The impact of cricket farming on rural livelihoods ... - GREEiNSECT

UNIVERSITY OF COPENHAGEN FACULTY OF SCIENCE

The impact of cricket farming on rural livelihoods, nutrition and the environment in Thailand and Kenya

PhD Thesis 2017 | Afton Marina Szasz Halloran

Title

The impact of cricket farming on rural livelihoods, nutrition and the environment in Thailand and Kenya

Author

Afton Marina Szasz Halloran, MSc

Department

Nutrition, Exercise and Sports, Faculty of Science, University of Copenhagen

Project

GREEiNSECT: Insects for Green Economy

Academic advisors

Associate Professor, Nanna Roos Department of Nutrition, Exercise and Sports, University of Copenhagen Associate Professor, Sander Bruun Department of Plant and Environmental Science, University of Copenhagen

Opponents

Professor, Roberta Salamone Università degli Studi di Messina, Italy Associate Professor, Elaine Ferguson London School of Hygiene and Tropical Medicine, UK Professor, Inge Tetens (Chairwoman) Department of Nutrition, Exercise and Sports, University of Copenhagen

Source of funding

This research was supported by the Social Sciences and Humanities Research Council of Canada (Doctoral grant number 752-2015-0271); the Consultative Research Committee for Development Research (FFU), Danish International Development Assistance (Danida), Ministry of Foreign Affairs, Denmark (GREEiNSECT Grant no. 13-06KU); and the Nordic Africa Institute PhD travel scholarships.

This thesis was submitted to the PhD School of Science, University of Copenhagen, May 3rd, 2017. This PhD thesis received preliminary recommendation by the assessment committee on July 4th, 2017. Contact information: [email protected]

PhD thesis 2017 © Afton Marina Szasz Halloran ISBN 978-87-7209-035-1 Printed by SL grafik, Frederiksberg, Denmark (slgrafik.dk)

Preface This thesis is based on data collected as a part of GREEiNSECT: Insects for Green Economy project. The studies contained in this thesis were carried out in northern and north-eastern Thailand and western Kenya. I have been involved in GREEiNSECT since the beginning of the project in February 2014. Before February, I assisted Nanna Roos in the development and writing of the successful proposal that was awarded 10 million DKK by the Consultative Research Committee for Development Research (FFU), Danish International Development Assistance (Danida), Ministry of Foreign Affairs, Denmark. My research project, like many others, deviated from the intended plan and aim due to the availability of new information, delays, and numerous other challenges. Originally, I intended to focus solely on examining and quantifying the environmental impact of cricket farming in Kenya; however, the plan evolved and I included Thailand in my analysis, expanding the scope of the research to include policy, rural development, and the adoption of cricket farming. Luckily, due to my background in agricultural development, I have been trained in analysing food systems and their respective inputs, outcomes, actors, influences and impacts. My PhD thesis reflects this approach. I would like to sincerely thank all of the farmers who participated in this study. They generously offered their time and knowledge for the sake of this study. In return, I hope that they will benefit from the knowledge generated through this research. I would also especially like to thank two very special people: Jackie Oloo and Monsikan (Eye) Baosri. These two ladies acted as my fearless research assistants in Thailand and Kenya. More importantly, they became close friends and taught me so much about their respective cultures. A big thank you to Silvenus Ochieng Konyole for his friendship and support during my fieldwork in Kenya, especially in assisting in the selection of the enumerator team. Without the help of my hardworking enumerator team in Kenya it would have been impossible to have completed this study. These amazing enumerators go by the names of Denish Ongola, Bonface Oketch, Godrick Maradona, Dennis Sewe, and Millicent Oganda. Thanks to the entertaining Mr. Big and Patrick for getting us to the research sites in Thailand and Kenya safe and sound. I also extend a big thank you to my supportive friends who were always there when I needed advice, an injection of enthusiasm and a good laugh. These wonderful people go by the names of Ditte Brøgger Rasmussen, Andrea Jiménez Cisneros, Cecilie Friis, Christopher Münke-Svendsen,

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Meghan Anderson, Anja Maria Homann, Ida Klockmann and Mette Tørnkvist Gade. Another big thank you to all my colleagues in the Paediatric and International Nutrition Section at the Department of Nutrition, Exercise and Sports. This work would not have been possible without the support of my colleagues from the GREEiNSECT project. It has been a pleasure to collaborate with such a multidisciplinary group. I am very grateful to my supervisors, Nanna Roos and Sander Bruun. Nanna, thank you for your support throughout the process and teaching me to discern between the nice-to-know and the essential-to-know. Sander, I appreciated the time that you always dedicated towards our discussions. Thanks for bearing with me and understanding my tendency to overachieve! I would also like to thank Yupa Hanboonsong for her guidance and friendship while I was carrying out fieldwork in Thailand. Aside from being a very inspiring woman and a great scientist, Yupa’s relentless enthusiasm and passion for her work are infectious. I would also like to thank another strong woman, Prof. Monica Ayieko, whose “get-it-done” attitude helped me to overcome many of the challenges associated with field work. I would also like to thank my partner, Roberto, for supporting, challenging, and inspiring me during the highs and lows of the past years. A big thank you to my parents, grandparents, and brother for always encouraging me to be ambitious and follow my passions, even when this means travelling far from home. This three-and-a-half year process has taught me so much more than can be written within the pages of this PhD thesis.

Afton Marina Szasz Halloran Copenhagen, August 2017

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Table of contents

List of papers ..................................................................................................................................................... vi  Related work ..................................................................................................................................................... vii  List of abbreviations ........................................................................................................................................ viii  Summary in English ........................................................................................................................................... 1  Dansk resumé .................................................................................................................................................... 4  1. Introduction ................................................................................................................................................... 7  1.2 Objectives of the PhD thesis .................................................................................................................... 8  2. Background .................................................................................................................................................... 9  2.1 Nutrition .................................................................................................................................................. 9  2.1.1 Agriculture‐nutrition linkages ........................................................................................................... 9  2.1.2 Insects as animal source foods ....................................................................................................... 11  2.1.3 Nutritional composition ................................................................................................................. 11  2.2 Insect farming systems .......................................................................................................................... 13  2.2.1 Domesticating insects ..................................................................................................................... 13  2.2.2 Cricket farming techniques ............................................................................................................. 14  2.3 Sustainable diets .................................................................................................................................... 15  2.3.1 Components of sustainable diets ................................................................................................... 15  2.3.2 Environmental impacts of animal production systems .................................................................. 16  2.4 Sustainable livelihoods .......................................................................................................................... 16  2.4.1 Defining a sustainable livelihood .................................................................................................... 16  2.4.2 Insects and rural livelihoods in Sub‐Saharan Africa and Southeast Asia ........................................ 16  2.5 Adoption of new technologies .............................................................................................................. 17  2.6 Regulatory frameworks governing the use of insects ........................................................................... 18  3. Methodology ............................................................................................................................................... 20 

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3.1 Study setting .......................................................................................................................................... 20  3.2 Study design .......................................................................................................................................... 21  3.3 Data collection and analysis .................................................................................................................. 22  3.3.1 Paper I ............................................................................................................................................. 22  3.3.2 Paper II ............................................................................................................................................ 23  3.3.3 Paper III ........................................................................................................................................... 23  3.3.4 Paper IV .......................................................................................................................................... 27  3.3.5 Paper V ........................................................................................................................................... 28  3.4 Ethical considerations ............................................................................................................................ 33  4. Paper I .......................................................................................................................................................... 35  5. Paper II ......................................................................................................................................................... 45  6. Paper III ........................................................................................................................................................ 61  7. Paper IV ....................................................................................................................................................... 75  8. Paper V ........................................................................................................................................................ 89  9. Discussion .................................................................................................................................................. 111  9.1 Summary of findings ............................................................................................................................ 111  9.1.1 Summary of Paper I findings......................................................................................................... 111  9.1.2 Summary of Paper II findings ....................................................................................................... 111  9.1.3 Summary of Paper III findings....................................................................................................... 111  9.1.4 Summary of Paper IV findings ...................................................................................................... 112  9.1.5 Summary of Paper V findings ....................................................................................................... 112  9.2 Status of legislation and policy governing insects as food .................................................................. 112  9.2.1 Recent developments in the regulatory arena ............................................................................. 112  9.2.2 Future challenges ......................................................................................................................... 114  9.3 Environmental sustainability and insect farming ................................................................................ 115  9.3.1 Global warming potential ............................................................................................................. 115  9.3.2 Feed, a major hotspot .................................................................................................................. 116 

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9.3.4 Data gaps ...................................................................................................................................... 116  9.4 Cricket farming as a livelihood diversification strategy ....................................................................... 117  9.4.1 Organizations and groups ............................................................................................................. 117  9.4.2 Motivation and resource sharing ................................................................................................. 117  9.4.3 Consumption ................................................................................................................................ 118  9.5 Cricket farming in Kenya and Thailand ................................................................................................ 118  9.6 Strengths and weaknesses .................................................................................................................. 119  9.6.1 Strengths....................................................................................................................................... 119  9.6.2 Weaknesses .................................................................................................................................. 120  9.7 Areas of future research ...................................................................................................................... 120  9.7.1 Potential role in humanitarian assistance programmes, school feeding and women’s  empowerment ....................................................................................................................................... 120  9.7.2 Dietary transition and sustainable diets ....................................................................................... 121  9.7.3 Metrics for agriculture and nutrition actions ............................................................................... 122  9.7.4 Multidisciplinarily ......................................................................................................................... 122  10. Conclusion ............................................................................................................................................... 123  References ..................................................................................................................................................... 125  Appendices .................................................................................................................................................... 137  Appendix A ‐ Conference presentations (academic and non‐academic audiences) ................................. 137  Appendix B – Supplementary material to the Journal of Cleaner Production publication ....................... 139 

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List of papers Paper I – Halloran A., Vantomme P., Hanboonsong Y., Ekesi S. 2015. Regulating entomophagy: the challenge of addressing food security, nature conservation, and the erosion of traditional food culture, Food Security, 7 (3): 739-746.

Paper II – Halloran, A., Roos, N., Eilenberg, J., Cerutti, A., Bruun, S. 2016. Life cycle assessment of edible insects for food protein: A review. Agronomy for Sustainable Development, 36: 57.

Paper III – Halloran, A., Roos, N., Hanboonsong., Bruun, S. 2017. Life cycle assessment of cricket farming in north-eastern Thailand. Journal of Cleaner Production. 156: 83-94.

Paper IV – Halloran A., Roos N., Hanboonsong Y. 2017. Cricket farming as a livelihood strategy in Thailand. Geographical Journal, 183 (1): 112–124.

Paper V – Halloran, A., Oloo, J., Ochieng Konyole, S., Ayieko, M., Roos, N. Awareness and adoption of cricket farming in Kenya. Submitted to Rural Studies.

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Related work The following publications are not included in the PhD thesis: 

Halloran A, Roos N, Flore R, Hanboonsong Y. (2016) The development of the edible cricket industry in Thailand. Journal for Insects as Food and Feed, 2 (2): 91-100.



Halloran A, Münke C, Vantomme P, Reade B, Evans J. (2015) Broadening insect gastronomy. Sustainable Food, Beverage & Gastronomy, Routledge.



Evans J, Alemu M, Flore R, Frøst M, Halloran A, et al. (2015) 'Entomophagy': an evolving terminology in need of review. Journal for Insects as Food and Feed, 1 (4): 293-305.



Halloran A, Flore R, & Mercier C. (2015) Notes from the ‘Insects in a Gastronomic Context’ workshop in Bangkok, Thailand. Journal for Insects as Food and Feed, 1 (3): 1-4.



Halloran A, Münke C, Vantomme P, van Huis A. (2014) Insects in the human food chain: global status and opportunities, Food Chain, 4 (2): 103-118.

Together with Nanna Roos, Paul Vantomme and Roberto Flore, I also took on the role as editor for a textbook: 

Halloran A, Roos N, Flore R, Vantomme P (Eds.) (Winter 2017). Edible insects in sustainable food systems. Springer Nature Academic Press.

Oral and poster presentations related to the disemination of the results of my PhD research can be found in Appendix A.

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List of abbreviations ACFS

National Bureau of Agricultural Commodity and Food Standards, Thailand

ASF

Animal source food(s)

EU

European Union

FAO

Food and Agriculture Organization of the United Nations

FGDs

Focus group discussions

FU

Functional unit

GAP

Good Agricultural Practice

GHG

Greenhouse gas

IGILS

Swiss Interest Group for Edible Insects

ILCD

International Reference Life Cycle Data System

JOOUST

Jaramogi Odinga Oginga University of Science and Technology

KKU

Khon Kaen University

KSH

Kenyan Shillings

LCA

Life cycle assessment

LMICs

Low- and middle-income countries

NAI

Non-adopters inside the adopter sub-location

NAO

Non-adopters outside the adopter sub-location

RNI

Recommended nutritional intake

TBH

Thai Bhat

VWB

Veterinarians without Borders

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Summary in English Background Over the past five years, a growing amount of attention has been placed on the potential of edible insect species to address the global challenge of food and nutrition security. Even greater attention has been put on the handful of insect species which can be easily domesticated and raised en masse. Some of these species belong to the Gryllidae (cricket) family. The oldest and most developed example of cricket farming for human consumption comes from Thailand. For nearly 20 years, thousands of rural Thai farmers have adopted and developed these unique farming systems, providing not only food for their households but also employment and income. This development has resulted in the subsequent promotion of small- and medium-scale insect farming systems in rural communities in low- and middle-income countries (LMICs), such as Kenya. However, the policy environment for cricket farming, the social and environmental impacts in Thailand and the adoption of cricket farming in Kenya are not well understood. Thus, there is a critical need for more research into the impacts of cricket farming on nutrition, rural livelihoods and the environment. My thesis addresses this research gap by reviewing the literature and empirically examining cases from Thailand and Kenya. The results of this thesis are a part of the ‘GREEiNSECT: Insects for Green Economy’, a research project that assesses the contribution of insects to green economy. Methods The thesis is presented in the form of five research papers. Paper I is presented in the form of case studies, where the policy and legislation governing the consumption and production/harvest of edible insects in four countries (Kenya, Thailand, Switzerland and Canada) are compared and contrasted. Paper II is a literature review of the previously published life cycle assessments that have been conducted on insects for food and feed. Empirical data collected in Thailand and Kenya in 2014 and 2015 are presented in Papers III, IV and V. Paper III uses life cycle assessment technique to evaluate the environmental impacts associated with current and future cricket production in contrast with broiler chicken production in Thailand. Paper IV employs questionnaires to assess the contribution of cricket farming to rural livelihoods in northern and north-eastern Thailand. Data from this study was used to inform the development of the household questionnaires used in Paper V, a study of the awareness and adoption of cricket farming amongst

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cricket farmers and households in Homa Bay, Kisumu, and Siaya counties, Kenya. Thirteen focus group discussions were also conducted in the same counties. Results The results of the case studies in Paper I showed that there is a lack of policies, regulations, and legislation governing global insect consumption by humans. In the countries where insects have been a part of traditional diets (Thailand and Kenya), edible insects have not yet been a significant part of well-designed policies concerning health, nutrition, agriculture, food safety, and conservation. In Paper II, a total of six life cycle assessment (LCA) studies were found to have been carried out in Europe. Each LCA had unique goals and scope, functional units, and impact categories. Future LCAs are recommended to address existing gaps in knowledge, such as quantifying greenhouse gas emissions from farmed insect species. In Paper III, a LCA was carried out to compare the environmental impacts of commercial cricket farming and broiler chicken farming. The LCA found that commercial cricket farming has fewer environmental impacts when compared to medium-scale broiler chicken production in the same region of Thailand. A future scenario that modelled a contained, climate-controlled cricket production facility demonstrated further resource efficiency and lower environmental impacts. A major hotspot in cricket production was found to be related to the production of feed that contains maize meal and soy meal. In Thailand, results from a study (Paper IV) of 49 cricket farms in three provinces found that farmers took up cricket farming to diversify their existing agricultural livelihood strategies and provide significant income to rural households. Social and human capital also played a role in the adoption and perpetuation of cricket farming and helped farmers negotiate market access. Overall, cricket farming had a positive impact on rural livelihoods in Thailand. In Paper V, 42 cricket farmers and 317 farmers who have not adopted cricket farming were interviewed. A number of variables influenced the awareness and adoption of cricket farming in Kenya, including distance from a cricket farm, crop diversity score, and frequency of visits to the extension office. Results from focus group discussions show that lack of adequate equipment, space and housing were most frequently cited as barriers to the adoption of cricket farming.

