Potential of defatted microalgae from the biofuel industry as an ingredient to replace corn and soybean meal in swine and poultry diets S. Gatrell, K. Lum, J. Kim and X. G. Lei J ANIM SCI published online February 4, 2014

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Running head: Microalgal biomass as animal feed

Potential of defatted microalgae from the biofuel industry as an ingredient to replace corn and soybean meal in swine and poultry diets 1,2

S. Gatrell, K. Lum, J. Kim, and X. G. Lei 3

Department of Animal Science, Cornell University, Ithaca, NY 14853

1

Based on a presentation at the Non-ruminant Nutrition Symposium titled “Breaking the Mold: Formulating Monogastric Diets Without Traditional Ingredients” at the Joint Annual Meeting, July 8-12, 2013, Indianapolis, IN, with publication sponsored by the Journal of Animal Science and the American Society of Animal Science.

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This study was supported, in part, by a grant from the Department of Energy-USDA National Institute of Food and Agriculture Biomass Research and Development Initiative.

3

Corresponding author: [email protected]

1 Downloaded from www.journalofanimalscience.org Mary, of London on June 16, 2014 Published Online First on Februaryat4,Queen 2014 as University doi:10.2527/jas.2013-7250

ABSTRACT: While feeding food-producing animals with microalgae was investigated several decades ago, this research has been reactivated by the recent exploration of microalgae as the third generation of feedtstocks for biofuel production. Because the resultant defatted biomass contains high levels of protein and other nutrients, it may replace a portion of corn and soybean meal in animal diets. Our laboratory has acquired four types of full-fat and de-fatted microalgal biomass from biofuel production research (Cellana, Kailua-Kona, Hawaii) that contain 13.9 to 38.2% crude protein and 1.5 to 9.3% crude fat. This review summarizes the safety and efficacy of supplementing two types of the biomass at 7.5 to 15% in the diets of weanling pigs, broiler chicks, and laying hens. Based on their responses of growth performance, egg production and quality, plasma and tissue biochemical indicators, and(or) fecal chemical composition, all three types of animals were able to tolerate the microalgal biomass incorporation into their diets at 7.5% (on as fed basis). Holistic analysis is also provided to explore the global potential of using the defatted microalgal biomass as a new feed ingredient in offsetting the biofuel production cost, reducing the dependence on staple crops such as corn and soybeans, decreasing greenhouse gas production of animal agriculture, and developing health value-added animal products. Key words: biofuel, broilers, laying hen, microalgae biomass, pigs

INTRODUCTION Global population is anticipated to increase from 7 to 9 billion by the mid-century (Secretariat, 2006). This anticipation, along with an accelerated urbanization, has led to a projected increase of annual meat production from 218 million t in 1999 to 376 million t by 2030. Consequently, this projected increase will require a 44, 132, and 75% increase in the world’s pork, chicken, and egg production, respectively, over this period (Bruinsma, 2003).

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Consequently, there will be a large increase in the need for animal feeds. Traditionally, corn and soybean meal (SBM) represent two major ingredients in animal diets to meet their energy and protein requirements. Approximately, 35% of the world consumption of cereal is used as feed for food-producing animals (Bruinsma, 2003). Because corn and soybeans are two staples for human diets, their massive use in the animal feeding creates a direct competition with human consumption. Currently, the world production of soybeans is approximately 28 million t of oil equivalent. To keep up with the food demand, soybean production will need to increase 110% by 2030 (Bruinsma, 2003). This translates to an increase of 32 million ha of harvested area for soybeans alone (Bruinsma, 2003), which is roughly equal to the size of the state of New Mexico. Unfortunately, increasing harvestable cropland is unrealistic because global cropland is rapidly declining due not only to soil erosion and desert expansion but also increased residential, industrial, and recreational uses (Brown, 2004). Apparently, the world may not afford to continue the use of large quantities of corn and soybean meal in animal feeding for the sake of human food security. Alternative ingredients should be explored to replace them or other major cereals in animal rations to sustain the current growth in animal production.

