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Home , Closed ecological system, Entomophagy

ENTOMOPHAGY AS PART OF A SPACE FOR HABITATION ON MARS

Naomi Katayama1, Masamichi Yamashita2, Hidenori Wada3, Jun Mitsuhashi3, Space Task Force3 1 Nagoya Women's University, Mizuho-ku, Nagoya, 467-8610, Japan 2 Institute of Space and Astronautical Science, JAXA, Sagamihara, 229-8510, Japan 3 Space Agriculture Task Force ([email protected])

Abstract In order to develop a basic design for an agricultural system that could support life on Mars, an appropriate space diet for humans is first required. We conducted a nutritional evaluation on a candidate menu. A combination of rice, , sweet potato, green-yellow vegetable (represented by Komatsuna), silkworm , and loach was found to be an appropriate diet that

Introduction A nutritional space diet must be studied in order to design a space agriculture system that makes habitation on Mars possible. Masuda et al. (2005) examined in detail a menu for life support in a closed ecological system. Their design of various vegetarian menus and plan for culturing plants based on their requirements provides a good example of a space menu. Silverstone (1993) described cooking of food materials harvested from agricultural composed in a closed dome. Koike et of animal origin are required for human diet as discussed in this article. Since space agriculture will be organized under constraints of its resource available at extraterrestrial environment, for a core component of the space diet. During the archeological age of hunter-gatherers, were an important portion of the human diet. This is evidenced by , , and many species found in fossil human feces, namely coprolite. Even after several species of animals and plants were domesticated, and stock raising and agriculture started, entomophagy remained a part of different food cultures all over the globe. We can see a diverged culture of entomophagy as an identity of each region. The development of stock raising and agriculture enables a stable food supply, and the human population has increased as a result. Farming induced a richer linguistic communication among humans, and initiated human civilizations. In an ecological view of the history of civilizations, Umesao (1975) argued that breeding was selected in areas where edible crop plants were hardly cultivated. Instead of farming edible plants, the inedible produced in these areas was converted to edible dairy products or by cows or sheep. This is one good example of gene-culture co-evolution, as this culture of cattle breeding has driven natural selection for a lactose tolerant gene among people who live there.. In this way, natural ecology has had a close relationship to human culture, including food habits and civilization. The improvements in agricultural production on Earth, and the consequent surplus of food, enable us a scope for the further improvement and fruitful future of our civilization. On the other hand, the consecutive increase in the human population and the loss of farmland at the global scale warn us of the unbalance between food supply and demand, which forms one of North-South gap in the world. Our concept of space agriculture for habitation on Mars is designed to optimize agriculture, i.e. keep cultivating plants or breeding animals under these constraints is important for both space and terrestrial agriculture and sustainable human life. In our present study, fundamental food materials were selected from this standpoint. Based on composition and amount of food components (e.g. , , Even though the number of food materials we examined in this study is small, we can derive many diverse menus from it.

Analysis of Nutritional Requirements As a nutritional reference for our study, we chose Standard of foods intake for Japanese (2005) intake and preferred amounts of . In addition to this target level, many items, though not all of adult under normal activity levels. Items analyzed in this study are listed in Table 1.

Table 1 Food components used in the nutritional evaluation

Energy Proteins Total amount, composition, Amino acids score Fat Total fat amount, Saturated fatty acid, n-6 series fatty acid, n-3 series fatty acid, Fat source (Mammalian/avian meat, Plant, Fish) ratio, n-6/n-3 ratio, Ratio between proteins, fat, and