 

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Dissatisfaction with the lack of market for crickets and lack of training were cited as the second and third most common barriers. Conclusion The results of this thesis show that there is limited policy and legislation that specifically addresses the production/harvest and consumption of crickets or other insect species. There are limited LCAs of insect farming and limited data on the environmental impacts associated with insect farming systems. Further, cricket production was found to have a lower environmental impact than broiler chicken production. Cricket farming had a notable impact on rural livelihoods in Thailand in terms of household income, and social and human capital. Finally, cricket farming is a livelihood strategy that few farmers in Kenya are aware of. The barriers to adoption must be addressed if cricket farming is to have a positive impact on food and nutrition security. The findings presented in this thesis have relevance for non-governmental organizations, civil society, policy makers, intergovernmental organizations and governmental agencies seeking to implement policies and interventions to improve access to a nutritional source of food with a relatively low environmental impact that can also improve rural livelihoods.

 

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Dansk resumé Baggrund Igennem de seneste fem år er interessen for potentialet af spiselige insekter til at løse den globale udfordring omkring mad og ernæringssikkerhed øget støt. Der har specielt været fokus på den gruppe af insektarter, der let kan opdrættes og masseproduceres. En af disse arter er Gryllidae familien (fårekyllinger), og en af de ældste og mest udviklede eksempler på domestificeret fårekyllingeproduktion findes i Thailand. I næsten 20 år har tusindvis af thailandske landmænd opbygget og udviklet et landbrugssystem omkring fårekyllingeproduktionen, som udover at levere mad til husholdningsbehov også har forbedret deres beskæftigelses- og indkomstmuligheder. Med inspiration i denne thailandske succeshistorie er interessen steget for at promovere små og mellemstore insektopdrætssystemer i andre lav- og mellemindkomstlande (LMIC), som for eksempel Kenya. Det politiske miljø for fårekyllingeproduktion, de sociale- og miljømæssige konsekvenser i Thailand og potentialet for- og tilpasningen af fårekyllingeproduktion i Kenya, er dog

ikke

udbredt.

Der

er

derfor

et

umiddelbart

behov

for

mere

forskning

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fårekyllingeproduktionens betydning for ernæring, for livet på landet og for miljøet. Denne afhandling adresserer den manglende forskning ved brug af en litteraturgennemgang og gennem en empirisk undersøgelse af to cases i Thailand og Kenya. I denne PhD afhandling undersøger jeg virkningerne af fårekyllingeproduktionssystemer i forhold til levevilkår, ernæring og miljø i landdistrikter i det nordlige Thailand og Kenya. Afhandlingen bidrager til forskningsprojektet ’GREEiNSECT: Insects for Green Economy’, der sætter fokus på insektproduktionens rolle i den grønne økonomi. Metode Afhandlingen består af fem individuelle forskningsartikler, der undersøger forskellige aspekter af problemstillingen. I artikel I præsenteres et case-studie, der sammenligner den lovgivning og de regulativer, der styrer forbruget og produktionen af spiselige insekter i fire lande (Kenya, Thailand, Schweiz og Canada). Artikel II præsenterer et litteraturreview af alle tidligere publicerede livscyklusanalyser af insektproduktion som fødevare og foder. Empiriske data indsamlet i Thailand og Kenya i 2014 og 2015 danner grundlag for analyserne i artikel III, IV, og V. Artikel III bruger metoder fra livscyklusanalysen til at vurdere miljøpåvirkningen af nuværende og fremtidig fårekyllingeproduktion i sammenligning med slagtekyllingeproduktion i Thailand. Artikel IV bygger på en spørgeskemaundersøgelse blandt husstande på gårde i det nord- og nordøstlige

 

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Thailand, og analyserer ud fra disse data fårekyllingeproduktionens bidrag til husstandenes levevilkår. På baggrund af disse resultater udviklede vi et spørgeskema til brug i studiet præsenteret i

artikel

V.

I

denne

artikel

undersøges

miljø-

og

levevilkårskonsekvenserne

af

fårekyllingeproduktion blandt fårekyllingeproducenter og husstande i amterne i Homa Bay, Kisumu og Siaya, Kenya. Fokusgruppediskussioner blev også brugt i de samme områder. Resultater Resultaterne fra case-studierne i artikel I viste, at der mangler politiske beslutninger, regulativer og lovgivning af sektoren for produktion af spiselige insekter. Selv i de lande hvor insekter traditionelt set har været en del af kosten (Thailand og Kenya), er spiselige insekter endnu ikke blevet inddraget i lovgivningen på områder såsom sundhed, ernæring, landbrugspolitik, fødevaresikkerhed eller miljøbeskyttelse. Artikel II viser, at seks livscyklusanalyser på insektproduktionsområdet er gennemført i Europa. Hver livscyklusanalyse havde sine egne mål og omfang, såvel som funktionelle enheder og kategorier. Fremtidige livscyklusanalyser bør adressere huller i den eksisterende viden, såsom kvantificering af drivhusgasser fra insektproduktionen. I Artikel III blev en livscyklusanalyse udført for at sammenligne miljøbelastningen ved hhv. fårekyllingeproduktion og slagtekyllinger. Livscyklusanalysen fandt at fårekyllingeproduktion har mindre miljøpåvirkning sammenlignet med en mellemstor slagtekyllingeproduktion i den samme region af Thailand. Desuden viste et fremtidsscenarie, der modellerede en fårekyllingeproduktion med et lukket og klimakontrolleret produktionssystem, at resourceeffektiviteten kan øges og miljøpåvirkningerne reduceres yderligere. De primære miljøbelastninger i fårekyllingeproduktionen er relateret til foderproduktionen, der pt. indeholder majs- og sojamel. I Thailand fandt et studie (artikel IV) af 49 fårekyllingeproduktioner i tre provinser, at landmænd indførte kommerciel fårekyllingeproduktion for at afveksle deres eksisterende landbrugsproduktion og for at øge indtægten i husstande i landdistrikterne. Husstandenes sociale og kulturelle kapital spillede også en vigtig rolle for oprettelsen og fortsættelsen af fårekyllingeproduktionen samt for adgangen til markedet. Samlet set har fårekyllingeproduktionen haft en positiv indvirkning på husstandsøkonomien og levevilkårene blandt landmændene i Thailand.

 

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I artikel V blev 42 fårekyllingeproducenter og 317 landmænd, som endnu ikke havde optaget fårekyllingeproduktion, interviewet. En række faktorer havde indflydelse på opfattelse og optag af fårekyllingeproduktionen i Kenya, bl.a. afstand fra en fårekyllingeproduktion, afgrødediversitets score og besøg til offentlig landbrugskonsulenttjeneste. Resultater fra fokusgruppediskussioner viste, at mangel på adgang til produktionsmidler, udstyr og plads var de hyppigst nævnte barrierer for deltagelse i fårekyllingeproduktionen. Utilfredshed med mangel på et egentligt marked for fårekyllinger samt mangel på oplæring blev nævnt som hhv. anden og tredje hyppigst nævnte barrierer for deltagelse. Konklusion Denne PhD afhandling viser, at der er begrænset politik og lovgivning, der specifikt adresserer produktionen af fårekyllinger og andre insekter i de undersøgte lande. Resultaterne viser endvidere, at der er få egentlige livscyklusanalyser af insektproduktion og at data omkring miljøpåvirkningen af insektproduktionssystemer er begrænsede. Derudover vises det, at fårekyllingeproduktionen har lavere miljøpåvirkning end slagtekyllingeproduktion. Fårekyllingeproduktionen har haft en betydelig positiv indvirkning blandt husstande i landdistrikter i Thailand i form af øget indtægt samt social og menneskelig kapital. Endelig viser afhandlingen, at kun få landmænd i Kenya er bevidste om at fårekyllingeproduktion kan være et indtægtsgrundlag. Hvis disse systemer skal udbredes yderligere med større fødevare- og ernæringssikkerhed til følge, skal barriererne for deltagelse adresseres. Resultaterne, som er præsenteret i denne afhandling, har relevans for ikke-statslige organisationer, civilsamfundet, lovgivere, mellemstatslige organisationer og statslige enheder, som ønsker at implementere lovgivning og indsatser for at forbedre adgang til en ernæringskilde med relativt lav miljøbelastning, som også kan forbedre landlige husstandes indtægtsgrundlag.

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1. Introduction A growing amount of attention is being placed on the potential of edible insect species to address food and nutrition security (1,2). Even greater attention is being directed towards the handful of insect species that can be easily domesticated and raised en masse. Globally, the oldest and most developed example of cricket farming for human consumption comes from Thailand. For nearly 20 years, thousands of rural Thais have adopted and developed these unique farming systems, providing not only food for their households but also employment and income (3–5). This development has resulted in the subsequent promotion of cricket farming systems in rural communities in low- and middle-income countries (LMICs) such as Kenya. In Kenya, different kinds of insects such as ants, termites, crickets and lake flies have been consumed by various ethnic populations (6–10). Activities supporting the development of cricket farming systems have occurred in the Lake Victoria region of Kenya since 2012 (11). The ubiquity of malnutrition and food insecurity has been a motivating force to explore the potential of increasing insect consumption in Kenyan households (12). At the same time, the dire need to shift towards more environmentally sustainable diets has highlighted edible insects as a potential alternative to traditional livestock such as cattle and swine (1,13,14). Physiological and biological differences between insect species and other conventional livestock species mean that insects do not use their metabolism to maintain body temperature, and, therefore, use resources more efficiently (13). While the potential benefits of cricket farming to nutrition, livelihoods, and the environment are becoming increasingly known to a wide range of actors, the dynamics of these systems are still understudied. Thus, an enhanced understanding of the value chain, legislation and regulations, impacts on rural economy, and possible improvements in production methods and techniques is required. Moreover, investigation of the linkages between agriculture and nutrition is essential for the creation of more socially, environmental, economically and culturally sustainable food systems.

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1.2 Objectives of the PhD thesis The main objective of this thesis is to assess the impact of cricket farming on rural livelihoods, nutrition, and the environment in rural Thailand and Kenya. The specific objectives of this thesis are: 1. To conduct four cases studies in Thailand, Kenya, Switzerland, and Canada on the actions that have been taken or are underway to develop the various multi-jurisdictional regulations and legislation governing the farming, collection, and consumption of insects (Paper I) 2. To review studies on the life cycle assessment of edible insect production systems and to develop a reference framework for future life cycle assessments on edible insects (Paper II) 3. To perform a life cycle assessment of cricket farming in north-eastern Thailand in relation to broiler chicken farming (Paper II) 4. To conduct a preliminary assessment of cricket farming as a livelihood strategy in northeastern and northern Thailand (Paper IV) 5. To evaluate the determinants and barriers to the adoption of cricket farming in rural Kenya (Paper V)

 

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2. Background This section provides background on some of the reoccurring themes in this thesis, including nutrition; insect farming systems; sustainable diets; sustainable livelihoods; adoption of new agricultural technology; and regulatory frameworks governing edible insects. 2.1 Nutrition 2.1.1 Agriculture-nutrition linkages

The nexus between agriculture and nutrition may be evident; however, the pathways to realising improved nutrition through agriculture are complex and involve many diverse stakeholders (15). These multiple pathways, or factors, occur at immediate, underlying and basic levels, and in turn, influence other levels (Figure 1). This thesis focuses particularly on the pathway of insufficient food security leading to nutrition insecurity.

Figure 1 - A diagram of the conceptual framework used in this study (Modified from UNICEF, 2013 (16))

In theory, the linkages between agriculture and nutrition in the smallholder value chain are circular, feeding into each other (Figure 2). Agriculture can allow individuals to produce food for their own

9

consumption or process it and sell the product. Either way, there is an increase in consumption of nutritious food, which is believed to improve nutritional status and allow individuals to increase their productivity. Thus, it is possible to improve nutrition via agricultural interventions (17–19). The base of evidence measuring the impact of these interventions on improved nutrition, however, is still weak (19–21). Many agricultural interventions focus only on increased production of food or changing consumption patterns of primary producers and their households (22), thus ignoring a multi-sectoral approach to the development of value chains (20,23–25). This does not clearly represent reality, as what happens between consumption and production plays a major role in determining the nutrition security of a household or community. As Hawkes and Ruel note, “food is stored, distributed, processed, retailed, prepared, and consumed in a range of ways that affect the availability, affordability, acceptability, and nutritional quality of foods for the consumer” (23). However, the specific causal relationships between food supply chains and their impacts on nutrition are still not well understood (23,26,27). Figure 2 presents a simplified example of the possible linkages between agriculture and nutrition along the smallholder value chain.

Figure 2 - Agriculture-nutrition linkages along the smallholder value chain (Modified from Wiegers et al. 2011(28))

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2.1.2 Insects as animal source foods

Nearly 800 million people are undernourished, malnourished, or hungry around the world (29). Maternal and child undernutrition is particularly prevalent in LMICs. Undernutrition is a significant public health concern which causes an estimated 3.1 million child deaths annually (30). Nearly half of all deaths of children under five years of age are caused by poor nutrition (31). Over the past years, greater attention has been paid to animal source foods (ASF) and their importance in addressing undernutrition. ASF provide concentrated dietary sources of macro- and micronutrients (32). Consumption of ASF has been found to decrease the risk of stunting and underweight. Moreover, ASF have been shown to improve dietary quality, micronutrient status, growth, and cognitive function in children (33–38). Consumption of ASF can help to meet amino acid and other nutritional requirements of malnourished children (38,39). The intake of ASF, as mediated by access, is a major limiting factor to addressing malnutrition, and consumption of ASF is still insufficient in many low-income countries (40–43). Other factors influencing access are availability/seasonality (44–46) and affordability (47). Insects are also significant ASFs. However, like other kinds non-domesticated animals, the consumption of wild insects is also limited by availability/seasonality and affordability (48). For example, a national survey in Lao People’s Democratic Republic (Lao PDR) showed that the availability of edible insects was primarily determined by season, and 86% of respondents would have eaten more if greater amounts were available year-round or if they were less expensive (49). 2.1.3 Nutritional composition

A 2013 literature review compiled the nutritional composition of 236 different edible insect species (50). In general, the nutrient content of insects varied between and within species and by metamorphic/developmental stage. For example, house crickets (Acheta domesticus) can contain 55-70% protein, 10-24% fat, and 414-455 kCal/100g and can supply significant levels of micronutrients such as calcium, potassium, iron and zinc (50). From samples of a wild cricket species (most likely Brachytrupes membranaceus) in Kenya, Christensen et al. found that 100g of dry matter significantly exceeded the daily recommended nutrient intake1 of iron and zinc for children, adolescents, women, and men (7). The calcium content of 100g of dry matter was half of                                                              1

 

 As per the FAO/WHO guidelines (51) 

11 

 

the recommended daily intake for children and adults, and about a third of the recommended daily intake for adolescents. Nurhasan et al. found that wild crickets (Teleogryllus testaceus) contain 4.6% fat (wet weight basis), with 26.6% n-6 PUFA and 9% n-3 PUFA (3:1 ratio) (52). The fatty acid profiles of Acheta domesticus or Gryllus bimaculatus are currently not available.

Even small amounts of crickets, such as 25g of dry matter, can provide substantial amounts of micronutrients, particularly for women and children (Figure 3 and Figure 4). Twenty-five grams of dry matter corresponds to approximately 100g of live crickets. This amount exceeds the RNI for riboflavin (all), biotin (infants and children) and folate (infants), and zinc (infants and children). Crickets can also be a complementary source of niacin (all), pantothenate (all), biotin (children and pregnant/lactating women), folate (children and pregnant/lactating women), magnesium (infants and children), iron (all), and zinc (for pregnant and lactating women)2. 800% 700% 600% 500% Infant (7‐11 months) 400%

Child (1‐3 years)

300%

Child (4‐6 years) Child (7‐9 years)

200%

Woman (Pregnancy) 100%

Woman (Lactation)

0%

Figure 3 - Percentage daily RNI of selected water and fat soluble vitamins for infants, children, and pregnant and lactating women provided by 25g (dry weight) of crickets (Acheta domesticus) (As per FAO/WHO Human Vitamin and Mineral Requirements and Rumpold and Schlüter, 2013 (50,53)).

The bioavailability of iron and zinc in crickets has not yet been measured. However, this thesis assumes it to be similar to meat. 2

12

800% 700% 600% Infant (7‐11 months)

500%

Child (1‐3 years) 400%

Child (4‐6 years) Child (7‐9 years)

300%

Woman (Pregnancy) 200%

Woman (Lactation)

100% 0% Calcium

Magnesium

Iron (15% Zinc (High bioavailability) bioavailability)

Selenium

Figure 4 - Percentage daily RNI of selected minerals for infants, children, and pregnant and lactating women provided by 25g (dry weight) of crickets (Acheta domesticus) (As per FAO/WHO Human Vitamin and Mineral Requirements and Rumpold and Schlüter, 2013 (50,53)).