A NEW JUNCTION OF FEED, ENVIRONMENT, AND BIOFUEL Crops for animal diets are grown on arable land often requiring fresh water irrigation and typically chemical fertilizers, both of which impose a substantial degree of environmental liability (Tilman et al., 2002). Oftentimes, intensive animal agriculture may cause pollutions to the surrounding habitats and ecosystems in the form of excess manure phosphorus and nitrogen (Bourgeois, 2012). In the U.S., a minimum of 120 million t of manure is generated annually (Burkholder et al., 2007), entering the surrounding atmosphere, water, and soil by means of volatilization, runoff, and leaching (Tilman et al., 2002). Animal agriculture contributes to 18% 3 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

of all anthropogenic greenhouse gas emissions and 65% of all anthropogenic nitrogen released into the atmosphere (Steinfeld et al., 2006), causing acidification of non-agricultural eco-systems and the development of acid rain (Heederik et al., 2007). Nitrogen runoff that enters either coastal or fresh waters results in eutrophication, which diminishes the quantity and diversity of ecosystems (Mallin and Cahoon, 2003). The challenge arises to improve the sustainability of animal agriculture, while intensifying its practices to feed an imminent increase in global population and diminishing food competition between humans and animals without exacerbating its environmental impacts. One such alternative may be replacing corn and soybean meal in animal diets with microalgae that seem to be more environmentally friendly (Christaki et al., 2011). Because the global supply of petroleum continues to decline, renewable fuels have been explored as alternative energy sources. Biofuel production has shown its promise of harnessing adequate energy, while reducing greenhouse emissions. Corn and other crops that produce sugars and vegetable oils were used to produce the first generation of liquid biofuel, whereas lignocellulosic biomass or woody crops became the feedstocks for the second generation biofuel (Schenk et al., 2008). However, there were major limitations associated with these first two generations of biofuel production. Thus, microalgae have recently gained popularity as feedstocks for the third generation of biofuel production. They demonstrate rapid growth rate, rich oil content (Chisti, 2007), strong ability to sequester CO2, and rapid conversion of CO2 into a reusable biomass such as methane or hydrogen (Li et al., 2008; Mostafa, 2012). Because the defatted microalgal biomass contains significant amounts of protein, carbohydrates, and other nutrients after the oil extraction (Becker, 2004; Chisti, 2007; Brune et al., 2009; Shields and Lupatsch, 2012), it can be an excellent replacement of conventional ingredients in animal diets.

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Thus, the fuel and feed dual application of microalgae stands as a propitious mediator to reshape the junction between intensifying animal agriculture and our unmet needs for global renewable energy, food, and environmental sustainability.

CHEMICAL COMPOSITION OF MICROALGAE The CP contents in a variety of species of algae range from 6 to 71% of DM (Becker, 2007). The CP of the microalgae used in our laboratory ranges from 13.9 to 38.2%, which is 30 to 80% of that in the SBM, but 0.9 to 4.2-fold greater than that in corn (Figure 1). The precise inclusion of microalgae and ratio of corn and SBM replacement should be tailored for each production species to maximize the benefit. It also must be noted that about 10% of the nitrogen found in microalgae consists of non-protein nitrogen, including nucleic acids, amines, glucoasamides, and nitrogen-containing cell wall components (Becker, 2007). Therefore, the protein content of microalgae alone is not regarded as the major argument to propagate their utilization in animal feeds. Its nutritional quality depends on amino acid profile and availability (Becker, 2004). The amino acid profile of various microalgal species compares favorably with conventional protein sources. The content of the essential and typically limiting amino acids for microalgae, relative to those in corn and SBM, are shown in Figure 1. Lysine, the first limiting amino acid in typical swine corn-SBM based-diets, ranges from 0.57 to 2.27% in the microalgae, compared with 0.26 and 3% in corn and SBM, respectively. The green microalgae had good amounts of methionine, threonine, and tryptophan. The crude fat of microalgae used in our laboratory ranges from 1.5 to 9.3%, compared with 1.3 and 3.3% in SBM and corn, respectively. Notably, marine microalgae contain greater amounts of the omega-3 (n-3) fatty acids, eicosapentaenoic (EPA) and docosahenaenoic acid (DHA), compared with conventional animal protein sources (Fredriksson et al., 2006; 5 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

Kalogeropoulos et al., 2010). Microalgae also contain naturally-occurring carotenoids that may help the n-3 fatty acid stabilization (Barclay et al., 1994). The four microalgal products contain very high levels of sodium and good levels of phosphorous. The diatom microalgae contain high levels of ash and calcium, whereas the green microalgae contain high levels of ADF and NDF (Figure 1).

