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Insects as poultry feed: a scoping study for poultry production systems in Australia

2012, World's Poultry Science Journal

https://doi.org/10.1017/S0043933912000554

Abstract
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This study explores the potential of using insects as an alternative protein source in poultry feed to address rising grain costs and provide a sustainable, high-quality nutrition option. Insects can offer significant nutritional benefits, including better amino acid profiles compared to traditional protein sources like soybeans, making them a viable candidate for enhancing poultry production systems in Australia.

Key takeaways
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  1. Insects can significantly reduce protein supplement costs for poultry by providing a high-quality alternative to soybean meal.
  2. Protein content of edible insects ranges from 30% to 80%, surpassing that of traditional plant sources.
  3. Poultry feed conversion ratios for insects may exceed those of conventional livestock, enhancing production efficiency.
  4. Insects are bio-transformers, converting organic waste into protein-rich biomass for poultry, promoting sustainable practices.
  5. Economic feasibility of insect rearing relies on utilizing low-cost waste materials and ensuring efficient breeding methods.
doi:10.1017/S0043933912000554 Insects as poultry feed: a scoping study for poultry production systems in Australia M. KHUSRO1, N.R. ANDREW1* and A. NICHOLAS2 1Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale NSW 2351 Australia; 2Tamworth Agricultural Institute, NSW Department of Industry and Investment, 4 Marsden Park Road, Calala NSW 2340 Australia *Corresponding author: nigel.andrew@une.edu.au The feasibility of feeding insects on different types of waste materials and subsequently feeding insects to poultry is reviewed. Research in this area has demonstrated that a number of insect taxa including silkworms, locusts, 2y larvae, crickets and grasshoppers can be safely fed to chickens without compromising the quality and palatability of the meat. Most studies on the topic have dealt with which species of insects can be fed to chickens; they did not investigate rearing insects commercially which requires knowledge of insect rearing, feeding and production methods. This review examines this issue in greater depth by reviewing current literature and through discussions with the poultry farmers in the states of New South Wales and Queensland, Australia. A survey of poultry farmers found an acceptance of feeding insect to poultry provided it could be done economically and indicated that insects could be reared and fed on a variety of organic waste materials which are available in adequate amounts in different regions. The technique of feeding insects to poultry will be bene1cial in developing agriculture based recycling systems, reducing waste and potentially aid in reducing environmental pollution. Depending on the insect species and whether the diet of insects is fed to meat producing or egg laying birds it will likely need to be supplemented with either or both calcium and limiting amino acids to meet the chicken's dietary requirement. The safety and economic viability of breeding and rearing insects on organic wastes and feeding to poultry needs to be assessed. In order to be economically feasible, the overall cost of rearing and feeding insects to poultry needs to be lower than the cost of feeding conventional protein sources like grains and soybean meal. The technique of feeding insects to poultry needs to be able to be easily adopted and readily adaptable by the industry to a range of farming systems. Further research needs to investigate these issues in more detail © World's Poultry Science Association 2012 World's Poultry Science Journal, Vol. 68, September 2012 Received for publication July 25, 2011 Accepted for publication September 21, 2011 435 Insects as poultry feed: M. Khusro et al. both by establishing small experiments and developing production models which include insects reared onsite in the poultry diet. Keywords: insects; poultry; feeding; waste materials; technique Introduction The poultry industry is highly ef1cient with feed to meat conversion ratio ranging between 1.5 to 1.8 (Sengor et al., 2008) which makes chicken one of the most economically viable and important sources of meat for human consumption. Globally, poultry production relies heavily on plant protein supplements especially soybean meal. Soybean meal is a major protein supplement source for poultry and pig production systems in Australia due to its excellent amino acid composition and high level of digestibility (Willis, 2003). However, the availability of soybean meal for use in animal nutrition in the Asia-Paci1c region is limited due to its use as human feed and low productivity (Ravindran and Blair, 1992). Most soybean meal used by the poultry industry in Australia is imported from South American countries and the US (Willis 2003) which adds to the overall cost of feeding. Poultry production is based on grain, which is used for human consumption and therefore a high value commodity, which, combined with the increasing consumption of chicken on a global basis, has seen the cost of grain increase signi1cantly. Furthermore, many of the traditional ingredients used in poultry diets are forecast to be in short supply within the next ten years mainly due to an increase in the human population and unfavourable climatic conditions (Cribb, 2010). The increasing cost of grain has prompted the poultry industry to explore alternative sources of poultry feed. There is a need to identify alternative protein sources either for total or partial replacements which meet the dietary requirements and reduce feed costs (Ramos- Elorduy et al. , 2002; Das et al., 2009). Protein-rich insects are one option being considered to reduce the cost of protein supplements in poultry feed. Insects have been used as a food source for a number of different species of animal, however relatively few studies have focused on incorporating insects into the diets of domestic livestock (Finke et al. , 1985). World-wide, approximately 2,000 species of edible insects have been identi1ed for human or animal nutrition (Ramos-Elorduy, 2005). The number of edible