There are still major data gaps in relation to human nutrition and the consumption of insects. Few studies have examined the impact of the consumption of edible insects on nutritional status. The Winfood study in Cambodia and Kenya measured the effects of the addition of indigenous ASFs and fortification to improved complementary feeding products. Experimental food products included tarantulas in Cambodia (54) and termites in Kenya (55–57). Results from Cambodia and Kenya did not show significant impacts of a product containing tarantula/termites on nutritional status in infants (56–58). However, neither study was designed to isolate the specific impact of specific ingredients, such as termites (55). Furthermore, the bioavailability of minerals and chitin in the exoskeleton of crickets is also relatively unstudied and requires further analysis (55,59,60). 2.2 Insect farming systems 2.2.1 Domesticating insects

Wild insect species have been a traditional part of food systems and diets in most regions of the world (2,61). However, the seasonality and availability of different insect species often restricts their consumption. As such, domestication of wild insect species has been proposed to relieve pressure on the hunting and collecting of wild populations as well as create a safe food products for

13

consumers and generate income (62–64). Through the domestication of insects, greater quantities can be farmed and, in turn, consumed. The ownership of livestock has been shown to improve the likelihood of ASF consumption (65,66). However, research on this topic has not yet extended to include cricket farming. Bees, for the production of honey, are among the first insects to have their habitats manipulated by human beings to produce food (67). Insect farming for direct human consumption, however, is a relatively new innovation, especially considering domestication of plants and animals over the last 12,000 years (68). Beginning in the 21st century, cricket species were farmed for laboratory experiments as well as feed for reptiles or zoo animals. In Thailand, basic technology for rearing different species of crickets for human consumption has been around since 1997 and has grown into a multi-million dollar industry (5). Over 20,000 cricket farms can be found, mainly, in the northern and north-eastern regions of the country (5). In 2015, the European Food Safety Authority administered a scientific report which listed the types of insects that have been domesticated to date (69). Of the 2,111 edible insect species recorded worldwide (61), only nine were found to be farmed for human consumption. Three of these nine species were classified as members of the Gryllidae (cricket) family (69). 2.2.2 Cricket farming techniques

Cricket species like Acheta domesticus (house cricket), Gryllus bimaculatus (two-spotted cricket) and Teleogryllus testaceus (field cricket) have been popular to farm as they have significantly shorter life cycles than traditional livestock (4,70). Acheta domesticus and Gryllus bimaculatus can be harvested after 45 to 60 days under optimal conditions (5) as opposed to, for example, six months for pork, 8-12 months for lamb and 36 months for beef (71). Cricket farming is an easy to implement and relatively low-investment farming technique compared to other livestock production systems (5,72). The main inputs to small-scale cricket production systems can include concrete blocks, egg cartons, feed, water, rice husk ash or sand, and small plastic containers. Hanboonsong et al. (2013) estimated the cost of building a shed and pens to range from 130 to 1,900€, depending on the choice of pens and building materials. Net profits in successful farms can range from 910 to 1,766 € per harvesting cycle (5).

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2.3 Sustainable diets 2.3.1 Components of sustainable diets

There is a growing need for diets that are economically accessible; respectful of biodiversity and ecosystems; culturally acceptable; and nutritionally adequate (73). A sustainable diet is defined by the Food and Agriculture Organization of the United Nations (FAO) and Biodiversity International as “diets with low environmental impacts which contribute to food and nutrition security and to healthy life for present and future generations” (74). This definition highlights the need to shift from considering food as just a source of nutrients, to a more holistic understanding of diets and their impacts (75). Johnston et al. argue that the major determinants of sustainable diets can be categorized as 1) agricultural; 2) health; 3) sociocultural; 4) environmental; and 5) socioeconomic (75). In a systematic review of the measurement of sustainable diets, Jones et al. identified 30 different components of sustainable diets (76). Estimated greenhouse gas emissions were most commonly measured, and land use and the consumption of animal-source foods were the second and third most commonly measured. However, the same authors also found that there is a lack of literature from LMICs. While the environmental impact of the diets of rural farming households in Kenya or Thailand can be assumed to be relatively low when compared to more wealthy urban households, the inadequacy of their diets may prevent against maintaining a healthy life, and, in turn, a sustainable diet. Thus, achieving a sustainable diet is therefore a balancing act between environmental and human health, and socioeconomic sustainability, governance, and cultural heritage; a balance which is difficult to achieve in the context of resource scarcity, poverty and food and nutrition insecurity. Consensus on what exactly comprises a sustainable diet has not yet been reached as the complexity of a diet as a whole must be captured (77). A vast number of scholars have highlighted traditional or indigenous diets as perhaps some of the most relevant examples of what sustainable diets might look like across cultures (e.g., 27,29–31). Different insect species have been a part of traditional diets across the world (2) and have therefore been mentioned as foods worth protecting and promoting as a component of a sustainable diet for the reasons mentioned in Chapter 1 of this thesis (81,82).

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2.3.2 Environmental impacts of animal production systems

Research into alternative ASFs with lower environmental impacts is essential to lessening the ecological footprint of global food production (83). While greenhouse gas emissions and other environmental impacts vary between foods and food categories, the highest emissions and impacts are associated with foods of animal origin, such as meat and dairy products (83–86). The emissions are determined by the species, farming system/production method under consideration, amount consumed and nutritional value (84). Feed composition and production period may also affect the environmental impacts of livestock (85). However, insects are physiologically and biologically different from vertebrate livestock; thus, they can convert feed into edible body mass more efficiently (13,87). Within farming systems, the farmer controls the feed source, which is also referred to as substrate. Compound chicken feed, plant matter or by-products/waste streams can be fed to farmed crickets. The production of feed ingredients like soy and maize can have larger environmental impacts when compared to other potential substrates for crickets (88). 2.4 Sustainable livelihoods 2.4.1 Defining a sustainable livelihood

In 1992, Chambers and Conway coined the term sustainable livelihood. A livelihood is sustainable if it can cope with and recover from stress and shocks, maintain or enhance its capabilities and assets, and provide sustainable livelihood opportunities for the coming generations (89). Thus, a sustainable livelihood is not one that is free from vulnerability, but rather one that can buffer the impact of internal and external stresses and shocks. Lowering a household’s level of economic risk and overall vulnerability is often done by changing or diversifying livelihood strategies. Diversification is defined as the way in which rural households construct a diverse portfolio of activities and social support capabilities to survive and improve living standards (90). This thesis builds upon this definition and considers diversification as a means of increasing the multiplicity of household’s activities, as well as moving away from traditional rural activities. In light of this, diversification can be seen as a form of self-insurance that leads to more sustainable livelihoods (91). 2.4.2 Insects and rural livelihoods in Sub-Saharan Africa and Southeast Asia

Insects are an important natural resource. Aside from providing food, the collection and sale of insects is a lucrative trade in many parts of the world, and it can generate income for rural

16

communities in Sub-Saharan Africa. A South African study found that 29% of villagers in six villages sold mopane caterpillars (Imbrasia belina) for income generation (92). In northern Zambia, caterpillar collection is also a significant seasonal income generating activity (93). In Kinshasa, women are mainly responsible for the sale of edible insects, which helps to buffer against poverty (94). Termite consumption and utilization in Zimbabwe provides a sustainable livelihood diversification strategy in poor regions and has addressed food insecurity (95). In Lao PDR, edible insects were popular due to the income that could be generated from collecting them (49). Nineteen percent of insect vendors in Lao PDR sold insects as a full-time job, and 64% sold them as a part-time job. Durst and Hanboonsong found that tens of thousands of people in Thailand are engaged in insect farming, processing, transport and marketing (4). Cricket farming is a relatively new agricultural technology. However, there are examples from different parts of the world where cricket farming has been introduced and has contributed to livelihood diversification. For example, the Annâdya Project in Ratanakiri Province, Cambodia was developed to improve food and nutrition security of rural households through the introduction and adoption of sustainable agricultural technologies, one of which was cricket farming (70). A study in Indonesia found that small-scale cricket farming could provide significant profit and stable source of income, and could become an alternative livelihood activity (96). The edible cricket industry was found to have a positive impact on rural economic development, entrepreneurship, and employment (3). Cricket farming is also expanding in Laos (mostly around Vientiane) to increase the production and consumption for improving household food security and income generation (72). 2.5 Adoption of new technologies While direct nutritional supplementation is a short-term strategy to alleviate acute undernutrition, agriculture has the potential to be a catalyst for long-term improvement in nutrition and health (97). Globally, agriculture is the main livelihood for 70% of the rural poor (98). Agriculture can provide food and income but can also serve as a tool to empower poor households, giving them control over their resources and assets (99). When rural farmers are able to start agricultural side-businesses they can diversify their on-farm income-generating activities (100). However, on-farm technology or innovation adoption is dynamic and requires the involvement of multiple actors (101,102). It is rare that farmers will adopt

17

all new technologies introduced to them due to external and internal socio-economic, institutional and environmental forces (103). Ensuring successful technology transfer is, therefore, significant to realising the benefits of the linkages between cricket farming and nutrition at the household level: if the barriers to adoption of cricket farming are too great, then direct and indirect impacts on household nutritional status cannot be realised. Therefore, it is fundamental to understand how to mitigate barriers and understand what factors influence the adoption of cricket farming. 2.6 Regulatory frameworks governing the use of insects The production, processing, consumption, trade and use of edible insects concern a variety of regulatory bodies, from food safety and conservation authorities to ministries of environment, health and agriculture (2). Similar to the discourse on mainstreaming nutrition across all sectors and stakeholder groups (104), a topic such as edible insects is so broad that it risks falling between the cracks. Edible insect species, in most cases, have simply been off the radar of decision-makers (105) as they are often a part of the informal trade or are considered as unimportant. This lack of attention has contributed to a lack of institutional governance surrounding the consumption and production of edible insects (106). A lack of clear policy can make it difficult for insect farming to be recognised as a farming practice and a livelihood, impeding the development of small-scale cricket farming at the community level. Policy formation that aims to conserve traditional diets; encourage agricultural entrepreneurship; promote food and nutrition security and sovereignty; ensure food safety; conserve biodiversity; and reduce the environmental impacts associated with food production is important to realizing the benefits of cricket farming in LMICs. The food safety status of edible insects may change with time (107). Edible insects are often considered safe in the country of origin in which they have been consumed for a long periods of time, however, as food safety knowledge and technology changes with time, so do food safety regulations. Thus, formalisation is a doubled edged sword which can enable or prevent the growth of cricket farming. On the one hand, formalisation can help protect wild insect species; formalise the informal; encourage improved food safety and quality control; acknowledge insects as a significant

18

animal-source food; and improve nutritional status. On the other hand, it can create barriers to entry; fail to integrate cultural and biological conservation; increase prices; and threaten local, informal economy.

Similar

pros

and

cons

have

also

been

described

during

the

institutionalisation and legitimisation of urban agriculture (108,109) or the use of the Traditional Speciality Guaranteed designation for traditional foods in the European Union (110). Rakodi found that formalisation may unintentionally complicate a farmer’s ability to enter the sector and potentially exclude those who could benefit the most from being a part of it (111).

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3. Methodology 3.1 Study setting The first two papers (Paper I and II) were desk studies. The research in papers III and IV took place in Thailand. Paper III investigated the case of a cricket farm located in Khon Kaen Province while Paper IV investigated cricket farms located in five provinces of northern and northeastern Thailand (Khon Kaen, Mahasalakam, Nakhon Ratchasima, Sisaket, and Sukhothai). Cricket production systems in Thailand were chosen for the analysis because they have a longer history than those in Kenya. Paper V investigated the case of farmers who had adopted and not adopted cricket farming. The data was collected in Kenya. While Thailand displays a high level of food security, food availability at community, household and individual levels is often governed by socio-economic differences (112). According to the World Health Organization (WHO), 16.3% of children under five are stunted, 6.7% are wasted, and 9.2% are underweight (113). Thailand is an economic success story in Southeast Asia, reducing poverty rates significantly over the last decades (114). However, poverty can still be found, mainly in north-eastern and northern Thailand (115). Since 1997, cricket farming has been promoted and carried out in these two regions of the country (Figure 5). As a result, they were selected as the regions of focus in this thesis.

Figure 5 – An example of a cricket farm in Sisaket Province, Thailand

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The study in Paper V took place in Homa Bay, Siaya, and Kisumu counties that make up half of Nyanza Province, western Kenya. The majority of cricket farming activities currently take place in these three counties (Figure 6).

Figure 6 – An example of a cricket farm in Homa Bay county, Kenya

According to the Government of Kenya, 239,400 children experience moderate acute malnutrition; 2,900 children suffer from severe acute malnutrition; and 1.1 million people are acutely food insecure (116). Agriculture, the backbone of the Kenyan economy, engages approximately 70% of the population. Food insecurity is found in both urban and rural areas of the country (117), and 17 million people in rural areas live below the poverty line (118). Poverty rates range between 35.6% and 45% in Siaya, Kisumu, and Homa Bay counties (119). 3.2 Study design This thesis aims to analyse the impacts cricket farming on rural livelihoods, nutrition, and the environment in Thailand and Kenya. This is done by analysing the direct and indirect linkages, processes and influences to the introduction of cricket farming as a means to achieving technology adoption, production and improved nutritional status (Figure 7).

21

Figure 7 – The processes, linkages and influences of technology adoption, production and improved nutritional status in relation to cricket farming (white = directly addressed; grey = indirectly addressed)

3.3 Data collection and analysis The following sections discuss the methods used to collect and assess the data contained in this thesis. 3.3.1 Paper I

Four countries representing four different continents were selected to provide case studies on the legislative and multi-jurisdictional regulations concerning the production and consumption of edible insects. Canada, Switzerland, Thailand and Kenya were chosen as case studies in order to represent the widest possible range of countries where data was available. Data collection was carried out from March to May 2014. Reports, governmental websites, research papers, peer-reviewed journal articles, books, and regulations were reviewed to identify any information that was specific to the

22

development and implementation of regulations, legislation or policy governing edible insects in the four countries. Stakeholders in Canada (Canadian Food Inspection Agency) and Switzerland (Swiss Interest Group for Edible Insects (IGILS)) were also asked to provide additional information concerning current regulations and actions that were being taken to change these regulations. Further, co-author Yupa Hanboonsong provided information about the current situation in Thailand as she has been involved in the development of the Good Agricultural Practice (GAP) standard, and co-author Sunday Ekesi from the International Centre for Insect Ecology and Physiology provided information about Kenya from the experience of a major stakeholder in the development of insects as food and feed in Africa. 3.3.2 Paper II

A literature review was conducted. The inclusion criteria was life cycle assessments (LCA) of insect production intended for human consumption or animal feed published in English in international peer-review journals before September 2016. The terms “LCA” OR “life cycle assessment” AND “insect*” OR “insect production” OR “insect protein” in the Web of Science and Google Scholar. LCA studies on animal feed were featured due to the very low number of studies conducted on insects intended as food (n = 3). A total of six LCA studies were included in the review. Based on the findings and themes uncovered in the literature review – as well as hands-on experience conducting a LCA in Thailand – a reference framework was developed to identify common pitfalls and advise future LCAs. 3.3.3 Paper III

For this paper, a LCA was used to measure the environmental impact of cricket farming in relation to broiler farming in north-eastern Thailand. LCA is a tool that can be used to quantify the impacts of products and systems on the environment (120,121). LCA is an iterative process comprised of four phases (Figure 8): 1. Goal and scope definition: decisions are made about the objectives, the system/product under study and the assumptions that are need; 2. Life cycle inventory: data is gathered as defined under the goal and scope phase and emissions are calculated; 3. Impact assessment: impacts of the system/product in question are evaluated 4. Interpretation: data from the three stages above are interpreted.

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Figure 8 – The four phases of LCA 

Broiler chicken production systems were selected as the system of comparison. While this choice can be disputed, there are similarities between the two products that come from these systems: they are ASFs which contain similar amounts of protein, and both are common street foods and sidedishes in the region. This study compared cricket and broiler chicken farming under three different scenarios: 1. Current cricket farm scenario (with two species of crickets: Acheta domesticus and Gryllus bimaculatus) 2. Current broiler farm scenario (with one species of cricket, Acheta domesticus) 3. Future cricket farm scenario (with one breed of broiler chicken, Charoen Pokphand (CP) Brown) The current cricket farm scenario represented the current state of cricket production in north-eastern Thailand. The future cricket farm scenario represented a future, scaled-up cricket farm, similar to those currently under development in Europe or North America (i.e. contained and climate controlled). The current broiler farm represented the type of broiler production currently carried out in north-eastern Thailand to produce broilers that are specifically used for gai-yang, a type of grilled chicken that is popular in this region (Figure 9).