MICROALGAE ON ANIMAL NUTRITION AND HEALTH Algae incorporation into animal diets has been investigated for decades (Grau and Klein, 1957). Approximately, one-third of the current world supply of algae is used in animal feeds (Belay et al., 1996). Despite that, the potential of defatted microalgal biomass generated from the biofuel production in animal feeding remains scant in the literature. Our laboratory has conducted a series of experiments to determine effects of the defatted microalgal biomass in diets of weanling pigs, broilers, and laying hens. Our initial objectives were to find out: 1) if it was nutritionally feasible and physiologically safe to feed these animals with the microalgal products from the biofuel production research facility; 2) what were the maximal dietary replacements of corn and soybean meal with the microalgal products; and 3) how the microalgal supplements affected growth performance, plasma biochemical status, chemical composition of excreta, and(or) quality of animal product. Our preliminary findings are summarized in Figure 2. Swine Initially, the feasibility of algae as a protein supplement was evaluated in growingfinishing pigs fed a barley and fishmeal-based diet supplemented with up to 10% (on an as fed basis) of sewage-grown Chlorella sp. and Scenedesmus sp. (Hintz and Heitman, 1967). Growth rate and feed conversion efficiency were unaffected in algae-fed pigs compared with those fed

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the basal diet. When early weaned piglets and sows were fed a diet in which S. maxima replaced up to 12% of the total protein from skim milk and SBM, apparent digestibilities of the diets were reduced without effect on the growth of the piglets (Février and Sève, 1975). While feed efficiency was improved in the algae-fed pigs, they also supplied 12% less lysine. A greater direct replacement of 33% soy protein in the diets of weanling pigs with either a mixture of S. maxima and A. platensis, or Chlorella sp. showed a similar effect on weight gains to those pigs fed a basal diet, as well as an absence of diarrhea, apparent toxicity, or gastro-intestinal lesioning (Yap et al., 1982). Notwithstanding the repeated establishment of algae as a viable swine feed supplement, little is known about the effects of the defatted microalgal biomass from the biofuel production on the overall growth performance and health of pigs. The first pilot pig study in our laboratory investigated the feasibility and safety of the Staurospira sp. in both lipid-extracted and full-fat biomass forms to directly replace SBM in the corn-SBM diets of weanling pigs for 6 wk (Isaacs et al., 2011). Either 6.6% of the whole-fat diatom microalgae (WFA) or 7.2% of the de-fatted diatom microalgal biomass (DFA; provided by Cellana, Kailua-Kona, Hawaii) showed no negative effects on body weight gain or overall health status. Biochemical indicators of plasma including urea nitrogen concentration, alanine aminotransferase activity, and alkaline phosphatase activity were not affected by the biomass inclusion in the diets. We conducted a follow-up study to determine the maximal inclusion levels of the defatted diatom and their effects on plasma lipid profile, as well as fecal and plasma mineral levels of pigs. Weanling pigs were fed up to 15% DFA in replacement of a combination of SBM and corn for 6 wk (Lum et al., 2012). Compared with pigs fed the control diet, the overall ADG and G:F were reduced by 9 and 11%, respectively, in pigs fed 15% DFA or 7.5% DFA to replace the