Water soluble B1, Vitamin B2, Niacin, Vitamin B6, Folic acid, Vitamin

B12 Fat soluble vitamins Vitamins A, E, D, K Electrolytes Sodium, Potassium as energy intake, was evaluated. The amount of essential amino acids were examined to determine if they reached the target value, and the amino acid score was used to determine if their composition was adequate. The recommended balance between these food components is based on the physiological load of processing excess intake. For example, excess amino acids are processed under heavier load in the metabolic pathway at poor amino acid score. Fat is an energy source complementary to carbohydrate. Because of the difficulty in defining a requirement for its uptake, the ratio of energy uptake from fat is taken as a standard. In Japan the recommended amount of energy that is derived from fatis 20 to 50% for adults, 45% for infants under six months, 30 to 40% for infants between 6 and 12 months, 25 to 30% for growing children and young adults, and 25 to 30% for pregnant and lactating women, respectively. It is important to keep the balance of fatty acids within the appropriate range. Firstly, the ratio of acid (SFA), monounsaturated fatty acid (MUSFA), and polyunsaturated fatty acid (PUSFA) should from plants which are rich in linoleic acid, and n-3 fatty acid from fish which are rich in linolenic For cholesterol consumption, the Japanese food intake reference recommends only a daily upper family necessary for the synthesis of bile acid, adrenal cortex , and sex . At the menstrual irregularity. Phospholipids have a chemical structure of two fatty acids bound to glycerin, and a third hydroxyl group of glycerin forms an ester bond with phosphate. These phospholipids form the double lipid layer of cell membranes. Both cholesterol and phospholipid are essential to sustain the function of the biomembrane. Eighty percent of the fat in our body is reused. The other 20% of fat must be obtained from foods. Polyunsaturated fatty acids, such as linoleic acid or linolenic acid, can not be synthesized in our body.. These are called essential fatty acids, and are required for regulation of body growth. . If they are occur. From a series of n-6 and n-3 fatty acids, polyunsaturated fatty acids with longer chains can be synthesized. There are some items for which either the upper or lower limit is not given. If over uptake of a needs to be carefully evaluated. We may also need to define intake levels for trace elements or chemicals, or other ratios between food items, which may come to light after further studies on human , especially in the space environment. We should consider those indices in future. Since there are individual and cultural food preferences, we must design a space menu based on those factors, in addition to nutritional considerations. When proposing exotic food materials or cooking methods, we need to consider those aspects to make it acceptable.

Choice of Elementary Crop Species Agricultural production that makes full use of limited resources, namely inner volume and effective area of the space system, available flux of incident solar light and so forth, is a factor that must be considered when designing a basic combination of space foods. Farming of crops has an advantage by providing high nutritional value and a stable supply of food (because storage of and sweet potato are compared in Table 2. Assuming multiple cropping in a year, annual yield of each crop is calculated from yield per unit area, during the period between seeding and harvest. Based on this yield, energy content, and required energy intake of humans, the necessary farming area can be estimated. In the order of sweet potato, potato, rice and soybean, required farming area increases. Farming area for rice is three times smaller than that for wheat, if cultivation time for wheat is postulated to be as long as seven months. In a similar way, farming area required to provide protein can be estimated. are the best in this aspect, and potato, rice, and quinoa are good in this order. Amino acid score is 100 for buckwheat, and in a range of 86 to 42 for other crops. The materials. Amino acid score of wheat is the lowest among the crops compared in this study. The type of plant reproduction is another consideration in the selection of crop plants. Those species We selected rice, soybean, and sweet potato for our major plant species after consideration of the above points. In addition to these species, Komatsuna, Japanese mustard spinach, is included as a

Crop Plant Yield Period of Energy Required Protein Required Amino Mode of Culture Content Farming Area Content Farming Acid Reproduction for Energy Area for Protein kg/1000m2 month kcal/100g 2000 kcal/day g/100g 60g protein Score m2 m2 Rice 526 4 356 130 6.8 204 64 Anemophilous Wheat 280 7 337 451 10.6 430 42 Anemophilous Soybean 367 3.5 417 139 35.3 49 86 Entomophilous Buckwheat 106 2.5 364 394 12.0 359 100 Entomophilous Quinua 178 3 403 254 13.4 230 85 Anemophilous Potato 3000 3 76 80 1.6 114 73 Vegetative Sweet potato 3180 5 150 64 0.9 319 83 Vegetative the nutritional requirement. This combination is called a fundamental vegetable menu. Energy and element, respectively.