insects for human consumption in different countries as reported by DeFoliart (2005) is presented in Table 1 . Hundreds of insect species have been used as food for a range of animals. Some of the more important groups include grasshoppers, caterpillars, beetles (usually the immature stages), winged termites, bee, wasp and ant brood (larvae and pupae) winged ants, cicadas, and a number of aquatic species. Insects have high nutritive value, not only in proteins, but for fats, minerals and vitamins (Chapman, 1998). Protein content of edible insects ranges from 30% (wood worms) to 80% (certain wasp species). Insects generally have a comparable, if not higher, number of calories/100g to cereals, vegetables, legumes and meats. Edible insects contain a diverse range of mineral salts ( e.g. sodium, potassium, calcium, zinc, iron, and magnesium) comparable or in higher amounts than conventional human food stuffs, such as beef, 1sh, turkey, milk and eggs (DeFoliart, 1992). Insects have good conversion ef1ciency due to their poikilothermic nature, i.e. not needing to maintain their body temperature. For example, crickets convert plants into biomass 1ve times faster than beef cattle (Nakagaki and DeFoliart, 1991). Once selected, using appropriate 436 World's Poultry Science Journal, Vol. 68, September 2012 Insects as poultry feed: M. Khusro et al. breeding methods, suitable species have the potential to provide a reliable and sustainable source of high-quality protein for poultry consumption (Anand et al. , 2008). Table 1 Number of edible insects for human consumption reported from different countries*. Country Number of each taxon Orders Families Genera Species Burma 7 14 17 17 China 10 30 36 46 India 7 17 22 24 Indonesia 8 15 20 25 Japan 11 19 22 27 Philippines 6 13 17 21 Thailand 10 31 69 80 Vietnam 8 18 20 24 Australia 7 22 39 49 Papua New Guinea 11 22 31 34 Congo 7 15 25 30 Madagascar 7 15 22 22 South Africa 7 16 32 36 Zaire 5 21 47 62 Zimbabwe 7 14 25 32 Brazil 7 14 19 23 Colombia 8 20 36 48 Mexico 10 42 99 136 USA 10 27 53 69 * Adapted from DeFoliart (2005) If the insects are fed on alternative food sources or organic waste products, they may add value to other agricultural industries. Acting as bio-transformers they would convert waste into protein rich animal biomass for use in poultry nutrition. The potential role of insects in agricultural diets has not been fully exploited, and culturing and rearing of insects as animal feed is not well established (apart from classic examples such as Apis mellifera and silk worms). Generally, the breeding and mass-rearing of insects does not require a complex infrastructure and their care is reportedly simple as demonstrated under laboratory conditions by Haldar et al. (1999) and Das et al. (2009). Haldar et al. (1999) reported that 84 females of Oxya fuscovittata (Marschall) (short-horned grasshopper Family Acrididae) in cages can generate approximately 1 kg of gross mass in 29-35 days. Here we assess the feasibility of utilising insects as poultry feed and what types or species of insects and at what life stage could be fed to chickens safely and economically with special focus on poultry production systems prevalent in Australia. To ensure economic viability, a key feature of this study was to examine the prospects of using industrial waste by-products as insect feed and how these waste products could be recycled or modi1ed for their subsequent use as insect feed. The bene1ts and disadvantages associated with the use of insects as feed for poultry are reviewed brie2y in the following section. Characteristics of insects as food sources Insects have characteristics which make them an excellent alternative for use as feed for World's Poultry Science Journal, Vol. 68, September 2012 437 Insects as poultry feed: M. Khusro et al. humans (Ramos-Elorduy, 2005) which would apply equally to animals. Some of the important characteristics of insects as described by Ramos-Elorduy (2005) are summarised below: (a)High species richness, biodiversity and short life cycle : Depending on dietary and other requirements like size, winged or wingless, physical and bio-chemical composition, a wide range of insects are available for use as poultry feed. Their relatively short development time and high fecundity rate would allow breeding insects in large numbers on a regular basis. (b)Prevalent in most ecosystems and colonize a wide range of habitats : Many insect species are found in abundance in most geographical regions and some exhibit rapid and relatively simple developmental strategies, making their commercial breeding potentially straight forward and cost effective. (c)Low breeding costs potential : Many insects do not require a sophisticated and expensive infrastructure for breeding, however good colony hygiene measures are essential. (d)Large population and biomass : A short development time and high fecundity rate facilitates multiplication into a large population and biomass which can be easily used as poultry feed commercially. (e)Breeding can be simple and controlled : Breeding of insects can be controlled in a relatively simple manner without involving complicated infrastructure and expensive labour costs. (f)Contain good quality of proteins : Insect protein has been found to be of better nutritional quality than most proteins from grains and other sources of plant origin. (g)Feed conversion ef ciency 1 : Insects have better feed conversion ef1ciency than most other animals which can be utilized to minimise production costs and simultaneously reduce wastage. Nutritional value of insects Numerous studies have focused on investigating the nutritional contents of a wide variety of alternative foodstuffs that could be used as protein or mineral supplements for poultry and other animals. There are numerous bene1ts of including insects in the diet of poultry. For example, in India, pupae of silkworms ( Bombyx mori ) are fed to chickens after oil has been extracted (Rao, 1994). The feeding of 2y larvae to free range chickens could assist in the recycling of animal manure in addition to the development of insect based recycling systems for the conversion of organic waste matter into feed supplements (Gullan and Cranston, 2005). Some studies have focused on recycling organic waste material and utilising the material as animal feed (Gullan and Cranston, 2005). The