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Figure 9 - An example of gai-yang, grilled chicken that is typically eaten in north-eastern Thailand

The system boundaries for the three scenarios considered all of the direct and indirect activities involved in the production of crickets and broilers. These included production and processing of feed ingredients; production of construction/housing materials and consumables; production of broilers/crickets (including breeding and hatchery for the broilers); processing; transportation; and manure/biofertiliser application. Some processes were omitted including the use of antibiotics and other inputs, such as vitamins and vaccines in broiler production; packaging; and the cooking of the crickets and the broilers. Two functional units (a measure which is used to qualify the function of the product) were chosen to compare cricket production with broiler chicken production: 1 kg of edible mass and 1 kg of protein in edible mass. The percentage of the edible mass of a cricket was assumed to be 100% because the whole insect is most commonly eaten and 58% edible mass in chicken meat (Sukontarattanasook, pers. comm., 2016). Regarding protein, Acheta domesticus contain 63%, and Gryllus bimaculatus contain 56% on a dry weight basis based on measurements that are described in the following section. Broiler protein content is 63% on a dry weight basis (122). Data collection

Data was collected from 10 cricket farms in Mahasalakam and Khon Kaen Provinces in northeastern Thailand in November 2014. Sampling of the farms was done through convenience sampling: contact with the farms was facilitated through the Department of Entomology at Khon

25

Kaen University as there are no available databases that list all of the existing cricket farms in Thailand. Data supporting the LCA of broiler farming in north-eastern Thailand was gathered from three farms in Mahasalakam province in November 2014. Access to these farms was granted through the provincial Agricultural Extension Department; thus, the farms were selected using convenience sampling. A questionnaire was developed to gather foreground data on the inputs and outputs to and from broiler and cricket farms. This data included water, feed, construction materials, energy, biofertiliser and consumables. The questionnaire was carried out on each farm with the assistance of a translator. The questionnaire was translated from English to Isan (a dialect of Lao) to English. Each questionnaire took approximately one-and-a-half hours for the farmers to answer. For accuracy, measurements of the pens were also taken with a measuring tape. Samples of the feed, crickets and biofertiliser were taken from each farm. Additional primary data on cricket processing was obtained through a wholesale trader in Mahasalakam who buys from over 100 farmers in the region. The Department of Entomology at Khon Kaen University identified this wholesaler. The selection was, therefore, purposive. The future farm scenario was modelled after a scaled-up version of the current cricket farm in Mahasalakam. One of the major differences was the inclusion of a climate-controlled facility that was modelled after the facility used for broiler farming featured within this study. Supplementary data on broiler meat processing as well as the hatchery and breeder farm was gathered from the World Bank (123) and through personal communication with a Thai poultry expert (Sukontarattanasook, pers. comm., March 21, 2017). Data analysis

The collected data was then analysed in Excel. Carbon and nitrogen mass balances were used to assess the validity of the input and output data. Nine of the ten cricket farms were rejected due to inaccuracies in the reported foreground data. One farm was selected for the LCA. This farm is representative of medium-scale cricket farms in the region. In a similar mass balance analysis of the broiler farms, two of the three farms were rejected, leaving one for analysis. According to a local poultry expert, this farm was representative of a broiler farm that raises chickens to be used for a type of grilled chicken eaten in this region (Figure 9).

26

The nitrogen and carbon content of the feed, crickets, and biofertiliser were analysed with a carbon, nitrogen and sulphur (CNS) analyser (vario MACRO cube 88 CNS, Elementar). The phosphoruous and potassium content of the biofertiliser samples were measured using inductively coupled plasma optical emission spectrometry (ICP–OES, Optima 5300 DV, Perkin Elmer, Ontario, Canada). Massbalance calculations were used to calculate the carbon dioxide (CO2) emissions for all three scenarios. Nitrous oxide (N2O) and methane (CH4) emissions were measured in a pilot experiment. Live crickets (140g) were placed in a 1,300mL container (Exetainer ©LABCO) with 8g of feed and 8g of water. Air samples were extracted with a 5mL syringe (Braun Omnifix) at intervals of 10 minutes over the total span of 80 minutes. The samples were then analysed by gas chromatography (Greenhouse Gas Analyser, 450-GC, Bruker, Germany). The life cycle impact assessment was performed using the ILCD method, which considers 15 different impact categories: climate change (global warming potential), ozone depletion, human toxicity (cancer effects), human toxicity (non-cancer effects), particulate matter/respiratory inorganics,

ionising

radiation,

photochemical

ozone

formation,

acidification,

terrestrial

eutrophication, aquatic eutrophication, ecotoxicity, water resource depletion and mineral and renewable resource depletion (120). Gabi ts (2015, compilation 7.0.0.19) LCA modelling software was used to analyse and compare the three different scenarios featured within this study. The hotspots, which are processes that have the largest share of environmental impacts, were analysed. A sensitivity analysis was performed to evaluate the effect of a 20% increase in transportation distance and a 20% substitution of fish meal for soy meal. 3.3.4 Paper IV

This study gathered preliminary information that was used to inform the development of the questionnaire used in Paper V. Field work for this study took place in November 2014 and March 2015. An 11 part questionnaire with sub-questions was designed to collect data from cricket farmers on themes including socio-demographics, cricket farming experience, motivation to start cricket farming, institutional interactions, markets, workload, future development, previous livelihood activities and home consumption. The questionnaire was administered to 49 cricket farmers in Khon Kaen (n = 12), Sisaket (n = 11), Mahasalakam (n = 3), Nakhon Rachisima (n = 13) and Sukhothai Provinces (n = 10). The Khon Kaen University Department of Entomology assisted in the identification of cricket farming villages and key cricket farmers acted as gatekeepers.

27

Once given permission to conduct the questionnaire within a given village, snowball sampling (124) was employed to identify individuals or groups of cricket farmers. The study was, therefore, purposive, and the selection of the participating cricket farmers was non-random. The questionnaire was translated into Isan (a dialect of Lao) and Thai by a translator. Face-toface interviews were conducted at each household and interviews lasted between 30 minutes and two hours. Based on the exploratory nature of this study, the data was coded and sorted into reoccurring themes. The predominant themes included: motivation to start cricket farming; impact of income generated from cricket farming; training and knowledge gaps; institutional knowledge and support; adaptability and complementarity; local and trans-provincial cooperation; rules of membership and belonging; market channels; markets and price; and mediating factors for market access. 3.3.5 Paper V Data collection

A household questionnaire was developed based on results from the exploratory study in Thailand (Paper IV). Focus group discussions including ranking exercises complemented the quantitative and qualitative data provided by the questionnaire. Data collection was carried out between October and November 2015 in Homa Bay, Siaya, and Kisumu counties. Participants in this questionnaire were divided into three categories: i) adopters; ii) non-adopters in the adopter sub-location3 (NAI); iii) and non-adopters outside the adopter sub-location (NAO). For adopters, 45 active cricket farmers were identified through Jaramogi Odinga Oginga University of Science and Technology and the Anglican Development Service (a partner in the Flying Foods project). Forty-two of the 45 identified farmers were available to participate in this study. The sample size for the non-adopters (NAI and NAO) was determined based on the total number of households in the three counties covered by this study. According to the Kenyan National Bureau of Statistics, there is a total of 586,688 houses in these three counties (125). A sample size of 317 households was determined using a confidence level of 95% and confidence interval of 5.5. Two sub-counties were randomly selected from each of the three counties to determine the sites for

3

A sub-location is an administrative unit beneath a sub-county.

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the random sampling of NAO. From these sub-counties, two sub-locations were randomly selected. Randomization was done using www.randomizer.org. Four enumerators were selected and trained before conducting the questionnaire. All of the enumerators from the region where the research took place, and all spoke Luo. The questionnaire was translated into Luo to assist the enumerators in the correct explanation of each question. A meeting with the chief or a representative of the community to explain the research project upon arrival in the selected sub-locations,. Permission to conduct the questionnaire in the sub-location was granted, and the enumerators were transported to separate locations to begin the data collection. The enumerators visited every third household4 and carried out face-to-face interviews in Luo. The questionnaire took an average of 28 minutes for the respondents to answer. The questionnaire gathered data on the following themes: farmer/household characteristics; human capital; physical/natural capital; financial capital; social capital; and farmer behaviour. Focus group discussions (FGDs) were used for triangulation and to add complementary data to the qualitative household questionnaires. Thirteen focus group discussions were conducted in the same sub-locations as the household questionnaires. However, the three categories of participants were slightly different: i) adopters; ii) non-adopters who had been trained in cricket farming; and iii) nonadopters who had never been trained in cricket farming. Non-adopters were identified by the chief or representative of the community. The purpose of the FGDs was to understand the constraints to adopting new agricultural technologies; the motivation for adopting new technologies; the impact of the adoption of new agricultural technologies in the sub-location; and how cricket farming as a new technology was perceived in rural communities. Ranking exercises (a kind of participatory rural appraisal technique (124)) were used during the FGD to assess how the participants ranked, for example, factors taken into consideration when deciding whether or not to adopt a new agricultural technology. Firstly, the group was allowed to brainstorm the most common factors on a large piece of paper. Then, each participant was allowed to vote once for their top choice. This was done by placing a stone or similar object on their top choice (Figure 10). The results were then tallied.

4

A household was defined in this study as a traditional Luo household which is comprised of many built houses.

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Figure 10 – Non-adopters participating in a ranking exercise as a part of a FGD in Siaya County 

All FGDs were held in Luo and were recorded and transcribed. A research assistant provided simultaneous English-Luo translation. The FGDs took an average of 1.5 hours. Participants were compensated for any costs related to travel to the FGD. Data analysis

Following past studies that have used logistic regression to analyse adoption of agricultural technologies (14,103,126,127), the data in this study was also analysed with logistic regression. The data was modelled in R (version 3.3.3) by logistic regression to select the significant variables that were believed to contribute to the awareness or adoption of cricket farming. The modelling method was based on Mariano et al. and Conteh et al. (103,127). Let ∗



be the latent response variable

i = 1,2,….N



Where the observed dummy variable 1 if

∗

∗

is defined by

0

0 otherwise Xi represents the explanatory variables,

denotes the estimated coefficients and

a continuous variable independent of X with a standard logistic distribution.

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is assumed to be

The probability that the farmer, i, is willing to adopt or aware of cricket farming is ∗

1

0

0



1



,

where F is the standard cumulative density function of

that takes a value between 0 and 1.

The equation to estimate the parameters is where





…

is the dependant variable, willingness to adopt or awareness; is the intercept and is the

coefficients of each explanatory variable. The odds ratio (OR) was calculated from the logit coefficient by raising e to the power of the coefficient. ORs were calculated to provide a value that was easier to interpret than the logit as the OR ratio represents the odds that an individual will adopt of be aware of cricket farming over the odds of an individual not adopting or being unaware for a 1 unit increase in the independent variable for continuous variables or as compared to the reference category for categorical values (128). The variables included in the questionnaire were defined based on previous empirical data from Thailand (Paper IV) and published literature on agricultural adoption (Table 1). Past studies have shown that there are multiple factors that influence a farmer or household to take up a given technology or innovation (14,129–134). The explanatory variables and the literature/data which informed them are presented in below (Table 1). Table 1  – Explanatory variables and the literature/data which informed them (14,126,130–133,135–141)  Explanatory variables

Variable definition

Farmer characteristics Distance from nearest cricket farm

Empirical data from Thailand

Household size

Abebe et al. 2013 & Jara-Rojas et al. 2012

Gender of respondent

Empirical data from Thailand

Human capital indicators Last new agricultural technology adopted

Proxy for classification of adopters as per Rogers' Innovation Adoption Curve

Sources of agricultural information

Empirical data from Thailand & Läpple and Rensburg, 2011

Frequency of vegetable consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of vegetable consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

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Frequency of animal-source food (non-dairy) consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of pulse consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of dairy consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of fruit consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of nut consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of oil consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Frequency of sugar consumption

Jerneck and Olsson, 2014 & Victora et al., 2008

Natural/physical capital indicators Farm size

Daberkow and McBride, 2003 & Jara-Rojas, 2012

Food crop diversity

Prokopy et al. 2008

Livestock diversity

Jara-Rojas, 2012

Financial capital indicators Household food spending

Proxy for wealth, Jara-Rojas et al. 2012 & Langyintuo and Mungoma, 2008

Receives remittances

Proxy for wealth, Jara-Rojas et al. 2012 & Langyintuo and Mungoma, 2008

Household has off-farm income

Langyintuo and Mungoma, 2008

Member of a SACCO

Simtowe and Zeller, 2008

Social capital indicators Visits to extension officer in the last year

Empirical data from Thailand

Visits from extension officer in the last year

Empirical data from Thailand

Member of an agricultural organization

Empirical data from Thailand

Member of a non-agricultural organization

Conley and Udry, 2010, van Rijn et al., 2012,Tumbo et al., 2013,

Has a mobile phone

Fischer and Qaim, 2012

Farmer behaviour Social influenceability

Estrada & Vargas-Estrada, 2013

Risk aversion

Jerneck and Olsson, 2014

Consumes termites

Empirical data from Thailand

Consumes crickets

Empirical data from Thailand

This study used convergent design (Figure 11)

to compare and relate the qualitative and

quantitative data in order to achieve a complete understanding of the adoption and awareness of cricket farming (142).

Figure 11 – Convergent design for the analysis of qualitative and quantitative data (Adapted from Creswell, 2015 (142))

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3.4 Ethical considerations A research plan was provided to Khon Kaen University and the National Research Council of Thailand before carrying out research in Thailand. Permission to conduct the research was granted. In Kenya, permission to conduct the research was provided by the National Commission for Science, Technology and Innovation. At the county level, letters of permission to conduct research in Homa Bay, Siaya, and Kisumu counties were provided by the County Commissioner and Ministry of Education offices. Permission from the Sub-county Commissioner was also required in Siaya County. Village chiefs were also contacted before the research was carried out and to seek permission to conduct the research. The farmers who participated in the research in Kenya and Thailand were also informed of the nature of the study and the use of the data before conducting the interview. All farmers personally granted their approval to be included in this study.

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34 

 

4. Paper I Regulating edible insects: the challenge of addressing food security, nature conservation, and the erosion of traditional food culture Afton Halloran, Paul Vantomme & Yupa Hanboonsong, Sunday Ekesi Food Security. 2015 Apr. 7:739–746

 

35 

 

36

Food Sec. (2015) 7:739–746 DOI 10.1007/s12571-015-0463-8

ORIGINAL PAPER

Regulating edible insects: the challenge of addressing food security, nature conservation, and the erosion of traditional food culture A. Halloran 1 & P. Vantomme 2 & Y. Hanboonsong 3 & S. Ekesi 4

Received: 17 October 2014 / Accepted: 30 March 2015 / Published online: 28 April 2015 # Springer Science+Business Media Dordrecht and International Society for Plant Pathology 2015

Abstract Entomophagy is a common practice in many regions of the world but there are few examples of national regulations that govern insects for human consumption. Where entomophagy is not common, the current regulatory discourse focuses primarily on food safety and consumer protection. In countries where insects contribute to local diets, nature conservation is often an issue of high importance. This paper investigates the variation in the ways in which entomophagy and its related activities are currently regulated in Thailand, Switzerland, Kenya and Canada. Authoritative bodies who are responsible and the roles they play are discussed. Insects have only recently entered into the sustainable food dialogue, but have not yet been incorporated into policy documents and have been largely omitted from regulatory frameworks. Moreover, even in nations where there is a tradition of consuming a variety of insect species, they do not appear explicitly in dietary guidelines. Although food safety is a major concern, it can undermine the importance of nature conservation, traditional food culture, food security, and potential economic development. Thus, entomophagy should be viewed holistically and development of future legislation must take into consideration its multi-dimensional nature.