Demand for Foods of Animal Origin Nutritional analysis on the basic vegetable menu consisting of rice, soybean, sweet potato and

Komatsuna reveals a shortage of vitamins D and B12, cholesterol and sodium salt. Since deficiency results in demineralization of bone, it might be critical in the micro- or low gravity environment. Vitamin B12 is essential to prevent pernicious anemia. Under stressful situations, demand for sodium salt increases. In the Japanese food intake standard of contain about 2g of sodium salt, an additional 7g is required in the form of cooking or table salt. The American standard recommendation for sodium chloride intake is only 5.8g at its maximum. If these body decreases as a whole, increasing the load on the kidneys. Reduction of salt uptake, similar to recommendations for kidney patients, is one measure against this problem. In this context, 3g of sodium salt in the form of cooking or table salt, and 5g in total might be considered appropriate. 15-20% fat and 55-65% carbohydrate. Plant food is quite diverse in these factors, ranging from root crops characterized by their high sugar content to soybean characterized as rich in protein. In general, earlier (e.g. growth retardation and decreased immune function) are seen. For composition of amino acids, is in short supply in plant foods. Addition of animal foods improves the amino acid score to 100.

The other nutrients that are short in the vegetarian menu (i.e. cholesterol, vitamins D and B12) can be obtained by adding other vegetables and foods of animal origin. Vitamin D can be found in mushroom,

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Menu Including Insects In order to supplement the deficient nutrients of the core vegetarian menu, we considered adding insects. In our space agriculture concept, tree cultivation is part of the agricultural ecology. Photosynthesis of plant produces biomass and oxygen. If this biomass is oxidized or metabolized, the produced oxygen is stoichiometrically consumed. By utilizing wood lumber for living space and furniture, excess oxygen can be stored. Tree leaves can be composted to synthesize agricultural soil. Insect rearing is also possible with leaves. rearing protocol for silkworms is well established. In addition to this, the mulberry tree has been extensively studied for feeding silkworms. Many cultivars of mulberry are available, and is possible for a long period in a year. Furthermore, there is technology to make silkworm polytrophic In terms of its utilization as a food source, silkworms must be at a growth stage of either pupa metamorphosed in cocoon or adult . Analysis of the nutritional content of silkworm has been conducted for major items, but not for vitamins or minor elements. In order to conduct a nutritional evaluation of our model menu for space agriculture, silkworm was substituted with other insect species (e.g. grasshopper) for which the complete set of nutritional data is available.

Merits and Constraints of Entomophagy Plants produce biomass by converting solar light to a form of chemical energy. Based on this energy carried by plant biomass, various organisms form predator-prey relationships and ecological systems emerge. One level up the food chain, 80-90% of food energy is lost as dissipation of heat. This decreases the exploitable energy down to one tenth for one step up in the ecological system (Odum, 1971). Insects are at a lower level of the food chain because they eat plant leaf, , pollen and sap. Some insect species play a role of decomposer in the ecological system by eating animal feces. Silkworms have been domesticated with mulberry trees for 5,000 years, and cannot propagate their found in the mulberry leaf. If a genetic mutation occurs in this taste sensory mechanism, disabling the energy to building body mass has been examined in wild silkworm, Antheraea yamamai. Amount of leaf provided per was 95.5g. Each larva ate 43.1g, and body weight at pupa stage was 7.3g for is about 10 % in this case. One issue that should be well considered when designing a space menu with animal food materials when climbing one level up the food chain, the cultivation area of primary producers, i.e. plants, should be more than ten times larger, depending on the number of levels up the food chain. Even if inedible biomass is given to cattle, if the production of such feed competes with culturing edible biomass for the same agricultural resources, then there is a problem of determining optimum allocation of limited resources. Merits of entomophagy lie in the improvement of biomass quality or exploiting inedible biomass such as tree leaves or metabolic waste. Either insects are eaten directly, or fed to cultured mammalians or fish to convert them to edible meat. By allocating agricultural system components in this way, animal food can be supplied without competing for resources against edible biomass production.

Cultural Acceptability of Entomophagy When designing a menu associated with space agriculture, an important factor is whether the prepared food is accepted culturally or not. The practice of eating insects is an interesting subject from Japan. In the commercial market today, we can purchase prepared silkworm, grasshopper, and larva of . In the food composition tables issued by a governmental committee, two insect food items are listed, i.e. grasshopper and larva of bee. We have a history of entomophagy all over the world. Because of high nutritional value and easiness of gathering, the practice of entomophagy is widely distributed (Nonaka, 2005). Mitsuhashi (1997) described the nutritional value of various insects. Most insects are rich in protein, fat and essential amino acids. In some cases, specific insects were powdered after drying, and used for furnishing nutrition. Insects may contain chemicals that are effective at regulating physiological function, and the high nutritional value of insects might be effective in supplementing proteins for helping people who is in sickly condition.