studies found no signi1cant differences between the food conversion rate, food intake, weight gain, carcass quality and carcass palatability of young chickens when soybean meal was replaced by 2y larvae or pupae. Ramos-Elorduy et al. (2002) reported that the amino acid content of larvae is dependent on larval size/weight and the type of waste material used to feed the developing larvae, implying the choice of waste matter for rearing insects as per the nutritional requirements of birds at different development stages is important. Protein is regarded as the most expensive ingredient in the diets of poultry (Teotia and Miller, 1973), therefore feeding insects to chickens appears to be an economically viable option providing insect selection and appropriate breeding programs can be achieved (Ramos-Elorduy, 2005). Animal proteins are of superior quality than those of plant origin (Ravindran and Blair, 1993). A review by Ravindran and Blair (1993) demonstrated that essential amino acids 438 World's Poultry Science Journal, Vol. 68, September 2012 Insects as poultry feed: M. Khusro et al. derived from animal protein supplements are superior in terms of amino acid composition to those obtained from plant protein supplements in poultry feed formulations. Similar 1ndings were reported by Bukkens (2005) who stated that the amino acid composition of most insects is better than that of legumes or grains. Anand et al. (2008) evaluated four acridid (short-horned grasshoppers commonly found in India) species for their nutritional composition and stated that acridids have a higher proportion of protein content in comparison to conventional 1sh and soybean meals. The authors concluded that acridids could be used as high protein feed supplement for poultry nutrition. Any of the four species evaluated by Anand et al. (2008) could be used for feeding chickens as all have comparable nutrient levels, although carbohydrates are lowest in Asclepias exaltata . The authors reported that all four species of acridids have a high proportion of minerals, including calcium, magnesium, zinc, iron, and copper, which are suf 1cient to meet the daily requirements of important trace minerals for poultry. Barker et al. (1998) evaluated nutrient composition of selected species of insects (mealworms, crickets, waxworms, and fruit 2ies) and found that the insects sampled had low concentrations of calcium and suf1cient levels of copper, iron, magnesium, phosphorus, and zinc to meet requirements for domestic birds. Vries (2000) stated that the overall crude protein consumption by chickens is signi1cantly increased by the intake of insects and weeds. Similar research with other insect species will be able to determine their nutrient content so an insect species can selected appropriate to the chickens dietary need at different stages of development. However, a majority of insects and/or insect meals may have inadequate levels of calcium to meet chicken dietary needs especially for layer birds, e.g. Oyarzunet al. (1996) found relatively low concentrations of calcium in termites ( Nasutitermes spp .). Other examples of insects with low calcium levels include crickets (Acheta domesticus ) and mealworms (T. molitor ) (Bernard and Allen, 1997; Barker et al. Galleria , 1998), waxworms ( mellonella Drosophila melanogaster ), fruit 2ies ( Lumbricus terristris ), earthworms ( ) (Barker et al. , 1998), and bee brood (pupae and larvae; Finke, 2005). Similarly, some insect proteins are de1cient in speci1c types of amino acids. Bergeron et al. (1988) demonstrated that 2our prepared from three genera of aquatic insects (Chironomidae Chaoborus , , and Povilla ) in Uganda had cysteine as the limiting amino acid. Rao (1994) evaluated spent silk worm ( Bombyx mori) pupae and reported tryptophan as the limiting amino acid. Ramos-Elorduy et al. (1997) analysed seventy eight species of edible insects in Mexico and found that some species were de1cient in tryptophan and lysine. Finke (2005) found methionine and cystine to be the limiting amino acids in bee brood. Landry et al. (1986) evaluated larvae of six lepidobteran species for their protein quality and potential use as protein supplements for poultry nutrition. They found that the amino acids, arginine, methionine, cysteine, and possibly lysine were de1cient when larvae were included in the chick ration. These 1ndings indicate that insect feed will need to be supplemented with calcium and limiting amino acids prior to feeding poultry especially in the layer birds whose dietary calcium requirements are higher than that of broilers. Food safety is an important issue with research showing that feeding of insects or insect meals has led to adverse effects on avian species. Stoewsand et al. (1987) reported deposition of cadmium in the tissues of Coturnix quail that fed on honey bees containing cadmium. In an experimental study, Webb et al. (2004) reported that feeding of eastern tent caterpillars ( Malacosoma americanum ) to mares in the United States led to abortions (Mare Reproductive Loss Syndrome). Some insects produce toxic chemicals and serve as vectors or intermediate hosts for pathogenic microorganisms like bacteria and viruses, and helminth parasites. Therefore, the risk factors associated with the use of insects as feed must be assessed prior to their use on a commercial basis (DeFoliart, 1992). World's Poultry Science Journal, Vol. 68, September 2012 439 Insects as poultry feed: M. Khusro et al. Another issue that warrants attention prior to including insects in the poultry ration is to investigate whether feeding insects could affect the overall palatability and quality of chicken meat. Teotia and Miller (1973) fed 2y pupae to broilers and found no signi1cant differences in carcass quality or taste in comparison to birds fed conventional soybean meal. In another study, Finke et al. (1985) investigated the impact of feeding corn-cricket Anabrus simplex ( ) diet to broiler chicks and reported that no adverse impact on taste was evident. These 1ndings indicate that the scope of feeding insects to poultry has immense potential. However, further research is required to examine the impact of feeding different species of insects on carcass quality, growth rate, and palatability prior to the widespread application of this system of feeding chickens on a commercial basis. Processing