Edible and medicinal termites: a global overview

Journal of Ethnobiology and Ethnomedicine

Rômulo Romeu Nóbrega Alves²  Iamara Silva Policarpo¹  Alexandre Vasconcellos¹  Rozzanna Esther Cavalcanti Reis de Figueirêdo¹ 

[1] Departamento de Sistemática e Ecologia, CCEN, Universidade Federal da Paraíba, Laboratório de Termitologia, PB, 58051-900, João Pessoa, Brazil;Departamento de Biologia, Universidade Estadual da Paraíba, Laboratório de Termitologia, PB, 58051-900, João Pessoa, Brazil

关键词: Entomotherapy;    Entomophagy;    Ethnozoology;    Ethnoentomology;   

Others  :  1212450
DOI  :  10.1186/s13002-015-0016-4

 received in 2015-01-27, accepted in 2015-03-14,  发布年份 2015

【 摘 要 】

Termites are mainly known for damage caused to human beings, both in urban and rural areas. However, these insects play an important role in the decomposition of organic matter in tropical regions and are important natural resources, which are widely used in traditional medicine and are also consumed by human populations in several parts of the world. This study aimed to catalogue termite species used worldwide through a literature review, characterizing them by its human populations’ use. The results showed that at least 45 species of termites, belonging to four families, are used in the world, with 43 species used in human diet and/or in livestock feeding. Nine termite species are used as a therapeutic resource. There is an overlapping use of seven species. The use of termites was registered in 29 countries over three continents. Africa is the continent with the highest number of records, followed by America and Asia. The results suggest that, in addition to their ecological importance, termites are a source of medicinal and food resources to various human populations in various locations of the world, showing their potential for being used as an alternative protein source in human or livestock diets, as well as a source for new medicines.

