nutrition in times of strain. Among the most renowned species are the witchetty grubs (Endoxyla leucomochla Leach) consumed in Australia

(Meyer-Rochow, 2005). The bamboo caterpillar (Omphisa fuscidentalis Hampson), is

also common in Thailand and the Lao People’s Democratic Republic (Yhoung-Aree and

Viwatpanich, 2005).

In Sub-Saharan Africa where the consumption of caterpillars is prevalent, van Huis

(2003b) indicated that 30% of all edible insect species in Sub-Saharan Africa are caterpillars. According to Malaisse (1997) who listed 38 species of edible caterpillars in an intensive study in a region populated by Bemba (Bantu-speaking people in the northeastern plateau of Zambia and neighbouring areas of the Democratic Republic of the

Congo and Zimbabwe). Latham (2003) further suggested that caterpillars make up 40% of the total animal protein consumed in the Democratic Republic of Congo.

The mopane caterpillars thrive in the vast habitat of the mopane woodlands which are mostly found in Botswana, Namibia, Zimbabwe and the Northern parts of South Africa.

The ecology and biology of the caterpillars amongst the native folks is extensively known in most rural communities (Mbata and Chidumayo, 2003) with its distribution largely connected to that of its principal host, the mopane tree (Colophospermum mopane Kirk ex J. Leonard). Stack et al. (2003) and Ghazoul (2006) stated that the mopane caterpillar is bivoltine in most areas, thus, it produces two generations each year. The first generation is produced between November and January (its major outbreak) and the second generation between March and May each year. Similar to other species of edible insects, mopane caterpillars are not merely “famine foods” consumed in times of food shortage, they also form a regular part of the diet (Stack et al., 2003). Aside being a source of livelihood for many, the gathering, processing, trading and consumption of the

mopane caterpillar is an integral part of local cultures and the marginalised (Illgner and

Nel, 2000; Stack et al., 2003).

2.3.2 Palm weevil

The larvae of the palm weevil (Rynchophorous spp.) is a delicacy the world over. They are consumed in Asia (R. ferrugineus Olivier), Africa (R. phoenicis Fabricius) and Latin

America (R. palmarum Linnaeus). Their delicious flavour (Cerda et al., 2008) is attributed to their elevated fat content (Fasoranti and Ajiboye, 1993). The palm weevil occurs all-year-round in the tropics where hosts are found. Fasoranti and Ajiboye (1993) reported that trees under stress (that is trees that have been destroyed by other insects, such as the rhinoceros beetles (Oryctes spp.) usually serve as hosts for the palm weevil.

Fallen palms can also serve as breeding sites and support hundreds of larvae for which reason palms are often felled intentionally by some farmers. van Itterbeeck and van Huis

(2012) noted that many native folks have excellent ecological knowledge of the palm weevil and can increase its availability and predictability through semi-cultivation practices. Research at Kade and the Jema districts of Ghana are currently exploring ways of rearing and producing oil palm weevils (R. phoenicis) in a more sustainable manner without felling the oil palm trees.

2.3.3 Termites

In the West, termites are usually identified as pests and famous for devouring wood. In the United States of America alone, termites are said to cause damages of more than half a billion dollars annually, despite the fact that they are considered a delicacy in several parts of the world. They are eaten as a main and/or side dishe or simply as a snack after they have been fried or sun-dried (Kinyuru et al., 2010).

2.3.4 Stink bugs

Eating of the nymphs and adults of stink bugs (Hemiptera: Pentatomidae) is a common practice throughout the world especially Mexico, southern Africa and Southeast Asia

(Ramos-Elorduy and Pino, 1989; 2002; DeFoliart, 2002). In Southern Africa,

Encosternum (Natalicola) delegorguei Spinola are considered delicacies. Stink bugs are consumed in Malawi, South Africa, Zimbabwe, China, Democratic Republic of Congo and Thailand (Faure, 1944; van Huis, 2003b; Morris, 2004). For example, Tessaratoma species, T. papillosa Drury (litchi stink bug), T. javanica Thunberg (longan stink bug) and T. quadrata Distant (“mien kieng”), a local name in the Lao People’s Democratic

Republic) are widely consumed in China, the Lao People’s Democratic Republic of

Congo and Thailand (Nonaka, 1996; Chen et al., 2009).

2.3.5 The long-horned grasshopper, Ruspolia difference

The edible grasshopper (Ruspolia differens Serville), formally known as

Homorocoryphus nitidulus vicinus Walker, is a long-horned grasshopper of the

Tettigoniidae family. It is a common food source in many parts of eastern and southern

Africa. In the Lake Victoria region of East Africa, where the grasshoppers are known as

“nsenene” they form a major part of food culture (Kinyuru et al., 2010). The Bahaya ethnic group in Tanzania’s Bukoba district consider grasshoppers a delicacy. In Uganda,

“nsenene”are traditionally collected by women and children. Grasshopper eggs which are laid in batches in the haulms of grasses do not develop under dry conditions. Rainfall triggers development, which takes about four weeks (McCrae, 1982). Nymphs and adults feed on grass anthers or grains such as rice, millet, sorghum and maize. Traditionally, grasshoppers are gathered during the day from these grasses (Mors, 1958). During collection of grasshoppers, the land is considered communal (Kinyuru et al., 2010), hence a farm owner cannot drive harvesters away.

2.4 Factors determining entomophagy

The harvesting of edible insects by humans and other predators vis-à-vis the limited domestication of these insects affects the insect populations (Choo, 2008). Insects are a popular prey to mammals, birds, reptiles and amphibians. Also, various insect species cross-prey on other species. Regrettably, people who recognize the benefits of insects form a minority. This is to a large extent due to the poor attitude towards the consumption of insects in Western societies. Some authors including Silow (1983) have

blamed the growth of negative attitudes towards entomophagy to the actions of some missionaries who spoke against consumption of insects such as termites. Morris (2004) identified this phenomenon among some Malawians who taboo insects on the basis of their Christian belief. In other places, consumers are often reluctant to proclaim the consumption of insects due possibly to stigmatisation (Ponzetta and Paoletti, 1997). The influence of western civilisation has also been suggested by some writers to have impacted negatively on research pertaining to edible insects in Africa (Kenis et al., 2006).

DeFoliart (1999) however warned against this discouraging attitude against insect consumption as it hampers the utilisation of a vital source of protein without providing any good substitute.

Various factors have been reported to have occasioned the deep-rooted practice of entomophagy in the tropics, although some are with little evidence. According to

Kirkpatrick (1957), insects in the tropics have relatively larger body size which facilitates harvesting.

The advancement of entomophagy in the tropics is also explained by the good supply of insects that occur in substantial quantities (Van Itterbeeck and van Huis, 2012). For instance, swarms of locusts commonly settle in large numbers at night making harvesting easier. This also applies to winged termites and caterpillars that have a similar behaviour of congregating at night and in the forest respectively. This makes harvesting easier and less stressful. Although some insects such as the Mormon cricket (Anabrus simplex

Haldeman) and the oak processionary caterpillar (Thaumetopoea processionea Linnaeus)

are noted to congregate in significant numbers in the temperate regions (Madsen and

Kirkman, 1988), it is relatively less pronounced as in the tropics.

This knowledge is said to better exist in the tropics than in the temperate where urbanisation and westernisation has, according to Holt (1885), resulted in a decline of entomophagy. For instance, in Ghana, knowledge of the location of palm weevils (in fallen palm trees) makes it easier to harvest these insects. Sometimes trees are deliberately felled to lure beetles to lay eggs to trigger the growth of the palm weevil larvae (Choo et al., 2009). Similar instances include the bamboo caterpillar that are found in stems of bamboo, in mounds where solder termites can be found as well as many insect species that are harvested by locals based on knowledge about their behaviour and breeding. It is, however, important to note that this factor does not hold for all insect species. For instance, locusts which are usually harvested during swarm invasion of farms are generally not predictable.

The uncontrolled and less selective insect harvest due partially to limited knowledge about the reproduction trends is reported to affect the regeneration of insect populations

(Latham, 2003; Illgner and Nel, 2000; Ramos-Elorduy, 2006). Where mature insect populations are indiscriminately harvested especially when this coincides with their reproductive period, their regeneration would be adversely affected (Cerritos, 2009). Due to the vital ecocosystem services provided by insects, the decline in their population also affects various ecological processes such as decomposition and pollination. Over- exploitation through the practice of entomophagy has also been reported to impose a

threat to the survival of edible insects (Morris, 2004; Schabel, 2006), especially where the harvest rate exceeds the recruitment rate of such insects (Cerritos, 2009).

The inadequate knowledge about insects has limited people’s ability to effectively estimate the trend of growth in insect population. In the past it was believed that insects faced no serious threat of extension hence insects were generally perceived as an inexhaustible resource (Schabel, 2006). However, recent studies have alluded to looming factors that threaten the extinction of many insect species especially edible ones.

2.5 Edible insects as a natural resource

Insect ecology refers to the interplay between insects and their breeding and other activities within their habitat. This interaction transcends their feeding habits, migration, reproduction and other interaction with their immediate environment. In his work,

Boulidam (2010) referred to edible insects as non-wood forest products (NWFP) that are harvested from various locations. Insects survive in both aquatic and terrestrial ecosystems. Different species of insects feed on a variety of material ranging from vegetable foliage (common with caterpillars), the bark of trees (cicadas) as well as soil matter as in the case of dung beetles.

Insects offer critical ecosystem services including degradation of organic materials, pollination in plants as well as pest control (Losey and Vaughan, 2006). Among the insects noted to provide such essential ecosystem services are the weaver ants, dung beetles, honeybees and various predators and parasitoids which are credited for their

contribution to sustaining the ecosystem. Some of these insects are also a popular delicacy in most countries within the tropics.

2.6 Semi-cultivation of edible insects

Research has demonstrated that it is possible to simulate and influence the production of edible insect species and promote year-round availability of selected edible insect species through semi or full production. This process, referred to as semi-cultivation, enables the application of skills and labour to manage the cultivation of edible insects (Van

Itterbeeck and van Huis, 2012). The difference between semi-cultivation and actual cultivation lies in complete or partial avoidance of tending in the case of semi-cultivation.

Semi-cultivation therefore avoids captivity of insects but rather alters the natural habitat to increase population growth and ease harvesting. There are some few instances where edible insect species such as the palm weevil larvae are captured at any developmental stage and farmed using artificial (plastic containers) environments as in Venezuela

(Cerda et al., 2001) and now Ghana. Semi-cultivated insects are therefore not completely isolated from their natural environment and populations. Some of the semi-cultivated insects include the palm weevil larvae, the mealworn and the black soldier fly.

2.6.1 Semi-cultivation of palm weevil larvae

The semi-cultivation of different species of the palm weevil larvae is gaining popularity in Africa (R. phoenicis), South and Central America (R. palmarum) and in Southeast Asia

(R. ferrugineus). This has been made possible mainly due to the easy availability of palm

trees and the ability of people to fell them in various locations. The disposition of the palm weevil which allows for semi-domestication is a major factor that has enhanced the process of semi-cultivation. It makes semi-cultivation comparatively simplier as cultivators simply fell palm trees and after one to three months visit the felled tree to harvest the larvae from the tree trunks (Choo et al., 2009).

A fallow method of hunting which involves deserting a settlement for an extended period of time was used by some tribes in Bolivarian Republic of Venezuela to hunt palm weevils. Inhabitants vacated and resettled in new locations after felling palm trees to allow palm weevils (Bearded weevil (Rhinostomus barbirostris F.) and R. palmarum to oviposit in the trunks of the felled trees which are later harvested by the indigenes

(Dufour, 1987). There is a difference in the oviposition behaviour of the two species. The adult R. palmarum oviposits on the exposed inner tissue of felled palm trees while the adult R. barbirostris oviposits on the undamaged surface of the palm trunk, hence makes use of the entire trunk length to ovisipit. This knowledge is used by the indigenes to select the species they desire to produce on the felled tree by either exposing soft tissue

(for R. palmarum) or leaving the trunk intact. Moreover, due to the relatively early invasion of R. palmarum compared to R. barbirostris the technique allows cultivation of large populations of the preferred species.

2.6.2 Caterpillars

Conserving and increasing the population of caterpillars can be achieved through various strategies. However, van Huis et al. (2013) recommended fire management and shifting

cultivation as effective ways of maintaining habitat of caterpillars and increasing their population. Fire management helps to avoid the killing of vulnerable stages of the insects which unlike the adults can’t fly or quickly move to avoid danger. Shifting cultivation on the other hand helps farmers to cultivate crops which will mature early or later than the caterpillar season to avoid damage. Examples include the selective collection of young caterpillars of Endoxyla leucomochla Turner, Cirina butyrospermi Vuillot and Cirina forda Westwood from the field to trees close to the home so they can grow and then be harvested.

2.7 Domesticating edible insects: opportunities to the environment

Feeding a growing world population with more demanding consumers will necessarily require an increase in food production. This will inevitably place heavy pressure on the already limited resources such as land, oceans, fertilizers, water and energy. Livestock and fish are important sources of protein in most countries. The opportunity for insects to help meet rising demand for meat products and replace fishmeal and fish oil is enormous.

Large-scale livestock and fish production are economically viable because of their high productivity, at least in the short term. However, these activities incur huge environmental costs (Tilman et al., 2002).

Manure, for example, contaminates surface and groundwater with nutrients, toxins

(heavy metals) and pathogens (Tilman et al., 2002; Thorne, 2007). Any increase in animal production will, moreover, require additional feed and cropland and will likely trigger deforestation. The Amazon is a case in point: pasture now accounts for 70% of

previously forested land, with feed crops covering a large part of the remainder (Steinfeld et al., 2006).

2.8 Advantages of rearing edible insects

Firstly, edible insects have high feed-conversion efficiency (an animal’s capacity to convert feed mass into increased body mass, represented as kg of feed per kg of weight gain). Secondly, they can be reared on organic wastes thereby reducing environmental contamination, while adding value to waste. Thirdly, they emit relatively fewer green house gases (GHGs) and relatively little ammonia. They also require significantly less water than cattle rearing and have few animal welfare issues, although the extent to which insects experience pain is largely unknown. Finally, they pose low risk of transmitting zoonotic infections (van Huis et al., 2013).

However, replacing a part of conventional meat with edible insects implies an end to unlimited harvesting from nature, as this would reduce enormous pressure on wild populations. The production of edible insects would need to shift towards rearing either at the cottage-scale level or in large industrial units.

2.8.1 Feed conversion

As the demand for meat rises, so too is the need for grain and protein feed. This is because far more plant protein is needed for an equivalent amount of animal protein.

Pimentel and Pimentel (2003) calculated that for 1 kg of high-quality animal protein,

livestock are fed about 6 kg of plant protein. Feed-to-meat conversion rates vary widely depending on the class of the animal and the production practices used. Typically, 1 kg of live animal weight in a typical United States production system requires the following amount of feed: 2.5 kg for chicken, 5 kg for pork and 10 kg for beef (Smil, 2002). Insects require far less feed (van Huis et al., 2013, van Huis, 2015).

The production of 1 kg of live animal weight of crickets requires as little as 1.7 kg of feed

(Collavo et al., 2005). When these figures are adjusted for edible weight (usually the entire animal cannot be eaten), the advantage of eating insects becomes even greater (van

Huis et al., 2013). Nakagaki and DeFoliart (1991) estimated that up to 80% of a cricket is edible and digestible compared with 55% for chicken and pigs and 40% for cattle. This means that crickets are twice as efficient in converting feed to meat as chicken, at least four times more efficient than pigs, and 12 times more efficient than cattle (Figure 2.3).

Figure 2.3: Feed conversion efficiencies of crickets versus conventional meats.

2.8.2 Organic waste products

A benefit of insects as an alternative animal protein source is that they can be reared sustainably on organic waste products (e.g. manure, pig slurry and compost). The use of organic waste products in insects starts by rearing the insects on biowaste. The insects are processed and fed to a specific animal (Plate 2.1), the meat of which is then sold to the consumer (Veldkamp et al., 2007).

Insect species such as the black soldier fly (Hermetica illucens), the common house fly

(Musca domestica) and the yellow mealworm (Tenebrio molitor) are very efficient at bioconverting organic waste. For this reason, these species are receiving increasing

attention, as they could collectively convert 1.3 billion tonnes of biowaste per year

(Veldkamp et al., 2007). Other insect species, such as crickets, are raised on insect farms on high-quality feed such as chicken feed. Substituting such feed with organic waste products can help to make insect farming more profitable (Offenberg and Wiwatwitaya,

2009a, 2009b). However, at present this is not permitted because of food and feed legislation.

a. Adult house fly b. Maggots c. Feed from maggots d. Feed for poultry

Plate 2.1: Illustration of insect use in the animal feed chain

Recycling agricultural and forestry wastes into feed greatly reduces organic pollution.

According to DeFoliart (1989), “Practically every substance of organic origin, including cellulose, is fed upon by one or more species of insects, so it is only a matter of time before successful recycling systems was developed”. The possibility of rearing insects on organic waste for human consumption is still being explored, given the unknown risks of pathogens and contaminants.

2.8.3 Greenhouse gas (GHG) and ammonia emissions

Livestock rearing is responsible for 18% of GHG emissions (CO2 equivalent), a higher share than the transport sector (Steinfeld et al., 2006). Methane (CH4) and nitrous oxide

(N2O) have greater global warming potential (GWP) than CO2: if CO2 has a value of 1

GWP, CH4 has a GWP of 23 and N2O has a GWP of 289 (IACUC, 2007).

Among insect species, only cockroaches, termites and scarab beetles produce CH4

(Hackstein and Stumm, 1994), which originates from bacterial fermentation by action of

Methanobacteriaceae in the hindgut (Egert et al., 2003). Insects deemed viable for human consumption in the Western world include species such as mealworm larvae, crickets and locusts, which produce lower GHG emissions than pigs and beef cattle (they are lower by a factor of about 100) (Oonincx et al., 2010) (Figures 2.4a and 2.4b).

Figure 2.4a: GHG’s emission of three insect species versus pig and beef cattle (Source: Oonincx et al., 2010).

Figure 2.4b: Ammonia emission of three insect species versus pig and beef cattle (Source: Oonincx et al., 2010)

Livestock wastes (urine and faeces) also contribute to environmental pollution (e.g. ammonia) that can lead to nitrification and soil acidification (Aarnink et al., 1995).

2.8.4 Nutritional value of insects for human consumption

The nutritional content of various edible insect species vary. This variation exists even within the same family of insect species. The variation is influenced by the metamorphic stage and the diet and habitat of the insects. Variation due to the metamorphic stage is more pronounced among insects with complete metamorphosis (referred to as holometabolous species) such as moths and butterflies, bees, ants and beetles (van Huis et al., 2013). Similar to most foods, the process and method of preparation such as boiling, drying or frying also affect the nutritional content of edible insects.

Generally, insects have been found to contain substantial amounts of nutrients vital for the human body, especially protein and amino acids. A study on 236 edible insect species identified satisfactory levels of essential macronutrients (protein, amino acid) and micronutrients (including iron, manganese, phosphorous, copper, riboflavin, magnesium) in most of the insects despite some variations (Rumpold and Schlüter, 2013). The energy content of various insect species at different processed stages varies.

In a study, FAO (2012b) identified as high as 1,272 kcal/100 g in the raw green ant

(Oecophylla smaragdina F.) to a low of 89 kcal/100 g in a raw grasshopper

(Cyrtacanthacris tatarica L.) (Table 2.4).

Like the energy content of various insect species, the protein content of insects varies based on certain factors. The processed state such as dry-roasted and dried have been found to affect the protein content of edible insects. The protein content of the mopane caterpillar was found to be lower when dried-roasted (48%) than that simply dried (57%).

Significant variations were also observed in the termite when raw (20%), fried (32%) and smoked (37%) (Bukkens, 2005). This was attributed to the varied water content.

Xiaoming et al. (2010) also observed varying protein content among 100 insect species

(Table 2.5).

Table 2.4: Energy content of various insect species from various parts of the world.