* A. Halloran [email protected] 1

Department of Nutrition, Exercise and Sports, University of Copenhagen, Rolighedsvej 26, 1958 Frederiksberg C, Denmark

2

Forestry Department, Food and Agriculture Organization of the United Nations, Viale delle Terme di Caracalla, 00153 Rome, Italy

3

Entomology Division, Faculty of Agriculture, Khon Kaen University, Khon Kaen 40002, Thailand

4

International Centre of Insect Physiology and Ecology (icipe), PO Box 30772-00100, GPO, Nairobi, Kenya

Keywords Entomophagy . Regulatory frameworks . Food security . Food safety . Nature conservation . Traditional diets

Introduction In May 2014, the Food and Agriculture Organization (FAO) of the United Nations and Wageningen University and Research jointly hosted the Insects to Feed the World Conference in Ede, The Netherlands. Approximately 450 participants gathered from more than 45 countries to discuss issues related to insects as food and feed. The conference summary concluded that the Bmajor challenges include… : further awarenessraising among the general public to promote insects as healthy food for humans and feed for animals; influencing policy makers to approve insect inclusive food and feed legislations; and further research efforts to provide and expand with validated data the available scientific evidence and benefits of using insects in the food and feed chains^ (FAO/WUR 2014). Unsurprisingly, the issue of insect inclusive food and feed legislation featured in the vast majority of the presentations as an unresolved issue. As noted by Halloran and Münke (2014), the greatest barriers to the growth of an edible insect sector is the lack of allinclusive legislation that governs the production, use and trade of insects as both food and animal feed. Although the discourse regarding the regulatory frameworks influencing insects as food and feed has gained momentum in the past couple of years, it is not new. For example, at the national level, research regarding the need for the recognition of insects as a food resource in Mexico has been extensively discussed by Ramos-Elorduy and Paoletti (2005). The willingness of some decision making bodies, such as the Directorate-General of Health and Consumers (SANCO) of the European Commission, to discuss the possibilities for incorporating insects into

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food and feed legislation has gradually increased. A case in point is that of Laos PDR which proposed a regional food standard for insects in 2010 under the Proposal for new work on development of regional standards for edible crickets and their products. This proposal was supported by the neighbouring countries of Cambodia, Thailand and Malaysia (FAO 2010). National governments, such as the Netherlands, are actively funding researchers investigating issues of legislation for governing insect farms, health and safety standards, and marketing through retail outlets (Pascucci and Magistris 2013). This paper reviews various actions taken or underway in Thailand, Canada, Kenya and Switzerland in order to address and understand the relevant stakeholders and multijurisdictional regulations and legislations governing the use of insects as food and feed. It builds on an earlier draft by FAO BDiscussion paper: regulatory frameworks influencing insects as food and feed^ (Halloran and Münke 2014) and assesses regulatory frameworks including legislation, standards and other regulatory instruments which are legally binding or otherwise in the use of insects as food and feed.

Thailand Thailand boasts a large and successful commercial insect sector that produces primarily for human consumption. Locusts, crickets, giant water bugs, bamboo caterpillars, beetles, palm weevil larvae and ants are the most commonly consumed and marketed in the country and beyond. These species are either wild harvested, semi-cultivated or farmed (Hanboonsong et al. 2013). Among the various insects, cricket farming is the most advanced. The technology was developed by Kohn Kaen University 15 years ago, and then promoted by the Thai government through a small and micro-community enterprise scheme. Despite the fact that there are over 20,000 operating cricket farms with average production of 7500 tonnes per year, research on commercial production is sparse. Moreover, few production and management standards for cricket farming exist, such as hygiene for minimizing disease outbreaks. In many cases, best practices in breeding, nutrition, or pest control are not well understood by farmers (Hanboonsong et al. 2013). The Ministry of Public Health is the main authoritative body currently regulating insect production and consumption in Thailand. All products processed from insects that are sold in the local markets and exported have to be passed by law through the Food and Drug Administration (FDA) under the Ministry of Public Health. Insect producers have to apply for a licence, and an inspector from the FDA monitors the production site, and also samples and monitors products for proper hygiene standards on a regular basis.

A. Halloran et al.

No specific standards for insects as food exist; thus, they are treated like any other food product under the Food Act of B.E.2522 (1979) (Food and Drug Administration Thailand 2014). This is probably attributed to the fact that Thailand, as well as the greater region of South-eastern Asia has a long history of entomophagy and paradoxically has not developed specific food standards to protect consumer safety. Discussions are now underway on how to make the farm GAP (Good Agriculture Practice) index for cricket farming. This should provide some guideline for farmers to follow at farm sites. However, there is little support from extension services to improve techniques and farming conditions (Hanboonsong et al. 2013). Many of the insects consumed in Thailand are wild harvested. Environmental and habitat changes have caused their decline. The Royal Forest Department under the Ministry of Natural Resources has played a major role in protecting many insect species. However, Thailand, like many other countries, has struggled to conserve wild insect populations despite the availability of legal regulations for species protection that have been put in place by the government (Boongird 2010). For example, there are four official acts for forest conservation and protection which relate to wild bees (Boongird 2010). Due to declining numbers of palm trees, improved techniques for palm weevil semi-cultivation have been developed. The Department has also developed techniques for semicultivating bamboo caterpillars in order to ensure a more sustainable caterpillar harvest (Hanboonsong et al. 2013). Despite ministerial involvement, the insect food industry has been largely overlooked by government in relation to other agrifood industries. As mentioned by Fellows (2014), the widespread use of Ecommerce through internet access has allowed producers in Thailand to easily gain access to high value markets in industrialized countries. Products like dried and flavoured crickets have been exported to Europe (mainly France and Belgium) and even the United States. With the expansion of training and education in computing and information technology in many universities in developing countries, Fellows (2014) predicts that an increased amount of insect products will be available to international markets via internet sales. All insect exports from Thailand must be certified by the Royal Forest Department to ensure that no species listed under the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) are being traded.

Switzerland Switzerland is an example of a country that has been quick to address requests from its citizens to incorporate insects as food into national legislation. The Federal Department of Home Affairs Ordinance on foodstuffs of animal origin governs

Regulating entomophagy: the challenge

animal-derived food products. However, the Ordinance (Article 2) does not recognize insects as an animal species accepted for food production. In 2013, there was active involvement from civil society, namely the organization Grimiam, in placing insects for both food and feed on the agenda. On 25 November 2013, Councillor Isabelle Chevalley posed an interpellation (Nr. 13.4013) to the Federal Assembly by asking: Pourquoi interdire la consommation d’insectes? (Why forbid the consumption of insects?). The interpellation challenged the Federal Council on the following points (Federal Assembly of the Swiss Parliament 2014a): 1. Is the Federal Assembly prepared to propose to Parliament a legislative amendment to allow the consumption of insects? 2. How can the prohibition of eating insects be justified since hundreds of millions of people have consumed insects for millennia (Aristotle praised the exquisite taste of cicada nymphs)? These interpellations were welcomed by members of the Federal Assembly, as solutions for sustainable food is an area of interest and priority. The Assembly reported back on 12 February 2014 and addressed the following issues (original text in French) (Federal Assembly of the Swiss Parliament 2014a): 1. Insect consumption in Switzerland is not prohibited and consumers can consume insects they breed or collect in the wild themselves. However, selling and serving insects as food is prohibited as insects have not been described in the food and commodities regulation (LGV, SR 817.02); 2. Reliable scientific data on the risk of allergies and the transmission of disease is needed in order to amend the current legislation; 3. The handling of non-native invertebrates in closed systems and free-range trials is regulated for the sake of environmental protection and biodiversity. However, no standardized methods of breeding and production of insects for food have been created to date. 4. While the rearing of selected insect species could contribute to sustainable food and animal feed production in Switzerland many of the fundamental questions remain unanswered. 5. The consumption of specified insects could contribute to sustainable food production, including as an ingredient for animal feed. However, many fundamental questions currently remain and will need answering in order to come to a final decision. Following this rebuttal two additional interpellations were made on 21 March 2014: 1) Interpellation Nr. 3273 - Pourquoi interdire en Suisse la commercialisation d’insectes qui sont

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consommés couramment dans d’autres pays? (Why forbid in Switzerland the commercialization of insects that are widely consumed in other countries?) (Federal Assembly of the Swiss Parliament 2014b), and 2) Interpellation Nr. 14.3274 Pourquoi interdire l’alimentation des poissons, des volailles et des porcs par des insectes? (Why forbid the feeding of fish, poultry and pigs with insects?) (Federal Assembly of the Swiss Parliament 2014c). These interpellations were supported by 63 and 68 of 200 councillors, respectively. The Assembly responded to each of the latter interpellations. In particular, the council noted that insects represent an untapped animal feed source for Switzerland. Switzerland is participating in discussions at the European Union level so as to avoid the negative consequences in case insects are not approved in the European Union. Moreover, the use of insects as feed should be accelerated, pending risk analysis (Federal Assembly of the Swiss Parliament 2014c). In terms of insects that are utilized for human consumption, the Assembly acknowledged that there is a growing evidence base supporting entomophagy. Nonetheless, strict regulations and further evidence would need to be generated in order to protect consumer health and safety. Moreover, selected insect species that are fit for human consumption would need to be pin-pointed (Federal Assembly of the Swiss Parliament 2014b). A round-table discussion of the Swiss Parliament concerning insects as foodstuff will be inaugurated in the first quarter of 2015 (J. Vogel, personal communication, 6 October, 2014).

Kenya In Kenya, the national food safety and quality system is managed by various statutory government agencies operating from different ministries with the broad objective of promoting public health, and protecting consumers against health hazards while enhancing economic development (FAO/WHO 2005; GAIN 2005). Although the country lacks a defined and published policy on food safety as part of a wider National Food and Nutrition Policy, food laws exist that are designed to protect the consumers. Food safety control agencies operate under the Ministries of (1) Trade, (2) Industrialization, (3) Public Health and Sanitation, and (4) Livestock, Fisheries Development, and Agriculture. A summary of the legal and policy framework of these agencies and the implementing mechanisms for the laws is documented by FAO/WHO (FAO/ WHO 2005). The agencies include Kenya Bureau of Standards (KEBS), Kenya Agricultural Research Institute (KARI), Kenya Plant Health Inspectorate Services (KEPHIS), Department of Public Health (DPH), Weights and Measures Department (WMD), Government Chemist’s Department, Department of Veterinary Services (DVS), Kenya Dairy Board (KDB), and Horticultural Crops Development Authority (HCDA), among others (GAIN 2005; Mwangi et al. 2009).

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The functions of these agencies include sensitization and implementation of codes of hygiene and agricultural practices by stakeholders throughout the food chain. Standards for food and agricultural products are developed by technical committees, with their secretariats at KEBS. Food standards give specifications for the compositional requirements, microbial requirements, the tolerance limits for contaminants, packaging, labeling and the hygiene conditions necessary for manufacture of products. While there are specific standards for various food and feed items, there are no specific standard for use of insects as food and feed. Rather insects are considered as impurities or contaminants in food that have to be eliminated. The majority of the Kenyan standards are adopted from international ones, International Organization for Standardization (ISO) and Codex Alimentarius Commission – Codex (CAC), following the philosophy of the World Trade Organization (WTO) Sanitary and Phytosanitary Standards (SPS) and Technical Barrier to Trade (TBT) agreements (World Bank 2005). There is now support for standards dealing with the use of insects as food and feed and consultations are currently underway with Kenya Bureau of Standards (KEBS) and other relevant agencies to establish a technical committee to draft standards that will govern the application of insects as food and feed. Kenya Bureau of Standards (KEBS) coordinates all activities concerning the development and implementation of both local and international standards relevant to Kenya (KEBS 2014). Kenya Bureau of Standards is a statutory Public body under the Ministry of Industrialization, operational since July 1974, and mandated by the Standards Act Chapter 496 (NCST 2009). The KEBS board of directors, the National Standards Council, is its policy-making body for supervising and controlling the administration and financial management. To improve on efficiency and provide more effective services to clients, KEBS established a Certification Unit (CU), accredited by the Quality Systems Accreditation Committee (QSAC) that offers certification services. Kenya Bureau of Standards gathers information on quality concerns through industrial visits and receives private complaint samples for analysis in its laboratories as part of quality assurance and testing services components of its operations. KEBS is also the National Codex Contact Point serving as the secretariat of the National Codex Committee (NCC). As the Codex Contact Point, KEBS acts as a link between the Codex Secretariat and Kenya. In addition to the establishment of standards through KEBS, the main nature conservation authority (i.e., Kenya Wildlife Services), also requires permits for large-scale farming of insects especially crickets. These permits are required in order to: 1) conform to wildlife domestication regulation process; and 2) match regulations on transporting livestock. This is required when moving animals from one zone to another and also includes an approved method of transportation. A zone is a jurisdictional area (part of a district).

A. Halloran et al.

The Kenya National Guidelines on Nutrition and HIV/ AIDS recognizes entomophagy as a part of traditional food culture, and states that Bcommon sources of animal proteins in Kenya include milk and milk products, beef, poultry, chicken, eggs, fillet, dried small fish (Rastrineobola argentea) and edible insects such as termites^ (Republic of Kenya 2006; p. 11). Moreover, it recommends that food security in HIV-affected households could be addressed in rural areas by promoting traditional practices of harvesting, preserving and consuming indigenous foods such as edible insects like termites. It is especially recommended when planning for the lean season (Republic of Kenya 2006). Indigenous foods are allowed for consumption, but not allowed for trade unless registered under the National Bureau of Standards.

Canada Food and food safety regulation in Canada occurs at federal, provincial and municipal levels. In general, the federal government deals with laws on food pertaining to import and export, novel foods, and interprovincial transport of food. The provincial levels deal with farming and food processing regulation. The municipal level mainly enforces the provincial laws, and also has a few bylaws pertaining to public health. They also work closely with the types of enterprises commonly found in cities and towns (like restaurants, markets, grocery stores etc.) (A. Jean, personal communication, 1 Dec 2014). Health Canada is the key administrative body in Canada that is responsible for regulations governing the use of insects as food and feed. The Canadian Food Inspection Agency (CFIA) falls under Health Canada and handles issues related to food safety and public health. The CFIA conducts novel food safety assessments under the Food Directorate. The purpose of the directorate is to establish policies, set standards and provide advice and information on the safety and nutritional value of food (A. Jean, personal. communication, 1 Dec 2013). According to the Government of Canada Bsince the CFIA’s inception in 1997, Canada’s demographic makeup has been changing at a fast pace. With immigration continuing to increase and accounting for a large percentage of the country’s population, the Agency has found itself facing demands for a larger variety of ethnic and imported foods from an ever increasing number of countries, especially developing countries. This demand, coupled with increasing globalization, has meant that the Agency has had to change and evolve at a fast pace to keep up with consumer’s needs^ (Government of Canada 2009). Most of the popular insects used as food around the world do have a history of safe use for human consumption as it is estimated that over 2,000 species of insects are consumed in

Regulating entomophagy: the challenge

80 % of the world’s nations (van Huis et al. 2013). Insects that do not have a history of safe use as food may be considered as novel food and, as such, they may need an assessment from the Novel Food Section of the Bureau of Microbial Hazards, Food Directorate, Health Canada. Insects that are not considered as Bnovel food^ may be offered for sale to Canadian consumers as long as they are not in violation of the Food and Drugs Act and Regulations; namely Sections 4, 5 and 7 of the Act and Division 28 of the Regulations. Division 28 of the Food and Drug Regulations applies to Novel Foods, their assessment and their pre-market notification. This process is similar in nature to EU Novel Food legislation (A. Jean, personal communication, 1 Dec 2013). Canada is one of the most culturally and ethnically diverse countries in the world. It experiences food culture through the exchange of traditions and world cuisines that are adopted as mainstream trends. Ethnic foods are in high demand and readily available at grocery stores and restaurants (Swiss Business Hub Canada 2011). This could partially explain the general legislative stance and attitude that has been seen in Canada by accepting the contribution of entomophagy to human diets worldwide. Some restaurants across Canada already serve insects on their menus (Gordon 2011). Restaurants may be allowed to sell dishes containing insects so long as the insects used in the dishes meet the Food and Drugs act regulations. However, municipal or provincial health authorities may have provisions in their own regulations that would condition, limit or prohibit the sale of dishes containing insects (A. Jean, personal communication, 1 Dec 2013).