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same level of SBM (Figure 1). In pigs fed 7.5% DFA to replace a combination of SBM and corn, the G:F was 8% less than the control group. Across all treatment groups, no differences were seen in the ADFI, plasma biochemical parameters including lipid profiles, and predicted body lean yield. As a co-product of the biofuel industry, the microalgal biomass may contain high levels of ash. Our particular diatom biomass was found to contain 45% ash, and high sodium and silica, which might adversely affect the health status and growth performance of pigs by altering dietary electrolyte balance. Additionally, the much lower CP content of the DFA in comparison with SBM (i.e., 19 vs. 47.5%) may have contributed to the depressed growth performance in those fed 15% DFA or 7.5% DFA replacing SBM. While the plasma biochemical measures of health status showed that pigs fed up to 15% DFA had no signs of toxicity, their fecal and plasma mineral profiles were altered. Fecal Cu, Se, and Zn concentrations in these pigs were less than in the control group of pigs, but their fecal Cr, Ni, Pb, S, Si, Sr, and Ti, as well as their plasma Fe and Se concentrations were elevated. The decreased fecal Cu, Se, and Zn in pigs fed the biomass led us to speculate if these reductions were associated with the adverse effects of DFA and if dietary supplementations of these elements alleviated those effects. As such, we conducted a third study, whereby weanling pigs were fed 10% WFA alone, or supplemented with 50% more of Cu, Se, and Zn, or 2% fumaric acid for 6 wk (Jung et al., 2013). Pigs fed 10% WFA alone displayed 7% less ADG and 2% less G:F than pigs fed the control diet. Amenably, the supplementation of fumaric acid alleviated the adverse effects of the WFA, whereas the inclusion of Cu, Se, and Zn did not recover the growth losses. Thus, bioavailability of Cu, Se, and Zn was unlikely a limiting factor in growth performance of these pigs. It is possible that the high ash and sodium contents of the diatom skewed the acid-base balance in the digestive tract and the tissues, and the incorporation of an

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organic acid might help rescue that skew. Broiler Chicks Algae inclusion into poultry diets seems to offer the most promising prospect for industrial applications (Grau and Klein, 1957; Mokady et al., 1979; Becker, 2004). Early research focused on sewage-grown algae, such as Chlorella (Grau and Klein, 1957; Mokady et al., 1979), due to its high protein and carotenoid contents. Chicks could tolerate up to 20% of aluminum-free algae meal without impaired growth (Grau and Klein, 1957). Feeding 10% of Chlorella pyrenoidosa improved feed efficiency and body weight gain compared with the basal diet deficient in riboflavin, vitamin B12 and vitamin A, but decreased growth performance compared with a complete diet (Combs, 1952). The inclusions of the blue-green algae Spirulina in diets for chicks demonstrated consistent results: while lower levels of inclusion were tolerated, higher levels led to depressed growth. Toyomizo and colleagues (Toyomizu et al., 2001) fed broiler chicks diets containing 0, 4 or 8% Spirulina for a period of 16 d and observed no differences among treatments in body weight or relative liver, abdominal fat, kidney or Pectoralis profundus weight. However, broilers fed 12% Spirulina for 41 d grew slower than those chicks consuming Spirulina at lower inclusion levels (Ross and Dominy, 1990). As in the case of weanling pigs, our laboratory has studied the inclusion of DFA (Staurosira sp) into the broiler diets in replacing SBM or a mixture of corn and SBM (Austic et al., 2013, Figure 1). Replacing 7.5% SBM alone or 10% mixture of corn and SBM with DFA resulted in decreased body weight gain (P < 0.0001) and feed efficiency (P = 0.11) during wk 0 to 3, but not wk 3 to 6 or the entire 6-wk period. Additionally, broilers fed 7.5% DFA diets replacing SBM alone demonstrated performance characteristics comparable to the controls when

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the diets were supplemented with essential amino acids (Met, Lys, Ile, Thr, Trp, and Val), but not a commercial protease or minerals. Thus, the reduction in growth performance caused by DFA was not due to electrolyte balance or protein hydrolysis, but rather a deficiency of one or more essential amino acids. Because uric acid is the end product of catabolism of amino acids from food or the turnover of existing body tissues (Hernandez et al., 2012), plasma or serum uric acid is often used as an indicator of amino acid utilization (Donsbough et al., 2010). Plasma uric acid was not altered in male broiler chicks fed a 7.5% DFA-containing diet in replacing SBM compared with those fed the control diet (Austic et al., 2013). Plasma uric acid was also not affected by the addition of a protease or essential amino acids in the DFA-containing diets. However, males fed a diet containing 10% DFA in replacing a mixture of corn and SBM had lower plasma uric acid concentrations than females fed the control diet (Austic et al., 2013). This difference indicates a possible sex and microalgae interaction on plasma uric acid concentrations (Bell et al., 1959). Overall, little recent research has investigated the full effect of dietary microalgal biomass on broiler protein metabolism. Male broiler chicks fed the 7.5% DFA-containing diet for 6 wk had no differences in plasma total cholesterol, triglycerides, NEFA, glucose, alkaline phosphatase or alanine transaminase activity compared with control birds (Austic et al., 2013), indicating that microalgal inclusion in the diet at this level posed no adverse health effects. However, similar to the results seen by Grau and Klein (1957), chicks fed the DFA-containing diets had a visually increased volume and wetness of excreta compared with the excreta of control chicks (Austic et al., 2013). Our ongoing research is evaluating impacts of feeding defatted green microalgal biomass on water intakes of broiler chicks. The relatively high ash content, salt in particular, may