Energy content (kcal/100g fresh Location Common name Scientific name weight) Australian plague locust, Chortoicetes terminifera Australia raw Walker 499 Oecophy smaragdina Australia Green (Weaver) ant, raw Fabricius 1272 Canada, Red-legged grasshopper, Melanoplus Quebec whole, raw femurrubrum DeGeer 160 USA, Yellow mealwom, adult, Illinois raw Tenebrio molitor L. 206 USA, Yellow mealworm, adult, Illinois raw Tenebrio molitor L. 138 Termite, adult, dewinged, Macrotermes Ivory Coast dried, flour subhyallnus Rambur 535 Mexico, Veracruz Leaf-cutter ant, adult, raw Atta Mexicana Smith 404 Mexico, Myrmecocystus melliger Hidalgo Honey ant, adult, raw Forel 116 Gryllus bimaculatus de Thailand Field cricket, raw Geer 120 Lethocerus indicus Lep. Thailand Giant water bug, raw and Serv. 165 Oxya japonica Thailand Rice grasshopper, raw Willemse 149 Cyrtacanthacris Thailand Grasshopper, raw tatarica L. 89 Domesticated silkworm, Thailand pupa, raw Bombyx mori L. 94 The Netherlands Migratory locust, adult, raw Locusta migratoria L. 179

Source: FAO, 2012b.

Table 2.5: Crude protein content of selected insect species by order.

Insect Order Stage Per cent Protein

Coleoptera Adults and larvae 23 – 66

Lepidoptera Pupae and larvae 14 – 68

Hemiptera Adults and larvae 42 - 74

Homoptera Adults, larvae and eggs 45 -57

Hymenoptera Adults, pupae, larvae and eggs 13 – 77

Odonata Adults and naiads 46 – 65

Orthoptera Adults and nymphs 23 – 65

Source: Xiaoming et al., 2010

The amount of protein is also influenced by the feed such as grains and vegetables consumed by the insects. In Nigeria, grasshoppers fed on bran contained about twice as much protein as those fed on maize (Ademolu et al., 2010). Ademolu et al., (2010) also reported that the protein content of insects varied according to their metamorphic stage.

Adult Zonocerus variegatus contains more protein content than its instars (Table 2.6).

However, estimates on the significance of insect protein in traditional diets on a global scale, is not well documented due to the limited availability and disaggregated nature of such studies. Nonetheless, the few available evidence provides a fair impression of the essence of edible insects in traditional diets. This makes a case for more attention to be focused on developing the edible insect sector.

Table 2.6: Protein content variation at various metamorphosis stages of the raw variegated grasshopper (Zonocerus variegatus L.), Ogun State, Nigeria.

Insect instar stage Weight of protein/100 g fresh weight

First 18.3

Second 14.4

Third 16.8

Fourth 15.5

Fifth 14.6

Sixth 16.1

Adult 21.4

Source: Ademolu et al., 2010

Amino acids are essential nutrients needed for human health. These nutrients are however often limited in protein sources such as cereals which are common staple foods the world over. There have been reported cases of amino acid (tryptophan and lysine) deficiencies in countries such as Kenya, Angola, Zimbabwe and Nigeria, where maize is a common staple food (van Huis et al., 2013). Cereals such as maize mostly have limited lysine, tryptophan and threonine which can be found in sufficient quantities in some edible insects. The larvae of insects such as the palm weevil, Saturniidae family of caterpillars and some aquatic insects have been recommended as a good protein supplement

(Bukkens, 2005). These insects contain about 100 mg of amino acid (lysine) per 100 g crude protein (van Huis et al., 2013).

Edible insects are a great source of fat including polyunsaturated fatty acids as well as linoleic and α-linolenic acids. These fatty acids which are a very rich source of energy are essential for healthy development in infants and children (Michaelsen and Chamnan

2010). Edible insects such as the witchetty grub of Australia contain substantial amount of fat (38% of dry weight) including oleic acid that is an omega-9 mono-unsaturated fatty acid (Naughton et al., 1986) (Table 2.7). Bukkens (2005) suggested that the fat composition of insects is influenced by the plants on which the insects feed.

Table 2.7: Fat content and major fatty acids in edible insects consumed in Cameroon.

Fat Main fatty acids (% of oil SFA, MUFA Edible insect species content content) or PUFA African palm weevil Palmitoeic acid (38%) MUFA 54% (Rhynchophorus phoenicis) Linoleic acid (45%) PUFA Palmitoleic acid (28%) MUFA Edible grasshopper (Ruspolia Linoleic acid (46%) PUFA differens) 67% α-Linolenic acid (16%) PUFA Palmitoleic acid (24%) MUFA Oleic acid (11%) MUFA Variegated grasshopper 9% Linoleic acid (21%) PUFA (Zonocerus variegatus) α-Linolenic acid (15%) PUFA γ-Linolenic acid (23%) PUFA Palmitic acid (30%) SFA

Termites (Macrotermes sp.) Oleic acid (48%) MUFA 49% Stearic acid (9%) SFA Palmitic acid (8%) SFA Saturniid caterpillar Oleic acid (9%) MUFA 24% (Imbrasia sp.) Linoleic acid (7%) PUFA α-Linolenic acid (38%) PUFA

Note: SFA = saturated fatty acids; MUFA and PUFA = mono and poly unsaturated fatty acids. Source: Womeni et al., 2010.

On this backdrop, researchers have suggested the need to harvest insect fat to complement access to vital fats (such as omega-3 and omega-6 fatty acids) which have been reported as becoming deficient among children (van Huis et al., 2013). It could even be more helpful in developing countries where the populace have limited access to fish as part of the diet (Roos et al., 2011).

Micronutrients such as minerals and vitamins play a vital role in the nutritional value of food. Micronutrient deficiencies can lead to major adverse health consequences including impairments in growth, physical and mental development, immune function, and reproductive outcomes which in some cases are irreversible through nutrition interventions (FAO, 2011c). Minerals play vital roles in many biological processes. Zinc deficiency is an additional public health issue, particularly for children and mothers. Zinc deficiencies can impede growth, delay sexual and bone maturation, cause alopecia and diarrhoea, impair appetite, skin lesions and increase vulnerability to infections mediated by defects in the immune system (FAO, 2011b). Generally, insects are good sources of zinc. Beef contains an average of 12.5 mg per 100 g of dry weight, whereas the palm weevil larvae (R. phoenicis) contain more than twice (26.5 mg per 100 g) that quantity

(Bukkens, 2005).

2.9 Insects as animal feed

Presently, around 10% of global fish production goes to fishmeal (i.e. either whole fish or fish remains resulting from processing) and is used mainly in aquaculture (FAO, 2012a).

South America is the biggest producer of fishmeal, through its catch of anchoveta (van

Huis et al., 2013). Anchoveta catch is highly variable because it is dependent on the El

Niño climatic cycle. Production peaked at 12.5 million tonnes in 1994 but declined to 4.2 million tonnes in 2010 and is expected to fall further (FAO, 2012a). Calvert et al. (1971) suggested the use of maggots as a replacement for some key ingredients in feeds and this was further echoed by Teotia and Miller (1974). Termites have reportedly been used as feed for chickens and guinea fowl in Togo, Burkina Faso (Farina et al., 1991, van Huis, et al., 2013) and northern Ghana. It is against this background that there is the need to identify major edible insects in Ghana and investigate their potential as human food and source of protein for the poultry industry, hence this work.

CHAPTER THREE

IDENTIFICATION AND CLASSIFICATION OF COMMON EDIBLE INSECTS

AND FACTORS AFFECTING ENTOMOPHAGY IN GHANA

3.1 INTRODUCTION

This study sought to determine which insects are neglected and underutilised in Ghana so as to assist in developing programmes for their full utlization as food and feed for humans and livestock.

Developing societies are faced with protein and other nutritional deficiencies especially during times of social unrest and natural disasters. Due to their high fecundity, ease of access, nutritional composition and simple rearing techniques, insects offer a cheap and sustainable opportunity to curtail malnutrition by providing emergency food and improving livelihoods of the vulnerable in society (van Huis et al., 2013).

Edible insects form a vital part of the diet of various ethnic groups especially at the beginning of the farming season. These insects are used in various dishes as well as for medicinal purposes. This illustrates that entomophagy evolved with the evolution of the human species.

The larvae of the palm weevil (Known as ‘Akokono’ among the Akans of Ghana) is portrayed as a vital delicacy during story-telling and it is used for special dishes on important occasions and consumed by royals including Ashanti kings. Insects are consumed at various developmental stages; from larval through to the adult stages.

Little information is available from secondary sources pertaining to the types of edible insects available in the various regions of Ghana. There is also no published work in

Ghana providing an empirical delineation of the various edible insect species consumed by the various ethnic groups in Ghana. It is therefore of necessity to determine and classify existing edible insects in Ghana to promote their utilisation in the diets of

Ghanaians. Knowledge of the frequency, composition, location and diversity of the different edible insect species in Ghana will help entomologists as well as consumers appreciate the kind of edible insects in the country. It will also help consumers know the seasonality and location of each species. This will go a long way to put Ghana on the map of entomophagical countries. Furthermore, as entomophagy is influenced by various factors which may be location specific, it is important to determine the factors that influence entomophagy in Ghana. Additionaly, it is necessary to geographically delineate using maps and other illustrations the location and the extent to which various edible insect species are utilised as food and feed in Ghana.

3.2 MATERIALS AND METHODS

A survey using direct observations, questionnaire administration, key informant interviews and insect collection was conducted throughout the ten regions of Ghana from

June to November, 2014 to obtain primary data. Approval was sought from the interviewees (participants) after which a consent form was signed by each participant.

3.2.1. Sampling sites and sample size

To ensure validity and fair representation of responses, various probability sampling methods were adopted and applied in choosing and administering the predesigned questionnaires to respondents. Multi-stage sampling was adopted in selecting respondents for the field survey. Initially, the ten geographic regions of Ghana were used as clusters which were further divided into sub-clusters (Districts and Metropolitan Assemblies).

The 216 administrative districts of Ghana were categorised into urban and rural districts.

Two districts (one rural and one urban) were selected from each region from which inhabitants were randomly selected and interviewed. At the district level, an urban and a rural community were selected and simple random sampling used to select respondents for the interview (Table 3.1). The 200 questionnaires allocated to each region were prorated and administered based on the population of the selected communities.

Table 3.1: Regional, communal and gender distribution of respondents in the survey.

Urban Rural No. of males No. of females Region community community interviewed interviewed

Ashanti Kumasi Doyina 120 80

Brong-Ahafo Kintampo Jema 114 86

Central Cape coast Kakum 110 90

Eastern Koforidua Kade 110 90

Greater Accra Adenta Chorkor 110 90

Northern Tamale Sagnarigu 110 90

Upper East Navrongo Chaina 110 90

Upper West Wa Yaala 110 90

Volta Ho Klefe 110 90

Western Secondi Nzulezu 110 90

TOTAL 1114 886

Two thousand respondents were interviewed throughout the country, based on calculations made using national population figures from the 2010 population and housing census. The sample size calculation was done using the Sloven formular shown in Section 3.2.2.

3.2.2 Sample size calculation:

Sampling frame (persons 18 years and above) = 13,632,299

푁 Adopted formula: 푛 = 1+푁(a2)

Where; n = sampling size, N = sampling frame, 1 = constant, a = margin of error

Source: Sloven (1960).

푁 Sample size: 푛 = 1+푁(a2)

N = 13,632,299 a = 0.023

13,632,299 = 2,000 Respondents 1+13,632,299 (0.0232)

3.2.3. Sources of data collected

As the first of its kind in the country, very little or no information was available from secondary sources pertaining to the types of edible insects available in the various regions of Ghana. Primary data were obtained from the field survey using four techniques namely key informant interviews, questionnaire administration, direct observations and insect collection.

3.2.3.1 Key informant interviews: Key informants provided vital insights on the various areas that edible insects could be found in the field. Key informants were mainly opinion leaders and elderly indigenes who had stayed in the target communities for very long periods (over 30 years). Ten key informants were selected in each district using purposive sampling.

3.2.3.2 Questionnaire administration: Structured questionnaires were used to obtain information on edible insects in all the ten regions of Ghana. A common set of pre-tested questionnaires with open and close ended questions were administered to respondents.

This was done using one-on-one interviews conducted by trained enumerators from the local communities. The enumerators translated the questions into the local dialect to enhance understanding of respondents. Pictures and real samples of various edible insects identified from literature were also used to help respondents identify the insects mentioned. Space was also provided for the participants to include names of more insects. To enhance the depth of information solicited, enumerators probed further for clarification on some responses and the interviewees were asked for explanation on issues such as why some insects were no longer consumed.

Major questions in the questionnaire were the gender, age, educational level, occupation of the participants, the availability and consumption of insects in the localities. Other questions were: the metamorphic stages consumed, sources of the insects, main consumers in terms of age group, purpose/reasons for consumption, other uses of the insects (i.e feed for animals and which insects are used), seasonality of insects,

processing methods, preferred form of eating (main meal, snack, dessert), dishes prepared from insects, challenges faced in hunting/eating insects, health risks if any and finally, why some people have stopped eating insects. In all, 24 questions were asked each participant (see questionnaire in Appendix 2).

3.2.3.3 Direct observations: In the field, direct observations of the activities of the available insects in the various localities were recorded. Where appropriate, some key informants assisted to observe available edible insects and their habitats. Pictures were taken to verify and support the results of responses obtained from the responders in various communities. In some cases, how some edible insects were prepared and consumed locally was observed.

3.2.4 Insect collection, identification and classification

Samples of edible insects were collected as part of the survey conducted from June to

November, 2014, by which time most edible insects were in season. The insects collected were stored in 70% alcohol and taken to the laboratory for identification.

A mix of primary data and taxonomical characters were used in identifying and classifying the various edible insect species of Ghana. Taxonomic characters were mainly from archival sources and published literature. Classification was achieved by comparing the sampled insects with archived samples at the African Regional Post-graduate

Programme in Insect Science (ARPPIS) laboratory of the University of Ghana, Accra,

Ghana and the entomology laboratory of the Kwame Nkrumah University of Science and

Technology, Kumasi, Ghana. Davis Henry Davis, an experienced taxonomist at ARPPIS

Centre assisted in the identification of all the insects collected in this survey.

3.2.5 Preparation of geographical map

Using the data gathered from the field, the Arch GIS software was used to design an entomophagical map based on five of the six ecological zones (Rain forest, Coastal savannah, Semi-deciduous forest, Transition zone, Guinea Savannah and Sudan

Savannah) of Ghana. The Sudan Savannah and the Guinea Savannah were put together as one due to the fact that they shared identical characteristics. The location of individual edible insect species on the map was based on respondent reports and direct observations made during the survey. In preparing the geographical map, the various insect species identified to be consumed in each community were grouped into traditional and non- traditional insects. Edible insects which were not traditional to a given ecological zone were not placed in that zone even though such insects may be consumed by some people in the area. The rationale was to showcase the insect species that are part of the traditional food system of the indigenes of the various zones.

3.3 DATA ANALYSIS

The completed questionnaires were cleaned and some information verified. The responses were then entered into a pre-coded SPSS template. Data were analysed using

SPSS (20) and Microsoft Excel. A combination of Chi square test (to measure statistical significance between variables such as locations, gender and age and entomophagy) and

Cramer's V (φc) statistic (to measure the strength of association between two nominal variables) (Cramér, 1946) were used to illustrate the correlation between insect consumption and the selected variables. Table 3.2 interprets the values of the level of

Association:

Table 3.2: Interpretation of the values of the level of association Level of Verbal Remarks Association Description Knowing the independent variable does not help in 0.0 No Relationship predicting the dependent variable.

0.00 to 0.15 Very Weak Not generally acceptable

0.15 to 0.20 Weak Minimally acceptable

0.20 to 0.25 Moderate Acceptable Moderately 0.25 to 0.30 Strong Desirable

0.30 to 0.35 Strong Very desirable

0.35 to 0.40 Very Strong Extremely desirable Worrisomely Either an extremely good relationship or the two 0.40 to 0.50 Strong variables are measuring the same concept The two variables are probably measuring the same 0.50 to 0.99 Redundant concept. Perfect If we know the independent variable, we can perfectly 1.00 Relationship. predict the dependent variable.

3.4 RESULTS

3.4.1 Socio-economic background of respondents

The ages of respondents ranged from 18 to 60 years (median age of 34 years) with 55.7% of them being males. About 30.9% of the respondents fell between 18-25 years of age whiles 4.8% represented people 60 years and above (Table 3.3). Although a significant proportion (84.25%) of the respondents was educated, there was an inverse relation between age and formal education level among the respondents. There was male (58%) dominance among the number of respondents who schooled up to the secondary (55%) and tertiary (59%) levels.

Table 3.3: Bio-data of respondents

Characteristics of Respondents Gender of Respondent Total Male Female Freq. % Freq. % Freq. % 18 – 25 329 29.5 288 32.5 617 30.9 26 – 30 248 22.3 192 21.7 440 22.0 Age 31 – 40 238 21.4 201 22.7 439 22.0 41 – 50 161 14.5 129 14.6 290 14.4 51 – 60 68 6.0 50 5.6 118 5.9 60+ 70 6.3 26 2.9 96 4.8 Total 1114 100.0 886 100.0 2000 100.0 Farmer 310 27.8 193 21.8 503 25.2 Gov’t/Salaried worker 358 32.1 243 27.3 601 30.0 Occupation Trader/Artisan 366 32.9 385 43.5 751 37.6 Other Occupation 15 1.4 6 0.7 21 1.0 Students 65 5.8 59 6.7 124 6.2 Total 1114 100.0 886 100.0 2000 100.0 No formal education 183 16.5 132 14.9 315 15.8 Basic 269 24.1 269 30.4 538 26.9 Level of Schooling Secondary/Technical 255 22.9 207 23.3 462 23.0 Tertiary 407 36.5 278 31.4 685 34.3 Total 1114 100.0 886 100.0 2000 100.0

Gov’t = Government

3.4.2 Taxonomic classification of the edible insects in Ghana

A total of nine species of major edible insects belonging to four orders were identified in the nationwide survey (Table 3.4). Plates 3.1a to 3.1i show pictures of the nine edible insects in Ghana.

Table 3.4: Major edible insects in Ghana

English Local name/Common Scientific name in Stage Order Family name name Ghana consumed Akokono Palm weevil Rhyncophorus in Akan/ Larvae & Curculionidae (larva) phoenicis Gbamedo Adults Coleoptera (Fabricius) in Ewe Phyllophaga Chibio Scarab beetle Scarabaeidae nebulosa nabra in Larvae (larva) (Harris) Kasem Night ‘butterfly’ Cirina Kantuli in Lepidoptera Saturniidae Larvae (caterpillar) butyrospermi Frafra and

(Vuillot) Dagaari Locusta Acrididae Locust migratoria Vetsuvi Adults (Linnaeus) (Ewe) Manchogo Zonocerus in Kasem Pyrgomorphidae Grasshopper Adults variegatus Abébé in (Linnaeus) Akan Orthoptera Acheta Gryllidae House cricket domesticus Chari in Adults (Linnaeus) Kasem Gryllus Paan-ta- Gryllidae Field cricket similis kyiiraa in Adults (Chapman) Dagaari Scapteriscus Gryllotalpidae Ground cricket vicinus Tiga chari Adults/Nymphs (Scudder) in Kasem Macrotermes Isoptera Termitidae Termite bellicosus Kwena in Adults (Smeathman) Kasem

Plate 3.1a: Phyllophaga nebulosa Plate 3.1b: Cirina butyrospermi

Plate 3.1c: Zonocerus variegatus Plate 3.1d: Scapteriscus vicinus

Plate 3.1e: Rhyncophorus phoenicis Plate 3.1f: Locusta migratoria

Plate 3.1g: Acheta domesticus Plate 3.1h: Macrotermes bellicosus

Plate 3.1i: Gryllus similis

3.4.3 Seasonality of edible insects

The scarab beetle larva is mostly harvested at the onset of the rains (May to July) in cow dung, compost and/or decomposing organic substrates. This insect is consumed among the Dagaartis, Sissalas and Walas in the Upper West Region and the Frafras in the Upper

East Region. Some Dagombas and Bimobas in the Northern Region of Ghana also consume it. With the exception of the palm weevil larva, all the other edible insects are only available from April/May (the onset of the rainy season) till the end of the year.