or treatment of insects prior to feeding poultry There are species of insects which are nutritionally rich in proteins and other minerals however due to the toxins secreted ( e.g.Finke, 2005) or harmful mineral content ( e.g. Stoewsand et al. , 1987) cannot be used as feed for poultry unless a safe and viable detoxifying process can be developed. Processed or dead insects are likely to be easier to handle and incorporate into existing feeding regimes making them suitable for both free range and caged production systems. Live insects may have potential dif1culties in handling, incompatibility with current automated feeding systems and a potential to act as vectors in the transmission of bacterial and viral diseases. Processed insect feeds would also simplify handling, automated feeding and storage. Given the above mentioned dif1culties associated with feeding live insects, the bene1ts of feeding live insects would need to be signi1cant and warrant evaluation. Live insects fed to free range chickens may be economically viable but are at risk of escaping into surrounding ecosystems causing environmental or plant pest issues. The wingless grasshopper for example is a pest of viticulture, agricultural crops, pastures and trees (e.g. Walker et al. , 2007). Rearing techniques for edible insects Insects having been identi1ed as suitable for poultry consumption can be bred on a large scale basis (Anand et al. , 2008; Das et al. , 2009) for free range and caged production systems. For any poultry feed to be economically feasible insect production costs must be lower or equal to the cost of conventional grain feeds. Therefore, a key component of any research must be to develop low cost insect rearing systems. Since there are potentially signi1cant costs involved in rearing insects in large numbers, namely insect feed, labour and transportation, it is important to assess the economics of breeding and rearing insects using standard economic analyses. Sources and availability of waste materials In general, the different types of waste materials commonly available on poultry farms surveyed in the states of New South Wales and Queensland are poultry manure, dead birds and egg shell wastes. In majority of farms, poultry manure is either sold for use as a fertilizer for agriculture or utilised on the farm itself for growing crops like lucerne and sorghum for feeding the birds. The dead birds and egg shell wastes are generally destined for composting. The types of waste matter generally available in different regions, 440 World's Poultry Science Journal, Vol. 68, September 2012 Insects as poultry feed: M. Khusro et al. excluding poultry farms, are green waste, food factory waste and industrial waste. A signi1cant amount of waste obtained from the farms and elsewhere is used for composting. The waste could be used for feeding and rearing insects and further studies are required to investigate this issue in more detail on a case by case basis. Insect requirements Rearing and breeding of insects on a commercial scale will require equipment and new techniques for handling and colony hygiene measures. It will also involve labour and transportation costs which need to be assessed beforehand. There may be the risk of spreading of animal as well as human diseases through insects when bred in large colonies (Lounibos, 2002). Therefore, proper hygienic measures and management conditions to protect humans are a prerequisite for breeding insects on a large scale. Housing can be as simple as a 20 l drum with egg cartons and green wastes added regularly (for grasshoppers), through to temperature and humidity controlled environmental chambers. Previous study by Nakagaki and DeFoliart (1991) has shown that mass-rearing of cricket (Acheta domesticus ) as a novelty food is possible and that the food conversion ef1ciency of crickets at a temperature of 30°C or more is higher than that reported for several species of domestic farm animals like broiler chicks, pigs, sheep, and cattle. Additionally, research by Sheppard (1983), Sheppard et al. (1994), Tomberlin (2001) and Barry (2004) has demonstrated that Hermetia illucens ( Diptera: Stratiomyidae ) could be economically used in poultry houses for reducing house2y production in poultry manure. The 2y could be mass reared under arti1cial conditions for use as poultry feed and hence would aid in developing ef1cient waste recycling system. A challenge of breeding insects commercially would be to develop ef 1cient management systems that would facilitate a regular supply of the insect crop for market requirements (DeFoliart et al. , 1982), which are available all year round, or for the rearing of multiple species on a seasonal basis. Harvesting insects from natural habitats and reduction in the use of pesticides in farming systems A wide majority of naturally occurring wingless insects could be harvested from natural habitats like farms, paddocks and swamps. For example, wingless grasshopper Phaulacridium vittatum ( ) is native to Australia and is found in abundance in almost all the states. The wingless grasshopper is a pest to viticulture, agricultural crops, pastures et al. and trees (Emery , 2005). Besides cultural and chemical control, biological control of this species has been found to be more effective. Birds such as ibis, crows, guinea fowl, magpies and chickens have been reported to effectively control wingless grasshoppers. Chasing a food source increases poultry movement and exercise, enabling them to forage further and exhibit a wider range of natural behaviours. Therefore, the feasibility of feeding wingless grasshoppers to poultry appears to have immense potential because harvesting from natural habitats would be an economical option as well. Harvesting insects from natural habitats will reduce, to a certain extent, the transfer of pesticides to humans via the food chain. In situations where insects could be harvested from the wild, such as during early swarming of locusts, it may serve as a means for the biological control of some pest species commonly found in agricultural systems. This in turn will also lead to a reduction in the widespread application of chemical pesticides World's Poultry Science Journal, Vol. 68, September 2012 441 Insects as poultry feed: M. Khusro et al. (DeFoliart, 1992) thereby reducing environmental pollution. The limitation or