Discussion Nature conservation Conservation policy can often fail to integrate biological and cultural conservation (Correal et al. 2009). In many societies, insects are not only considered as food or feed but also medicine and spiritual symbols (van Huis et al. 2013). Giving an example from the African continent, De Prins (2014) notes in her review of Edible insects: future prospects for food and feed security that Bthere is a conflict of interest between those who protect the tropical biodiversity and those who have the ingenuous wish to improve the agricultural economy in Africa^ (De Prins 2014; pg. 1). Therefore, the conservation of insects collected from the wild must also be included when developing legal frameworks. Thailand represents a country where insects as food are being regulated to a certain extent as a response to a growing number of enterprises commercially exploiting the increasing demand for them. However, since the demand for some insect species in Thailand is so huge that it cannot be met by

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domestic production, an additional supply of insects is received from neighbouring countries such as Lao PDR (Hanboonsong et al. 2013), which may enforce nature conservation laws less rigorously. While the examples of Thailand and Kenya demonstrate that satisfying the interests of diverse stakeholders may be a difficult undertaking, such an issue can be tackled. In the West, many national and local governments have governed the collection of wild foods such as mushrooms and game and the same could be undertaken for insects. In order to encourage food security and sustainable diets, regulation of wild harvesting, as well as semi-domestication of farmed insects has been promoted, as is typical for Thailand. The Swiss Federal Assembly has addressed the issue of nature conservation by regulating non-native invertebrates from being handled in closed systems (Einschliessungsverordnung vom 9. Mai 2012; SR 814.912), as well as in free-range trials for research purposes (Freisetzungsverordnung vom 10. September 2008; SR 814.911). However, there has been no standardization in terms of rearing and production of insects for food purposes to date. Formalization of local economy As seen in Kenya and Thailand there is a lack of a legal framework governing insects as food. However, this has proved not to be a major barrier to the expansion of the insect food sector. Insects as food have always been a part of the informal economy in those countries where entomophagy is a common practice. However, where entomophagy has not been a component of food culture, as in many western countries, their respective governments did not have the foresight to predict the future need to incorporate insects into legislation. Because of this, there is often little governance of this resource. In many countries, the collection, farming, processing and marketing of insects is primarily an informal activity. For example, in Kenya, the majority of the insect species that are consumed including termites, crickets, grasshoppers, lake flies and bees are collected from the wild. However, most recently, attempts are being made to rear these insects by developing simple technologies to assure year round availability and transferring these technologies to smallholder producers. In the process of scaling up, issues such as nature conservation, trade, and food safety will have to be addressed and formalization of rules and regulations governing the use of insect as food and feed will become increasingly crucial. Formalization through regulation can threaten local, informal economy. On the other hand, informal economy provides employment and income, especially in areas of high unemployment. As noted by Nelson and Bruijn Binformality offers opportunities of economic necessity to the poor, most of who will never be able to assimilate the costs of formalization, and

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partly because it offers others a low cost arena for experimentation that can lead to business growth^ (Nelson and De Bruijn 2005; pg. 579). Nonetheless, the informal sector is not homogeneous and formalization can in many cases provide positive outcomes, such as access to international trade as in the cases of Kenya and Thailand. Further, in order for insects as food and feed to develop, governmental involvement is essential in order to develop appropriate legislation to govern the sector. In Kenya and Thailand care should be taken to ensure that local populations can continue to consume their traditional foods without disrupting the food system due to an increasing demand from export markets and rising prices. An example of this complicated dynamic is given by how the booming export market for quinoa from Southern Bolivia has impacted the environment and home consumption (Jacobsen 2011; Winkel et al. 2012). Food-base dietary guidelines and food safety The World Health Organization (WHO) and the FAO have been responsible for the review of new research and information concerning diets worldwide. Due to the dynamic nature of diets, having a single snapshot of nutrient requirements and recommended nutrient intakes in a given region is an ongoing task. Such nutrients include protein, energy, carbohydrates, fats and lipids, a range of vitamins, and minerals and trace elements. Many countries are dependent on WHO and FAO to provide them with the necessary information, which is often adopted as national dietary guidelines or used as a basis for their own standards. In 1986, Gussow and Clancy, when discussing dietary guidelines for sustainability in the United States, noted that Bthe human race once enjoyed a diet drawn from a large variety of plant and animal (including insects!) life. Now the world’s population depends on a mere handful of species…^ A number of studies have shown the importance of insects in the diets of a variety of ethnic groups (van Huis et al. 2013; Christensen et al. 2006); however, the inclusion of insects as food is missing from most national food-based dietary guidelines. For example, termites, crickets and locusts are recognized under the Bmiscellaneous^ food group in the Tanzania Food-based Dietary Guidelines (Lukmanji et al. 2008). However, insects are acknowledged in policy documents, such as the aforementioned Kenya National Guidelines on Nutrition and HIV/AIDS and Uganda Food and Nutrition Policy. Insects are not included in the Canada Food Guide or in the Swiss Food-based Dietary Guidelines. The inclusion of locally consumed insect species may help to valorise the contribution of insects to regional or national diets. In terms of food safety, Switzerland has taken a precautionary approach to addressing insects as food due to the lack of knowledge of their potentially adverse health effects and standardization of rearing methods. Kenyan legislation is

A. Halloran et al.

comparable to that of Switzerland when it comes to the precautionary approach. Canada, on the other hand, addresses food safety issues in terms of the sanitary standards of the establishments handling food products. Therefore, insects are treated like most other food products. Thailand has a similar approach. The involvement of FAO in promoting insects as food and feed sources will be crucial in projecting and harmonizing dietary guidelines for insects in consultation with national systems.

Insects as a component of sustainable food policy There is broad scientific agreement that food systems are both the cause and solution to environmental problems. However, nutrition and sustainability is an emerging discourse in the food policy arena (Lang and Barling 2013). Insects have been highlighted in a number of high-level international conferences, such as Bthe International Conference on Forests for Food Security and Nutrition at the FAO, Rome May 15– 17^, 2013 as an important pathway to ensuring food and feed security. Of the recorded 2000+ edible insect species (Jongema 2014), few scattered studies have analysed the nutritional value of insects (van Huis et al. 2013). However, as demonstrated by Rumpold and Schlüter (2013) insects can provide satisfactory energy, protein, amino acids, monounsaturated and/or polyunsaturated fatty acids, and micronutrients.1 An effective system of legislation, food safety and agricultural health controls must be judged on its effectiveness and scientific and technical relevance. There is the need for continuous dialogue to inform policy on the use of insects as food and feed. Sufficient political will and socioeconomic priorities will be crucial for the introduction and maintenance of regulations for domestic consumption, trade promotion and the welfare of producers and consumers. Safe and high-quality insect products must result from efficient regulation at all stages of the supply chain in order to minimize the necessity of excessive corrective action having to be taken at a later stage in the process. However, in order to incorporate insects into sustainable food policy a better understanding of the environmental impact of insect production systems through consequential life cycle assessments is needed while ensuring appropriate legislation is in place to address the concerns highlighted above. Moreover, impact assessment of increased insect consumption and demand, and the effect on ecosystems are needed.

1 However, it must be noted that there have been no studies published to the knowledge of the authors, which have investigated the bioavailability of micronutrients and proteins from processed and unprocessed insects.

Regulating entomophagy: the challenge

Conclusion Addressing insects as a novel food focuses primarily on food safety and consumer protection. While these issues are highly relevant, they can also undermine the importance of nature conservation, traditional food systems, and economic development. In those countries where there was never a previous need to address regulations concerning insects as food we find that insects have been partially, or completely left out of legislation and decision making. Thus, the development of future legislation must take into consideration the multi-dimensional nature of insects as food and feed. Acknowledgments The author would like to acknowledge the following people for their contributions to this study Jürgen Vogel, Association Grimiam and André Jean, Health Canada. This paper is a product of the BGREEiNSECT: Insects for Green Economy^ research consortium (www.greeinsect.ku.dk), funded by the Danish International Development Agency’s Consultative Research Committee for Development Research Fund.

References Boongird, S. (2010). Honey and non-honey foods from bees in Thailand. In P. Durst, D. V. Johnson, R. N. Leslie, K. D. Shono, & V. Johnson (Eds.), Forest insects as food: Humans bite back, 165 (pp. 165– 172). Bangkok: Food and Agriculture Organization of United Nations Regional Office for Asia and the Pacific. Christensen, D. L., Orech, F. O., Mungai, M. N., Larsen, T., Friis, H., & Aagaard-Hansen, J. (2006). Entomophagy among the Luo of Kenya: a potential mineral source? International Journal of Food Sciences and Nutrition, 57(3–4), 198–203. Correal, C., Zuluaga, G., Madrigal, L., Caicedo, S., Plotkin, M., Kuhnlein, H., et al. (2009). Ingano Traditional Food and Health: phase 1, 2004–2005. Indigenous people’s food systems: the many dimensions of culture, diversity and environment for nutrition and health (pp. 83–108). Rome: CINE/FAO. De Prins, J. (2014). Book review on edible insects: future prospects for food and feed security. Advances in Entomology, 2(1), 47–48. Food and Drug Administration Thailand (2014). Laws and Regulations. http://www.fda.moph.go.th/eng/food/laws.stm. FAO. (2010). Development of regional standard for edible crickets and their products (Paper presented at the Joint FAO/WHO meeting Food Standards Programme). Bali: FAO/WHO Coordinating Committee for Asia. FAO/WHO (2005). Practical Actions to Promote Food Safety: Regional conference on food safety for Africa, Final Report. Harare, Zimbabwe. 3 – 6 October 2005. FAO/WUR (2014). Insects to feed the world: summary report. In P. Vantomme, C. Münke, A. van Huis, J. van Itterbeeck, & A. Hakman (Eds.), Insects to Feed the World. Ede, Netherlands. Federal Assembly of the Swiss Parliament (2014a). 13.4018 – Interpellation: Pourquoi interdire la consommation d’insectes? http://www.parlament.ch/e/suche/Pages/geschaefte.aspx?gesch_id= 20134018. Accessed 25 July 2014. Federal Assembly of the Swiss Parliament (2014b). 14.3273 – Interpellation: Pourquoi interdire en Suisse la commercialisation d’insectes qui sont consommés couramment dans d’autres pays? http://www.parlament.ch/e/suche/Pages/geschaefte.aspx?gesch_id= 20143273. Accessed 2 October 2014.

745 Federal Assembly of the Swiss Parliament (2014c). 14.3274 – Interpellation: Pourquoi interdire l’alimentation des poissons, des volailles et des porcs par des insectes? http://www.parlament.ch/f/ suche/pages/geschaefte.aspx?gesch_id=20143274. Accessed 2 October 2014. Fellows, P. (2014). Insect products for high-value Western markets. Food Chain, 4(2), 119–128. GAIN (2005). Food and Agricultural Import Regulations and Standards United States Department of Agriculture (USDA) Foreign Agricultural Service. Global Agricultural Information Network Report No. KE 5011. November 2005. Gordon, D. (2011). Cricket Parantha: creative Vancouverites incorporate insects into contemporary. http://www.foodinsectsnewsletter.org/ pdfs/Vij’sArticlebyDGGordon.pdf Accessed December 15 2013. Government of Canada (2009). ARCHIVED - Annual Report on the Operation of the Canadian Multiculturalism Act 2007–2008. http://www.cic.gc.ca/english/resources/publications/multireport2008/part1.asp. Accessed 24 June 2014. Gussow, J. D., & Clancy, K. L. (1986). Dietary guidelines for sustainability. Journal of Nutrition Education, 18(1), 1–5. Halloran, A., & Münke, C. (2014). Discussion paper: regulatory frameworks influencing insects as food and feed. Rome: Food and Agriculture Organization of the United Nations. Hanboonsong, Y., Jamjanya, T., & Durst, P. B. (2013). Six-legged livestock: edible insect farming, collecting and marketing in Thailand. Bangkok: Food and Agriculture Organization of the United Nations Regional Office for Asia and the Pacific. Jacobsen, S. E. (2011). The situation for quinoa and its production in southern Bolivia: from economic success to environmental disaster. Journal of Agronomy and Crop Science, 197(5), 390–399. Jongema, Y. (2014). World list of edible insects. http://www. wageningenur.nl/upload_mm/7/e/6/c79e66db-00d5-44c9-99cbf38943723db6_LIST%20Edible%20insects%201st%20of% 20April.pdf. Accessed 04/06/14. KEBS (2014). The Outline of Services offered by the Kenya Bureau of Standards, Kenya Bureau of Standards. www.kebs.org. Accessed 27 October 2014. Lang, T., & Barling, D. (2013). Nutrition and sustainability: an emerging food policy discourse. Proceedings of the Nutrition Society, 72(01), 1–12. Lukmanji, Z., Hertzmark, E., Mlingi, N., Assey, V., Ndossi, G., & Fawzi, W. (2008). Tanzania food composition Table. Dar es Salaam: MUHAS- TFNC & HSPH. Mwangi P., Nambiro, E. and Murithi, F.M. (2009). Safe and High Quality Food Supply Chains and Networks (SAFEACC) project Vegetable and Fruits, Fish and Beef products: The Kenya Component. KARI/ Global Food Network. NCST. (2009). A Proposed Coordination Structure for Biosafety Regulatory Agencies in Kenya (NCSTth ed.). Nairobi: The National Council for Science and Technology. Nelson, E. G., & De Bruijn, E. J. (2005). The voluntary formalization of enterprises in a developing economy—the case of Tanzania. Journal of International Development, 17(4), 575–593. doi:10.1002/jid. 1176. Pascucci, S., & Magistris, T. d. (2013). Information bias condemning radical food innovators? The case of insect-based products in the Netherlands. International Food and Agribusiness Management Review, 16(3). Ramos-Elorduy, J., & Paoletti, M. G. (2005). Insects: a hopeful food source. Ecological implications of minilivestock: potential of insects, rodents, frogs and snails. 263–291. Republic of Kenya. (2006). Kenyan national guidelines on Nutrition and HIV/AIDS. Republic of Kenya: Ministry of Health. Rumpold, B. A., & Schlüter, O. K. (2013). Nutritional composition and safety aspects of edible insects. Molecular Nutrition & Food Research, 57(5), 802–823.

746 Swiss Business Hub Canada. (2011). The Canadian food retail sector. Toronto: Swiss Buisness Hub Canada. van Huis, A., Van Itterbeeck, J., Klunder, H., Mertens, E., Halloran, A., Muir, G., et al. (2013). Edible insects: future prospects for food and feed security. Food and Agriculture Organization of the United Nations Winkel, T., Bertero, H., Bommel, P., Bourliaud, J., Chevarría Lazo, M., Cortes, G., et al. (2012). The Sustainability of Quinoa Production in Southern Bolivia: from Misrepresentations to Questionable Solutions. Comments on Jacobsen (2011, J. Agron. Crop Sci. 197: 390–399). Journal of Agronomy and Crop Science, 198(4), 314–9. World Bank (2005). The Role of Standards under Kenya’s Export Strategy Contribution to the Kenya Diagnostic Trade and Integration Study. World Bank.

Afton Halloran is as PhD fellow within the GREEiNSECT research consortium (greeinsect.ku.dk), a group of public and private institutions investigating how insects can be utilized as novel and supplementary sources of protein in small to large-scale industries in Kenya. Her research focuses on the nutritional, socio-economic and environmental impacts of insect production systems. She formerly worked as a consultant with the Insects for Food and Feed Programme at the Food and Agriculture Organization of the United Nations (FAO). She is a co-author of the FAO’s most popular publication BEdible insects: future prospects for food and feed security.^ At the FAO, she also developed a discussion paper on the regulatory frameworks governing insects as food and feed. Afton holds an MSc in Agricultural Development from the University of Copenhagen where she wrote her thesis on the legitimization and institutionalization of urban agriculture systems in Dar es Salaam, Tanzania and Copenhagen, Denmark. Her research interests include sustainable food systems, food policy, rural–urban interactions, undervalued foods, farmer organizations and sustainable diets.

Paul Vantomme is an agricultural engineer and has worked for FAO since 1978 in agro- forestry projects worldwide. From 1996 onwards he has coordinated the FAO global programme to promote Non-Wood Forest Products (NWFP), particularly wild gathered food products such as mushrooms and medicinal plants (http://www.fao.org/forestry/ nwfp/en/). His focus is on enhancing the contribution of wild gathered edible plant and animal products to food security. Mr. Vantomme has wide experience in awareness raising, communication and outreach activities at the global level in the field of NWFP and since 2002 on the promotion of edible insects in particular (http://www.fao.org/ forestry/edibleinsects/en/). Mr. Vantomme is another one of the co-

A. Halloran et al. authors of the popular FAO publication BEdible insects: future prospects for food and feed security.^ Mr. Vantomme represents FAO as an international partner of GREEiNSECT.

Dr. Yupa Hanboonsong is an Associate Professor of Entomology at Khon Kaen University, Thailand. Dr. Hanboonsong has also worked as a project leader and technical consultant with the FAO on indigenous foods such as insects in Thailand and Laos. She is a co-author of the FAO publications BSix-legged livestock: Edible insect farming, collecting and marketing in Thailand^ and BEdible insects in Lao PDR: Building on tradition to enhance food security.^ She is a team leader of the research programme on appropriate cricket farming management in Thailand. Dr. Hanboonsong represents the University of Khon Kaen as an international GREEiNSECT partner.