The Macrotermes bellicosus for instance is available for harvesting only in June and July

(Table 3.5).

The shea tree caterpillar is available in only the three Northern regions of Ghana where the shea tree (Vitellaria paradoxa Gaertn, formerly Butyrospemum parkii) thrives. The caterpillar is consumed by the Dagaartis, Sissalas, and Walas in the Upper West Region, the Frafras, Kasena/Nankana, Moshies and Kusasis in the Upper East Region and the

Dagombas, Bimobas, Gonjas and Mamprusis in the Northern region.

The palm weevil larva is consumed by the Akans in the Central, Western, Eastern and the

Ashanti Regions as well as the Ewes, Gas and Bonos in the Volta, Greater Accra and

Brong-Ahafo regions, respectively. The palm weevil larva is available all-year-round in all palm growing communities but it is most abundant from May to October – the main rainy season.

Table 3.5: Seasonality of the major edible insects in Ghana.

Insect Months of the year

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Palm weevil larva

Scarab beetle larva

Shea tree caterpillar

Locust

Grasshopper

House cricket

Ground cricket

Termite

Field cricket

3.4.4 Consumption of edible insects in Ghana

In Ghana, the nine edible insects were found to be consumed by at least 30% of the respondents in the survey. The termite (94.7%) was the most available insect while the shea tree caterpillar was the least available with 37% (Figure 3.1). In terms of consumption, the palm weevil larva with 47.2% was the most consumed insect followed by the termite (45.9%), ground cricket (33.3%), grasshopper (30.5%), locust (10%), house cricket (9.5%), shea tree caterpillar (8.7%), field cricket (5%) and the least consumed being the scarab beetle larva (2%) (Figure 3.1).

100 94.7 89.4 89.8 90 75.2 78.4 80 66 67.2 70 55 60 45.9 47.2 50 37 40 30.5 33.3 30 20 8.7 9.5 5 10 10 2

0 % Availability/Consumption %

Insect species

Availability (%) Consumption (%)

Figure 3.1: Availability and Human Consumption of Insects as Food in Ghana

With regards to insects as feed for animals, respondents were asked to identify insects that could be used as feed for animals. Four were identified; the Black Soldier Fly,

termites, ants and the house fly larvae. All of the respondents confirmed the availability of the ant and the house fly whilst 56.8% and 98% confirmed the availability of the Black

Soldier Fly and the termite, respectively. For their usage in feed, 91.3% of the respondents argued for the use of the house fly whilst 66.7%, 12.3% and 1.2%, responded positively for termites, ants and the Black Soldier Fly, respectively (Figure 3.2).

120

100 100 98 100 91.3

80 66.7

60 56.8

% Availability/Consumption % Availability (%) 20 12.3 1.2 Feed usage (%) 0 Black Soldier Ant House Fly Termite Fly Insect species

Figure 3.2: Availability and Use of Insects as Feed for Animals in Ghana

3.4.5 Developmental stages consumed and purposes of consuming edible insects

Tables 3.6a and 3.6b show the developmental stages of the edible insects as well as insects used as feed and means of acquiring them. The purpose and significance of insect consumption among various age and gender groups is shown in Figure 3.3. About 81.6% of the respondents consume insects as a source of protein, 9.6% for cultural reasons,

5.6% for medicinal values and 3.0% and 0.2%, respectively for recreational and religious

reasons (Figure 3.3).

Table 3.6a: Developmental stages of identified insects consumed by humans and means of acquiring them.

Insect Development Stage(s) Means of Acquiring Insect Harvest Uses Consumed Period Egg Larva Pupa Nymph/ Hunting/ Rearing Buying Adult Trapping Scarab Beetle Food larvae × √ × × √ × × Rainy season / Feed Food Termite × × × √ √ × √ Rainy season / Feed Rainy season/ early part of Field cricket × × × √ √ × × dry season Food Shea tree caterpillar × √ × × √ × √ Rainy season Food Rainy season/ early part of Food Grasshopper × × × √ √ × √ dry season / Feed Palm weevil larva × √ × √ √ √ √ Year-round Food House Food cricket × × × √ √ × × Year-round / Feed Ground Food cricket × × × √ √ × × Rainy season / Feed Food Locust × × × √ √ × × Rain season / Feed

Legend: × = No, √ = Yes.

Table 3.6b: Developmental stage of identified insects used as animal feed and means of acquiring them.

Insect Development Stage Utilised Means of Acquiring Insect Nymph/ Hunting/ Harvest Egg Larva Pupa Adult Trapping Rearing Buying Period Uses Black Year- Soldier fly × √ × √ √ √ × round Feed Year- House fly × √ × √ √ × × round Feed Rainy Food / Termite × × × √ √ × × season Feed Year- Cockroach × × × √ √ × × round Feed

Legend: × = No, √ = Yes.

0.2% 5.6% 3%

Source of protein 9.6%

Cultural practice

Religious reasons

Recreational purpose

Medicinal value

81.6%

Figure 3.3: Percentage distribution of reasons for eating insects in Ghana

3.4.6 Factors that influence the practice of entomophagy in Ghana

The study revealed a significant difference between gender and entomophagy and highly significant differences between locality, level of schooling, age and occupation and the practice of entomophagy. But the level of association was very weak/negligible (using the Cramer’s V statistic) (Table 3.7). More male respondents (83.2%) consumed insects than the female respondents (79.5%) (Table 3.8). In all, 81.6% of the respondents consumed insects whiles 18.4% did not (Table 3.8).

Table 3.7: Correlation between entomophagy and some selected variables Cramer's V Variable Chi-Square Value df Significance (φc) Locality (rural / urban) 44.04 1 0.001 0.148 Level of Education 32.90 3 0.001 0.128 Age 31.33 5 0.001 0.125 Occupation 30.36 4 0.001 0.123 Gender 4.62 1 0.031 0.048

Interpretation of Cramer’s V (φc) statistic results > 0.5 = High association 0.3 to 0.5 = Moderate association 0.1 to 0.3 = Low association 0 to 0.1 = Little association - if any

Source: Cramér (1946).

Table 3.8: Distribution of insect consumers by gender.

Gender of Respondents Consumption Male Female Total Status Frequency Percentage Frequency Percentage Frequency Percentage Consumers 927 83.2 704 79.5 1631 81.6 Non-consumers 187 16.8 182 18.5 369 18.4 Total 1114 100.0 886 100.0 2000 100.0

χ2 value = 4.62 df = 1 p < 0.05

In terms of age, 90%, 78% and 74% of the aged (60+), middle age (31-50) and the youth

(18-30), respectively were recorded to consume various edible insects (Table 3.9). There was a significant (p < 0.05) correlation between a person’s age and the propensity for consuming insects.

Table 3.9: Distribution of insect consumers by age

Consumption Status Age Group of Consumers Non-Consumers Total Respondents Frequency Percentage Frequency Percentage Frequency Percentage 18 – 25 532 32.6 85 23.4 617 30.9 26 – 30 350 21.5 90 24.4 440 22.0 31 – 40 326 19.9 113 30.6 439 21.9 41 – 50 237 14.5 53 14.4 290 14.5 51 – 60 99 6.1 19 5.2 118 5.9 60+ 87 5.3 9 2.4 96 4.8 Total 1631 100 369 100 2000 100.0

χ2value = 31.33 df = 5 p < 0.05

Eighty two per cent of the respondents with no formal education have ever consumed one or more edible insect species (Table 3.10). About 87% of respondents with tertiary education were found to have engaged in or still engage in entomophagy. There exists a significant correlation between level of schooling and entomophagy although the strength of relation (using Cramer’s V) was weak (0.128).

Table 3.10: Distribution of insect consumers by formal education.

Consumption Status Highest Level of Education Consumers Non-Consumers Total of Respondents Freq. % Freq. % Freq. % No formal Education 259 82 56 18 315 100 Basic Education 398 74 140 26 538 100 Secondary/Technical 380 82 82 18 462 100 Tertiary 594 87 91 13 685 100 Average 1631 82 369 18 2000 100

χ2value = 32.89 df = 3 p < 0.05

3.4.7 Insect consumption by locality in Ghana

Out of a total of 1631 respondents who practiced entomophagy, 63.5% of them were rural dwellers whilst urbanites represent 36.5%. The correlation between locality and practice of entomophagy was significant (p < 0.05) (Table 3.11). With reference to insects serving as a source of income for people, 44% of rural folk as against 32% of urban dwellers were of the view that insects had the potential to serve as a source of income. Overall,

39.8% of the respondents were optimistic about the potential of edible insects serving as a sustainable livelihood to generate income to support households (Table 3.12).

Table 3.11: Distribution of respondents on insect consumption by locality in Ghana.

Status of Insect Consumption YES NO TOTAL Community Frequency Percentage Frequency Percentage Frequency Percentage Rural 1035 63.5 165 44.7 1200 60.0 Urban 596 36.5 204 55.3 800 40.0 TOTAL 1631 100.0 369 100.0 2000 100

χ2value = 3.84 df = 1 p < 0.05

Table 3.12: Respondents’ View on Insects Serving as a Source of Income in Ghana.

Edible Insects as Source of Income YES NO TOTAL Community Frequency Percentage Frequency Percentage Frequency Percentage Rural 508 71.8 648 60.6 1156 65.0 Urban 200 28.2 422 39.4 622 35.0 TOTAL 708 100.0 1070 100.0 1778 100.0

χ2value = 23.46 df = 1 p < 0.05

3.4.8 Zonal and seasonal variations in insect availability and consumption

There were some zonal and seasonal variations associated with the consumption of the various insect species identified in the forest and savannah zones. The geographical map

(Figure 3.4) depicts the localities (based on ecological zones) where the identified insects were traditionally consumed. A chi-square test showed that the correlation between availability and consumption of the various entomophagical insect species was significantly different.

Figure 3.4: Species of insects consumed in the various ecological zones of Ghana

3.4.9 Acquiring edible insects

Entomophagy in all the ten regions was affected by the difficulty hunters and consumers go through in acquiring the insects (Table 3.13). Over 87% of the respondents who consume edible insects reportedly acquire them through hunting/trapping. On the

average, people travelled 10.5 kilometres to hunt/trap insects (Table 3.14). A significant proportion of respondents (12%) also reportedly buy insects from the market. About

39.8% of the respondents confirmed high demand for edible insects and indicated prospects of trading in edible insects as a means of income generation (Table 3.12). The study revealed that 39% of respondents see the price of insects as low whiles 58% thought it is moderate (Figure 3.5).

Table 3.13: Distribution of respondents on difficulty of hunting insects

Response Frequency Percentage Difficult 785 39.2 Not Difficult 809 40.5 Don’t know 406 20.3

Total 1594 100.0

Table 3.14: Distance travelled in hunting/trapping edible insects

Distance Travelled (km) Location of Harvest Insect 0.1-5 6-10 11-15 16-20 Farm Forest Home Scarab beetle larva 20 5 0 0 8 17 10 Termite 20 11 2 1 105 429 204 Field cricket 5 21 1 0 39 98 83 Shea tree caterpillar 25 32 0 0 29 202 49 Grasshopper 15 4 2 0 41 345 131 Palm weevil larvae 38 18 3 0 165 214 366 House cricket 12 3 1 0 74 349 152 Field cricket 15 5 0 0 10 242 59 Locust 8 4 2 1 28 248 77

39% Low Moderate Expensive

58%

Figure 3.5: Consumers' perception about the price of insects

About 41% of the respondents indicated that trapping the insects was not difficult (Table

3.13). Table 3.14 shows the distance harvesters travelled in search of insects.

About 4.5% of the respondents attributed their reluctance to consume insects to some possible health risks while about 11% of the respondents did not know whether or not edible insects had any adverse health implications for consumers (Table 3.15). The purposes for rearing/harvesting insects in the various regions of Ghana are presented in

Table 3.16. The results show that the major reason for rearing/harvesting insects in all the ten regions of Ghana is for their protein (1406 respondents). This is followed by cultural practices (166), medicinal value (96), recreational purposes (52) and the least beign for religious reasons.

Table 3.15: Response on health risk posed by eating insects.

Response Frequency Percentage Yes 90 4.5 No 1694 84.7 Don’t know 216 10.8

Total 2000 100.0

Table 3.16: Purposes for rearing/harvesting insects in the various regions of Ghana.

Purpose for Rearing/Harvesting Insects Source of Cultural Religious Recreational Medicina Region protein practice reasons purpose l value Total Ashanti 90 20 0 2 7 200 Brong Ahafo 86 5 1 2 7 197 Central 146 23 0 7 22 200 Eastern 117 43 0 25 12 197 Greater Accra 127 36 0 4 16 197 Northern 168 14 2 6 4 200 Upper East 176 5 0 2 10 200 Upper West 189 0 0 1 10 200 Volta 163 4 0 2 3 191 Western 146 20 0 4 9 200

Total 1406 166 3 52 96 1982

Respondents who believed that insects have adverse health implications for consumers constituted a small minority. Response from some respondents concerning the health risks and reasons for their reluctance to consume insects further confirmed that there was limited knowledge about edible insects; resulting in some people wrongly attributing some illnesses such as Malaria to the consumption of edible insects.

3.5 DISCUSSION

3.5.1 Socio-economic background of respondents

The traditional food system of every ethnic group is established based on certain social, economic and environmental factors (Sobal and Bisogni, 2009). Education, gender and age have been noted to have a significant influence on a person’s choice of food.

Overtime, these variables contribute to the alteration of the traditional food systems of a society. Educated people usually travel more and are open to trying other experiences and probably be in a position to spend more money on insects. A higher proportion of the female respondents (86%) were found to have formal education than their male counterparts. Higher level of education is mostly associated with better economic and psychological control (Lareau, 2003).

Overall, majority of the people who participated in the study were employed. Most of them were engaged in informal occupations such as farming and trading. Farming and trading offer them the opportunity to do additional, but less labour-intensive jobs, to earn extra income. Families with higher and expendable income can accumulate wealth and focus on meeting immediate needs (Boushey and Weller, 2005).

3.5.2 Taxonomic classification, seasonality and consumption of edible insects in

Ghana

The nationwide survey identified nine major edible insects in Ghana. Orthopterans dominate the edible insects with five species belonging to four families, Coleopterans are

two whiles Isoptera and Lepidoptera have only one species each. This deviates from the report by van Huis et al. (2013) that coleopterans were the world’s most commonly consumed group of insects, accounting for 31%. This also differs from the results of other surveys conducted across Africa by the International Center for Insect Physiology and

Ecology (ICIPE) in Kenya, which indicated Lepidopterans (caterpillars) as the most commonly consumed group of insects (Kelemu et al., 2015). Our survey results, however, are similar to those recorded by Ramos-Elorduy (1997) who also recorded a greater numbers of edible orthopterans in Africa.

In similar studies in Southern Africa, for instance, Obopile and Seeletso (2013) identified

27 edible insects in Botswana while Mallaisse (1997) found 38 edible insects in Zambia,

Zimbabwe and the Democratic Republic of Congo; mainly among the Bemba speaking people. According to Takeda (1990), 21 species of insects are consumed by the Ngandu people of the DR Congo whiles Roulon-Doko (1998) documented 96 different insect species among the indigenous Gbaya people of Central Africa (Kelemu et al., 2015). Van

Huis (2005) reported 250 edible insects across Africa. In a current study by ICIPE, 470 edible insects were identified across Africa (Kelemu et al. 2015). In that same survey, whiles Central and Southern Africa were leading with 256 and 164 edible insect species, respectively, West Africa recorded a low 91 species. The ICIPE survey recorded seven edible insects in Ghana whiles Jongema (2015) identified only five.

The field survey revealed that insects formed part of the traditional diet of all ethnic groups throughout Ghana. Insect consumption is not dependent on only taste and

nutritional value, but also on customs, ethnic preference and prohibitions (van Huis,

2003a).

The queen, soldiers and the reproductive forms of termites are eaten. Roasted/fried termites can be purchased in season in any town in northern Ghana; most notably are

Navrongo, Sirigu, Chaina and Sandema in the Upper East region and Wa, Nandom and

Tumu in the Upper West region. Roasted/fried termites contain 32-36% protein (Nkouka,

1987). The grasshopper and the house cricket can also be caught in this manner or harvested early in the morning when they are less mobile due to their low body temperature (van Huis, 2003a). Other minor edible insects were identified to be consumed in some communities but many of these are no longer consumed due to scarcity and the cheap sources of other meat products. These include dragonflies, the giant water bug, Lethocerus indicus (Lep. and Serv.) and cockroaches (Periplaneta australasiae F.); which were reported by a few people. The cockroach was mainly used for medicinal purposes. However, the consumption of the stinking blattid cockroaches is reported in Cameroon (Bergier, 1947) and in China. Whereas honey from bees and termites are consumed in all the ten regions of Ghana, the palm weevil larva is consumed mainly in the middle belt and Southern Ghana; where the palm tree thrives. The other insects are consumed mainly in the northern part of Ghana. Termites, field crickets, ground crickets, house crickets, grasshoppers and locusts are consumed by almost all tribes in Ghana.

Although nine edible insects were identified in the survey, it was only one species, the palm weevil larva that was being semi-reared for food. It involved artificially inflicting

wounds/cuts on felled palm trees for the adult female palm weevil to lay eggs which hatch into larvae that grow into market-size of about 6-10 g within 3 or 4 weeks. Aspire

Food Group Ghana has also introduced palm rearing kits in Ghana which are currently being used in rearing palm weevil larvae at homes in the Ashanti and Brong-Ahafo regions of Ghana.

Generally, the bee is found and consumed together with honey even though the honey is the main product of interest in this case. Bees are found in all parts of Ghana and honey

(from bees) is a common product consumed globally. Some people are able to harvest bee larvae together with honey throughout the year. According to Gessain and Kinzler

(1975), when honey is harvested, honey, wax, combs and larvae can be separated, but their combinations including the bees themselves are consumed.

Aside directly consuming insects as food, the use of insects as feed for animals is an aged practice among many tribes in Ghana and more pronounced in the rural communities.

Four insects were identified as feed for animals. Among these, flies and termites were the popular insects consumed by animals (mostly cats, fish and birds). Although four insect species were identified in the survey as feed for animals, it was only the termite that was reportedly semi-reared for animal feed. The termite tunnel or mound is usually fed with either straw or cow dung in a gourd/bowl. As the termites infest and feed overnight, they are harvested early morning through trapping.

Interestingly, the tick was one arthropod that was mentioned among edible “insects” during the survey. Ticks are usually found on cattle and are mostly harvested by

herdsmen during their grazing expeditions. Ticks are simply taken off cattle and roasted or eaten raw.

This work is intended to provide a road-map for research for development in Ghana in the area of insects as food and feed. In a nutshell, 13 edible insects were identified of which nine are major edible insects. Some of these edible insects can be reared as food since they are already a delicacy in many communities. Poultry and fish feed is very expensive in Ghana due to the fact that, the main protein sources (Fish meal and Soy meal) are imported.

3.5.3 Harvesting of edible insects

The harvesting of edible insects in Ghana is mostly done by children and women, except the palm weevil larva which is done by men; this is due to the long distances to the harvesting areas (forests) and the difficulty of felling palm trees and the harvesting procedures for the larva.

Harvesting methods depend on the behaviour of the insect. Nocturnal insects (termites and house crickets) are mostly lured by light into traps, the ground and field crickets by their chirping sound and the palm weevil larva by the deep cuts artificially inflicted on palm trees. The ground cricket and field cricket are dug out of holes whiles the grasshoppers are also harvested using catapults by children who herd cattle during the raining season.

For termites, traditionally, a basin (big bowl) is filled with water and placed under a lamp or other light sources in the evening after rainfall. The light attracts the reproductive

termites which come out for nuptial flights. These are trapped in the water or collected by hand into the water to prevent them from escaping.

Inhabitants visit and harvest edible insects from farms and forests located close to or far from their homes. However, respondents who rear their own insects for food constituted a negligible proportion. Some insects such as the palm weevil larva and the bee (brood) are to some extent, indirectly reared.