【 授权许可】

   
2015 Figueirêdo et al.; licensee BioMed Central.

【 参考文献 】

• [1]Alves RRN, Mendonça LET, Confessor MVA, Vieira WLS, Lopez LCS. Hunting strategies used in the semi-arid region of northeastern Brazil. J Ethnobiol Ethnomed. 2009; 5:1-16. BioMed Central Full Text
• [2]Alves RRN. Relationships between fauna and people and the role of ethnozoology in animal conservation. Ethnobiology and Conservation. 2012; 1:1-69.
• [3]Meyer-Rochow VB, Chakravorty J. Notes on entomophagy and entomotherapy generally and information on the situation in India in particular. Appl Entomol Zool. 2013; 48:105-112.
• [4]Raubenheimer D, Rothman J. Nutritional Ecology of Entomophagy in Humans and Other Primates. Annu Rev Entomol. 2012; 58:141-160.
• [5]Dossey AT. Insects and their chemical weaponry: New potential for drug discovery. Nat Prod Rep. 2010; 27:1737-1757.
• [6]Alves RRN, Alves HN. The faunal drugstore: Animal-based remedies used in traditional medicines in Latin America. J Ethnobiol Ethnomed. 2011; 7:1-43. BioMed Central Full Text
• [7]Alves RRN, Albuquerque UP. Animals as a Source of Drugs: Bioprospecting and Biodiversity Conservation. In: Animals in Traditional Folk Medicine: Implications for Conservation. Alves RRN, Rosa IL, editors. Springer, Heidelberg; 2013: p.67-89.
• [8]Costa-Neto EM. Entomotherapy, or the Medicinal Use of Insects. J Ethnobiol. 2005; 25:93-114.
• [9]Meyer-Rochow VB. Entomophagy and its impact on world cultures: the need for a multidisciplinary approach. In: Forest insects as food: humans bite back. Durst PB, Johnson DV, Leslie RN, Shono K, editors. Food and Agriculture Organization of the United Nations, Thailand; 2010: p.23-36.
• [10]Srivastava SK, Babu N, Pandey H. Traditional insect bioprospecting-As human food and medicine. Indian J Tradit Knowl. 2009; 8:485-494.
• [11]Costa-Neto EM. The Use of Insects in Folk Medicine in the State of Bahia, Northeastern Brazil, With Notes on Insects Reported Elsewhere in Brazilian Folk Medicine. Hum Ecol. 2002; 30:245-263.
• [12]Lee KE, Wood TG. Termites and Soils. Academic Press, New York; 1971.
• [13]Vasconcellos A, Moura FMS. Wood litter consumption by three species of Nasutitermes termites in an area of the Atlantic Coastal Forest in northeastern Brazil. J Insect Sci. 2010; 10(72):1-9.
• [14]Solavan A, Paulmurugan R, Wilsanand V. Effect of the subterranean termite used in the South Indian folk medicine. Indian J Tradit Knowl. 2006; 5:376-379.
• [15]Coutinho HDM, Vasconcellos A, Lima MA, Almeida-Filho GG, Alves RRN. Termite usage associated with antibiotic therapy: enhancement of aminoglycoside antibiotic activityby natural products of Nasutitermes corniger (Motschulsky 1855). BMC Complement Altern Med. 2009; 9(35):1-4.
• [16]Lima JRB, Santos CAB. Recursos Animais Utilizados na medicina Tradicional dos Índios Pankararu no Nordeste do Estado de Pernambuco, Brasil. Etnobiologia. 2010; 8:39-50.
• [17]Alves RRN. Fauna used in popular medicine in Northeast Brazil. J Ethnobiol Ethnomed. 2009; 5:1-30. BioMed Central Full Text
• [18]Alves RRN, Dias TL. Usos de invertebrados na medicina popular no Brasil e suas implicações para conservação. Tropical Conservation Science. 2010; 3:159-174.
• [19]Van-Huis H. Insects as food in Sub-Saharan Africa. Insect Science and its Application. 2003; 23:163-185.
• [20]Wilsanand V. Utilization of termite, Odontotermes formosanus by tribes of South India in medicine and food. Nat Prod Rad. 2005; 4:121-125.
• [21]Johnson DV. The contribution of edible forest insects to human nutrition and to forest management: current status and future potential. In: Forest insects as food: humans bite back. Durst PB, Johnson DV, Leslie RN, Shono K, editors. Food and Agriculture Organization of the United Nations, Thailand; 2010: p.5-22.
• [22]Niaba KV, Atchibri LO, Gbassi KG, Beugre AG, Adou M, Anon AB et al.. Consumption survey of edible winged termites in Cote d’Ivoire. Int J Agric Food Sci. 2012; 2:149-152.