restricted application of chemical pesticides to food crops will bring the industry more in line with ever increasing awareness of consumers to the potential bene1ts of organic farming on a global basis. There is also a likelihood that the use of insects in poultry ration may improve the palatability of chicken meat. For example, it has been reported that in the Philippines free-range chickens fed on grasshoppers have a preferred taste and have a higher market price than those fed on conventional commercial feed. Reduction in organic pollution and the use of chemicals in agriculture The reduction in organic pollution can be achieved through recycling of agricultural and forestry waste material which can be later used as feed for insect colonies. Further research should identify insect species that grow well on plant and tree wastes. Previous research dealing with the recycling of organic waste matter and their subsequent use in animal nutrition has promising results and outcomes. For example, Ramos-Elorduy et al. Tenebrio molitor (2002) investigated the feasibility of feeding (pest of grain and distributed world-wide) on different types of organic waste matter and later feeding the mealworms to broiler chickens. Their results indicate that Tenebrio molitor has immense potential to be used as a protein source for feeding broiler chickens. The authors stated that (1) Tenebrio species (mealworms) have the potential to be used at an industrial level provided production systems utilizing a range of organic waste materials are developed and tested; (2) production costs at the industrial level would be signi1cantly lower than that of conventional protein sources such as soybean meal used in poultry nutrition; and (3) no adverse effects on broiler performance were evident when Tenebrio molitor larvae were fed to the birds. Further research and challenges in using insects as feed for free range poultry production systems One of the major challenges in using insects as poultry feed will be to persuade industry people to adopt the new technology once appropriate insect species along with adequate breeding methods have been identi1ed and tested. Another challenge would be to assess the economic viability of the new technique being adopted under farm conditions in Australia. Proposed new food source requiring different equipment and techniques of feeding insects to chickens will need to be simple and economical to adopt and implement under farm conditions. Impact of including insects in poultry ration on growth rate and carcass quality Previous research has shown that feeding certain types and species of insects has either improved or had no signi1cant impact on production in both layers and broilers. Calvert et al.(1971) conducted experiments to examine the nutritional content of young house 2ies as a source of protein for growing chickens. They found that 2y meal led to a slight improvement in the growth rate of chicks. The authors stated that the difference in feed intake/weight gain ratios for 2y meal and soybean meal diets was not signi1cant. Therefore, Calvert et al. (1971) further stated that the adult house 2y could replace soybean meal as a protein source for growing chickens. These 1ndings reveal that a 442 World's Poultry Science Journal, Vol. 68, September 2012 Insects as poultry feed: M. Khusro et al. range of insect species have the potential to replace conventional protein supplements in the poultry ration. Johnson and Boyce (1990) investigated the effect of insect reductions on the survival of sage grouse ( Centrocercus urophasianus ) chicks and reported that the quantity of insects in the diet was correlated with survival and growth. They found that an increase in the amount of insects in the diet led to an increase in survival and growth rate. Despins and Axtell (1994) evaluated the impact of feeding larvae of the darkling beetle Alphitobius diaperinus ( ) to turkey poults on feeding behaviour and growth rate. They found no signi1cant difference between the body weight of chicks that fed on larvae and starter feed in comparison to that of poults that fed on starter feed only. On the contrary, Despins and Axtell (1995) investigated the effect of feeding larvae of the darkling beetle Alphitobius diaperinus ( ) to broiler chicks on their feeding behaviour and growth. They reported that the body weight of chicks feeding on starter feed and larvae was signi1cantly higher than the body weight of chicks feeding on starter feed only. They stated that broiler chicks feeding on larvae only exhibited reduced growth rate and signs of distress, and therefore may lead to some mortality and poor performance in 2ocks. The authors also found that the beetle larvae had signi1cantly higher proportions of 18 amino acids than conventional starter broiler diets. Besides amino acids, the proportion of other feed nutrients in the beetle larvae and other species of insects is either comparable with or exceeds the starter feed. Therefore, the use of darkling beetle larvae in poultry nutrition needs to be further investigated (or not used) with regard to the age of birds as previous research by Despins et al. (1994) and McAllister et al. (1994) in turkeys and broiler chickens, respectively has demonstrated that the darkling beetle larvae are the carriers of viral, bacterial and fungal pathogens affecting gastrointestinal systems. Similar risk of hosting pathogens should also be investigated for other species of insects as well to minimise disease transmission via the food chain. Besides, the nutritional requirements of birds may vary with age and more likely to vary with differences in breeds, genetic make-up and differences between management systems. These aspects warrant further investigation. Depending on the species, insects have different proportions of amino acids. Therefore, a combination of different insect species could be analysed jointly for their amino acid content prior to choosing an optimum for feeding chickens. However, as pointed by Finke et al. (1985), depending on species examined and relevant data, the assessment of protein quality on the basis of amino acid analysis exclusively could be erroneous. Finke et al. (1985) argued that evaluation of protein quality through a bioassay technique is a more precise indicator of limiting amino acids than through amino acid analysis. This may