After exhausting harvesting of palm wine, consumers of the larvae of the palm weevil usually monitor and protect felled palm trees to allow the palm weevil oviposit in order to harvest larvae after two to four weeks. This process is, however, grounded on indigenous knowledge and methods. Aspire Food Group is currently empowering people in Ghana to commercially rear and harvest ‘akokono’ all-year-round.

3.5.4 Developmental stages consumed and purposes of consuming edible insects in Ghana.

Adult grasshoppers, house crickets, ground crickets and locusts are consumed by certain native tribes in Ghana. These insects, according to respondents, have a special taste when eaten alone or used in preparing meals. The grasshopper and termites which are commonly consumed in the northern part of Ghana are relished for their crispy texture and unique taste when fried or roasted. Same was said about the locusts which, according to the locals, have overtime become very scarce. These insects are usually harvested using trap nets or by hand-picking. The shea tree caterpillars which are commonly found on shea trees/shrubs are usually picked and consumed by herdsmen during their grazing

expeditions. The house cricket is eaten either raw or roasted over open fire. This activity was recorded in the Northern, Upper East and Upper West regions.

The shea tree caterpillar and the palm weevil larva are consumed at the larval stage because of their soft nature, with a substantial proportion of their nutritional value still intact. Also, at the larval stage, insects remain relatively cleaner and more hygienic as they are unable to visit unclean environments except those that dwell in filthy areas. Most of the identified insects are fairly harmless, unable to bite or secrete poisonous substances. This makes it easy and less dangerous to harvest them.

The rate of insect consumption decreased among some respondents due to, among other things, social stigma associating insect consumption to poverty and an activity for children.

3.5.4 Factors that influence the practice of entomophagy

From the results, males (83.2%) were more likely to eat insects than females (79.5%).

This might be attributable to the fact that more males than females were interviewed during this survey hence influencing this outcome. In terms of age, people within the older age cohorts showed a higher willingness to consume insects than the younger ones.

This may be due to the fact that the younger generation has a wider variety of meat sources to choose from unlike the older ones who grew up with very limited choices and hence had to rely on insects which eventually became a part of them. This might be due to the fact that many see edible insects as traditional food and associate it with the older

generation. Cunningham and Pelser (1991) observed that knowledge about traditional food is being lost because it is really not taught in schools. With reference to formal education, the study indicated that people with high level of formal education were more likely to engage in entomophagy than those with less or no formal education. This might be due to the fact that majority of those with high level of education were adults and have probably lived at a time when entomophagy was common.

3.5.5 Insect consumption by locality in Ghana

About 63.5% of rural dwellers are more likely to consume insects compared to 36.5% of urban dwellers. This is attributable to easier access to insects in rural areas than urban localities and the availability of indigenous knowledge on methods of harvesting by the rural dwellers.

With regards to insects serving as a source of income for people, more rural (44%) folk than urbanites (32%) were optimistic that insects could serve as a source of income. This is evident in rural communities along the major highways where people are often seen selling indigenous foods like mushrooms, crabs, snails and palm weevil larvae (akokono).

These are mostly patronised by urban dwellers travelling from the rural to the urban areas during the weekends and holidays. Therefore, it is likely that small indigenous businesses such as the sale of edible insects would do better in the urban than rural areas nevertheless.

3.5.6 Determinants of insect availability and consumption

Generally, edible insects serve as a source of protein in the traditional food systems of many tribes in Ghana. People are more comfortable with eating insects even though at different levels, and this was observed to be influenced by various environmental, economic and cultural factors. Vegatation largely influence the availability of various edible insect species in the northern and the southern parts of the country. This in turn influenced the kind of insects consumed in various parts of the country. A common observation with reference to the vegetation and weather condition is that, the southern

(forest zone) part of the country is characterised by forest cover that is green almost throughout the year whilst the northern part is mainly grassland with prolonged months of dry weather conditions.

The variation in species of trees available in the forest zone (such as palm trees) and the savannah zone (shea tree) that serve as habitats for different known edible insect species clearly affect the type of insects available and consumed in the various communities. For instance, the palm weevil larva that is found in felled palm trees is consumed in communities in southern Ghana. These include the Ashanti, Brong Ahafo, Western,

Eastern, Central, Volta and Greater Accra regions where palm trees are available. The consumption of the shea tree larva is commonly found where the shea tree grows (mainly in the savannah zone of the country including Navrongo, Bolgatanga and Sandema in the

Upper East region; Sagnarigu, Bunkurugu and Kpagayili in the Northern regions; and

Nadowli, Bamahu and Wa in the Upper West region).

It was, however, noted that almost all the edible insects identified are consumed throughout the country even though at varying levels. Some respondents indicated they consumed certain insect species that were generally not consumed where they have migrated to, especially those in cross ethnic marriages. Migration and cross ethnic and cross-tribal factors tend to influence the geographical patterns of entomophagy. The geographical map depicts the localities (based on ecological zones) where the identified insects are traditionally consumed. It is important, however, to note that the absence of a given edible insect in a zone on the map does not mean that consumers of such insects are not available. This was evident from the data gathered from all ten regions of the Ghana.

Consumers of all the identified insect species were found in each region. Stigmatisation appears to be the underlying factor barring some of the migrant consumers from eating insects consumed in their native communities.

Weather conditions influence the periods during which various insects can be harvested.

The availability of various insects for consumption is mostly influenced by environmental conditions which impact insect behaviour. For instance, insects like the termites are commonly harvested during the rainy season after a downpour (during nuptial flight). Termites are consumed throughout Ghana as a seasonal diet, available only during the rainy season.

3.6 Prospects and challenges to entomophagy in Ghana

3.6.1 Prospects

There is market for edible insects in all the ten regions of Ghana. It was noted that insects were sold in the markets in all the 20 districts visited but mainly during periods when such insects were in season. In Kumasi, Navrongo and Wa, people were found selling palm weevil larvae, termites and shea tree caterpillars, respectively in the various local markets. The price of a unit (about 200 g) of insects ranged from GH¢0.5 (USD $0.14) to

GH¢5 (USD $1.42). The least priced was termites (USD $0.0.075) sold in some communities including Paga, Navrongo and Chiana in the Upper East region. Twenty palm weevil larvae (120 – 140 g) was being retailed at GH¢5 (USD $1.42) in Kumasi.

Money from the sale of insects is used to supplement family income. This is especially vital for low income households that generally depend on subsistence agriculture and other activities as their source of livelihood. It was also gathered from some of the sellers that demand for these insects outstrips supply.

Overtime, some communities are innovating more sustainable ways to acquire edible insects with little harm to the vegetation and environment while promoting ease of access to insects. It was observed during one of the field surveys, that an oil palm farmer innovatively used stunted oil palm trees to trap palm weevils and harvest larvae. A hole was bored into the trunk of the palm plant (without felling the tree) to expose the inner core of the tree; where oil palm weevils breed (Plate 3.2). With the exposed yolk, oil palm weevils get attracted to feed and oviposit into the exposed inner core of the tree.

The eggs hatch and develop into Palm weevil larvae which are then harvested by the

farmer. Using this technique, a single palm tree can be used to trap these edible insects over a very long period of time.

Plate 3.2: Trapping palm weevil larvae using innovative strategies in the Ashanti Region of Ghana.

Currently, Ghana is one of the few countries in the world where the domestication of edible insects is ongoing. Aspire Food Group, a Canadian company specialized in supporting sustainable edible insect farming and consumption is currently operating in

Ghana. At the time of this study, the company was rearing palm weevil larvae as a commercial activity as well as supporting communities to farm the insect as part of

Aspire’s corporate social responsibility. It was realised that respondents from one of the

communities where Aspire Food Group operates were fully aware of the potential of edible insects serving as a source of income and a sustainable farming venture.

Price is a vital determinant of demand and level of consumption of goods and services.

This was observed in the harvesting/production and sale of ‘akokono’ in Kumasi. The demand is far greater than the supply to such an extent that 20 of the larvae (each weighing about 7-10 g) is sold for GHc5 ($1.42). A kilogram of the palm weevil larvae is sold at GHc35 (US$10) in the Kejetia market in Kumasi as against GHc15 (US$4.285) in the villages.

3.6.2 Challenges

The consumption of insects like any other product is influenced by the physical and economic accessibility to the product. Harvesting of insects is generally seasonal in

Ghana. Some respondents attributed the fall in consumption of insects to the increasing scarcity of the insects. The populations of most of the edible insect species such as grasshoppers, termites and palm weevil larvae are continuously dwindling due to various reasons. The most notable among the reasons was the high rate of depletion of vegetation and forest cover. Respondents observed that getting insects meant going farther into the forest to trap them. This was worsened by the fact that insect trappers were not assured of a catch when they embarked on such long expeditions. The effect of vegetation depletion is even dire in the savannah zone which has prolonged periods of dry weather (November

– March). The consumption of edible insects including termites, shea tree caterpillar,

grasshoppers and crickets is therefore seasonal in the Northern, Upper East and Upper

West regions due to the prolong drought and bush burning by some herdsmen during the dry season.

The difficulty and dangers involved in acquiring the insects seem to contribute to the declining access to edible insects. As observed in the study, hunting and trapping which were the common methods of acquiring insects were said to expose insect hunters to various risks. These included snake bites, stings, cuts from axe, machete/knife, and wild animal attacks during hunting especially for palm weevil larvae.

Aside injuries from cutlasses and snake bites that palm weevil larvae harvesters are exposed to, some respondents also complained about the difficulty in felling trees and cutting through the trunks as impediments to hunting for the insects. Some people therefore described the process of hunting/trapping edible insects as time wasting, stressful and dangerous, hence, would resort to meat (such as beef, chicken, mutton and pork) that can be readily acquired from the markets.

Closely related to the above factors is the scarcity and contamination of feed for various insect species consumed. The use of dangerous chemicals including persistent pesticides in farming and other agricultural activities such as palm wine tapping is a major impediment to the growth of many edible insect species in Ghana. Throughout the country, many dangerous pesticides were used by farmers to control pests including weeds. These activities consequently poison the feed and habitats of many insect species including edible ones. Palm wine tappers who fell mainly palm trees to tap palm wine use insecticides to prevent palm weevils from “invading” the felled palm trees. The scarcity

of palm weevil larvae according to indigenes of some communities including Donyina,

Bomfa, Ejisu and Jema is mainly due to the inability of the palm weevil to find breeding grounds. The chemicals also kill existing larvae in the trees. As more palm wine tappers are adopting chemicals to protect exposed palm surface, communities which were noted to have abundance of palm weevil larvae are facing increasing scarcity of the insects.

Common ailments including diarrhoea and cholera were reported as side effects of insect consumption, especially if the insects were not properly prepared. Also, unlike meat from cattle, pig and fish that can easily be checked for disease, edible insects are not checked - hence consumers are exposed to risk of eating contaminated insects. Some people also commented on the danger of eating poisonous insects as other inedible insects sometimes get mixed up with edible insects. The limiting factors to the practice of entomophagy identified from the study were:

1. Scarcity and difficulty in acquiring edible insects which in some cases make the

prices of insects high;

2. Lack of efficient and effective harvesting techniques in that harvesters use mainly

traditional methods to trap insects;

3. Bad perception about insect consumption and fear of stigmatization thereby

making people shy away from consuming insects;

4. Availability of other meat sources including beef, pork, poultry;

5. Urbanisation and modernity coupled with the insurgence of foreign culture which

does not have a good recognition for entomophagy;

6. Limited knowledge about nutritional value of insects and fading indigenous

knowledge essential for identifying and hunting edible insect species;

7. Fear of adverse health implication of eating insects including stomach pains,

diarrhoea, allergies and food poisoning resulting from consuming poisonous

insects mixed with edible insects;

8. Superstition and modern religious beliefs that do not support the practise of

entomophagy. i.e. the Seventh Day Adventist (SDA) church prohibits its members

from eating palm weevil larvae (‘akokono’) and other insects in the Brong-Ahafo

region.

According to Eva Muller, the Director of FAO’s Forest Economics, Policy and Products

Division, “Consumer disgust remains one of the important barriers to the adoption of insects as viable sources of protein in many Western countries,” Ms. Muller said in an interview in Rome on May 3, 2013. “Nevertheless, history has shown that dietary patterns can change quickly, particularly in the globalized world. She added that

“Western countries, most notably in Europe, have also been recently expressing interest in incorporating insects into their cuisine”.

In conclusion, this chapter among other things identified nine major edible insects of

Ghana and successfully classified them to the species level. The study also identified and evaluated five consumer-related factors that affect entomophagy in Ghana. These include locality, level of schooling, age, gender and occupation. Finally, a map showing the distribution and areas of consumption of edible insects has been developed.

CHAPTER FOUR

NUTRITIONAL CONTENT AND COMPARATIVE ANALYSIS OF VARIOUS EDIBLE INSECTS AND FEED FORMULATIONS

4.1 INTRODUCTION

Food insecurity and malnutrition are of major concern to human development and poverty reduction globally. While significant gains have been made to reduce poverty, rising food prices resulting in poor access to adequate nutrition continuously lead more people, especially in developing countries, into poverty (Asian Development Bank,

2012).

While the consumption of edible insects is gaining grounds in countries like Mexico

(Ramos-Elorduy et al., 2011), their use as part of traditional diet has been observed to continually decrease among many communities in Africa, specifically in Ghana, where these edible insects originally formed a vital source of food and nutrition of the local people (Anankware et al., 2015). This situation has generally been attributed to limited knowledge on the dietary value of edible insects.

The nutritional content of various edible insect species vary even within the same family of insect (van Huis et al., 2013). The variation is influenced by the metamorphic stage, the diet and habitat of the insects.

In a study, FAO (2012b) identified as high as 1,272 kcal/ 100 g contained in a raw green ant (Oecophylla smaragdina Fabricius) and as low as of 89 kcal/100 g in a raw

grasshopper (Cyrtacanthacris tatarica) (Linnaeus). In an earlier study by Ramos-Elorduy et al. (1997), a caloric content range of 293-762 kilocalories per 100 g (kcal/100g) was identified in 78 different insect species collected from the Oaxaca State of Mexico.

Generally, edible insects are rich sources of iron, not ignoring other elements, and their addition to daily diet could enhance iron status and prevent anaemia. WHO has identified iron deficiency as the commonest nutritional disorder globally. About 50% of all children in developing countries are anaemic (WHO, 2005). Anaemia is one of the major causes of deaths in mothers and children in Ghana and its deficiency results in poor mental ability among children (van Huis et al., 2013). The objectives of this study were to determine the protein content and conduct comparative proximate analysis among some edible insect species.

4.2 MATERIALS AND METHODS

4.2.1 Edible insecsts and analysis conducted

The edible insects used for these experiments were the African termite, Macrotermes bellicosus Smeathman, the palm weevil larvae, Rynchophorus phoenicis Fabricius, the house fly Musca domestica Linnaeus, the black soldier fly larvae, Hermetia illucens

Linnaeus and the shea tree caterpillar, Cirina butyrospermi Vuillot. Proximate, amino acid and fatty acid analyses were conducted at the Chemical Laboratory of the

International Centre for Insect Physiology and Ecology (ICIPE) in Nairobi, Kenya.

4.2.2 Amino acid profile

The amino acid profile was determined using High Performance Liquid Chromatography

(HPLC) as described by Ojinnaka and Ojimelukwe (2013) and Dhillon et al. (2014).

High Performance Liquid Chromatography (HPLC Waters Model 616/626) was used for the determination of the amino acid profile of the flour samples of the African termite, the palm weevil larvae, the house fly, the black soldier fly larvae, and the shea tree caterpillar. The preparation and analysis of the different samples was carried out as follows:

4.2.2.1 Hydrolysis

The samples were frozen in liquid nitrogen and lyophilized for 90 min. The vacuum-dried samples were then hydrolysed with 200 µL of constant boiling 6N HCL and 40 µL of phenol through vapour phase hydrolysis. The samples were dried in an oven at 112-

116oC for 20-24 h. After completion of hydrolysis, excess HCL was wiped off and the tubes were vacuum-dried for 90 min. The insect samples were reconstituted with 100 µL of 20 mM boiling HCL.

4.2.2.2 Derivatisation of amino acids

The reconstituted 20 µL samples were derivitised with AccQ-Flour reagent kit

(WAT052880-Waters Corporation, USA). AccQ-Flour borate buffer (60 µL) was added in the sample tube with a micropipette and vortexed. Thereafter, 20 µL of AccQ-Flour

reagent was added and immediately vortexed for 30 sec, and the contents were transferred to maximum recovery vials. The vials were heated for 10 min in a water bath at 55oC before separation of amino acids using HPLC (Dhillon et al., 2014).

4.2.2.3 Separation of the derivatised amino acids

The AccQ-Flour amino acids derivatives were separated on a Waters 2707 Module HPLC

System attached to a PDA (Model PDA 2998). A 10 µL sample was injected into a

Waters reverse phase AccQ Tag Silica-bonded Amino Acid Column C18 (3.9 mm x

150mm) using auto sampler (Waters 2707). The Waters AccQ Tag Eluent A Concentrate

(WAT052890) was diluted to 10% in Milli-Q water and used as eluent A, and 60% acetonitrile as eluent B in a separation gradient with a flow rate of 1.0 mL/min. The separation gradient used was 0-2 min (100% A), 2.0 min (98.0% A), 15.0 min (93.0% A),

19.0 min (90.0% A), 32.0 min (67.0% A), 38.0 min (0.0% A) and 56.0 min (100% A)

(Dhillon et al., 2014).

4.2.2.4 Data processing/interpretation and calculation of the final results

The amino acids were detected using PDA at 254 nm with the column condition set at

37oC. The amino acid peaks were acquired using Empower Pro Software® by Waters

Corporation (2005-08) and were calculated based on amino acid calibration standard

(Thermo Scientific Amino Acid Standard H, Prod # NCI0180) run at 5 concentrations;

10, 20, 30, 40, 50 uL having 2.5 µmoles/mL or 1.25 µmoles/mL of the L-forms in 0.1N

HCL. Amino acids assignments were visually checked to verify the peak assignment.

Injections (10 µL) of 10, 20, 30, 40 and 50 µL amino acid standard corresponds to 100,

200, 300, 400 and 500 pmol, respectively, of each amino acid, except cysteine which had half of their concentrations. The proportional molar concentrations for each amino acid was calculated based on the concentration of standard amino acids and expressed as µg amino acid/g sample (Dhillon et al., 2014).

4.2.3 Proximate analysis

Crushed insects (about 100 g) were analysed based on procedures employed by the

Association of Analytical Chemists (1990). Velp Solvent Extractor (SER 148/6) was used to determine fat content with ethyl ether as extractant. Crude protein (CP) was determined using the Kjeldahl method by determining the nitrogen content (%) and multiplying by the factor 6.25. The neutral detergent fibre (NDF) and acid detergent fibre

(ADF) were analysed with the Velp fibre analyzer (FIWE 6) (VELP Scientifica, Usmate

Velate, Italy) using reagents described by Van Soest et al. (1997). The ash content was determined by heating at 550°C overnight. The organic matter (OM) was then determined by subtracting ash content from 100.

4.2.3.1 Amino acids: The method for protein extraction was adopted from Hamilton et al. (2012). Processed and unprocessed insect samples were separately snap-frozen in liquid nitrogen and crushed into fine powder.

The samples (2 g each) were extracted for 1 h in ice cold 5 v/w 100 mM 4-(2- hydroxyethyl)-1-piperazineethanesulfonic acid (HEPES) pH 7.2, 2 mM dithiothreitol

(DTT), 2.5% Polyvinylpyrrolidone (PVP), 0.5 mM Ethylenediaminetetraacetic acid

(EDTA), 1 mM benzamidine 0.1 mM phenylmethanesulfonylfluoride (PMSF) in a magnetic stirrer. The samples were filtered through KERLIX™ Gauze Bandage Rolls

Sterile Soft Pouch 2.25" x 3.0 yds, centrifuged at 8000 rpm for 30 min at 4°C to remove solid debris.

Protein was precipitated between 45% and 80% (NH4)2SO4 and the pellet recovered by centrifugation at 21,000 rpm for 30 min at 4 °C. The protein pellets were desalted in 20 mM HEPES–NaOH pH 8 containing 2 mM DTT using Sephadex G-25 gel filtration chromatography (PD-10 columns, GE Healthcare) to give 80.2 mg and 77.9 mg of proteins from processed and unprocessed insect samples, respectively.