• [23]Van-Huis H. Potential of insects as food and feed in assuring food security. Annu Rev Entomol. 2013; 58:563-583.
• [24]Shockley M, Dossey AT. Insects for Human Consumption. In: Mass Production of Beneficial Organisms. Morales-Ramos J, Rojas G, Shapiro-Ilan DI, editors. Elsevier, London; 2014: p.617-652.
• [25]Jongema, Y. List of edible insect species of the world. 2014 [cited 2014 05 november]; http://www.wageningenur.nl/en/Expertise-Services/Chair-groups/Plant-Sciences/Laboratory-of-Entomology/Edible-insects/Worldwide-species-list.htm]
• [26]Moussa JB. Les chenilles comestibles du Congo: Intérêt alimentaire et circuits de commercialisation: Cas de Brazzaville. Rapport de Consultation. Food and Agriculture Organization of the United Nations, Rome; 2002.
• [27]Hoare AL. The use of non-timber forest products in the Congo Basin: Constraints and opportunities. The Rainforest Foundation. 2007; 1:1-57.
• [28]Malaisse F. Se nourir en foret Claire africaine: approche ecologique et nutritionnelle. Les Presses Agronomiques de Gembloux, Gembloux; 1997.
• [29]Oliveira JFS, Carvalho RFXP, Sousa B, Simão MM. The nutritional value of four species of insects consumed in Angola. Ecol Food Nutr. 1976; 5:91-97.
• [30]Silow CA. Notes on Ngangela and Nkoya Ethnozoology ants and termites. Goteborgs Etnografiska Museum, Goteborg; 1983.
• [31]Mbata KJ. Traditional use of arthropods in Zambia. Food Insects Newsletters. 1995; 8:5-7.
• [32]Bahuchet. Les pygmées Aka et la forêt Centrafricaine. Paris: Selaf; 1985.
• [33]Ponzetta MT. Rôle alimentaire des insects dans L’évolution humain. In: Motte-Florac E, Thomas JMC, editors. In Les “insectes” dans la tradition orale. Peeters, Paris: SELAF; 2003. p. 633.
• [34]Boesch C, Boesch H. Tool Use and Tool Making in Wild Chimpanzees. Folia Primatol. 1990; 54:86-99.
• [35]McGrew WC, Collins DA. Tool use by wild chimpanzees (Pan troglodytes) to obtain termites (Macrotermes herus) in the Mahale Mountains, Tanzania. Am J Primatol. 1985; 9:47-62.
• [36]McGrew WC, Roger E. Brief report: Chimpanzees, tools, and termites: New record from Gabon. Am J Primatol. 1983; 5:171-174.
• [37]Sanz C, Morgan D, Gulick S. New Insights into Chimpanzees, Tools, and Termites from the Congo Basin. Am Nat. 2004; 164:567-581.
• [38]DeFoliart GR. The human use of insects as food resource: a bibliographic account in progress. 2002; http://www.food-insects.com/book7_31/The%20Human%20Use%20of%20Insects%20as%20a%20Food%20Resource.htm]
• [39]DeFoliart GR. Insects as food: Why the Western Attitude Important. Annu Rev Entomol. 1999; 44:21-50.
• [40]Phelps RJ, Struthers JK, Moyo SJL. Investigations into the Nutritive Value of Macrotermes falciger (Isoptera: Termitidae). Zoologia africana. 1975; 10:123-132.
• [41]Blum MS. The limits of entomophagy: a discretionary gourmand in a world of toxic Insects. The Food Insects Newsletter. 1994; 7:6-11.
• [42]Fasoranti JO, Ajiboye DO. Some edible insects of Kwara State, Nigeria. Am Entomol. 1993; 39:113-116.
• [43]Kinyuru JN, Konyole SO, Kenji GM, Onyango CA, Owino VO, Owor BO et al.. Identification of traditional foods with public health potential for complementary feeding in western Kenya. J Food Res. 2012; 1:148-158.
• [44]Roulon-Doko P. Chasse, cueillette ET cultures chez lês Gbaya de Centrafrique. L'Harmattan, Paris; 1998.
• [45]Nkouka E. Les insectes comestibles dans lês societes d'Afrique Centrale. Muntu. 1987; 6:171-178.
• [46]Bequaert J. Insects as food: How they have augmented the food supply of mankind in early and recent times. Nat Hist J. 1921; 21:191-200.
• [47]Ayieko MA, Nyambuga IA. Termites and lake flies in the livelihood of households within the Lake Victoria region: Methods for harvesting and utilization. Technical report for the National Museums of Kenya, Research Program on Sustainable Use of Dryland Biodiversity, National Museums of Kenya, Nairobi, Kenya; 2009:1–11.