be attributed to the following reason. The 1rst technique (amino acid analysis) measures protein quality based on the proportion of each type of amino acid in each species of insects. On the contrary, when protein quality is assessed using bioassay, physiological mechanisms and biochemical pathways are most likely to affect the relative percentage of each type of amino acid in different species of insects thereby impacting the 1nal outcome. Conclusions In general, insects contain a high proportion of good quality protein and other necessary feed ingredients including energy, fat, 1bre, minerals and vitamins, and therefore great potential exists in utilizing insects as protein supplements for poultry production systems. Different species of insects have different composition with regard to mineral content and World's Poultry Science Journal, Vol. 68, September 2012 443 Insects as poultry feed: M. Khusro et al. insects in general are a rich source of minerals such as iron, magnesium, copper, and zinc, but are typically a poor source of calcium. However, as pointed by Studier and Sevick (1992), differences in the mineral composition of insects are also due to factors like season of collection, size and age of insects, and possibly sex. Therefore, these factors need to be taken into consideration when evaluating insects for their overall mineral composition. Depending on the insect, selected calcium supplements will need to be incorporated with insect diet, particularly when feeding layer hens. If adding a calcium supplement is not economically feasible, a combination of different species of insects could be fed to chickens on a rotation basis ensuring the birds receive the required intake of essential dietary minerals, including calcium. Understanding the precise nutrient composition of different species of insects will enable feed formulations to be developed to meet the requirements of birds at different stages of growth and production. Similarly, insects to be included in poultry diet will need to be reared or harvested at the right developmental stage of their life cycle in order to meet the dietary requirements speci 1ed for both layer and meat chickens. A preliminary assessment of the costs and other factors associated with the commercial breeding and rearing of insects for poultry consumption is required. Initially, different insect species need to be tested for their suitability as chicken feed, evaluating nutritional content, growth patterns and palatability. Insect-based diets in terms of the poultry products (meat and eggs) resulting from such a feeding strategy need to be assessed in terms of end-product palatability to humans. Insect breeding programs also need to be assessed and the impacts on animal (poultry) health, and the surrounding ecosystems. Research is required to develop and test methods for mass breeding and rearing of insects. The effect of feeding insects on the growth rate and other traits of economic signi1cance in a poultry enterprise, e.g. egg production, egg quality, yolk colour also needs to be examined. Recommendations The value of using insects as potential protein supplements for both free range and cage/ battery poultry production systems needs to be assessed in a variety of contexts. Some potential areas that need to be studied further include: " Investigating the possibility and ef1ciency of rearing different insects for use as a feed ingredient (protein source) in poultry diets, determine the nutritional value of these insects and assess the growth performance and nutrient digestibility when fed to free-range chickens. " Increasing the food security of free-range chickens via enhanced feeding systems by developing on-farm feeding systems. Once appropriate insects and waste products have been tested under laboratory conditions we would set up experimental feeding trails on free-range farms. " Supplementing and improve the diet, increase the foraging range and exercise of free-range chickens by developing novel feeding methods using live insects and reared locally sourced waste material. 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(1997) Feeding captive insectivorous animals: nutritional aspects of Nutrition Advisory Group Handbook Fact Sheet No insects as food. , . 003. BUKKENS, S.G.F. (2005) Insects in the human diet: nutritional aspects, in: PAOLETTI, M.G. (Ed.) Ecological implications of minilivestock (Potential of insects, rodents, frogs and snails ), pp. 545-577 (Science Publishers, INC.) CALVERT, C.C., MORGAN, N.O. and EBY, H.J. (1971) Biodegraded hen manure and aduly house 2ies: Proceedings of International Symposium on Livestock Wastes their nutritional value to the growing chick. . (American Society of Agricultural Engineering ), pp. 319-320. CHAPMAN, R.F. (1998) The Insects: structure and function. Cambridge University Press, Fourth Edition. pp. 69-91. CRIBB, J. (2010) The Coming Famine (The Global Food Crisis and What We Can Do to Avoid It). CSIRO Publishing . DAS, M., GANGULY, A. and HALDAR, P. (2009) Space requirement for mass rearing of two common Indian acridid adults (Orthoptera: Acrididae ) in laboratory condition. American-Eurasian Journal of Agricultural and Environmental Sciences 6: 313-316. DEFOLIART, G.R., FINKE, M.D. and SUNDE, M.L. (1982) Potential value of the mormon cricket (Orthoptera: Tettigoniidae Journal of Economic Entomology ) harvested as a high-protein feed for poultry. 75: 848-852. DEFOLIART, G.R. (1992) Insects as human food: Gene DeFoliart discusses some nutritional and economic aspects. Crop Protection 11 (Science Publishers, INC.) , pp. 395-399. DEFOLIART, G.R. (2005) Overview of role of edible insects in preserving biodiversity, in: PAOLETTI, M.G. (Ed.) Ecological implications of minilivestock ( Potential of insects, rodents, frogs and snails ), pp. 123-140. DESPINS, J.L., AXTELL, R.C., RIVES, D.V., GUY, J.S. and FICKEN, M.D. (1994) Transmission of enteric pathogens of turkeys by darkling beetle larva ( Alphitobius diaperinus Journal of Applied Poultry ). Research 3: 61-65. DESPINS, J.L. and AXTELL, R.C. (1994) Feeding behaviour and growth of turkey poults fed larvae of the darkling beetle,Alphitobius diaperinus Poultry Science . 73: 1526-1533. DESPINS, J.L. and AXTELL, R.C. (1995) Feeding behaviour and growth of broiler chicks fed larvae of the darkling beetle,Alphitobius diaperinus Poultry Science . 