Ten mg of each of the samples were separately transferred into a 5 ml micro- reaction vial into which 2 ml of 6N HCL were added and closed after careful introduction of nitrogen gas. The samples were hydrolyzed for 24 h at 110 °C. For tryptophan analysis, 10 mg from each of the samples were separately transferred into a 5 ml micro-reaction vial into which 2 ml of 6N NaOH were added and then capped after careful introduction of nitrogen gas. The samples were hydrolyzed for 24 h at 110 °C.

After the hydrolysis, the mixtures were evaporated to dryness under vacuum. The hydrolysates were reconstituted in 1ml 90:10 water: acetonitrile, vortexed for 30 sec, sonicated for 30 min (Plate 4.1), and then centrifuged at 14,000 rpm and the supernatant analysed using LC-Qtof-MS. The analysis was replicated three times.

Plate 4.1: vortexer and sonicator bath

4.2.4 Total carbohydrate

This was calculated by the difference from other proximate values obtained.

Total carbohydrate = 100 - % (moisture + c.fibre + c.fat + ash + c.protein).

Descriptive statistics was employed in analysing the data. The samples were determined according to AOAC (1990).

4.3 RESULTS

4.3.1 Nutrient composition

The results of these analyses are presented in Table 4.1. Shea tree caterpillar (STC) contained the highest amount of crude protein as a percentage of dry matter (63%). The

Black Soldier Fly larvae (BSFL) contained the highest percentage of ash as a percentage of dry matter of 17% and the lowest percentage of ash of 1.4% was recorded in Palm weevil larvae (PWL). The PWL had the highest fat content of 65.4%, followed by BSFL

(18.0%). The Shea tree caterpillar had the highest NDF (56.2%), followed by the house fly larvae (HSFL) (54.9%) and black soldier fly had the least (39.9%). House fly larvae had the highest ADF per cent value of 37.1, which was followed by Shea tree caterpillar

(32.4%) and Black soldier fly larvae had the least percent value (16.6%).

Table 4. 1 Nutrient content of selected edible insects

Dry Crude Crude matter Ash* protein* fat* NDF* ADF* Sample [g/g] [%] [%] [%] [%] [%] BSFL 0.9 17.7 44.8 18.0 39.9 15.6 STC 0.9 6.4 63.6 12.2 56.2 32.4 PWL 0.4 1.4 31.0 65.3 - - HSFL 0.9 9.8 61.0 11.5 54.9 37.1

*Results presented as percentage of dry matter. Dry matter presented as mean of three replicates; all other results presented as mean of duplicate analysis.

Key: BSFL (Black Soldier fly), STC (Shea tree caterpillar), PWL (Palm weevil larva) and HSFL (House fly), NDF (Neutral detergent fibre), ADF (Acid detergent fibre).

4.3.2 Composition of Amino Acids

Table 4.2 shows the amino acids present in the target insects. The highest amount of amino acid in the protein for STC was Isoleucine (76.8 µg/g), followed by methionine

(56.5 µg/g) and the least amount of amino acid was Arginine (3.7 µg/g). The predominant amino acid in HSFL was phenylalanine (36.5 µg/g), this was followed by methionine (30.1 µg/g). The limiting amino acid in HSFL was arginine (7.5 µg/g). The highest amino acids in PWL was phenylalanine (54.6 µg/g), followed by Isoleucine (53.0

µg/g). The limiting amino acid was tyrosine (8.6 µg/g). Isoleucine (112.7 µg/g) was the

predominant amino acid in BSFL. This was followed by Leucine (89.4 µg/g). The

limiting amino acids for BSFLwas lysine (18.6 µg/g) (Table 4.2).

Table 4.2. Amino acid content of selected insects Amino acid content [µg/g] Insects Arg Pro Val Met Tyr Leu Ile Phe Lys STC 3.7 27.9 53.9 56.5 8.4 44.4 76.8 38. 22.8 HSFL 7.5 9.7 22.9 30.1 9.4 24.2 46.4 36.5 8.8 PWL 50.3 23.9 33.7 26.9 8.6 44.5 53.04 54.6 15.2 BSFL 85.8 31.3 63.7 48.2 35.7 89.4 112.7 73.2 18.6

KEY: STC: Shea tree caterpillar, HSFL: House fly larvae, PWL: Palm weevil larvae, BSFL: Black Soldier fly larvae.

4.3.3 Composition of Fatty Acids

Tables 4.3a, 4.3b and 4.3c show the fatty acid content in the selected insects. The greatest

quantity of fatty acid found in BSFL was methyl dodecanoate with a percentage value of

about 8.4, followed by 9-Octadecenoic acid, methyl ester, (E) - of about 7.9%. The least

fatty acids found in the BSFL were Methyl 15-methylhexadecanoate and Methyl 18-

methylnonadecanoate with about 1.0% each. Elaidic acid in edible insects is usually

present in small amounts but its fatty acid methyl ester was the second highest fatty acid

present in the BSFL. The BSFL also contained 3.1% Oleic acid and 6.1% Methyl

hexadecanoate.

The Shea tree caterpillar larvae contained Methyl octadecanoate (18.6%) as the highest

fatty acid content followed by 9,12,15-Octadecatrienoic acid, methyl ester, (Z,Z,Z)

(17.4%). The least fatty acid was Methyl 13-methyltetradecanoate (0.7%). The highest fatty acid found in Palm weevil larvae (PWL) was Methyl 11-octadecenoate with a value of 28.6%, followed by Methyl palmitate (Methyl hexadecanoate) with a value of 15.9%.

The least fatty acid value was Trimethyl benzene<1,2,4-> (0.5).

The highest fatty acid content in HSFL was Methyl octadecanoate (6.9%). This was followed by Methyl 11-octadecenoate (5.2%). The least fatty acid constituent in HSFL was, (R)-3-Hydroxybutyric acid, methyl ether, methyl ester (0.5%). The fatty acid with the highest constituent in Termite (TM) was Methyl octadecanoate (15.0%), followed by

9-Octadecenoic acid, methyl ester, (E)- (12.5%). The least fatty acid was Oxalic acid, diisohexyl ester (2.1%). Among the insects in this study, it was only the termite that contained Hexadecanoic acid, ethyl ester (4.6%) and Octadec-9-enoic acid (4.4%).

Table 4.3: Average percentage fatty acid content of the selected insects

Fatty Acids BSFL STC PWL HSFL TM Methyl hexanoate 2.61 0.00 0.00 0.00 0.00 Methyl dodecanoate 8.37 0.99 1.59 1.47 0.00 Tridecanoic acid, methyl ester 2.84 0.00 0.00 2.63 0.00 Methyl tetradecanoate 5.01 2.94 4.69 3.39 8.98 Methyl 13-methyltetradecanoate 3.46 0.69 0.00 2.12 0.00 Pentadecanoic acid, methyl ester 3.46 2.71 0.81 1.93 0.00 Methyl hexadecanoate 3.36 4.55 0.00 1.78 6.35 7-Hexadecenoic acid, methyl ester, (Z)- 2.96 0.84 0.00 0.00 0.00 9-Hexadecenoic acid, methyl ester, (Z)- 3.17 2.58 4.29 3.78 0.00 Methyl hexadecanoate 6.14 7.90 15.97 1.06 7.59 n-Hexadecanoic acid 3.19 1.60 1.92 0.00 5.75 Methyl 15-methylhexadecanoate 1.02 0.00 0.00 1.92 0.00 Hexadecanoic acid, 14-methyl-, methyl ester 1.92 0.00 0.00 0.00 0.00 Heptadecanoic acid, methyl ester 3.17 2.95 1.06 0.00 0.00 Methyl linoleate 6.43 5.81 2.20 3.73 8.16 9-Octadecenoic acid, methyl ester, (E)- 7.91 0.00 0.00 5.09 12.48 11-Octadecenoic acid, methyl ester 6.10 0.00 0.00 0.00 0.00 Methyl octadecanoate 6.61 18.57 7.94 6.92 15.00 Oleic Acid 3.06 0.00 0.00 0.00 0.00 Methyl 9-cis,11-trans-octadecadienoate 3.07 0.00 0.00 0.00 0.00 Nonadecanoic acid, methyl ester 2.98 2.82 1.47 0.97 0.00 Methyl 11-eicosenoate 2.91 0.00 0.00 1.61 0.00 Methyl 18-methylnonadecanoate 1.02 1.96 0.91 0.00 5.35 Methyl 20-methyl-heneicosanoate 3.82 0.00 2.32 0.00 0.00 Farnesoic acid<2E,6E-> 4.95 0.00 0.00 0.00 0.00 Methyl nonanoate 1.55 0.00 0.00 0.00 0.00 Methyl decanoate 1.86 0.00 0.00 0.00 0.00 1,1-Dodecanediol, diacetate 1.73 0.00 0.00 0.00 0.00 Methyl palmitate (Methyl hexadecanoate) 2.95 0.00 8.51 1.55 0.00 Methyl myristoleate 2.45 0.00 0.00 0.70 0.00 cis-10-Heptadecenoic acid, methyl ester 3.41 1.70 0.90 0.00 0.00 gamma.-Linolenic acid, methyl ester 2.83 0.00 0.00 0.98 0.00 cis-13-Eicosenoic acid, methyl ester 3.84 0.00 0.00 0.00 0.00

Table 4.3 contd.: Average percentage fatty acid content of the selected insects

Fatty Acids BSFL STC PWL HSFL TM Eicosanoic acid, methyl ester 3.89 2.02 3.18 3.35 5.33 Methyl 9-methyltetradecanoate 3.00 0.00 0.00 1.25 0.00 Methyl 3-methyl-pentadecanoate 2.55 0.00 0.00 0.89 0.00 7,10-Hexadecadienoic acid, methyl ester 2.37 0.00 0.00 0.00 0.00 Methyl hexadec-9-enoate 4.38 0.82 1.64 3.24 0.00 Butanoic acid, 2-methyl-, methyl ester 3.45 0.00 0.00 0.00 0.00 3-Ethyl-3-methylheptane 1.17 0.00 0.00 0.00 0.00 Tetradecanoic acid, 12-methyl-, methyl ester 1.30 0.00 0.00 0.00 0.00 Methyl 14-methylhexadecanoate 1.28 0.00 0.00 0.00 0.00 9-Octadecenoic acid (Z)-, methyl ester 1.57 0.00 0.00 2.24 0.00 Octadecanoic acid, 17-methyl-, methyl ester 1.21 0.00 0.89 0.00 0.00 Tetracosanoic acid, methyl ester 1.27 1.45 0.00 0.00 0.00 Octanoic acid, methyl ester 0.00 1.11 0.00 0.00 0.00 cis-5-Dodecenoic acid, methyl ester 0.00 2.45 0.00 0.00 0.00 Hexadecanoic acid 0.00 1.14 0.95 0.00 0.00 Methyl 9-heptadecenoate or 9-17:1 0.00 1.40 0.68 0.00 0.00 Gamolenic Acid 0.00 0.79 0.00 0.00 0.00 9,12,15-Octadecatrienoic acid, methyl ester, (Z,Z,Z)- 0.00 17.39 0.00 0.00 0.00 6-Octadecenoic acid 0.00 1.15 1.18 0.00 7.97 Methyl 6-cis,9-cis,11-trans-octadecatrienoate 0.00 1.79 0.00 0.00 0.00 Methyl 11,14,17-eicosatrienoate 0.00 2.99 0.00 0.00 0.00 Docosanoic acid, methyl ester 0.00 2.81 0.00 3.29 0.00 cis-13-Octadecenoic acid 0.00 0.89 0.00 1.81 5.93 Triacontyl acetate 0.00 1.14 0.00 0.00 0.00 Hexanoic acid, methyl ester 0.00 0.65 0.00 0.00 0.00 Methyl 6,9,12-octadecatrienocate 0.00 0.66 0.00 0.00 0.00 cis-Vaccenic acid 0.00 0.73 0.95 0.00 0.00 Cyclopentane, 1,2-dimethyl-, trans- 0.00 0.00 0.87 0.00 0.00 Hexadecanoic acid, 15-methyl-, methyl ester 0.00 0.00 0.93 0.00 0.00 Methyl 11-octadecenoate 0.00 0.00 28.65 5.16 0.00 6-Octadecenoic acid, (Z)- 0.00 0.00 0.85 0.00 0.00 Methyl 11,14-octadecadienoate 0.00 0.00 0.61 0.00 0.00 Trimethyl benzene<1,2,4-> 0.00 0.00 0.49 0.00 0.00 Undecanoic acid, 10-methyl-, methyl ester 0.00 0.00 0.59 0.00 0.00

Table 4.3 contd.: Average percentage fatty acid content of the selected insects

Fatty Acids BSFL STC PWL HSFL TM Hexadecanoic acid, 14-methyl-, methyl ester 0.00 0.00 0.70 0.00 0.00 Methyl 8-heptadecenoate 0.00 0.00 0.94 0.00 0.00 Methyl 13-eicosenoate 0.00 0.00 1.36 0.00 0.00 Methyl 10-methyl-undecanoate 0.00 0.00 0.00 1.86 0.00 Methyl 7,10-hexadecadienoate 0.00 0.00 0.00 2.67 0.00 Methyl 11-hexadecenoate 0.00 0.00 0.00 2.24 0.00 50.33 Methyl linoleate 0.00 0.00 0.00 3.69 0.00 cis-5,8,11,14,17-Eicosapentaenoic acid, methyl ester 0.00 0.00 0.00 3.17 0.00 9-Octadecenamide, (Z)- 0.00 0.00 0.00 2.17 0.00 Nonahexacontanoic acid 0.00 0.00 0.00 1.84 0.00 Propanoic acid, 2-methyl-, 2-methylbutyl ester 0.00 0.00 0.00 0.51 0.00 (R)-3-Hydroxybutyric acid, methyl ether, methyl ester 0.00 0.00 0.00 0.50 0.00 Methyl p-tert-butylphenyl acetate 0.00 0.00 0.00 0.65 0.00 Methyl 10-methyl-dodecanoate 0.00 0.00 0.00 0.64 0.00 Methyl Z-11-tetradecenoate 0.00 0.00 0.00 1.13 0.00 Ethyl hexadecanoate 0.00 0.00 0.00 0.82 0.00 Methyl 10-methyl-hexadecanoate 0.00 0.00 0.00 0.91 0.00 Methyl 9,10-methylene-hexadecanoate 0.00 0.00 0.00 1.28 0.00 8-Octadecenoic acid, methyl ester 0.00 0.00 0.00 4.33 0.00 9,12-Octadecadienoic acid (Z,Z)-, methyl ester 0.00 0.00 0.00 0.94 0.00 Methyl 9,10-methylene-octadecanoate 0.00 0.00 0.00 0.87 0.00 5,8,11,14-Eicosatetraenoic acid, methyl ester, (all-Z)- 0.00 0.00 0.00 1.20 0.00 Tetratriacontane 0.00 0.00 0.00 2.26 0.00 13-Tetradecen-1-ol acetate 0.00 0.00 0.00 3.47 0.00 Octadec-9-enoic acid 0.00 0.00 0.00 0.00 4.41 Oxalic acid, diisohexyl ester 0.00 0.00 0.00 0.00 2.11 Hexadecanoic acid, ethyl ester 0.00 0.00 0.00 0.00 4.57

Legend: BSFL (Black soldier fly larva), STC (Shea tree caterpillar), PWL (Palm weevil larva), HSFL (House fly larva), TM (Termite).

4.4 DISCUSSION

4.4.1 Proximate analysis of the selected insects

The results of proximate analysis showed that C. butyrospermi contained the highest amount of crude protein as a percentage of dry matter (63%). This falls within the range of protein content reported by Xiaoming et al. (2010) for several insect orders including

Coloeptera (23-66%), Hemiptera (42-74%), and Hymenoptera (13-77%). The protein content of insects have been shown to be affected by both the developmental stage and diet, even for insects within the same order. The results report greater proportion of protein levels than reported in conventional food proteins of animal origin. For example, beef is reported to contain approximately 55% crude protein (on a dry matter basis)

(Finke, 2002).

The BSFL contained the highest percentage of ash as a percentage of dry matter of 17% with PWL having the lowest percentage of ash of 1.376%. The percent ash recorded for

BSFL was lower than the ash content of 25.9% for hover flies (Eristalis sp.) recorded by

Philip and Burkholder. (1995) but compare favourably with a range of percentage ash content recorded by Rumpold and Schlüter (2013) for several insect orders such as 1-

25% for Coleoptera; 1-21% for Hemiptera; 5.2-25.9% for Diptera of which the Eristalis sp. falls within. However, the percentage ash content for some termites such as

Macrotermes bellicosus Smeathman, Macrotermes natalensis Haviland, were recorded in a range of 1.2 – 4.21% (Banjo et al., 2006). These values were smaller than the values recorded in this study. These might be attributable to the disparities in the source of feed, the metaphorphic stage used and the sensitivity of equipment used for the analysis. The

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percent ash content recorded in this study and those by Rumpold and Schlüter (2013) show that, edible insects have high ash content. This is explained by their hard body due to the high chitin content (Raksakantong et al., 2010).

The PWL had the highest fat content (65.3%) followed by BSFL (18.0%). The fat content of PWL is comparable to the results obtained by Omotoso and Adedire (2007) who obtained 62.1%, 61.4%, 54.4% for late larval stage, early larval stage and adult stages, respectively for R. phoenicis in Nigeria.

The differences in the percentage fat varied widely between the different insect species.

Raksakantong et al. (2010), in their study on some Thai edible insects, obtained fat content of 5% for June beetles, Cotinis nitida (Linnaeus) and 37% for the queen termite,

Macrotermes sp. The giant water bug, which lives in freshwater, had the highest lipid content (20%), followed by the mole cricket (13%), which lives on grass, while the water scavenger beetle had the lowest (3%) (Yang et al., 2014). These results suggest that habitat, diet and insect species affect the lipid or fat content in insects (Verkerk et al.,

2007). Edible insects contain a considerable amount of fats and oils (Womeni et al.,

2010) that are rich in polyunsaturated fatty acids such as linoleic and α-linoleic acids which are essential for the development of children and infants (Michaelsen and

Chamnan, 2010). The plants on which the insects feed influence their fatty acid composition (Bukkens, 2005). Rapid oxidation will occur due to the presence of the unsaturated fatty acids when the insect food product is processed, thus causing rapid rancidity.

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Edible insects can play an important role in landlocked developing countries with lower access to other protein source such as fish). Lipids are also important in the biological and structural functioning of cells, helping in the transport of nutritionally essential fat- soluble vitamins (Omotoso and Adedire, 2007). Lipids are essential in diets as they increase the palatability of foods by absorbing and retaining their flavours (Verkerk et al.,

2007). Cholesterol levels in insects vary from low (e.g. none in the edible leaf-cutter ant, Atta cephalotes Latr.) to approximately the levels found in other animals (1 mg sterol g- 1 tissue), depending on species and diet (Belluco et al., 2013). Rumpold and Schlüter

(2013) explained ‘The nutrient quality of the insect protein is promising in comparison to casein and soy but varies and can be improved by the removal of the chitin.’

A number of published studies have shown that, insects contain variable and a significant amount of fibre which are measured as acid detergent fibre (ADF) and neutral detergent fibre (NDF) (Barker et al., 1998; Finke, 2002; Pennino et al., 1991). It was explained by

Van Soest et al. (1997) that, ADF is composed mainly of lignins and cellulose whilst

NDF is made up of lignin, cellulose and hemicelluloses. It has been established by Finke

(2007) that, even though insects are made up of significant amount of ADF and NDF, the components that make up these are not yet known. However, it has been suggested by many authors that, the fibre in insects represents chitin because the chitin structural formular (linear polymer of b-(1-4) N-acetyl-Dglucosamine units) is similar to cellulose

(linear polymer of b-(1-4)-D-glucopyranose units) (Barker et al., 1998). Moreover, ADF has been shown by various authors to contain nitrogen (Barker et al., 1998; Finke, 2002).

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It was suggested by Finke (2007) that, the fibre content of insects measured as ADF consists of chitin and small amounts of cuticular proteins.