• [48]Chavanduka DM. Insects as a source of protein to the Africain. The Rhodesia Science News. 1976; 9:217-220.
• [49]Banjo AD, Lawal OA, Songonuga EA. The nutritional value of fourteen species of edible insects in Southwestern Nigeria. Afr J Biotechnol. 2006; 5:298-301.
• [50]Bodenheimer FS. Insects as human food: a chapter of the ecology of man. Dordrecht: The Hague; 1951.
• [51]Costa-Neto EM, Ramos-Elorduy J. Los insectos comestibles de Brasil: etnicidad, diversidad e importância em La alimentación. Bol Soc Entomol Aragon. 2006; 38:423-442.
• [52]Paoletti MG, Buscardo E, Dufour DL. Edible invertebrates among Amazonian indians: a critical review of disappearing knowledge. Environ Dev Sustain. 2000; 2:195-225.
• [53]Araujo Y, Beserra P. Diversidad de invertebrados consumidos por las etnias Yanomami y Yekuanadel Alto Orinoco, Venezuela. Interciencia. 2007; 32:318-323.
• [54]Gahukar RT. Entomophagy and human food security. International Journal of Tropical Insect Science. 2001; 31:129-144.
• [55]Hanboonsong Y. Edible insects and associated food habits in Thailand. In: In Forest insects as food: humans bite back. Durst PB, Johnson DV, Leslie RN, Shono K, editors. Food and Agriculture Organization of the United Nations, Thailand; 2010: p.173-182.
• [56]Chung AYC, Chey VK, Unchi S, Binti M. Edible insects and entomophagy in Sabah, Malaysia. The Malayan Nature Journal. 2002; 56:131-144.
• [57]Chen X, Feng Y, Chen Z. Common edible insects and their utilization in China. Entomological research. 2009; 39:299-303.
• [58]Chen X, Feng Y. The edible insects of Chin. Science and Technology Publishing House, Beijing, China; 1999.
• [59]Nomura H. Entomologia pitoresca I – Os insetos nas crenças, superstições e medicina popular. Análise bibliográfica Sitientibus Série Ciências Biológicas. 2006; 6:145-158.
• [60]Sousa RS. Etnobotânica e Etnozoologia de Comunidades Pesqueiras da Área de Proteção Ambiental (APA) do Delta do Parnaíba, Nordeste do Brasil. MSc. dissertation. Universidade Federal do Piauí, Teresina; 2010.
• [61]Costa-Neto EM, Ramos-Elorduy J, Manuel PJ. Los Insectos Medicinales De Brasil: Primeros Resultados. Bol Soc Entomol Aragon. 2006; 38:395-414.
• [62]Costa-Neto EM, Universidade Federal de São Carlos. Etnoentomologia no Povoado de Pedra Branca, Município de Santa Terezinha, Bahia.Um Estudo de Caso das Interações Seres Humanos/Insetos. PhD. thesis. 2003.
• [63]Coutinho HDM, Lôbo KM, Bezerra DAC, Lôbo I. Peptides and Proteins with antimicrobial activity. Indian J Pharmacol. 2008; 40:3-9.
• [64]Coutinho HDM, Vasconcellos A, Freire-Pessoa HL, Gadelha CA, Gadelha TS, Almeida-Filho GG. Natural products from the termite Nasutitermes corniger lowers aminoglycoside minimum inhibitory concentrations. Pharmacogn Mag. 2010; 6:1-4.
• [65]Alves RRN, Leo Neto NA, Brooks SE, Albuquerque UP. Commercialization of animal-derived remedies as complementary medicine in the semi-arid region of Northeastern Brazil. J Ethnopharmacol. 2009; 124:600-608.
• [66]Souto WMS, Mourão JS, Barboza RRD, Alves RRN. Parallels between zootherapeutic practices in ethnoveterinary and human complementary medicine in northeastern Brazil. J Ethnopharmacol. 2011; 134:753-767.
• [67]Alves RRN, Lima HN, Tavares MC, Souto WMS, Barboza RRD, Vasconcellos A. Animal-based remedies as complementary medicines in Santa Cruz do Capibaribe, Brazil. BMC Complement Altern Med. 2008; 8:1-9. BioMed Central Full Text
• [68]Souto WMS, Mourão JS, Barboza RRD, Mendonça LET, Lucena RFP, Confessor MVA, Vieira WLS, Montenegro PFGP, Lopez LCS, Alves RRN. Medicinal animals used in ethno veterinary practices of the ‘Cariri Paraibano’, NE Brazil. J Ethnobiol Ethnomed. 2011; 7:1-19. BioMed Central Full Text
• [69]Ferreira FS, Albuquerque UP, Coutinho HDM, Almeida WO, Alves RRN. The Trade in Medicinal Animals in Northeastern Brazil. Evidence-Based Complementary and Alternative Medicine. 2012; 2012:1-20.