Dr. Sunday Ekesi is a Principal Scientist and Head of the Plant Health Division at the International Centre for Insect Pathology and Ecology (icipe). He obtained his PhD from Ahmadu Bello University, Nigeria in 1999 and undertook his post-doctoral research both at icipe and Rothamsted Research in the UK. His area of research interest is integrated pest management (IPM) that is based on the use of entomopathogens, baiting techniques, botanicals, orchard sanitation and classical biological control for the management of arthropod pests of horticulture. He has more than 20 years of working experience with arthropod pests of horticultural crops and has coordinated several research projects on the same topic. His current research activities are focusing on filling critical gaps in knowledge that are related to the impact of climate change on ecosystem services with emphasis on pest management and pollination and developing adaptation strategies to cope with changes. Other research activities focus on climate change and adaptation strategies and the use of insects for food and feed. Sunday sits on various international advisory and consultancy panels for the FAO, IAEA, WB and regional projects on fruit flies and several other important arthropod pests. He is currently a member of the International Fruit Fly Steering Committee (IFFSC) and member of the Editorial Board of the Newsletter of Tephritid Co-workers of Europe, Africa and the Middle East. Dr. Ekesi represents icipe as an international GREEiNSECT partner.

5. Paper II Life cycle assessment of edible insects for food protein: a review Afton Halloran, Nanna Roos, Jørgen Eilenberg, Alessandro Cerutti, Sander Bruun Agronomy for Sustainable Development. 2016 Oct. 36: 57

 

 

 

45 

 

46

Agron. Sustain. Dev. (2016) 36: 57 DOI 10.1007/s13593-016-0392-8

REVIEW ARTICLE

Life cycle assessment of edible insects for food protein: a review Afton Halloran 1 Sander Bruun 2

&

Nanna Roos 1 & Jørgen Eilenberg 2 & Alessandro Cerutti 3 &

Accepted: 1 September 2016 / Published online: 29 September 2016 # The Author(s) 2016

Abstract Compared to their vertebrate counterparts in traditional husbandry, insects are extremely efficient at converting organic matter into animal protein and dietary energy. For this reason, insects for food and feed show great potential as an environmentally friendly choice in future food systems. However, to obtain a true assessment of this, more information is needed about the production systems. Currently, only six studies applying the life cycle assessment (LCA) method to insect production systems have been published. The studies are heterogenous and thus difficult to compare. The aim of this paper was to establish a versatile reference framework that would allow for the selection of standardized settings for LCA applications in insect production systems, taking both the peculiarity of each system and the latest developments in food LCA into account. It is recommended that future LCAs of insect production systems take the following into account: (1) clear definition of the insect species and life stages included in the LCA, (2) use of at least two of the following types of functional units: nutritional, mass, or economic-based, (3) collection of empirical data in situ (e.g., on farms/production sites), (4) comparative analysis where production systems produce products that are realistic alternatives to the insect species under investigation, (5) inclusion of additional or

* Afton Halloran [email protected]; [email protected]

1

Department of Nutrition, Exercise and Sports, University of Copenhagen, Rolighedsvej 25, 1958 Frederiksberg C, Denmark

2

Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark

3

Department of Agricultural Sciences, Forestry and Food, University of Turin, Largo Braccini 2, 10095 Gugliasco, Turin, Italy

previously unconsidered unit processes, such as processing and storage and waste management, and (6) use of a wide range of impact categories, especially climate change, resource consumption, nutrient enrichment potential, acidification potential, and impacts on land and water consumption in order to allow for comparison between studies. Keywords Insect production . Life cycle assessment . Environmental impacts . Mini-livestock . Insect farming Contents 1. Introduction 2. Considerations for modeling insect production systems 2.1. LCA studies on insect production systems: general aspects 2.2 Goal and scope 2.2.1 Recommendations—choice of functional unit 2.3 Inventory analysis 2.3.1. Construction of facilities 2.3.2 Feed 2.3.3 Production 2.3.3.1 Temperature 2.3.3.2 Energy consumption 2.3.3.3 Feed conversion ratio 2.3.3.4 Water 2.3.3.5 Greenhouse gas emissions 2.3.3.6 Additional inputs 2.3.4 Transport 2.3.5 Processing and storage 2.3.6 Waste management and nutrient recycling 2.3.7 Recommendations—modeling of the insect production systems 2.4 Impact assessment

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2.4.1 Recommendations—life cycle impact assessment 3. Conclusion Acknowledgments References

1 Introduction Insects for human food consumption and animal feed are attracting increasing attention for their potential ability to address some of the most poignant issues threatening our environment. The main reason for this is the high feed conversion efficiency of insects and their ability to feed on various feed sources (van Huis et al. 2013; Halloran et al. 2014). Therefore, at first glance, insects appear almost as a proverbial “silver bullet”, providing an environmentally sustainable alternative for greening the supply of animal-source protein. However, a closer look at possible insect production systems reveals several complications and knowledge gaps that need to be addressed before the environmental benefits associated with species of edible insects in use can be assessed more precisely and their respective production systems can be utilized. Research about insects as both food and animal feed has developed rapidly over the past decade. A growing number of scholars from a variety of scientific fields such as entomology, livestock science, protein chemistry, human nutrition, and environmental science have become interested in this new interdisciplinary area. By now, the use of edible insects is rapidly outgrowing their novelty status and they are starting to be seriously considered as food on national, regional, and local levels (Halloran et al. 2015). One notable landmark was the 2013 publication Edible insects: Future prospects for food and feed security (van Huis et al. 2013). This book, representing one of the most complete and up-to-date compilations of research into this topic, captivated a multitude of stakeholders and successfully drew significant attention to this area. Other important publications include The Food Insects Newsletter (www.foodinsectsnewsletter.org), Ecology of Food and Nutrition special issue (Paoletti and Bukkens 1997), and Ecological implications of minilivestock (Paoletti 2005). New findings are being generated every month as scaled-up production has developed in many regions of the world. In most cases, however, these companies are not yet producing at capacity (Azagoh et al. 2015). Of particular interest in a discussion about sustainability are greenhouse gas (GHG) emissions. Eighty percent of GHG emissions generated within the agricultural sector originate from livestock production, including emissions from land used for grazing, energy for growing grains for feed, and transportation of grain and meat for processing and sale (McMichael et al. 2007). As such, alternative approaches for “greening” the protein supply abound. Insects have been identified as one of the solutions because insects’ unique physiological and biological features lead to high efficiency (Fig. 1).

Agron. Sustain. Dev. (2016) 36: 57

Compared to traditional livestock species, insects are extremely efficient at converting protein into animal protein and feed energy into food energy. This is mainly because insects are poikilothermic (cold-blooded), meaning that their metabolism is not used to maintain their body temperature, unlike homeothermic animals (Ramos-Elorduy 2008). The expected result is a higher feed conversion ratio (FCR) (also referred to in animal husbandry as feed conversion efficiency) (Nakagaki and Defoliart 1991; van Huis et al. 2013). While insects for food and feed show great potential as an environmentally friendly choice, there is still very limited information to enable an assessment of the sustainability of the production systems to be undertaken. There are several handbooks with more specific guidelines for how to conduct LCAs (e.g. ILCD 2010) and also guidelines that are specific to food production systems (e.g., Notarnicola et al. 2015). However, just a few papers apply an environmental impact assessment method, such as life cycle assessment (LCA), to insect production systems. The LCA approach, the assumptions adopted, and the system model considered may significantly affect the results of the assessment of food production systems (Notarnicola et al. 2015). Therefore, the main aim of this paper was to establish a versatile reference framework for choosing the best assumptions for LCA modeling of insect production systems considering both the characteristics of each system and the latest developments in food LCA. In order to achieve this aim, the objectives of the paper were (I) to describe current insect production systems highlighting critical aspects that should be considered when conducting LCA in insect production systems, (II) to review and discuss which assumptions are the most reasonable and are needed for modeling insect production systems for food and feed, and (III) to define best practices that can be adopted according to the case studies that have already published and actual critical environmental issues of insect production systems. It should be emphasized that the present paper considered studies on class Insecta (includes insects), which is the class considered by scientists in the relevant studies, and not other mainly terrestrial arthropod classes such as Arachnida (mites and spiders) and Diplopoda (including millipedes and others).

2 Considerations for modeling insect production systems 2.1 LCA studies on insect production systems: general aspects LCA is a tool for evaluating the environmental impacts of goods and services, considering the full life cycle of the relevant product or system. In the case of food products, environmental impacts arise from the production of inputs to the

Agron. Sustain. Dev. (2016) 36: 57

Page 3 of 13 57

Fig. 1 Gryllus bimaculatus farmed in Khon Kaen Province, Thailand Fig. 2 Stages of a life cycle assessment (LCA) as per ISO 14044:2006

agricultural process through to consumption in the home or restaurants and waste disposal. LCA is just one among several different environmental impact assessment methods; however, it is recognized as the most complete, it is used for the majority of food products and supply chains, and it has been adopted as the methodological base for environmental declaration schemes (Notarnicola et al. 2015). The procedure that should be used for conducting an LCA is specified in ISO standards (ISO 14040:2006 and ISO 14044:2006). An LCA requires four main steps: (1) goal and scope definition, (2) life cycle inventory, (3) life cycle impact assessment, and (4) interpretation of results (Fig. 2). The following sections follow the same structure and discuss the aspects and considerations necessary for insect production systems for the first three steps.

2.2 Goal and scope Case studies of LCA applications on edible insects for food or feed are few and far between. A search for such case studies in scientific literature yielded just six papers. The main features of the papers are preliminarily described in Table 1. In the goal and scope phase of an LCA, the goal of the study has to be defined as unambiguously as possible (ISO 14040: 2006 and ISO 14044:2006). This means defining the purpose of the study and usually the product or service alternatives to be compared. In order to be comparable, the products should have the same function, which is defined and quantified in the functional unit. For insect production systems, the functional unit could be the amount of edible parts (e.g., 1 kg of edible fraction) or animal protein (e.g., 1 kg of protein). The first study on LCA applied to insect farming for human consumption was published in 2012 (Oonincx and de Boer 2012), while the first LCAs related to insects as animal feed were published in 2015 (Roffeis et al. 2015; van Zanten et al. 2015). The various goals of the studies conducted since 2012 are given in Table 1. Despite the production of insects for food and feed in countries such as Thailand, South Africa, China,

Canada, and the USA, all of the six published LCA studies focus on case studies in Europe (Table 1). Oonincx et al. (2012) collected data from a commercial mealworm (Tenebrio molitor) producer in the Netherlands, and Smetana et al. (2016) collected data from an industrial-scale black soldier fly (Hermetia illucens) producer in Germany (although foreground data was also collected from production trials). Four studies used data from experimental trials or studies (Roffeis et al. 2015; van Zanten et al. 2015; Salomone et al. 2016; Smetana et al. 2016). Smetana et al. (2015) used data from Oonincx and de Boer (2012) in their comparative study of meat alternatives and chicken. Despite the current Eurocentric research focus, growing interest and research funds (van Huis et al. 2013; Azagoh et al. 2015; Kelemu et al. 2015) dedicated to this subject should generate future LCA studies in the coming years featuring insect species used for commercially produced food and feed. Of the known literature on the topic of insects as food and feed, each study had different objectives or goals, but of these papers, only one (Roffeis et al. 2015) had more than one objective. Three of the papers focused on the management of waste products (i.e., manure or food waste) (Roffeis et al. 2015; van Zanten et al. 2015; Salomone et al. 2016), while two papers aimed to understand the environmental impacts of insects when compared to other conventional livestock (Oonincx and de Boer 2012; Smetana et al. 2015). Smetana et al. (2016) focused on Hermita illucens for both feed and food production. Thus, there is considerable variety in the goals of the studies that have been conducted so far. Another important aspect, therefore, is the obvious yet seldom asked question: What does the edible insect product in question intend to substitute or compete with? In many cases, the motivation to produce insects is to provide an alternative source of animal protein. However, this may not necessarily mean that less meat overall is consumed. Most commercially produced insects, such as those in Thailand or western countries, are used as snacks or novelty products (Fellows 2014;

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Agron. Sustain. Dev. (2016) 36: 57

Table 1 A list of all papers from journals that present applications of life cycle assessment (LCA) in insects for food and feed production systems up to July 2016 Insect species and order

Country

Tenebrio molitor and Zophobas morio (Coleoptera) Musca domestica (Diptera)

Netherlands

1

Mass based (kg of fresh product and kg of edible protein)

Commercial insect producer

Ecoinvent 1.1; IPCC (Oonincx and 2007 (GWP); de Boer characterization 2012) factors from the literature

Netherlands

2

Mass based (ton of larvae meal on dry matter basis)

Experimental studies

Mass based (kg of manure dry matter)

Experimental trials

(van Zanten Characterization et al. 2015) factors from the literature; IPCC 2006 (GHG); Ecoinvent 2.0 ReCiPe (Roffeis et al. 2015)

Mass based (kg of product ready for consumptionafter assembly, processing, delivering, and frying by consumer); calorific energy content; digestible bulk protein Mass based (ton of food waste treated through larvae biodigestion, kg of protein and kg of lipids) Mass based (kg of dried defatted insect powder and kg of ready-for-consumption fresh product at processing gate)

Literature

ReCiPe V1.08; IMPACT 2002+

(Smetana et al. 2015)

Pilot plant

CML 2 baseline 2000; IPCC 2007 (GWP) IMPACT 2002+; Eco-indicator 99; CML; IPCC 2007; ReCiPe V1.08

(Salomone et al. 2016)

Musca domestica (Diptera) Tenebrio molitor and Zophobas morio (Coleoptera) Hermetia illucens (Diptera) Hermetia illucens (Diptera)

Slovakia, Spain

Goal Functional unit(s)

3, 4

Netherlands

5

Italy

6

Germany

7

Foreground data source Assessment method

Industrial-scale insect producer, production trials

Reference

(Smetana et al. 2016)

Country category considers the area in which the insect production takes place. Goals: 1 to compare the environmental impact of producing a given insect species with conventional sources of animal protein, 2 to assess the environmental impact of conventional livestock production when fed insects reared on waste products, 3 to estimate the sustainability and utility of insect-rearing techniques, 4 to assess substrate suitability, 5 to compare different meat substitutes with chicken, 6 to assess the environmental impacts of insect-based feed products fed with different waste products, and 7 to assess the environmental impacts of insect production for both food and feed on an industrial scale. As seen in the table above, each study addressed just one or two of these goals

Halloran et al. 2016) and therefore do not substitute animal-source foods. The definition of the functional unit is crucial in food LCA. Several studies have shown that the impact of the results may change significantly according to the functional unit adopted in the study (Cerutti et al. 2013). All of the studies above used massbased functional units (Table 1). However, not all of the functional units pertained to an insect-based product intended for animal or human consumption. In line with their respective objectives, Roffeis et al. (2015) considered the mass of 1 kg of manure dry matter as their functional unit. This infers that the insect product system is considered as a waste treatment system and the insects produced are considered by-products within this study. Van Zanten et al. (2015) considered the dry weight of fly larvae, while Oonincx and de Boer (2012) and Smetana et al. (2015) considered the fresh weight of mealworms as their functional unit. Smetana et al. (2015) also employed two alternative functional units: calorific energy content and digestible bulk protein.