Chitin is a macromolecular compound which contains a significantly high nutritional and health value (Burton and Zaccone, 2007). Chitin is neither degraded nor absorbed into the blood or small intestines (Vidanarachchi et al., 2010). This however can affect the digestibility of proteins, thus, the measurements of chitin is important when insects will be used in animal nutrition. Chitin also has some medicinal value (Chen et al., 2009).

Chitin reduces serum cholesterol, repairs tissues by acting as haemostatic agent, promotes wound and burn healing, acts as an anticoagulant, protects against certain pathogens in the blood and skin and also inhibits the growth of pathogenic soil fungi and nematode

(Chen et al., 2009).

In this study, the Shea tree caterpillar larva had the highest NDF, followed by the house fly and black soldier fly had the least. This may be attributable to the more fibrous feed

(Sheanut tree leaves) of the Shea tree caterpillar larva as well as the presence of bristles and setae on the caterpillar.

4.4.2 Composition of Amino Acids

Most edible insects provide the nutritional requirement of children by providing them sufficient range of amino acids. The most predominant amino acid in the protein of STC was Isoleucine, followed by methionine and the limiting one was Arginine. Igbabul et al.

(2014) analysed the nutritional composition of dried larva of STC and the highest amino acid was leucine, followed by lysine. Both leucine and lysine are two of the most

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essential amino acids for proper growth and development. Lysine plays a vital role in converting fatty acids into energy, by producing carnitine; a nutrient that can help lower cholesterol. Research by the University of Maryland Medical Centre (UMMC) suggests that, lysine may offer protection against herpes and relieve osteoporosis symptoms due to its effects on calcium. Like lysine, leucine also contributes to several metabolic processes. Research by Layman (2003) of the University of Illinois, however suggests that, leucine’s primary role is to aid in the synthesis of protein structures before other metabolic functions. Hence, the presence of lysine and leucine in the insects identified in this survey suggest that, their consumption is crucial for protection against diseases and for the proper growth and development of people who have poor access to meat and fish.

4.4.3 Composition of Fatty Acid

It has been established that, most people cherish less calories in their diets, hence the demand for animal sources with a lower proportion of saturated fatty acids and a higher proportion of monounsaturated and polyunsaturated fatty acids. Insects have fat content of less than 10% to more than 30% on a fresh weight basis, and are relatively high in the

C18 fatty acids, oleic acid (18: 1), linoleic acid (18:2) and linolenic acid (18:3). Calvert et al. (1969) conducted studies on the fatty acids of the house fly pupae, and it was established that, the fatty acid patterns resembled those of some fish oils. Diets and the stage of development of the insects strongly influenced the fatty acid profiles (Stanley-

Samuelson et al., 1988).

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The fat fraction of BSFL according to Sealey et al. (2007), consists of highly metabolizable fats, including 55% saturated fat, 30% monounsaturated fatty acids and

15% polyunsaturated fatty acids (Omega 3, 6 and 9). The most prevalent fatty acid in

BSFL was methyl dodecanoate, followed by 9-Octadecenoic acid and then methyl ester,

(E). The least found in the BSFL were Methyl 15-methylhexadecanoate and Methyl 18- methylnonadecanoate. Methyl dodecanoate (Methyl laurate) is a fatty acid methyl ester formed from the reaction between methanol and lauric acid. According to Baroutian

(2009) a ratio of 6:1 for reaction of alcohol/oil and a ratio of 4:2 of methanol/ethanol reaction condition for one hour at 50 °C produces 98.1% of methyl laurate. Although the composition of methanol in the esterification reaction is high, APAG (1997) explained that the fatty acid methyl ester has no carcinogenic potential. Studies by gavage feeding proved methyl laurate to be non-toxic to rats with LD50s exceeding the limit dose of 2000 mg/kg weight. Lauric acid is a medium chain triacylglycerols (TAG), which are mostly absorbed whole, thus making them very digestible. Lauric acids are mostly found in coconut oil and it is a saturated fat. It is believed that, lauric acid lowers the total high- density lipoprotein (HDL) cholesterol than any other fatty acid, thus can reduce the risk of cardiovascular disease (Ulbricht and Southgate, 1991). 9-Octadecenoic acid, methyl ester (E) - is fatty acid methyl ester also known as elaidic acid methyl ester. Elaidic acid methyl ester consists of elaidic acid and methanol. Elaidic acid (18:1) is a trans-isomer of oleic acid. Elaidic acid in edible insects is present in small amounts even though its fatty acid methyl ester was the second highest fatty acid present in the BSFL. The trans fatty acid in Elaidic acid can be man-made or naturally made, of which the man-made trans fatty acid is of health concern due to the fact that, it raises the low-density lipoprotein

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(LDL) cholesterol levels and lowers the HDL cholesterol levels. Due to this, the naturally occurring trans fatty acids in the BSFL is of utmost benefits.

The naturally occurring trans fatty acids are also known as the conjugated linoleic acids which protect the body against cancer, heart disease and obesity (Belury, 2002). Methyl

15-methylhexadecanoate (methyl palmitate) is a fatty acid methyl ester of methanol and palmitic acid. Palmitic acid (C16:0) is a saturated fat which accounts for about 27% of the fatty acids present in beef (Whetsell et al., 2003); this is lower than the value obtained in this study for the BSFL. According to Grundy (1994) (cited by Whetsell et al., 2003) the higher palmitic acid present in beef results in high LDL cholesterol content, thus, raising the risk of cardiovascular disease. However, in BSFL, the percentage value of the methyl palmitate is very low. Oleic acid (3.06) was also found to be present in the BSFL.

Research by Win (2005) showed that, oleic acid blocks the action of HER-2/neu, a cancer-causing gene (oncogene) found in about 30% of breast cancer patients. HER-

2/neu positive tumors are an aggressive form of the disease and have a poor prognosis.

Oleic acid suppressed the action of the oncogene and also synergistically improved the effectiveness of the breast cancer drug, Herceptin, a targeted therapy made by Swiss drug maker Roche Holding that works against the HER-2/neu gene.

Oleic acids, however, help lower levels of low-density lipoproteins in the blood stream and maintain the level of the high density lipoproteins. Methyl 9-cis,11-trans- octadecadienoate is a natural form conjugated linoleic acid and it has a lot of therapeutic properties (Williams et al., 2000). Therefore the BSFL may be recommended for breast

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cancer patients to suppress the action of the oncogene and synergistically improved the effectiveness of the breast cancer drug, Herceptin.

The BSFL contains 6.14% of Methyl hexadecanoate which is used as a supplementary fat for animal feed. According to Newton et al. (2005) BSF larvae are good manure recyclers and do not only reduce livestock waste but generate a food source for fish and animals.

There is little data on the use of BSFL in human diets, however, with the presence of other important fatty acids, it can be considered for human consumption.

The results showed that, Shea tree caterpillar larvae contained Methyl octadecanoate as the most prevalent fatty acid followed by 9,12,15-Octadecatrienoic acid, methyl ester,

(Z,Z,Z). The least fatty acid was Methyl 13-methyltetradecanoate (0.69%). Methyl octadecanoate is a methyl ester of stearic acid. Stearic acid is a long chain fatty acid but it does not raise the LDL cholesterol. Studies done on hamsters (Schneider et al., 2000) and rat (Ikeda et al.,1994) showed that, stearic acid reduces the absorption of cholesterol.

Again, 9,12,15-Octadecatrienoic acid, methyl ester, (Z,Z,Z), also known as methyl linolenate is an ester of linolenic acid.

The results showed that, STC contained mainly polyunsaturated fatty acids and few saturated fatty acids which are also healthy. It has been established that, saturated fatty acids are not good for human consumption because they have health implications such as cardiovascular disorders, cancer and aging (Halliwell, 1996). Therefore, high desirable unsaturated fatty acid contents of STC may be considered an important food component for those who have high blood cholesterol and probably at risk of cardiovascular disease.

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Akinnawo and Ketiku (2000) explained that, the high polyunsaturated fatty acids in STC could be used to supplement nutrition of low income people who take in less animal protein.

It can also be explained using data from this study that, even though plant oils are richer in unsaturates (Alais and Linden, 1999), STC has higher unsaturated fatty acids than even palm oil when compared with the data obtained by Adeolu (2003) who compared the fatty acids from STC, to that of plant and animal sources. The findings of this study confirm those of Adeolu (2003). As a source of polyunsaturates (PUFA), STC exceeds that contained in most food except soybean for which 85% has been reported (Elegbede,

1998) and melon oil (Adeolu, 2003). PUFA can help reduce bad cholesterol levels in the blood hence lowering the risk of heart diseases and stroke. They also provide nutrients to help develop and maintain the body cells.

Adeolu (2003) also showed that, STC contains high essential fatty acids with about

41.65% unsaturates. Linolenic acid is essential for the functioning of the retina and nerve formation. STC is a good source of unsaturated fatty acids, most especially Linolenic acid which is good for the diets of aged people. This is because, the activity of the enzyme Delta-6-desaturase (D6D) falls with age. The oil can be useful in the pharmaceuticals and other industries aside its food value.

The most prevalent fatty acid found in PWL was Methyl 11-octadecenoate, followed by

Methyl palmitate (Methyl hexadecanoate). Methyl 11-octadecenoate is also known as trans vaccenic acid and it is a monoene (Santora et al., 2000). It has been observed by scientific researchers that, feeding of dietary Methyl 11-octadecenoate results in

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desaturated feeding (Loor et al., 2002). Loor et al. (2002) also indicated that, feeding diets with elevated Methyl 11-octadecenoate contents resulted inincreased amount of

9/11 conjugated linoleic acids in human serum and the 9/11 conjugated linoleic acids improved the efficiency of growth and conversion of feed in rodents (Loor et al., 2002).

Methyl palmitate; a naturally occurring fatty acid methyl ester which helps suppress

Kupffer cell function (the producers of harmful cytokines in the liver) in a study done by

Rodríguez-Rivera et al. (2008) showed that, methyl palmitate prevents CCl4-induced liver fibrosis in rats. Research done by Ogbuagu et al. (2011) showed the presence of palmitoleic (30.28%) and stearic acid (69.72%) in PWL. The results obtained in this study are comparable to that obtained by Babajide et al. (2011) who evaluated the palm weevil larvae as food and obtained 35.30% palmitic acid and 60.47% stearic acid as well as 0.72% oleic acid and 3.51% linoleic acid. The fatty acid composition might be influenced by their environmental factors. The levels of unsaturated fat and good saturated fat could reduce the risks of cardiovascular disease to lower cholesterol levels in humans (Grodji et al., 2013).

The amount of Methyl octadecanoate found in the house fly was 6.92%. This was followed by Methyl 11-octadecenoate (5.16%). The least fatty acid constituent in house fly was (R)-3-Hydroxybutyric acid, methyl ether, methyl ester (0.50%). The results obtained in this study showed that, house fly contain mostly saturated fats. Research done by Yang et al. (2014) showed the insect contained 3.8% methyl octadecanoate, and other saturated fatty acids accounted for 36.9%. This compares with the amount found in the present study. Their results also showed that house flies contained linolenic, linoleic and

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oleic acids but these polyunsaturated fats were not identified in this study; this might be due to disparities in the diet, metamorphic stage of insect used and/or the equipment used in the analyses. House fly, however can be used as feedstock or biodiesel production.

The fatty acid with the highest occurrence in termite (TM) was Methyl octadecanoate, followed by 9-Octadecenoic acid, methyl ester, (E). The least fatty acid was Oxalic acid, diisohexyl ester. 6-octadecenoic acid is an unsaturated fatty acid and an isomer of oleic acid, and according to Avato et al. (2004), it can be employed in the pharmaceutical industries. Methyl octadecanoate is associated with lower LDL cholesterol when compared with other saturated fats.

In conclusion, proximate analysis was successfully conducted on selected insects that are used as food and feed; the results of which will be very useful to dieticians, paediatrics and feed producers in Ghana. The high lysine and leucine content in the insects is crucial for protection against diseases and for the proper growth and development of people who have poor access to meat and fish. Finally, the BSFL may be recommended for breast cancer patients to suppress the action of the oncogene and improved the effectiveness of the breast cancer drug, Herceptin.

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CHAPTER FIVE

MASS REARING PROTOCOLS FOR SOME EDIBLE INSECT SPECIES

5.1 INTRODUCTION

Feeding a growing world population with more demanding consumers will necessarily require an increase in food production. This will inevitably place heavy pressure on already limited resources such as land, oceans, fertilizers, water and energy (Van

Itterbeeck and van Huis, 2012). If agricultural production remains in its present form, increases in Greenhouse gas (GHG) emissions as well as deforestation and environmental degradation will continue. These environmental challenges, particularly those associated with raising livestock, need urgent attention (Van Itterbeeck and van Huis, 2012).

Livestock and fish are important sources of protein in most countries. According to FAO

(2006) livestock production accounts for 70% of all agricultural land use. With global demand for livestock products expected to more than double between 2000 and 2050

(from 229 million tonnes to 465 million tonnes), meeting this demand will require innovative solutions (van Huis et al., 2013). Similarly, fish production and consumption have increased dramatically in the last five decades. As a consequence, the aquaculture sector has boomed and now accounts for nearly 50% of world fish production (Van

Itterbeeck and van Huis, 2012). The sustainable growth of the sector will depend largely on the supply of terrestrial and aquatic plant-based proteins for feed (van Huis, 2015).

The opportunity for insects to help meet rising demand in meat products and replace fishmeal and fish oil is enormous (Van Itterbeeck and van Huis, 2012). Large-scale livestock and fish production facilities are economically viable because of their high

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productivity, at least in the short term. However, these facilities incur huge environmental costs (Tilman et al., 2002). Manure, for example, contaminates surface water and groundwater with nutrients, toxins (heavy metals) and pathogens (Tilman et al., 2002;

Thorne, 2007). Storing and spreading manure can involve the emission of large quantities of ammonia, which has an acidifying effect on ecosystems. Any increase in animal production will, moreover, require additional feed and cropland and will likely trigger deforestation. The Amazon is a case in point: pasture now accounts for 70% of previously forested land, with feed crops covering a large part of the remainder (Steinfeld et al., 2006).

However, replacing a part of conventional meat with edible insects minimise the unlimited harvesting from nature and reduce enormous pressure on wild populations. The production of edible insects would need to shift towards rearing either at the cottage-scale level or in large industrial units (Van Itterbeeck and van Huis, 2012). In the past, edible insects were ostensibly an unlimited resource derived from nature (van Huis et al., 2013).

Nevertheless, most edible insect species are currently in jeopardy due to pollution, overharvesting and habitat degradation. Furthermore, the distribution, ecology and availability of edible insects will likely be affected by climate change in ways that are still relatively unknown (van Huis et al., 2013). For centuries, many insects have been a cherished source of protein for both food and feed across continents other than Europe.

Insects have the potential to be effectively utilised as a natural ingredient in high-protein feed (van Huis et al., 2013). Jobs and improved livelihoods can be achieved by insect gathering and farming as mini-livestock at the household level or industrial scale. In

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developing countries, some of the poorest members of society, particularly women and landless dwellers can easily become involved in the gathering, rearing, processing and sale of insects. This can directly improve their diets and create cash income through the sale of surplus products as street foods.

In this chapter, the potential rearing techniques/protocols that can be employed for mass rearing of some major insects for food and feed were investigated. Research and experience have demonstrated that it is possible to simulate and influence the production of edible insect species. This will promote year-round availability of selected edible insect species through semi or full production.The following experiments were intended to develop a medium scale production system for black soldier fly (H. illucens), house fly, M. domestica and the palm weevil larva, R. phoenicis in the rural conditions of

Ghana.

5.2 MATERIALS AND METHODS

5.2.1 Production of larvae (maggots) of the black soldier fly, H. illucens

These experiments were conducted to produce black soldier fly larvae for poultry feeding trials. Details of the feeding trials are addressed in the next chapter.

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5.2.1.1 Evaluation of organic wastes

Some common organic wastes were tested to identify the most suitable substrate(s) for successful rearing of the black soldier fly. These were:

1. Chicken manure

2. Manure of small ruminants (goats and sheep) + fish offal from the market

3. Manure of small ruminants + ruminant blood from the abattoir

4. Chicken manure + brewery waste and yeast

5. Brewery waste + Dry fish feed factory waste + Brewery waste yeast + water

About 5 kg of the above substrates were inoculated with 0.05 - 0.21 g of BSF eggs. These were allowed to hatch and grow for two weeks. The larvae (prepupae) were then harvested and for the total number of larvae, larvae weight, purge weight of larvae and the dry weight of larvae were recorded. The purge weight refers to the weight of the larvae after they empty their guts. This was achieved by putting the freshly harvested larvae in dry saw dust for 12 h. These trials were done at a facility owned by Fish for

Africa and located at Ashaiman in the Greater Accra Region of Ghana. At the end of the trial, the most suitable substrate was Brewery waste + Dry fish feed factory waste +

Brewery waste yeast + water, hence, that combination was used throughout the research.

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5.2.1.2 Mass rearing larvae of of the black soldier fly

Adults of BSF were obtained by placing chicken manure covered with banana leaves in the open for two days. As adults visit to eat and oviposit, they were trapped with a sweep net and transferred to cages (Figure 5.1). The cage measuring 80 x 80 x150 cm was made of a metallic frame covered with a small mesh net (mosquito net). Each cage was mounted on a wooden table to prevent predators from invading the set-up.

Figure 5.1: A sketch of the cage used in rearing the adult BSF (Courtesy, G.M. Vergara)

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During the night and on rainy days, the cages were kept in a building roofed with transparent plastic sheets (to allow more sunlight) and they were often carried outside to receive direct sunlight. Temperature and relative humidity were not controlled and so depended on the weather. Five thousand adults were stocked at a time in a cage and they did not require any food; only water was provided using a water reservoir, which delivered water on an absorbent paper and water drops were sprayed every 30 min.

The oviposition sites were made of an odourous substrate (usually brewery solid wastes/pito mash or moist poultry manure) placed on a bowl, covered with cardboard strips and dried banana leaves. In general, females prefer laying eggs in dry small crevices. For this reason, pieces of cardboard were placed inside the cage for the purpose of oviposition. The eggs were collected from the oviposition sites every two days. Masses of eggs were weighed and transferred into small plastic containers (approximately 0.15 -

0.2 mg eggs per container) for 5 to 7 days duration for eggs to hatch.

After hatching, the small larvae were transferred into culture boxes (45 cm x 76 cm x 16 cm) prepared with a mixture of 3 kg moist spent grain (brewery solid waste) + 2 kg dry fish feed factory waste + 0.5 L yeast (liquid) + 4.5 L water. About 5,000 to 6,500 larvae were fed on this mixture for 6 to 7 days (feed is considered ad libitum to allow a maximized growth). All along the growth period, the boxes are covered with a nylon net

(plastic netting used for windows in Ghanaian homes) held by an elastic band to prevent oviposition by other flies.

Larvae were harvested (separated) from the substrate directly by hand collection. In each box, the substrate was pushed to one side of the box and left for a few minutes; the larvae

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were then easily harvested (collected) at the bottom of the box where they had migrated.

The substrate was removed progressively to allow for larvae migration and easier collection. About 800 g fresh weight larvae were collected on average per box. The larvae were then divided into two, a large portion representing about 80% to 90% of the harvest and a small portion representing 20% or 10%. The large portion was what was processed into dried larvae for protein whereas, the small portion was allowed to pupate and emerge into adults to continue the whole process.

The large portion larvae were washed with water and placed in buckets containing sawdust overnight to empty their guts. They were dried in a gas oven for 2 hours or by sun-drying for 2 to 4 days depending on the availability of sunshine.

When the retained larvae (larvae intended to continue the cycle) had reached the prepupae stage (defined by the change of the coluor from white/cream to brown), they were transferred into another container containing sawdust, and kept there till they had turned into imagos. The adults were put into a cage to lay eggs to continue the cycle.

Within a cohort or batch of production (i.e. larvae produced from the same batch of eggs) one or two boxes were not harvested in order to get new pupae to repopulate the cages.