Features and Limitations of Animalization of Biomass Made by Insects Although insects are animal, they are far from mammal on the phylogenic tree,. Even though insects the demand for animal food. chemical conversion gives the silkworm body an "animal" like composition, it can be called animalization of the mulberry plant. The question here is to what extent silkworm composition is "animal category food" that is required for human diet. Silkworm pupa can be characterized as follows. Fat content increases from 1% in mulberry leaf to 8.2% in silkworm. Feces of silkworm larva contain fat at 0.8%, i.e. lower than mulberry leaf. This indicates that a silkworm larva takes fat from the leaf, high content of polyunsaturated fatty acids like linoleic acid or linolenic acid. Those fatty acids are found at lower levels in silkworm. Thus, fat composition of silkworm is less animalized. It should be Amino acid content of silkworm showed a similar trend. A silkworm pupa contains more amino acid compared to mulberry leaf, and amino acid content in feces is less than leaf. Silkworms concentrate and (sulfur amino acid) are higher than other amino acids in silkworm. . It can be said that herbivorous cattle, and thus silkworm cannot replace all the animal food in our menu. Vitamins and trace elements play an essential role in maintaining the healthy status of humans. Although those nutrients are critical, the physical amount of their recommended intake is quite small. In cases where it is difficult to create an optimal menu that fulfills all the major nutritional requirements as well as those for trace elements and vitamins, those minor components could be period without losing their physiological function.

Design of Model Menu and Its Nutrition basic vegetarian menu consisting of rice, soybean, sweet potato and Komatsuna, plus sodium salt and insect.

1) Basic vegetarian menu plus insect, chicken, and mushroom

Avian eggs are known to have high levels of cholesterol, and vitamins D and B12. Quail or chicken eggs might be appropriate candidates for our space menu. Mammalian meat, especially the of pig, cow or young chicken, is a good source of vitamin B12. We selected chicken to rear in space Mushrooms convert inedible wooden biomass to their fruit body. Furthermore, mushrooms contain vitamin D, which is particularly high in Jew's ear or shiitake mushrooms. The cultivation protocol of mushrooms is well established for various species. Among them, shiitake mushrooms have been cultivated from early years, and are a common food item in the Japanese menu. Based on this advantage, we selected shiitake mushrooms. The precursor chemical of vitamin D in shiitake mushrooms is converted to vitamin D by irradiation of ultraviolet light. If powdered dry shiitake mushroom is exposed to ultraviolet light, the amount of vitamin D increases up to 10,000 times compared to plain mushrooms because of the high irradiation surface/volume ratio in the powdered form (The Mushroom Research Institute of Japan, 2005). Powdered mushroom can easily be stored for a long period. It is being tested whether shiitake mushroom could be cultivated by mulberry tree, and the feasibility of using powdered mushroom as a trace additive in cooking. We confirmed that the combination of 300g rice, 100g soybean, 200g sweet potato, 300g Komatsuna, 50g insect (represented by grasshopper), 30g chicken egg, 5g chicken liver, 10g chicken as mentioned above, the amount of mushroom can be reduced quite a lot by providing it in irradiated powdered form.

2) Basic vegetarian menu plus insect and loach

Fish contains both vitamins D and B12 species that are rich in vitamins. Tilapia has been included in the space menu of NASA. The vitamins in loach are similar to tilapia, except that vitamin D is lower, at 4 mg per 100g. Simultaneous production of crop and animal food was proposed by the International Rice Research paddies for nitrogen fixation by symbiotic cyanobacteria. This provides "green " for rice such as that with low levels of dissolved oxygen, loach will swim up to the water surface, gulp air into the digestive tube, and expel an air bubble from the anus after making gas exchange in the gut. Thus, culture conditions are quite permissive for loach, and we selected loach for this reason. As well, since soup in which whole boiled loach is minced. rice, 100g soybean, 200g sweet potato, 300g Komatsuna, 50g insect (represented by grasshopper), 120g loach, and 3g sodium salt. This ratio for fat is slightly lower than the recommended number. The ratios of protein and carbohydrate are within the recommended range. mg per day. Menu of either insect, chicken and mushroom, or insect and loach, has no shortage of range. Other indices, n-6/n-3 fatty acid ratio, SMP ratio, and cholesterol are not far from recommended values. found in rearing chickens in a space base. We should trade merit and demerit of rearing ordinary cattle animals on Mars. Based on the view of efficient use of biomass energy produced by plants in our concept, we decided to use the menu consisting of the basic vegetarian menu plus insect and loach for further conceptual design of space agriculture.