74: 331-336. EMERY, R., MANGANO, P. and MICHAEL, P. (2005) Insect and allied pests of extensive farming. In: Crop Insects: The Ute Guide, Western Grain Belt Edition . FINKE, M.D., SUNDE, M.L. and DEFOLIART, G.R. (1985) An evaluation of the protein quality of Mormon Crickets ( Anabrus simplex ) when used as a high protein feedstuff for poultry.Poultry Science 64: 708-712. FINKE, M.D. (2005) Nutrient composition of bee brood and its potential as human food. Ecology of Food and Nutrition 44: 257-270. GULLAN, P.J. and CRANSTON, P.S. (2005) The insects: an outline of entomology. Blackwell Publishing Limited p. 13. HALDAR, P., DAS, A. and GUPTA, R.K. (1999) A laboratory based study on farming of an Indian grasshopper Oxya fuscovittata (Marschall) (Orthoptera:Acrididade Journal of Orthoptera Research ). 8: 93-97. JOHNSON, G.D. and BOYCE, M.S. (1990) Feeding trials with insects in the diet of sage grouse chicks. Journal of Wildlife Management 54: 89-91. LANDRY, S.V., DEFOLIART, G.R. and SUNDE, M.L. (1986) Larval protein quality of six species of Saturniidae Sphingidae Noctuidae Journal of Economic Entomology lipidoptera ( , , ). 79: 600-604. Annual Review of Entomology LOUNIBOS, L.P. (2002) Invasions by insect vectors of human disease. 47: 233- 266. MCALLISTER, J.C., STEELMAN, C.D. and SKEELES, J.K. (1994) Reservoir competence of the lesser mealworm (Coleoptera: Tenebrionidae ) for Salmonella typhimurium (Eubacteriales: Enterobacteriaceae ). Journal of Medical Entomology 31: 369-372. World's Poultry Science Journal, Vol. 68, September 2012 445 Insects as poultry feed: M. Khusro et al. NAKAGAKI, B.J. and DEFOLIART, G.R. (1991) Comparison of diets for mass-rearing Acheta domesticus (Orthoptera: Gryllidae ) as a novelty food, and the comparison of food conversion ef1iency with values Journal of Economic Entomology reported for livestock. 84: 891-896. OYARZUN, S.E., CRAWSHAW, G.J. and VALDES, E.V. (1996) Nutrition of the Tamandua: I. Nutrient composition of termites ( Nasutitermes spp .) and stomach contents from wild Tamanduas ( Tamandua tetradactyla Zoo Biology ). 15: 509-524. RAMOS-ELORDUY, J., MORENO, J.M.P., PRADO, E.E., PEREZ, M.A., OTERO, J.L. and DE GUEVARA, O.L. (1997) Nutritional value of edible insects from the state of Oaxaca, Mexico. Journal of Food Composition and Analysis 10: 142-157. RAMOS-ELORDUY, J., GONZALEZ, E.A., HERNANDEZ, A.R. and PINO, J.M. (2002) Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. Journal of Economic Entomology 95: 214-220. RAMOS-ELORDUY, J. (2005) Insects: a hopeful food source, in: PAOLETTI, M.G. (Ed.) Ecological implications of minilivestock (Potential of insects, rodents, frogs and snails), pp. 263-291 (Science Publishers, INC.). RAO, P.U. (1994) Chemical composition and nutritional evaluation of spent silk worm pupae. Journal of Agricultural Food Chemistry 42: 2201-2203. RAVINDRAN, V. and BLAIR, R. (1992) Feed resources for poultry production in Asia and the Paci1c. II. Plant protein sources. Worlds's Poultry Science Journal 48: 205-231. RAVINDRAN, V. and BLAIR, R. (1993) Feed resources for poultry production in Asia and the Paci1c. III. Animal protein sources. World's Poultry Science Journal 49: 219-235. SENGOR, E., YARDIMCI, M., OKUR, N. and CAN, U. (2008) Effect of short-term pre-hatch heat shock of incubating eggs on subsequent broiler performance. South African Journal of Animal Science 38: 58-64. SHEPPARD, D.C. (1983) House 2y and lesser house 2y control utilizing the black soldier 2y in manure management systems for caged laying hens. Environmental Entomology 12: 1439-1442. SHEPPARD, D.C., NEWTON, G.L. and THOMPSON, S.A. (1994) A value added manure management system using the black soldier 2y. Bioresource Technology 50: 275-279. STOEWSAND, G.S., MORSE, R.A., BACHE, C.A. and LISK, D.J. (1987) Deposition of cadmium in tissues of Coturnix quail fed honey bees. Bulletin of Environmental Contamination and Toxicology 38: 783- 788. STUDIER, E.H. and Sevick, S.H. (1992) Live mass, water content, nitrogen and mineral levels in some insects from south-central lower Michigan. Comparative Biochemistry and Physiology Part A: Physiology 103: 579- 595. TEOTIA, J.S. and MILLER, B.F. (1973) Fly pupae as a dietary ingredient for starting chicks. Poultry Science 52: 1830-1835. TOMBERLIN, J.K. (2001) Biological, behavioral, and toxicological studies on the black soldier 2y (Diptera: Stratiomyidae). PhD Thesis, University of Georgia. VRIES, D. (2000) Observations on behaviour and feed intake of chickens kept on free range in Muy Muy, Nicaragua. Proceedings of the 21st World's Poultry Congress, Montreal, pp. 1-3. WALKER, P., HUNTER, D. and ELDER, R. (2007) Locusts and grasshoppers of Pastures and Rangelands. In: Bailey P.T. (Eds), Pests of Field Crops and Pastures: Identi1cation and Control, CSIRO Publishing, p. 498. WEBB, B.A., BARNEY, W.E., DAHLMAN, D.L., DEBORDE, S.N., WEER, C., WILLIAMS, N.M., DONAHUE, J.M. and MCDOWELL, K.J. (2004) Eastern tent caterpillars (Malacosoma americanum) cause mare reproductive loss syndrome. Journal of Insect Physiology 50: 185-193. WILLIS, S. (2003) The use of soybean meal and full fat soybean meal by the animal feed industry. Proceedings of the 12th Australian Soybean Conference 12: 1-8. 446 World's Poultry Science Journal, Vol. 68, September 2012

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  15. DESPINS, J.L. and AXTELL, R.C. (1994) Feeding behaviour and growth of turkey poults fed larvae of the darkling beetle, Alphitobius diaperinus. Poultry Science 73: 1526-1533.
  16. DESPINS, J.L. and AXTELL, R.C. (1995) Feeding behaviour and growth of broiler chicks fed larvae of the darkling beetle, Alphitobius diaperinus. Poultry Science 74: 331-336.
  17. EMERY, R., MANGANO, P. and MICHAEL, P. (2005) Insect and allied pests of extensive farming. In: Crop Insects: The Ute Guide, Western Grain Belt Edition.
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  19. FINKE, M.D. (2005) Nutrient composition of bee brood and its potential as human food. Ecology of Food and Nutrition 44: 257-270.
  20. GULLAN, P.J. and CRANSTON, P.S. (2005) The insects: an outline of entomology. Blackwell Publishing Limited p. 13.
  21. HALDAR, P., DAS, A. and GUPTA, R.K. (1999) A laboratory based study on farming of an Indian grasshopper Oxya fuscovittata (Marschall) (Orthoptera: Acrididade). Journal of Orthoptera Research 8: 93-97.