• [70]Albuquerque UP, Melo JG, Medeiros MF, Menezes IR, Moura GJ, El-Deir ACA, Alves RRN, Medeiros PM, Araujo TAS, Ramos MA et al.. Natural Products from Ethno directed Studies: Revisitingthe Ethnobiology of the Zombie Poison. Evidence-Based Complementary and Alternative Medicine. 2012; 2012:1-19.
• [71]Alves RRN, Barbosa JAA, Santos SLDX, Souto WMS, Barboza RRD. Animal-Based Remedies as Complementary Medicines in the Semi-Arid Region of Northeastern Brazil. Evidence-Based Complementary and Alternative Medicine. 2011; 2011:1-15.
• [72]Alves RRN, Silva CC, Barboza RRD, Souto WMS. Zootherapy as an alternative Therapeutic in South America. J Alt Med. 2009; 1:21-47.
• [73]Alves RRN, Soares TCS, Mourão JS. Uso De Animais Medicinais Na Comunidade De Bom Sucesso, Soledade, Estado Da Paraíba, Brasil. Sitientibus Série Ciências Biológicas. 2008; 8:142-147.
• [74]Alves RRN, Oliveira MG, Barboza RRD, Singh R, Lopez LCS. Medicinal Animals as Therapeutic Alternative in a Semi-Arid Region of Northeastern Brazil. Forsch Komplementmed. 2009; 16:305-312.
• [75]Ferreira FS, Fernandes-Ferreira H, Leo Neto N, Brito SV, Alves RRN. The trade of medicinal animals in Brazil: current status and perspectives. Biodivers Conserv. 2013; 22:839-870.
• [76]Kinyuru JN, Konyole SO, Roos N, Onyango CA, Owino VO, Owiuor BB, Fris H, Aagaard-Hansen J, Kenji GM. Nutrient composition of four species of winged termites consumed in western Kenya. J Food Compos Anal. 2013; 30:1-19.
• [77]Riggi L, Veronesi M, Verspoor R, MacFarlane C, Tchibozo S. Exploring entomophagy in Northern Benin: Practices, perceptions and possibilities. Book of Abstracts of Conference on Insects to Feed the World, The Netherlands 14-17 May 2014.
• [78]Collins DA, McGrew WC. Termite fauna related to differences in tool-use between groups of chimpanzees (Pan troglodytes). Primates. 1987; 8:457-471.
• [79]MCBeath N, McGrew WC. Tools used by wild chimpanzees to obtain termites at Mt. Assirik, Senegal: the influence of habitat. J Hum Evol. 1982; 11:65-72.
• [80]McGrew WC. Chimpanzee Material Culture: Implications for Human Evolution. Cambridge University Press, Cambridge; 1992.
• [81]Sugiyama Y, Koman J. A preliminary list of chimpanzees’ alimentation at Bossou, Guinea. Primates. 1987; 28:133-147.
• [82]Suszuki S, Kuroda S, Nishihara T. Tool-set for termite fishing by chimpanzees in the Ndoki Forest. Congo Behaviour. 1995; 132:219-235.
• [83]Deblauwe I, Janssens G. New insights in insect prey choice by chimpanzees and gorillas in southeast Cameroon: The role of nutritional value. Am J Phys Anthropol. 2008; 135:42-55.
• [84]McGrew WC, Tutin C, Baldwin P. Chimpanzees, tools, termites: crosscultural comparisons of Senegal, Tanzania, and Rio Muni. Man. 1979; 14:185-214.
• [85]Nishida T, Uehara S. Chimpanzees, tools and termites: another example from Tanzania. Curr Anthropol. 1980; 21:671-672.
• [86]Uehara S. Seasonal changes in the techniques employed by wild chimpanzees in the Mahale Mountains, Tanzania, to feed on termites (Pseudacanthotermes spiniger). Folia Primatol. 1982; 37:44-76.
• [87]Goodall J. The behavior of free-living chimpanzees in the Gombe Stream Reserve. Animal Behaviour Monographs. 1968; 1:161-311.
• [88]Lesnik JL. Termites in the hominin diet: A meta-analysis of termite genera, species and castes as a dietary supplement for South African robust australopithecines. J Hum Evol. 2014; 71:1-11.
• [89]Dufour DL. Insects as food: a case study from the northwest Amazon. Am Anthropol. 1987; 89:383-397.
• [90]DeFoliart GR. An Overview of the role of edible in preserving biodiversity. Ecol Food Nutr. 1996; 36:109-132.
• [91]Marconi S, Manzi P, Pizzoferrato I, Buscardo E, Cerda H, Hernandez DL et al.. Nutritional evaluation of terrestrial invertebrates as tradicional food in Amazonia. Biotropica. 2002; 34:273-280.