Smetana et al. (2016) considered dried defatted insect powder and fresh product at processing gate as the functional units. Finally, Salomone et al. (2016) considered the amount of treated waste as the functional unit. It is evident that the functional unit closely reflects the purpose of the production system, for example if it is a waste treatment system or a production system. Cradle-to-plate (consumer use) was applied as a system boundary in two of the studies (Smetana et al. 2015; Salomone et al. 2016), while the remaining four studies used the cradle-to-farm gate system boundary (Oonincx and de Boer 2012; Roffeis et al. 2015; van Zanten et al. 2015; Smetana et al. 2016). None of the studies considered a recycling process within system boundaries. Relatively limited system boundaries were used due to a lack of data (Roffeis et al. 2015). Only three different insect species have been the subject of LCAs on insects as food or feed (Table 1). According to the European Food Safety Agency, approximately 16 very

Agron. Sustain. Dev. (2016) 36: 57

different types of insect species from the orders Coleoptera, Diptera, Hemiptera, and Lepidoptera are currently farmed on a commercial basis both inside and outside Europe (EFSA Scientific Committee 2015). 2.2.1 Recommendations—choice of functional unit Owing to the diversity of the scopes of the studies, it is not possible to define a specific functional unit to be applied. Clearly, it depends case by case on what the insects are being compared to. Nevertheless, it is important that the chosen functional unit is linked to one or more of the characteristics held in common between insect-based foods and competing product(s). For example, if the study focuses on the substitution of animal protein from livestock with other sources, a simple mass-based functional unit should not be used. Instead, a nutrient-based unit, such as the protein content fraction that is available to humans (or animal), should be used. Other variations of mass-based functional units that have also been used for other livestock products include per kilogram or tonne of product or per kilogram of carcass weight (de Vries and de Boer 2010; de Vries et al. 2015). On the other hand, products based on livestock proteins, vegetable protein, or edible insects may have very different prices; therefore, one way to take this into consideration is to apply an economicbased functional unit (van der Werf and Salou 2015), such as one dollar of flour used for final product preparation. When conducting studies related to insect production as a means of addressing direct malnutrition, it is relevant to employ a functional unit that considers the amount of protein or micronutrients in the product. As a general recommendation, it is suggested that different functional units be used together, in particular at least two of the three functional units, i.e., mass, nutrient, or economic-based. 2.3 Inventory analysis In the inventory phase of an LCA, a system model is constructed that models the emissions and resource consumption in each of the stages of the life cycle of the analyzed product (ISO 14040: 2006 and ISO 14044:2006). In the subsections below the different stages of insect production systems are presented and the aspects that should be considered in insect production systems are discussed. 2.3.1 Construction of facilities According to Sainz (2003), “intensification of animal production systems has required external inputs to achieve the high yields expected from the investment in facilities, equipment and breeding stock”. Of the six LCA studies conducted on insect production (Table 1), only one considered the materials used in the constructions of buildings (Roffeis et al. 2015).

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However, a sensitivity analysis found that the construction of production facilities did not substantially influence the results. Requirements for housing and other facilities, as well as the scale and intensity of the production, vary dramatically between regions. Small-scale production found in warmer climates may be protected by simple structures. For example, the majority of Acheta domesticus and Gryllus bimaculatus production systems in Thailand are created from pens made of AAC concrete, with open sides and tin roofs, and represent a potentially low impact system (Halloran 2014). On the other hand, more advanced systems—such as those found in the Netherlands or Canada—could resemble modern facilities similar to those for domesticated livestock. Therefore, materials used for construction are often much more dependent on local conditions (i.e., climate and availability of materials) than on the type of farmed animal in question. Here, an important question remains: are there any advantages concerning the housing or construction of other facilities for insect production when compared to other types of animal protein production? Modern industrial chicken production, for instance, is highly optimized with temperature-controlled facilities. Such units are contained within walls and have some degree of insulation. In comparison with existing A. domesticus and G. bimaculatus production systems in Thailand, this is expensive and associated with larger impacts. While the future development of insect production systems is difficult to predict, one determining factor may be whether or not it is economically advantageous to control the temperature so that insects can be produced continuously all year round. In the case of small-scale insect farming, up-scaled production will need to be treated on a case-by-case basis. 2.3.2 Feed As seen from the livestock sector, the environmental impacts associated with feed production contribute a major part of total environmental impacts. Approximately 33 % (470 million hectares) of the total global arable land is dedicated to animal feed production (Steinfeld et al. 2006). The increased conversion efficiency of insects compared with other kinds of livestock holds the potential for decreasing the impacts associated with feed production. However, feed production is still likely to be responsible for a large part of the impacts. Vollrath et al. (2013) conclude that 49 % of the energy used in silk production is attributed to the manufacture of fertilizers and energy for the irrigation of mulberry trees, whose leaves are consumed by the monophagous Bombyx mori. In another LCA, the main environmental impacts of Tenebrio molitor production—including global warming potential and energy and land use—are associated with mixedgrain feed in all cases (Oonincx and de Boer 2012). The latter issue may be addressed by finding alternative feed sources. For example, Lundy and Parrella (2015) note that “identifying regionally scalable waste substrates of

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sufficient quality to produce crickets that have no direct competition from existing protein production systems might be the most promising path for producing crickets economically, with minimal ecological impact, and at a scale of relevance to the global food supply.” Overall, their study concludes that the feed that the crickets are fed and the livestock systems to which they are compared will ultimately determine the environmental sustainability of crickets as a human food supply. There may be cases where the high metabolism of insects would allow them to feed on waste or other products that could not be used for livestock. Efforts are being made to develop such systems that are efficient and not hampered by problems which may threaten hygiene and consequentially food safety (van Huis et al. 2013). Waste can be spent grains or other by-products from the food industry. However, Shockley and Dossey (2014) argue that while organic biomass such as agricultural and food by-products or low-value or novalue biomass can be used, this does not always mean that it is the option that has the lowest potential environmental impact. As such, Garnett et al. (2015) note that the by-product is a societal construct and cultural, economic, technological, and other practical factors play an important role in the consideration of what is called a by-product. While the poikilothermic nature of insect species improves their ability to efficiently convert food into body mass, this alone cannot be the sole characteristic by which to denote edible insects as an environmentally sustainable food option. As such, scaled-up global production will ultimately mean that livestock (and even humans) and some insect species such as crickets will require and compete for the same resources. This fundamental issue, shared across other forms of livestock production, has led to the exploration of organic side streams or waste streams. Whether or not some edible insect species intended for human consumption will be permitted to be reared on such streams will ultimately be a matter of regional or national food safety regulations (EFSA Scientific Committee 2015). Lundy and Parrella (2015, p.2–3) note that “determining the feed and protein conversion efficiencies of scalable, organic side-streams is a necessary step to determining the potential for crickets to be used as a protein recovery/ recycling pathway...” Furthermore, they also note that crickets fed a similar diet to other conventional livestock will ultimately be added to the competition for feed under the trend of increasing global feed prices. It should also be considered that not all insects require a similar diet to conventional livestock. The class Insecta comprises at least one million described species and potentially several million undescribed species (Grimaldi and Engel 2005). Their natural diets differ significantly: there are foliage feeders such as crickets and many lepidopteran larvae, and there are species that naturally feed on wood or roots (Ayayee et al. 2015). Yet, other species such as aphids and mosquitoes pierce and suck from plants or animals. Predators and detrivorous species are also to be found

Agron. Sustain. Dev. (2016) 36: 57

among insects. In other words, whether or not produced insects can be compared with conventional livestock with respect to feeding must be a case-by-case evaluation. In production systems where productivity and high turnover are core functions, insects also require feed that is formulated for rapid growth. As such, some farmed insect species may be fed high-quality, high-protein feeds (e.g., chicken feed) in order to decrease the time required to harvest. In Thailand, for example, chicken feed is preferred by farmers because its high protein content (14–21 %) enables faster growth. In their study, Nakagaki and DeFoliart (1991) fed their crickets on chicken, cricket and rabbit feed with a protein content of 22.3, 17, and 14 %, respectively. Feed optimization in the livestock sector has been an important aspect of economic efficiency. Highly formulated feeds have been designed to provide animals with the right nutrition to grow quicker and larger. There is little doubt that further demand for edible insect species will generate the interest of feed producers to formulate similar feeds for insects. This has already been observed in Thailand (Halloran et al. 2016). Less feed per body mass gained equates to less water required to water crops (van Huis et al. 2013). However, only one study focusing specifically on the water footprint of edible insect species has been carried out. In a cradle-to-farm gate approach, Miglietta et al. (2015)1 conclude that commercially produced T. molitor and Z. morio intended for human consumption have a lower water footprint (0.003 m3/year/mealworm) than other traditionally farmed animals, including cattle, pigs, and broilers (631, 521, and 26 m3/year/animal, respectively). However, they found that the water footprint of these species was largest when considering feed production. Therefore, three additional aspects must also be considered when evaluating the virtual water footprint associated with edible insect production: (1) how much they consume, (2) feed composition, and (3) the origin of the feed itself (Miglietta et al. 2015). 2.3.3 Production Temperature Some studies have addressed the effect of temperature on the growth of crickets. According to Hoffmann (1973), the preferred temperature range for larvae of G. bimaculatus is between 34 and 36 °C. This temperature range may be considered as optimal in terms of developmental speed; however, when physiological parameters such as weight gain and mortality are taken into consideration, 34– 36 °C is not at all optimal. Insects have a fluctuating metabolism reflecting fluctuating temperature. According to Ayieko et al. (2015), production times for A. domesticus are highly dependent on temperature. 1

This study was based on Oonincx and de Boer (2012).

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A. domesticus that grow at an optimal temperature of 30 °C can finish a cycle in approximately 8 weeks, while A. domesticus that grow at 18 °C can take up to 8 months to develop. Longer life cycles may possibly equate to a greater demand for inputs such as water and feed.

et al. 2015). Feed conversion efficiency, also known as feed conversion ratio (FCR), is calculated as follows:

Energy consumption Insects are poikilothermic; therefore, their core temperature varies with environmental conditions, and thus, they have a limited ability to metabolically maintain core temperature when compared to birds and mammals (NRC 2011). As such, Clifford and Woodring (1990) recommend the use of incubators, temperature cabinets, or rooms with heat blowers to keep the ambient temperature above 25 °C when rearing A. domesticus; temperatures below 25 °C have been found to be detrimental to growth and even threatening to survival. Metabolic heat generation should also be considered: Larger larvae in mealworm production systems in the Netherlands were found to produce a surplus of metabolic heat and suggesting that this heat could be used to generate heat for smaller, more heat-demanding larvae (Oonincx and de Boer 2012). At this point, insect-rearing systems have not been mechanically optimized and depend greatly on manual labor (Rumpold and Schlüter 2013). Technically sophisticated systems will, in turn, require higher energy inputs for mechanical operation and temperature control. Thus, larger, climatecontrolled facilities also bare their own environmental burdens, often through the use of fossil fuels. Oonincx et al. (2012) found high energy use on a T. molitor farm in the Netherlands. While this may certainly be the case in Europe and North America, tropical climates are better suited to providing relatively high temperatures for rearing insect species such as A. domesticus. Therefore, geographical location plays a particular role in influencing the amount of energy required to regulate temperature. According to Oonincx et al. (2012), low ambient temperatures will require higher energy inputs in insect production. In an LCA comparing mealworm, pork, milk, beef, and chicken production, mealworm production required more energy than chicken and milk production. Therefore, energy use may contribute significantly to total GHG emissions and energy use from a given production system.

FCR is not a fixed number. Table 2 demonstrates that FCR is difficult to compare between studies. Most studies have been conducted in laboratory settings and may not accurately represent variations between farms. Moreover, previous studies conducted on feed-to-protein conversion by edible insect species (Nakagaki and Defoliart 1991; Collavo et al. 2005; Offenberg 2011) have been conducted on low population densities which are not economically viable (Lundy and Parrella 2015) or with different diets and densities. Thus, the context under which the system is analyzed will define the relative environmental benefits of cultivating insect species. For example, in their study of biomass output and feed conversion ratios, Lundy and Parrella (2015) note that commercially produced A. domesticus fed grain-based diets exhibit improved feed conversion efficiency when compared to livestock species. They also found that higher-density A. domesticus populations have higher or less efficient FCRs. In another explanation of the differences in FCRs for insects, Oonincx et al. (2015) note that protein density and composition are the most important determinants of growth rates and efficiencies. This is because insects do not use energy to maintain body temperature. On the other hand, the energy content of feed plays a much more important role in the growth rates and efficiency of conventional livestock. FCR is also linked to temperature (see 2.2.1.3). For example, Nakagaki and DeFoliart (1991) found that crickets have a lower reported FCR than broiler chicks and pigs at a temperature of 30 °C or higher. At the same temperature, crickets have an even lower FCR when compared to sheep and cattle. Another example of the differences in FCR is that of B. mori. Ingesting the same amount of mulberry leaves under different environmental, feeding, and nutritional conditions affects its ability to digest, absorb, and convert the ingested leaves to body matter (Rahmathulla and Suresh 2012). Additional factors influencing FCR include the dressing percentage (the body of an animal after the hide, head, tail, extremities, and viscera have been removed) and the carcass refuse. The edible fraction of an insect is generally much higher than that of vertebrate livestock (Nakagaki and Defoliart 1991). In contrast, often the entire insect (except appendages and wings for adults) is eaten. Current vocabulary for comparing edible parts with vertebrate “meat” and other parts such as “liver” is simply missing (Evans et al. 2015), which hampers comparisons of the efficacy of insects versus vertebrates. However, using FCR to evaluate the environmental impacts of some insect species compared to livestock

Feed conversion ratio Feed conversion ratio is a common method to evaluate efficiency in livestock production. According to Nakagaki and DeFoliart (1991), “food conversion efficiency of animals is one of the important factors that must be considered in choosing environmentally sound food alternatives for the future.” Other scholars have also indicated that this efficiency is an important asset in the production of commercial livestock production (Ramos-Elorduy 2008; Oonincx and de Boer 2012; van Huis et al. 2013; Oonincx

Mass of the feed consumed ¼ FCR Fresh weight of edible component

57 Page 8 of 13 Table 2

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Select examples of feed conversion ratio (FCR) in the production of edible insects for human consumption

Species

FCR

Tenebrio molitor

2.2

Feed

Mixed grains (wheat bran, oats, soy, rye, and corn supplemented with beer yeast) and carrots 3.8 ± 0.63 High protein, high fat diet (60 % spent grains, 20 % beer yeast, 20 % cookie remains) 5.3 ± 0.81 Low-protein, high-fat diet (50 % cookie remains and 50 % bread) Acheta 1.47 Poultry feed (primarily of maize and domesticus soy grain products) 1.91

1.65 1.08

Metamorphic state

Average temperature

Source

Adult

Unknown (a temperature-controlled environment)

(Oonincx and de Boer 2012)

116 days ± 5.2 28 °C

(Oonincx et al. 2015)

191 ± 21.9

28 °C

(Oonincx et al. 2015)

33 days

29.0 ± 2.1 SD °C

(Lundy and Parrella 2015)

Grocery store food waste enzymatically converted into 90 % liquid fertilizer and 10 % solids Purina Rabbit Chow

44 days

29.0 ± 2.1 SD °C

(Lundy and Parrella 2015)

Eighth instar

33–35 ± SD °C

Selph’s cricket feed (ingredients not disclosed)

Eighth instar

33–35 ± SD °C

(Nakagaki and Defoliart 1991) (Nakagaki and Defoliart 1991)

1.69

Human refuse diet (fruits and 45 days vegetables 34 %, rice and pasta 27 %, pork and beef meat 11 %, bread 11 %, cheese skins 11 %, yolk 6 %) 4.5 ± 2.84 High protein, high fat (60 % spent grains, 55 ± 7.3 20 % beer yeast, 20 % cookie remains)

species is questionable. The reason for this has to do with the fact that FCR considers fresh weight. This means that a high FCR can be achieved if the final product has a high water content. FCR does not consider the digestibility of the product. For example, for insect species where the exoskeleton is eaten, a low FCR is achieved; however, the exoskeleton is not digestible and does not provide nutritional value. However, it should be noted that chitinases (enzymes which breakdown chitin) have been found in the intestines of human populations with a higher rate of entomophagy (Paoletti et al. 2007). As Garnett et al. (2015) ask: “But what is efficiency? What are we being efficient with and efficient for?” Rather than being a scientific means for calculating efficiency and environmentally sustainable optimization of feed resources, FCR appears to be a unit employed to calculate economic efficiency rather than resource efficiency.

Water The high feed conversion rates of insects, therefore, correspond to their water use efficiency (Oonincx and de Boer 2012; Shockley and Dossey 2014). However, there has been limited research on the topic of water consumption by production insects.

30.5 °C

(Collavo et al. 2005)

28 °C

(Oonincx et al. 2015)

Greenhouse gas emissions GHG emissions play an important role in the impacts generated during livestock production, and one of the potential benefits of instigating insect production systems may be the reduction of these emissions. It is well known that some insects produce large amounts of methane. However, in general, very little information is available about emissions of greenhouse gases from insects used in production systems. In 2010, Oonincx et al. conducted a study of the greenhouse gas and ammonium emissions associated with T. molitor, A. domesticus, and Locusta migratoria. They note that CO2 production is highly dependent on species, metamorphic stage, temperature, feeding status, and level of activity. A follow-up LCA study on T. molitor production demonstrates that the land use and GHG emissions are less than for pigs, chickens, and cattle per kilogram of animal protein (Oonincx and de Boer 2012). Termites are consumed in many countries, most commonly in sub-Saharan Africa (van Huis et al. 2013). While termites are reportedly very difficult to farm intensively (Kinyuru et al. 2015), methanogenic bacteria that inhabit their guts can generate a significant amount of methane (between