Pupae were usually kept in a small plastic cage awaiting emergence of adults so as to protect them against parasitoids. Adults were transferred into the large cages when they emerged (Devic et al., 2014).

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5.2.3 Production of oil palm and raffia weevil

5.2.3.1 Source of adults

Adult palm weevils were harvested from dead palm trees that were producing palm wine in the wild. This was achieved through the help of palm wine tappers who do not use chemicals but rather use fire to burn the area of incision in the felled trees. Bucket traps baited with a pheromone (Rynchophol) manufactured by ChemTica, Costa Rica were also installed in oil palm fields to trap adults. The effectiveness of the pheromone was greatly enhanced by the use of fermented fruit. The traps were inspected three times a week to collect adult weevils. Typically, five pairs of wild adult weevils were needed to inoculate a bucket with a sufficient quantity of fertilized eggs.

Male and female palm weevils were placed in a plastic bowl/bucket containg palm yolk

(inner core of the palm tree) and sugar solution to feed and mate. Plate 5.1 shows the process of preparing a holding container for mating. Adults were put in round plastic containers.

Plate 5.1: Sample of containers (bowl/bucket) used for rearing the PWL

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5.2.3.2 Sex determination

The adults were sexed based on description provided by Tanyi-Tambe et al. (2013). The males were separated from the females using the presence of hairs in a row on the central antero-dorsal end of the rostrum and at the distal segments of the forelimbs. Also the two sexes can be differentiated by the presence or absence of the tibial spur, which is large and modified in the males but absent in the female (Tanyi-Tambe et al., 2013) (Plate 5.2).

Males produce aggregation pheromone which attracts both sexes.

Plate 5.2: Adult Palm Weevils (in both pictures, females are on the right and males on the left)

5.2.3.3 Preparation of feed for the weevils

The inner core of raffia and palm trees herein called ‘yolk’ were collected and either mechanically shredded or coarsely chopped into small pieces. The yolk (5 kg) was soaked separately for raffia and oil palm liberally in a basin or large vat (Plate 5.3)

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containing water. After three days, water was drained from the yolk (Plate 5.4) and allowed to stand for 2 hours to drain excess water prior to using it for adult inoculation.

Adult weevils either collected from infested palms in the wild or previously bred were used to inoculate containers containing about 5 kg of raffia and/or palm yolk. About 100 g of sugar was added to serve as nourishment for the adults. This also promotes egg- laying.

Plate 5.3: Palm yolk soaked in a Plate 5.4: Palm yolk in container ready for container adult inoculation

Three pairs of adults were introduced to the 5 kg of yolk in the containers. Eggs were laid within 3-5 days after mating. More quantities (about 3 kg) of raffia and palm yolk slices soaked in water were washed and added to the containers containing the newly hatched larvae. After four to five weeks, larvae weighing about 6 to 10 g were matured for consumption or sale. If they are not harvested at this time, they weave cocoons using the

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long palm fibres (Plate 5.5). Cocoons stay for three to four weeks and emerge as sexually active adults. The adults were harvested and used for inoculating fresh substrates to continue the cycle.

Plate 5.5: PWL on feed Plate 5.6: Container showing long palm fibres

Once adults were added into new containers, a wire mesh was used to cover the containers (Plate 5.6). This was done to prevent adult weevils from flying away. Adults may be allowed to continuously lay eggs in a particular container until death.

5.2.4 Mass rearing of the house fly, M. domestica (Linnaeus) larvae (maggots)

The method for rearing the house fly maggots was adopted from works done by Gabriella

M. Vergara, Devic Emile and myself at Fish for Africa in Ashaiman, Accra. Two formulations were developed for sustainable rearing of the maggots.

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These are:

2 kg Chicken manure (CM) + 2 kg Fish feed waste (FFW) + 3-5 LWater (W)

3 kg Brewery waste (BW) + 1 kg Chicken manure (CM) + 1 kg Yeast (Y) + 1 LWater

(W)

The adult house flies were placed in a cage (Figure 5.1) and fed on milk powder and sugar in a ratio of 2:1. Water was also provided using a drinking glass inverted on a plate

(as drinking trough) to avoid drowning of the adult flies. An ordourous material

(fermented pito mash or pig manure) was then placed in a bowl to enable them lay eggs.

The eggs were collected daily, weighed and placed in a metallic box containing any of the above two formulations. About 2 g of eggs were put in each box which hatched and grew into larvae (maggots) which were eventually harvested within four days. The flow chart shown in Figure 5.2 summarises the entire process of the maggot production.

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Figure 5.2: A flow chart showing house fly maggot production (By Vergara Gabriella and Jacob Anankware).

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5.2.5 Statistical Analysis

Analysis of variance was conducted on the data collected using GenStat Discovery

Edition Version 12, 2012 and LSD was used to separate the means that were found to be significant at the 5% significance level. For the BSF larval substrate, covariate analysis was done with the egg weight being the covariate and the other parameters (number of larvae, purge weight and dry weight of larvae) being the variates.

5.3 RESULTS

After several trials, it was observed that the best yield for BSFL could be obtained from 3 kg moist spent grain (brewery waste) + 2 kg dry fish feed factory waste + 0.5 litre yeast

(liquid) + 4.5 litres of water. This combination (formulation) was adopted for the mass rearing of the Black Soldier Fly larvae (BSFL). The performance of BSF larvae on various substrates is presented in Table 5.1. Treatment 5 (Brewery waste + Dry fish feed factory waste + Brewery waste yeast + water) recorded the highest number of BSF larvae

(6106) which was significantly (p < 0.05) different from the other substrates used. The least number of larvae (3105) was recorded on substrate 3 (Manure of small ruminants + ruminant blood from the abattoir). The weight of the BSF larvae also showed significant

(p < 0.05) differences. Larvae in Treatments 5 (Brewery waste + Dry fish feed factory waste + Brewery waste yeast + water) and 2 (Manure of small ruminants + fish offal from the market) which were statistically (p > 0.05) not different, were both statistically

(p < 0.05) superior to the other substrates. The purge weight of the larvae for Treatments

5 and 1 (Chicken manure containing straw) were significantly (p < 0.05) better than

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Treatments 2, 3 and 4 (Chicken manure + brewery waste and yeast) which were similar

(p > 0.05). Consistently, the dry weight of the larvae showed the same trend of results as the number of larvae per treatment. Treatments 1 (Chicken manure containing straw) and

5 (Brewery waste + Dry fish feed factory waste + Brewery waste yeast + water) were relatively better (p < 0.05) than the other substrates.

Figure 5.3 gives the life cycle of the BSF and summarises the rearing procedure.

Adult BSF Harvesting BSF eggs

Sorting parasitised BSF larvae BSF pupae

BSF pupae

Figure 5.3: Steps involved in rearing the adult BSF, larvae and pupae

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Table 5.1: Performance of BSF larvae reared on different substrates.

Parameters Larval Type of Total number of Larval Purge Larval Dry substrate larvae weight (g) weight (g) weight (g)

1 3194b 623b 733a 246a

2 3606b 649a 702 b 215 b

3 3105b 549b 595b 161b

4 3406b 557b 631b 192b

5 6106a 859a 957a 445a

Lsd 1413.3 226.9 231.2 200.7

P-value 0.002 0.044 0.025 0.047

Means in the same column with different alphabets are significantly (p < 0.05) different.

Substrates:

1 = Chicken manure (containing straw) 2 = Manure of small ruminants + fish offal from the market 3 = Manure of small ruminants + ruminant blood from the abattoir 4 = Chicken manure + brewery waste and yeast 5 = Brewery waste + Dry fish feed factory waste + Brewery waste yeast + water

5.4 DISCUSSION

Insect rearing presents a sustainable way for people especially those who do not have access to land to produce animals for protein and improve their nutritional status.

According to Afton Halloran, a consultant for the FAO Edible Insects Programme,

“Domesticating and rearing insects can help sustain insect populations while also helping

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counter nutritional insecurity and improve livelihoods,” He further posited that “Farming insects has a huge global potential for both animal feed and food production. We are already seeing producers create animal feed from insects and research and such development is occurring around the world in order to incorporate insects into menus and processed foods.”

The Black soldier fly model described in this research can be used to breakdown household organic wastes as well as metropolitan wastes which pose a serious health concern in Ghana. The findings of the present study are in tandem with the results of Devic et al.

(2014) who collected chicken manure from several farms in Ashaiman, Adjei-Kojo, the

University of Ghana poultry farms and several places to rear BSFL after which the richly decomposed-manure was used as biofertilizer to nourish onion farms. The superiorty of substrate 5 (Brewery waste + Dry fish feed factory waste + Brewery waste yeast + water) over the rest was probably due to the addition of the fish feed waste which made it more palatable and nutritious. Unfortunately, people who do not have access to fish feed waste can not use this substrate for larval production. It is only available to those living close to feed producing factories. In view of this, substrate 1 (Chicken manure containing straw) is the most ideal since it is readily available, almost free and comes close to substrate 5 in terms of the dry weight of the larvae. Farmers in Ghana and other African countries who spend huge sums of money to import protein for the fish and poultry industries can use these methodologies to sustainably rear insects for protein. This will greatly reduce their budgetary allocations for feed resulting in improved livelihoods. This will also create jobs in rural areas and reduce or mitigate the rural-urban migration and the exodus of the

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working class in Africa to seek non-existent jobs abroad. Apart from the nutritional value, other benefits of insects include their potential effect on the environment and in addressing the rapidly increasing demand for food worldwide.

While the idea of eating a worm, grasshopper or cicada at every meal may seem strange,

FAO (2013) maintains that this has many health benefits. Insects are high in protein, fat and mineral contents and can be eaten whole or ground into a powder or paste, and incorporated into other foods.

At the Forests for Food Security and Nutrition conference at the FAO headquarters in

Rome in 2013, it was agreed that, farming insects for human and animal consumption is particularly relevant at a time when population growth, urbanization, and the rising middle class have increased the demand for food in the midst of the increasing harm to the environment.

In conclusion, mass rearing protocols have been successfully developed for selected edible insect species. This will enhance the all-year-round availability of these insects.

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CHAPTER SIX

POTENTIAL OF BLACK SOLDIER FLY, H. illuscens AS A REPLACEMENT FOR FISH/SOYBEAN MEAL IN THE DIET OF BROILERS

6.1 INTRODUCTION

The high rate of increase in the world population has made advances in agricultural technology imperative. Dairy, poultry, livestock and fish are the main sources of animal protein for human nourishment. It is therefore, important that the animals and fishes are properly reared with complete diets formulated by the combination of essential nutrients in the right proportions (AIFP, 2004). It is well known that maggots, which appear during the biological treatment of chicken droppings, improve the growth rate of broiler chicken

(Awonyini et al., 2003). The pollution problems caused by livestock effluent, and the mass accumulation of poultry waste, could be solved by using chicken droppings as a growth medium for certain living organisms, including house flies (M. domestica L.)

(Boushy, 1991) as the resulting maggots offer a high protein feed for poultry and fish

(Zuidhof et al., 2003; Ogunji et al., 2007).

Poultry keeping, according to Abbey et al. (2008), is still an economically viable occupation for many Ghanaians. However, the cost of poultry production keeps rising due to the high cost of feedstuffs. This has stimulated interest in the development of non-conventional feeds (Adejuyitan, 2011) which may increase the profitability of farmers. The cost of feed constitutes up to 70% of the cost of producing broilers (The

Poultry Site, 2007) and this makes broiler production too expensive for many farmers in

Ghana. Alternatives to conventional feed ingredients used in formulating broiler feed will help reduce the cost of production and boost local chicken production.

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Maggot meal has been reported to be a possible alternative to the expensive protein sources (Sheppard, 2002; Ogunji et al., 2006; 2007). Calvert et al. (1971) suggested the use of maggots as a replacement for some key ingredients in feeds and this was further corroborated by Teotia and Miller (1974). It has good nutritional value, cheaper and less tedious to produce than other animal protein sources. It is also produced from wastes, which otherwise would constitute an environmental nuisance. According to Hwangbo et al. (2009), dried maggots and pupae contain 56.9 and 60.7% crude protein and 20.9 and

19.2% crude fat, respectively. They have protein and amino acid compositions similar to fish meal and can replace 7% of the fish meal in broiler chicken feed (Hwangbo et al.,

2009). Some earlier studies are available on the utilisation of maggots as poultry feed supplement (Onifade et al., 2001).

However, the efficacy of the black soldier fly meal in broiler chicken production is still debatable. In particular, the efficiency of black soldier fly larvae (BSFL) on broiler growth performance is still unknown in terms of carcass characteristics and the success of reaching market weight. Therefore, the objective of this study was to evaluate the use of black soldier fly meal as a replacement for fish/soybean meal in the diets of broiler chickens in Ghana.

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6.2 MATERIALS AND METHODS

The study was conducted at the Poultry Section of the Department of Animal Science,

Faculty of Agriculture of the Kwame Nkrumah University of Scienceand Technology

(KNUST), Kumasi spanning eight weeks (February-April, 2015).

6.2.1 Source (s) of black soldier fly larvae (BSFL)

The BSFL were obtained from a specially prepared unit for the growing of the BSFL using the method of Devic et al. (2014). The method described in Chapter 5 was employed in rearing enough BSFL for this experiment. Plate 6.1 shows the cage used in rearing the adult BSF.

Plate 6.1: Rearing cage for black soldier fly

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6.2.2 Experimental diets

Three experimental diets for both starter and finisher phases of broilers were formulated as outlined in Tables 6.1 and 6.2. In the experimental diets, BSFL replaced fish meal and soybean meal in Treatment 1 (T1) and Treatment 2 (T2), respectively whilst all other components of the diet remained same in all the treatments. This is the first time such an experiment was conducted and so there was no existing benchmark to use for the levels of BSFL to be included in the diets. Hence, the ratios of fish meal and soybean meal in conventional feed were simply replaced by the BSFL.

Table 6.1: Per cent ingredients in starter diet used to raise broiler birds

Starter diet % in Formulation Item (%) T0 (Control) T1 T2 Maize 56 56 56 Fishmeal 12 0 12 Soybean meal 15 15 0 Wheat bran 15 15 15 BSF Prepupae 0 12 15 Oyster shell 1.25 1.25 1.25 Premix 0.50 0.50 0.50 Salt 0.25 0.25 0.25 Total (%) 100 100 100

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Table 6.2: Per cent ingredients in grower-finisher diet used to raise broiler birds

Grower-finisher diet % of Formulation Item (%) T0 (Control) T1 T2 Maize 60 60 60 Fishmeal 10 0 10 Soybean meal 13 13 0 Wheat bran 15 15 15 BSF Prepupae 0 10 13 Oyster shell 1.25 1.25 1.25 Premix 0.50 0.50 0.50 Salt 0.25 0.25 0.25 Total (%) 100 100 100

6.2.3 Experimental birds and design

Two hundred unsexed day old Cobb-500 commercial strains of broiler chickens were used for the study. The chicks were obtained from Akate farms, a commercial hatchery located in Kumasi, Ghana and reared in a common brooder house for the first 28 days (0-

4 weeks). One hundred watt electric bulbs were used to provide continuous light and heat during the brooding stage. One hundred and eighty birds were selected and randomly assigned to the three treatments with four replicates in a completely randomised design.

From the first day of the experiment, birds were grouped into 15 birds per replicate for the three treatments.

The birds were raised in a deep litter house partitioned into 12 pens measuring 1.82 m x

1.75 m x 0.75 m giving a floor space of 0.20 m2 per bird. The pens were thoroughly cleaned and washed with disinfectant before the start of the experiment. Wood shavings were spread on the floor to about 5 cm depth to provide litter for the birds.

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6.2.4 Management of birds

Feed and water were offered ad libitum because the experiment did not require any form of restricted feeding. Routine and periodic management practices such as vaccination, drug administration and maintenance of cleanliness within and outside the poultry pens were carried out. Birds were vaccinated against Gumboro and Newcastle diseases and medication for Coccidiosis was provided at three days of age and again at 21 days using

Sulfadimidine Sodium 33% (Bremer Pharma GMBH, Germany) via the drinking water.

Besides, all necessary biosecurity measures (Traffic control, sanitation and culling of sick birds) aimed at preventing diseases were put in place during the experiment. Furthermore, the international protocols on the use of animals for experiments were followed using the

Institutional Animal Care and Use Committees Guidebook (IACUC, 2002).

6.2.5 Data collection

Among the parameters of interest in the present study were daily feed intake, total feed intake, water intake, live weight gain, mortality and blood metabolite profile. At the end of the feeding study, a sample of the birds (5 males and 5 females) were slaughtered and carcass parameters taken. The carcass parameters included: live weight, bled weight, defeathered weight, heart, liver, shank, head, neck, gizzard, full intestine, empty intestine, abdominal fat and dressed weights. Feed conversion efficiency was also determined.

Proximate analysis of BSFL was carried out at the Nutrition laboratory, Department of

Animal Science of KNUST, Kumasi and repeated at the International Centre for Insect

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Ecology and Physiology (ICIPE) in Nairobi, Kenya. The metabolisable energy (ME) of

BSFL was determined using the equation of NRC (1994): ME (kcal/kg) = (35 x %CP) +

(85 x %SM) + (35 x %NFE).

6.2.6 Statistical Analysis

Analysis of variance was conducted on the data collected using GenStat Discovery

Edition Version 12, 2012 and Tukey was used to separate the means that were found to be significant at the 5% significance level.

6.3 RESULTS

6.3.1 Proximate composition of feed

The chemical composition of BSFL, Fish meal and Soybean meal is shown in Table 6.3.

BSFL had the highest crude protein (44.82%), followed by T0 (Fish+Soy) (22.61), T2

(BSFL+Fish) (21.53) and the least being T1 (BSFL+Soy) (20.76). In terms of crude fat,

BSFL had the highest value (18.03%) followed by T2 (BSFL+Fish), T1 (BSFL+Soy) and

T0 (Fish+Soy) with 7.56%, 5.94% and 5.45%, respectively.

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Table 6.3: Chemical composition of BSF, fish meal and soybean meal

Sample Dry Ash* Crude Crude NDF* ADF* Energy matter [%] protein* fat* [%] [%] (Kcal/g) [g/g] [%] [%] BSFL 0.92 17.71 44.82 18.03 39.94 15.57 - BSFL+Fish 0.87 10.92 21.53 7.56 59.74 10.41 331.43 BSFL+Soy 0.87 7.67 20.76 5.94 43.21 10.37 332.97 Fish+Soy 0.87 14.32 22.61 5.45 43.75 8.13 327.42

6.3.2 Effect of BSFL on growth performance of birds

Table 6.4 presents the effect of BSFL formulated meal on the growth performance of the birds. The highest feed intake was recorded for T2 (BSFL+ Fish) (5.72 kg) and the control group had the highest water intake (12.15 l). Total feed intake, daily feed intake, daily water intake and total water intake followed the same trend. Treatment T0 (control) and T2 (BSFL+Fish) were significantly (p < 0.05) better than T1 (BSFL+Soy) in terms of the above parameters. In terms of total weight gain and final weight, T2 (BSFL+Fish) was superior (p < 0.05) to T1 (BSFL+Soy) but statistically (p > 0.05) similar to the control. However, there were no significant (p > 0.05) differences between the treatments with respect to feed conversion ratio (FCR) and mortality rate (Table 6.4).

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Table 6.4: Growth of broiler chicken fed on diets containing different oncentrations of black soldier fly larvae.

Growth performance indices of the birds

Daily Total Initial Daily Total Final Daily Water Mortality feed feed weight weight weight weight F.C.R.* Water Intake (%) intake intake (kg) gain gain (kg) Intake (l) Treatments (kg) (kg) (kg) (kg) (l)

To 0.101a 5.63a 0.51a 0.031ab 1.70ab 2.35ab 3.41a 0.215a 12.15a 11.7a

T1 0.084b 4.72b 0.66a 0.024b 1.32b 1.98b 3.60a 0.18b 10.08b 5.0a

T2 0.103a 5.72a 0.64a 0.037a 2.07a 2.71a 2.78a 0.208a 11.66a 1.7a

SEM 0.002 0.12 0.089 0.002 0.1 0.098 0.25 0.003 0.13 4.19

P-value 0.001 0.001 0.483 0.002 0.002 0.002 0.111 0.001 0.001 0.279

Values in the same column with different alphabets are significantly (p<0.05) different. *F.C.R. = Feed conversion ratio; SEM= Standard Error of Means; T0 (Control), T1 (BSFL+Soy), T2 (BSFL+Fish)

6.3.3 Effect of BSFL on carcass parameters of birds

There were significant (p < 0.05) differences between treatments in all carcass parameters measured except for empty intestine and abdominal fat weights (Tables 6.5a and 6.5b).