Insect Cooking Methods One important factor when designing a menu is whether visual presentation and quantity are acceptable as a for ordinary people. It is true that including large quantities of insects in a human diet requires certain treatment. Silkworm pupae were dried and ground to make powder. Silkworm cookies were then made from 200g rice powder, 50g soybean flour, 50g sliced sweet potato, 5g powdered silkworm pupa, 2g sodium salt and 300ml soy milk. By taste sensory test, the cookie with

Nutrient Unit Recommendation Basic Basic Basic (2005) Vegetarian Menu Menu Menu + Insect, + Insect,

Energy kcal 2000 1773 2032 1976 Protein g 55 62.6 90.6 91.9 Potassium mg 1800 5036 5944 5456 Magnesium mg 310 637 695 695 Phosphor mg 1000 1677 2058 2457 Iron mg 9 25.5 29.7 33.5 mg 4.0 9.32 10.51 10.31 Retinol equivalent mg 700 785 913 838 Vitamin D mg 5.0 0 6 4 mg 9 11.3 13.3 13.3 mg 70 648 659 653

Vitamin B1 mg 1.0 2.55 2.87 2.67

Vitamin B2 mg 1.3 0.87 2.10 2.46 Niacin mg 12 25.7 36.1 30.6

Vitamin B6 mg 1.3 2.80 3.18 2.96

Vitamin B12 mg 2.4 0.0 0.6 8.6 Folic acid mg 240 739 897 782 Pantothenic acid mg 6.0 8.48 12.27 9.36 g 21.0 36.4 45.2 36.4 Sodium Salt (upper limit) g 9.0 5.9 8.6 8.5 n-3 fatty acid (lower limit) g 2.4 2.1 2.3 2.3 n-6 fatty acid (upper limit) g 11.0 11.3 12.6 11.5

(mg) Basic Basic Menu Basic Vegetarian + Insect, Menu Menu Mushroom, + Insect,

Iso- 180 147 152 150 + 390 135 133 128 210 108 113 114 70 115 116 107 220 146 148 146 the constituents above was judged the best among several other combinations of ingredients.

Image of Space Agriculture Based on the Menu with Insect We have estimated the farming area on Mars will be 200m2 per person, considering that solar light intensity on Mars is about half of that on Earth (Yamashita et al., 2005, 2006a). Annual per person consumption of the four major crops is 110kg rice, 37kg soybeans, 72 kg sweet potato, and 110 kg Komatsuna. If multiple cropping is made for those plants, production is possible within the estimated farming area. Estimation of planting area required for mulberry trees to rear 18 kg of silkworm pupa is 64m2. Maximum production of loach per unit water surface area is 10 kg/m2, and it takes about 1 year to get adult loach at an appropriate size for cooking from its egg stage (Kagehira, 2005). In order to produce 44 kg of loach per year, the minimum area for aquaculture is 4.4 m2. Since loach will be cultured in rice paddies with Azolla on their surface, we can manage all these items within the original farming area . Amount of sodium salt consumed by a person for a year is 1.8 kg. Salt or inorganic fertilizer can be considered as consumables supplied from Earth, if the total amount for the mission length is less than the mass and volume of the recycling system. A trade study (Yamashita et al., 1985) was conducted on several concepts for treating sodium in space agriculture. Several biological processes for treating sodium-rich human waste are studied for recycling sodium and other bio-elements in space agriculture (Yamashita et al., 2006b).

Concluding Remarks The model recipe with basic vegetarian foods with insect and additional chicken or loach was confirmed to fill the nutritional requirement. Based on our candidate space menu, we determined specification of requirements for component system of space agriculture. Use of the agricultural resource on Mars could be optimized by the combination of crop production with chosen species, resources, and to close the materials recycle loop high as possible. We scope spin off of such feature of space agriculture could be made to support and develop sustainable civilization on the earth.

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