• [92]Hamad I, Delaporte E, Raoult D, Bittar F. Detection of termites and other insects consumed by African great apes using molecular fecal analysis. Sci Rep. 2014; 4:1-9.
• [93]Kinyuru JN, Kenji GM, Njoroge SM, Ayieko MA. Effect of processing methods on the in vitro protein digestibility and vitamin content of edible winged termite (Macrotermes subhylanus) and grasshopper (Ruspolia differens). Food Bioprocess Technol. 2010; 3:778-782.
• [94]O'Malley RC, Power ML. The energetic and nutritional yields from insectivory for Kasekela chimpanzees. J Hum Evol. 2014; 71:46-58.
• [95]Agbdye FS, Ofuya TL, Akindele SO. Some edible insect species consumed by the people of Benue state. Nigeria Pak J Nutr. 2009; 8:946-950.
• [96]Womeni HM, Linder M, Tiencheu B, Mbiapo FT, Villeneuve P, Fanni J et al.. Oils of insects and larvae consumed in Africa: potential sources of polyunsaturated fatty acids. Ocl. 2009; 16:230-235.
• [97]Chuanhui YI, Qiuju HE, Wang L, Kuang R. The utilization of insect-resources in Chinese Rural Area. J Agric Sci. 2010; 2:146-154.
• [98]DeFoliart GR. Insect fatty acids: similar to those or poultry and fish in their degree of unsaturation but higher in the polyunsaturates. Food Insects Newsl. 1991; 4:1-4.
• [99]Branch LC, Silva MF. Folk Medicine of Alter do Chão, Pará, Brazil. Acta Amazon. 1983; 13:737-797.
• [100]Oliveira ES. Uso e conservação da fauna por populações humanas no Rio Grande do Norte, Nordeste do Brasil. MSc. dissertation. Universidade Federal do Rio Grande do Norte, Departamento de Botânica, Ecologia e Zoologia; 2011.
• [101]Marie R, Strasbourg University. Contribution a I’histoire des insects en thérapeutique. Phd. thesis. 1955.
• [102]Wilsanand V, Preema V, Rajitha P. Therapeutics of insects and insects products in South Indian traditional medicine. Indian J Pharm. 2007; 6:563-568.
• [103]Sileshi GW, Nyeko P, Nkunika POY, Sekematte BM, Akinnifesi FK, Ajayi OC. Integrating Ethno-Ecological and Scientific Knowledge of Termites for Sustainable Termite Management and Human Welfare in Africa. Ecol Soc. 2009; 14:1-21.
• [104]Krishna K, Grimaldi DA, Krishna V, Engel MS. Treatise on the Isoptera of the World. Bulletin of the American Museum of Natural History, New York; 2013.
• [105]Deblauwe I. Temporal Variation in Insect-eating by Chimpanzees and Gorillas in Southeast Cameroon: Extension of Niche Differentiation. Int J Primatol. 2009; 30:229-252.
• [106]Anankware PJ, Fening KO, Osekre E, Obeng-Ofori D. Insects as food and feed: a review. Int J Agric Res Rev. 2015; 3:143-151.
• [107]Chang AYC. Edible insects and entomophagy in Borneo. In: Durst PB, Johnson DV, Leslie RN, Shono K, editors. Forest insects as food: humans bite back. Thailand: Food and Agriculture Organization of the United Nations; 2010: 141:150.
• [108]Mitsuhashi J. The future use of insects as human food. In: Forest insects as food: humans bite back. Durst PB, Johnson DV, Leslie RN, Shono K, editors. Food and Agriculture Organization of the United Nations, Thailand; 2010: p.115-122.
• [109]Ramos-Elorduy J. Insects: a hopeful food source. In: Ecological implications of minilivestock. Paoletti MG, editor. Science Pub, Enfield NH, USA; 2005: p.263-291.
• [110]Lamberty M, Zachary D, Lanot R, Bordereau C, Robert A, Hoffmann JA et al.. Insect immunity constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem. 2001; 276:4085-4092.
• [111]Bulmer MS, Crozier RH. Duplication and diversifying selection among termite antifungal peptides. Mol Biol Evol. 2004; 21:2256-2264.
• [112]Bulmer MS, Crozier RH. Variation in positive selection in termite GNBPs and Relish. Mol Biol Evol. 2006; 23:317-326.
• [113]Chaves TP, Clementino ELC, Felismino DC, Alves RRN, Vasconcellos A, Coutinho HDM, et al. Antibiotic resistance modulation by natural products obtained from Nasutitermes corniger (Motschulsky, 1855) and its nest. Saudi J Biol Sc. 2014. In press.