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increase water intake and excreta volume. The ash content of various microalgae ranges from 6.5 to 41% on an ‘as is’ basis (Tokuşoglu and Üunal, 2003; Austic et al., 2013) and includes substantial amounts of Na, K, Mg, Fe and Cl. Extra water intake and excreta output is a potential liability to dietary microalgae inclusion. Further processing of microalgae to reduce their ash content, potentially by washing or other measures, may improve their feeding values. Laying Hens Herber and Van Elswyk (1996) supplemented 2.4 or 4.8% golden marine algae to the diet of 24- and 56-wk-old Single Comb White Leghorn hens. Young hens (i.e., 24 wk old) showed transient depression in egg and yolk weight, but old hens did not show any changes in egg traits. Egg production at both ages was not affected by diet. Nutritional value of Chlorella vulgaris, processed by spray drying or spray dried after bullet-milled was also determined (Halle et al., 2009). During an 8-mo experiment, spray-dried after bullet-milled Chlorella vulgaris (0.75%) supplementation decreased feed intake without affecting laying intensity, egg weight, and feed conversion ratio. Egg yolk weight was increased when spray dried after bullet-milled Chlorella vulgaris was incorporated into diets with reduction of albumen weight. Yolk color, determined by Roche color fan, was also increased in both spray-dried only and spray-dried after bulletmilled Chlorella vulgaris supplemented groups, but there was no dose-dependent effect. Likewise, we conducted a layer hen study to determine whether DFA (Staurosira sp) could replace a portion of SBM or a combination of corn and SBM in diets without affecting egg production and quality (Leng et al., 2012). A total of 100 ISA Babcock White leghorn laying hens (47-wk old) were randomly assigned to 4 dietary treatments. The 4 experimental diets included a corn-SBM basal diet, the basal diet with 7.5% DFA and the 5 most limiting amino acids substituting for soybean meal, and the basal diet with 7.5% or 15% DFA substituting for

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SBM and corn. During the 8-wk experiment, hens fed 15%, but not 7.5% DFA, had lower egg production rate (−12%), daily feed intake (−9 g), and plasma uric acid concentration than those fed the basal diet. Feeding the 15% DFA elevated egg albumen weight and height compared with the 7.5% DFA diet, and the two levels of DFA produced dose-dependent changes in three color measures and four fatty acid (i.e., C16:1, C18:1, C18:2, and C18:3) profiles of egg yolk. There were no significant differences in egg weight, shell strength, and shell specific gravity or activities of plasma alanine aminotransferase and alkaline phosphatase among the 4 dietary treatment groups. Altogether, it was feasible to include 7.5 DFA plus amino acids, in substitution for SBM or for a combination of corn and SBM, in the diets of laying hens for 8 wk without adverse effects on hen health or egg production. Obviously, the 8-wk feeding was a relatively short period to examine the full effect of microalgae on hen egg production and quality. We recently conducted much longer experiments and are currently completing the sample and data analyses.

MICROALGAE “ONLY” BENEFITS Microalgae may bear species-specific nutrient enrichments for practical applications in both animal and human nutrition. Pigs fed naturally iodine-rich algae, Laminaria digitata, at 5 or 8 mg I/kg feed for 3 mo had up to a 10% greater daily body weight gain in comparison with the control group (He et al., 2002). Meanwhile, iodine was enriched by 45% to 207% in fresh muscle, adipose, heart, liver, and kidney tissues. Consequently, the iodine-enriched pork and pig tissues may be used to prevent or alleviate human iodine deficiencies around the world. Interestingly, we observed a 22% increase in plasma iron concentration in pigs fed 15% DFA compared with those fed the control diet, as well as marginally significant elevations (P = 0.06) in the packed cell volume and blood hemoglobin of pigs fed 10% WFA (Jung et al., 2013). These findings 12 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