  22. JOHNSON, G.D. and BOYCE, M.S. (1990) Feeding trials with insects in the diet of sage grouse chicks. Journal of Wildlife Management 54: 89-91.
  23. LANDRY, S.V., DEFOLIART, G.R. and SUNDE, M.L. (1986) Larval protein quality of six species of lipidoptera (Saturniidae, Sphingidae, Noctuidae). Journal of Economic Entomology 79: 600-604.
  24. LOUNIBOS, L.P. (2002) Invasions by insect vectors of human disease. Annual Review of Entomology 47: 233- 266.
  25. MCALLISTER, J.C., STEELMAN, C.D. and SKEELES, J.K. (1994) Reservoir competence of the lesser mealworm (Coleoptera: Tenebrionidae) for Salmonella typhimurium (Eubacteriales: Enterobacteriaceae). Journal of Medical Entomology 31: 369-372.
  26. World's Poultry Science Journal, Vol. 68, September 2012
  27. NAKAGAKI, B.J. and DEFOLIART, G.R. (1991) Comparison of diets for mass-rearing Acheta domesticus (Orthoptera: Gryllidae) as a novelty food, and the comparison of food conversion ef1iency with values reported for livestock. Journal of Economic Entomology 84: 891-896.
  28. OYARZUN, S.E., CRAWSHAW, G.J. and VALDES, E.V. (1996) Nutrition of the Tamandua: I. Nutrient composition of termites (Nasutitermes spp.) and stomach contents from wild Tamanduas (Tamandua tetradactyla). Zoo Biology 15: 509-524.
  29. RAMOS-ELORDUY, J., MORENO, J.M.P., PRADO, E.E., PEREZ, M.A., OTERO, J.L. and DE GUEVARA, O.L. (1997) Nutritional value of edible insects from the state of Oaxaca, Mexico. Journal of Food Composition and Analysis 10: 142-157.
  30. RAMOS-ELORDUY, J., GONZALEZ, E.A., HERNANDEZ, A.R. and PINO, J.M. (2002) Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. Journal of Economic Entomology 95: 214-220.
  31. RAMOS-ELORDUY, J. (2005) Insects: a hopeful food source, in: PAOLETTI, M.G. (Ed.) Ecological implications of minilivestock (Potential of insects, rodents, frogs and snails), pp. 263-291 (Science Publishers, INC.).
  32. RAO, P.U. (1994) Chemical composition and nutritional evaluation of spent silk worm pupae. Journal of Agricultural Food Chemistry 42: 2201-2203.
  33. RAVINDRAN, V. and BLAIR, R. (1992) Feed resources for poultry production in Asia and the Paci1c. II. Plant protein sources. Worlds's Poultry Science Journal 48: 205-231.
  34. RAVINDRAN, V. and BLAIR, R. (1993) Feed resources for poultry production in Asia and the Paci1c. III. Animal protein sources. World's Poultry Science Journal 49: 219-235.
  35. SENGOR, E., YARDIMCI, M., OKUR, N. and CAN, U. (2008) Effect of short-term pre-hatch heat shock of incubating eggs on subsequent broiler performance. South African Journal of Animal Science 38: 58-64.
  36. SHEPPARD, D.C. (1983) House 2y and lesser house 2y control utilizing the black soldier 2y in manure management systems for caged laying hens. Environmental Entomology 12: 1439-1442.
  37. SHEPPARD, D.C., NEWTON, G.L. and THOMPSON, S.A. (1994) A value added manure management system using the black soldier 2y. Bioresource Technology 50: 275-279.
  38. STOEWSAND, G.S., MORSE, R.A., BACHE, C.A. and LISK, D.J. (1987) Deposition of cadmium in tissues of Coturnix quail fed honey bees. Bulletin of Environmental Contamination and Toxicology 38: 783- 788.
  39. STUDIER, E.H. and Sevick, S.H. (1992) Live mass, water content, nitrogen and mineral levels in some insects from south-central lower Michigan. Comparative Biochemistry and Physiology Part A: Physiology 103: 579- 595.
  40. TEOTIA, J.S. and MILLER, B.F. (1973) Fly pupae as a dietary ingredient for starting chicks. Poultry Science 52: 1830-1835.
  41. TOMBERLIN, J.K. (2001) Biological, behavioral, and toxicological studies on the black soldier 2y (Diptera: Stratiomyidae). PhD Thesis, University of Georgia.
  42. VRIES, D. (2000) Observations on behaviour and feed intake of chickens kept on free range in Muy Muy, Nicaragua. Proceedings of the 21st World's Poultry Congress, Montreal, pp. 1-3.
  43. WALKER, P., HUNTER, D. and ELDER, R. (2007) Locusts and grasshoppers of Pastures and Rangelands. In: Bailey P.T. (Eds), Pests of Field Crops and Pastures: Identi1cation and Control, CSIRO Publishing, p. 498. WEBB, B.A., BARNEY, W.E., DAHLMAN, D.L., DEBORDE, S.N., WEER, C., WILLIAMS, N.M., DONAHUE, J.M. and MCDOWELL, K.J. (2004) Eastern tent caterpillars (Malacosoma americanum) cause mare reproductive loss syndrome. Journal of Insect Physiology 50: 185-193.
  44. WILLIS, S. (2003) The use of soybean meal and full fat soybean meal by the animal feed industry. Proceedings of the 12 th Australian Soybean Conference 12: 1-8.