Consistently, values for T1 (BSFL+Soy) were significantly (p<0.05) smaller than T0

(control) and T2 (BSFL+Fish) for liveweight, bled weight, defeathered weight, liver weight, head weight, neck weight, full and empty gizzard weights and dressed weight.

Statistically, T2 (BSFL+Fish) was better (p < 0.05) than T1 (BSFL+Soy) for heart weight

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and liver weight. For full intestine weight, the control (T0) was statistically (p < 0.05) superior to T2 (BSFL+Fish) (Tables 6.5a and 6.5b).

Table 6.5a: Carcass parameters of broiler chicken fed on diets containing different concentrations of black soldier fly larvae.

Carcass Parameters (g) Live Bled Defeathered Heart Liver Shank Head Diets weight weight weight weight weight weight weight

T0 3002a 2930a 2840a 11.25ab 66.5a 104.88ab 67.13a

T1 2290b 2230b 2100b 9.75b 44.5b 94.38b 51.25b

T2 3100a 3000a 2820a 12.75a 69.13a 113.13a 67.63a

SEM 740.0 680.0 630.0 0.85 4.67 4.87 2.00

P-value 0.0001 0.0001 0.0001 0.0669 0.0019 0.0414 0.0001

Values in the same column with different alphabets are significantly (p < 0.05) different. * SEM= Standard Error of Means; T0 (Control), T1 (BSFL+Soy), T2 (BSFL+Fish)

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Table 6.5b: Carcass parameters of broiler chicken fed diets containing different concentrations of black soldier fly larvae.

Carcass Parameters (g) Full Empty Full Empty Experiment Neck gizzard gizzard intestines intestines Abdominal Dressed diets weight weight weight weight weight fat weight weight

T0 162.38a 68.25a 45.38a 143.25a 81.88a 35.13a 2430a

T1 143.38b 48.13b 34.13b 117.13ab 77.88a 45.13a 1670b

T2 168.3a 62.38a 45.88a 123.88b 71.88a 41.32a 2360a

SEM 5.34 2.53 1.66 7.67 5.58 3.73 680.00

P-value 0.0096 0.0001 0.0001 0.0065 0.4563 0.1849 0.0001

Values in the same column with different alphabets are significantly (p < 0.05) different. * SEM= Standard Error of Means; T0 (Control), T1 (BSFL+Soy), T2 (BSFL+Fish)

6.3.4 Effect of BSFL on primal cuts of birds

Wing, breast and thigh weights were significantly (p < 0.05) influenced by BSFL but not for drumstick, and back weights (Table 6.6). Birds fed with T1 (BSFL+Soy) had relatively lower (p < 0.05) wings compared to those fed with T2 (BSFL+Fish). With respect to thigh and breast weights, T1 (BSFL+Soy) was statistically (p < 0.05) lower than the control and T2 (BSFL+Fish) which were similar.

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Table 6.6: Primal cuts of broiler chicken fed diets containing different concentrations of black soldier fly larvae

Dietary Primal cuts/bird (g) Treatments Wings Thighs Drumsticks Back Breast

T0 264ab 323a 345a 508a 809a

T1 181b 204.5b 275a 348.5a 491.5b

T2 270a 313a 354a 429.5a 708a

SEM 19 16.83 40.12 41.72 76.1

P-value 0.0761 0.0268 0.423 0.157 0.1237

Values in the same column with different alphabets are significantly (p<0.05) different. * SEM= Standard Error of Means; T0 (Control), T1 (BSFL+Soy), T2 (BSFL+Fish)

6.3.5 Effect of BSFL on haematology of birds

Values recorded for haematology were not significantly (p > 0.05) different between treatments except for white blood cells (WBC) and mean cell volume (MCV) (Table

6.7a). For WBC, BSF larvae-supplemented treatments (T1 and T2) were significantly (p

< 0.05) lower than the control (T0) and in terms of MCV, T1 (BSFL+Soy) was significantly (p < 0.05) higher than the control (Table 6.7a).

The mean levels of absolute content of lymphocytes showed that, the highest value was recorded in the control with 211437.500 ul. Significant differences were recorded between the treatments with respect to the absolute content of platelets (Table6.7b). The

T1 (BSF+Soy) was significantly (p<0.05) lower than the control and T2 (BSFL+Fish)

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which had the highest value for relative distribution width, RDWcv (%). The mean values of the other indices measured were not significantly (p > 0.05) different.

Table 6.7a: Haematology of broiler chicken fed diets containing different concentrations of black soldier fly larvae

Haematological indices MCH MCHC MCV RBC WBC Diets HCT (%) Hb (g/dl) (pg) (g/dl) (fl) (x109/l) (x109/l)

T0 31.6a 10.9a 40.5a 32.24 a 125.5b 1.90a 2.59a

T1 30.92a 9.86a 42.14a 31.89a 132.19a 2.35a 2.32b

T2 30.66a 9.65a 40.93a 31.45a 129.98ab 2.37a 2.29b

SEM 0.96 0.32 0.68 0.28 1.63 0.24 0.064

P-value 0.7761 0.493 0.2294 0.1642 0.0267 0.031 0.0076

Values in the same column with different alphabets are significantly (p < 0.05) different.

HCT=Haematocrit, Hb=Haemoglobin, MCH=Mean cell haemoglobin, MCHC=Mean cell haemoglobin concentration, MCV=Mean cell volume, RBC=Red blood cells, WBC=White blood cell, pg=pictogram, g/ld=gram per decilitre, l=litre, fl=Femtolitre, %=percentage.

* SEM= Standard Error of Means; T0 (Control), T1 (BSFL+Soy), T2 (BSFL+Fish)

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Table 6.7b: Haematology of broiler chicken fed diets containing different concentrations of black soldier fly larvae.

Haematological indices Diets PLT LYM MXD NEUT RDWc MXD NEUT (ul) (%) (%) (%) v (%) LYM (ul) (ul) (ul)

T0 1875a 78.91a 16.71a 4.13a 16.19a 211437.5a 43325a 10725a

T1 2500a 74.81a 20.46a 4.73a 13.96b 172887.5b 47875a 11100a

T2 1000a 75.0a 19.91a 5.09a 17.55a 170987.5b 45900a 11912.5a

SEM 490.2 2.31 1.74 0.81 0.65 8571.7 4703 2071.1

P-value 0.0868 0.3833 0.2804 0.6992 0.003 0.0044 0.7923 0.918

Values in the same column with different alphabets are significantly (p < 0.05) different.

PLT (ul) = Platelets, LYM (%) = relative (%) content of lymphocytes, LYM (ul) = the absolute content of lymphocytes, MXD (%) = relative (%) content of mixture, MXD (ul) = the absolute content of the mixture, NEUT (%) = relative (%) content of neutrophils, NEUT (ul) = the absolute content of neutrophils, RDWcv (%) = the relative distribution width of red blood cells by volume, coefficient of variation.

* SEM= Standard Error of Means; T0 (Control), T1 (BSFL+Soy), T2 (BSFL+Fish)

6.4 DISCUSSION

The crude protein of BSFL was the highest and T1 (BSFL+Soy) the lowest. The crude protein of BSFL as recorded per the analysis was higher than dried black soldier fly meal

(42% crude protein and 35% fat) recorded by Newton et al. (1977). The differences may be attributed to the differences in the diets of the maggots. However, the crude protein value (44.817%) in this study compares favourably with the 45.2% reported by Hale

(1973). Dry matter and ash values for BSFL were greater than the other formulations.

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This differs from the findings of Newton et al. (1977) who reported that the dry matter and ash values for soybean were significantly (p < 0.05) higher than the larval diet.

The highest feed intake was recorded from T2 (BSFL+ Fish) and the control recorded the highest water intake. The high feed intake might be due to the increased acceptability of the BSFL and the fish meal. Generally, there is a high correlation between feed intake and water intake. So it was surprising that, the highest feed intake was recorded from T2

(BSFL+Fish) whilst the highest water intake was recorded in the control. From metabolic point of view, the fibre, proteins and fatty acids in the control enhanced water intake by the birds compared to the T2 (BSFL+Fish). Also, the components of the control T0

(Fish+Soy) tend to be denser than the T2 (BSFL+Fish) hence, the increased water intake

(Lott et al., 2003). In terms of total weight gain and final weight, T2 (BSFL+Fish) was superior to T1 (BSFL+Soy) but statistically similar to the control. The findings of this study corroborate the findings of other researchers. For instance, Pretorious (2011) reported that house fly larvae meal supplementation in a three-phase feeding system significantly increased average broiler total feed intake, cumulative feed intake, and average daily gain when compared with commercial corn-soy oil cake meal diet.

Hwangbo et al. (2009) performed studies using diets containing 5, 10, 15, or 20% maggots fed to broilers, to determine their effects on growth performance and carcass quality. The results showed that feeding diets containing 10 to 15% maggots improved carcass quality and growth of broiler chickens. Atteh and Ologbenla (1993) and

Bamgbose (1999) concluded that inclusion rates greater than 10% in the diet of broilers decreased intake and performance, perhaps due to the darker colour of the meal, which may be less appealing to chickens.

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Consistently, T1 (BSFL+Soy) produced significantly lower livebird weight, bled weight, defeathered weight, liver weight, head weight, neck weight, full and empty gizzard weights and dressed weight than T0 (control) and T2 (BSFL+Fish). The effect of maggot meal on carcass characteristics of broiler chickens was reported by Teguia et al. (2002).

They observed that broilers fed maggot meal diets had carcass quality that were similar to the control, and the liver and gizzard increased in size, but no signs of toxicity were observed. Indeed, none of the numerous studies on maggots as animal feed has revealed any health problems (Sheppard and Newton, 1999). In feeding broilers, nutritional factors such as the protein and energy content of feed can greatly affect carcass characteristics and fat accumulation (Leenstra, 1989). The T1 (BSF+Soy) had poor carcass characteristics because it had the least protein, fat and energy contents.

Wing, breast and thigh weights were influenced by BSFL meal but not for drumstick, and back weights. Birds fed with T1 (BSFL+Soy) had relatively lower wings compared to those fed with T2 (BSFL+Fish). With respect to thigh and breast weights, T1 (BSF+Soy) was lower than the control and T2 (BSFL+Fish), both of which were similar. This might be attributable to the poor nutritional composition of T1 (BSFL+Soy). However, Awoniyi et al. (2003) observed that maggot meal supplementation had no significant influence on dressing percentage and breast muscle weights. Besides, Hwangbo et al. (2009) reported that birds from the groups that received maggot supplementation showed significantly higher dressing percentage, breast muscle, and thigh muscle (presented as a ratio to carcass weight) than the control group. The observed discrepancies between this work and that of the Awoniyi et al. (2003) and Hwangbo et al. (2009) may be due to the fact

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that, whereas they did partial replacement (supplemented the feeds), this study had total replacement of soy in one treatment and fishmeal in the other.

All the haematological parameters measured fell within the normal physiological ranges of haematological components of broilers. Similar results were reported by Aeangwanich et al. (2004). The mean levels of absolute content of lymphocytes was highest in the control. This probably improved the immune system of birds fed this meal since lymphocytes determine the specificity of the immune response to infectious microorganisms and other foreign substances. This should have reduced mortalities in the birds fed on the control diet, but, the highest mortality was recorded in the control.

Black Soldier Flies (BSFs) are abundant in Ghana. These insects do not transmit diseases and so they do not pose any health threat to man as house flies do. These convenient converters of waste can also be employed in the sanitation industry to degrade municipal waste and at the same time generate cheap protein that can be used in the feed industries.

BSF larvae are capable of out-competing larvae of other flies and so could be wisely used to prevent the proliferation of other fly species in public wastes. BSFL that are reared on household wastes (fruits and leftover food) can also be consumed by man.

Furthermore, decomposed waste can serve as a rich organic manure for the production of vegetable and ornamental crops. The use of BSFL for decomposing waste will greatly reduce the eutrophication of nutrients and associated toxins into water bodies. BSFL can successfully be used as a replacement of soy and fish meal to reduce cost of poultry

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production. A major limitation of the study was the absence of palpability tests for meat from birds fed on the various diets. Future work should include palatability tests as well as the cost benefit analysis of the three treatments. It would also be useful to evaluate the effect of BSFL on layers.

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CHAPTER SEVEN

CONCLUSSIONS AND RECOMMENDATIONS

7.1 CONCLUSSIONS

Studies were done to determine which insects are consumed in Ghana and to ascertain social and environmental factors that affect entomophagy with a view to initiating a programme on their incorporation into human and poultry nutrition in Africa. The major findings were:

1. Nine species of major edible insects belonging to five orders were identified.

2. The nine edible insects in Ghana are: palm weevil (Rhyncophorus phoenicis

Fabricius) larvae, termites (Macrotermes bellicosus Smeathman), ground crickets

(Scapteriscus vicinus Scudder), field crickets (Gryllus similis Chapman), house

cricket (Acheta domesticus Linnaeus), grasshopper (Zonocerus variegatus

Linnaeus), locust (Locusta migratoria Linnaeus), shea tree caterpillar (Cirina

butyrospermi Vuillot) and scarab beetle (Phyllophaga nebulosa Harris) larvae.

3. Proportionally, the scarab beetle (2%), field cricket (5%), shea tree caterpillar

(8.7%), house cricket (9.5%) and the locust (10%) were the least consumed

insects whereas palm weevil larvae (47.2%), termites (45.9%), ground cricket

(33.3%) and grasshopper (30.5%) were the most consumed insects in Ghana.

4. The practice of entomophagy was more pronounced in rural than urban areas.

5. With the exception of the palm weevil, all the other edible insects are only

available from May to the end of the year.

6. There is a market for edible insects in all the ten regions of Ghana

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7. An entomophagical map of Ghana has been developed. This will help both

entomologists and consumers to easily know where to find each species.

8. Overall, entomophagy was found to be influenced by age, gender, education and

occupation. Ranking from the highest to the least association, the locality was

observed to have the most influence on entomophagy. Urbanisation to some

extent limited the practice of entomophagy in the study localities. The difference

in insect consumption between males and females was negligible. The study has

shown that gender has the least influence on entomophagy.

9. Entomophagy is practiced across all age groups and gender. Proportionally, 90,

78, 74% of the aged (60+), middle age (31-50) and the youth (18-30) were

observed to consume various edible insects, respectively.

10. Edible insects were generally harvested through hunting/trapping. Over 87% of

the survey respondents who consume edible insects reported of acquiring them

through hunting/trapping.

11. From the nutritional analysis, C. butyrospermi contained the highest amount of

crude protein as a percentage of dry matter (63%). The BSFL contained the

highest percentage of ash as a percentage of dry matter of 17 % with PWL having

the lowest percentage of ash of 1.376 %.

12. BSFL can completely replace soymeal and partially replace fish meal in fish feed.

13. BSFL in place of soy improves the live weight of fowls by 100 g more that even

fish+Soy combination. It also improves feed intake, wings and drumstick weight

and more importantly reduces mortality.

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14. The high levels of unsaturated fat and good saturated fat in PWL can help reduce

the risks of cardiovascular disease and cholesterol levels in man.

7.2 RECOMMENDATIONS

1. The Ministry of Education should consider including insect farming in the

educational curriculum of Agricultural and Vocational Training Institutions so as

to empower citizens with the requisite skills to sustainably farm insects and earn a

living.

2. Researchers, Scientists and the media should collaborate to curtail the bad

perceptions about insect consumption which make people shy away from

consuming insects.

3. The high desirable unsaturated fatty acid contents of C. butyrospermi makes it an

important food component for those who have high blood cholesterol content.

4. Future work should include palatability tests and cost benefit analysis of the three

treatments used in the feeding experiment. It would also be useful to evaluate the

effect of BSFL on layers.

5. Further work should also be done on the design of more efficient rearing and

harvesting techniques for insects since the methods described in this work are

rather laborious.

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APPENDIX 1: QUESTIONNAIRE USED FOR THE SURVEY

KWAME NKRUMAH UNIVERSITY OF SCIENCE AND TECHNOLOGY/ UNIVERSITY OF NAIROBI

FACULTIES OF AGRICULTURE AND SCIENCES

DEPARTMENT OF CROP AND SOIL SCIENCE AND THE DEPARTMENT OF BIOLOGICAL SCIENCE

EDIBLE INSECTS OF GHANA

This questionnaire has been prepared by a PhD Entomology student from the Kwame Nkrumah University of Science and Technology/ University of Nairobi. The focus of this questionnaire is to identify all edible insects in Ghana. Please, all information would be kept confidential, so feel free to provide accurate information.Thank you for your co- operation.

1. Gender Male [ ] Female [ ] 2. Age a.18- 25 [ ] b. 26- 30 [ ] c. 31- 40 [ ] d. 41- 50 [ ] e. 51- 60 [ ] f. 60+[ ] 3. Educational background No [ ] Primary [ ] JHS [ ] SHS [ ] Tertiary [ ] 4. Occupation ……………………………………………………………………… 5. What insects are available in this locality and which are consumed? Please tick appropriately using the table below: Insect Available in locality Consumed

a. Scarab beetle larva

b. Locust

c. Termite

d. Ant

e. Bee

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f. Shea tree aterpillar

g. Grasshopper

h. Palm weevil larva

i. House cricket

j. Ground cricket

k. Field cricket

l. Black Soldier Fly

6. Which communities consume these edible insect? (Tribe, ethnic) ...... 7. Which metamorphic (Developmental) stage is consumed? Egg [ ] Larvae [ ] Pupae [ ] Nymph [ ] Imago/adult [ ] 8. How do you get these insects? Rearing [ ] Buying [ ] Hunting/trapping [ ] 9. If hunting, a. How far do you go? ………………………………………………………………. b. Any difficulty encountered? ……………………………………………………… c. State .....…………………………………………………………………………

10. If rearing, a. What is the number of insects that can be harvested in a season? ...... b. What do the insects feed on? ...... c. How do you get their feed? ……………………………………………………. d. Any challenges faced? ...………………………………………………………. e. State ……………………………………………………………………………. f. Would you encourage anyone to go into this venture and why? ……………….

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......

11. If buying, a. How do you get these insects? b. What is the pricing of these insects? Low [ ] Moderate [ ] Expensive [ ] Specific cost GH¢………………………… c. Any difficulty encountered? ………………………………………………….. 12. Who are the main consumers? Children [ ] Adults [ ] Male [ ] Female [ ] 13. What is the purpose for rearing or hunting these insects? Source of protein [ ] Cultural practices [ ] Religious reasons [ Recreational purposes [ ]Medicinal value [ ] Aphrodisiac [ ] Any other, state…………………………………………………… 14. Apart from human consumption, what are other uses of these edible insects? ......

15. When are these insects available? Before rainy season [ ] During rainy season [ ] After rainy season [ ] 16. How do you process these insects before consumption? Frying [ ] Grilling [ ] Roasting [ ] Boiling [ ] Raw [ ] Any other, state …………………………………………………………… 17. How do you prefer eating these insects? Main meal [ ] snack [ ] dessert [ ] Any other, state ………………………………………………………….. 18. What are the local dishes containing edible insects? ………………………………….. a. Do you see the potential of edible insects as an alternative source of generating income? Yes [ ] No [ ] If Yes, how? ……………………………………………………………………… 19. Is there any challenge faced in eating these insects? Yes [ ] No [ ] 20. If yes, what is the challenge? ……………………………………………………… 21. How do you deal with this challenge? …………………………………………… 22. Does eating of these insects pose any health risk? Yes [ ] No [ ] 23. What type/kind disease is encountered? ……………………………………………….…………………………………… ………………………………………………………………………………………

24. Why have people stopped eating insects?

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APENDIX 2: ANOVA TABLES

Appendix 2.1: ANOVA Table: Daily_Weight_gain