imply that diatom microalgae supplementation may improve the iron status of pigs for hemoglobin synthesis. Because pigs are an excellent model to study human iron nutrition, we are currently following up the potential and mechanism of such improvement in pigs by microalgal supplementation. Enhancing n-3 fatty acid intake in humans may help reduce risks of chronic diseases including diabetes, hypertension, coronary heart disease, arthritis and cancer (Daviglus et al., 1997; Albert et al., 1998). It is also believed that decreasing dietary ratio of omega-6 (n-6) to n-3 fatty acids is beneficial because the ratio in the modern Western diets is > 10:1 (Lands, 2005). These notions have led to enriching n-3 fatty acids and altering the fatty acid profiles of commonly consumed animal foods. Because the average American consumes about 40 kg of broiler chicken and 250 eggs annually (USDA Economic Research Service, 2006), both chicken meat and eggs are excellent candidates for the n-3 fatty acid enrichments. As mentioned previously, marine microalgae contain great amounts of EPA and DHA (Fredriksson et al., 2006; Kalogeropoulos et al., 2010) and many naturally occurring carotenoids to stabilize the n-3 fatty acids (Barclay et al., 1994). Our laboratory is currently determining if feeding various levels of the 4 types microalgal biomass to broiler chicks and layer hens results in enrichment of n-3 fatty acids, in particular EPA and DHA, and shifts of n-6 to n-3 fatty acids in their meat and eggs. Commercially available eggs contain relatively greater concentrations of n-6 than those of n-3 fatty acids. A number of studies have been conducted to enrich eggs with n-3 fatty acids through diet manipulations (Kenyon, 1972; Jiang et al., 1991; Jia et al., 2008). Abril et al. (1999) used fermented Schizochytrum sp. at 0.86, 2.57 and 4.29% inclusion for producing DHAenriched eggs. The DHA content per egg reached 134 and 220 mg when hens were fed the 0.86 and 4.29% algae diets, respectively. Flaxseed or flaxseed oil is commonly used to produce n-3

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fatty acids-enriched eggs. However, the flaxseed products contain mainly α-linolenic acid with little DHA or EPA. Due to low conversion of α-linolenic acid into DHA in poultry, it is hard to produce DHA-fortified eggs with the supplementation of flaxseed or flaxseed oil (Van Elswyk, 1997; Gerster, 1998). Carotenoids (β-carotene or astaxanthin) are lipid-soluble pigments that are primarily produced within phytoplankton, algae, and plants. Astaxanthin, the main carotenoid in microalgae (Dominguez-Bocanegra et al., 2004), is a dark-red pigment with stronger antioxidant activity compared with other carotenoids (i.e., 10 times greater than β-carotene and 300 times greater than α-tocopherol). Zahroojian et al. (2011) reported that dietary supplementation of 2.5% (on an as fed basis) microalgae (Spirulina platensis) produced egg yolk color similar to that by feeding a synthetic pigment. Dietary inclusion of Chlorella (i.e., 1 to 2% on an as fed basis) increased total yolk carotenoids and color as determined by the Roche color fan (Kotrbáček et al., 2013).

SUMMARY AND CONCLUSIONS Collectively, our laboratory has conducted a series of experiments to demonstrate the feasibility of partially replacing dietary corn and SBM with several types of microalgal biomass in diets for weanling pigs, broilers, and laying hens. In pigs, dietary incorporation of DFA up to 15% (on an as fed basis) or WFA up to 10% (on an as fed basis) induced no overt toxicity, as shown by plasma biochemistry (i.e., alkaline phosphatase activity, alanine aminotransferase activity, urea nitrogen concentration, lipid profile, blood hemoglobin, packed cell volume, inorganic P, tartrate-resistant acid phosphatase activity) and body lean yield, similar to those of pigs fed a conventional corn-SBM diet. A diet replacing up to 7.5% corn and SBM showed no adverse effects on body weight gain. Male broilers fed 10% DFA (on an as fed basis) showed 14 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

lower uric acid than female broilers fed the control diet, indicating a sex-dependent effect of DFA replacement of corn and SBM in the diet of broilers. For laying hens, replacing corn and SBM with 10% DFA (on an as fed basis) did not affect either the egg production or body weight. Thus, supplementing microalgae, at appropriate levels, into diets for these animals did not produce adverse effect on their performance or overt toxicity. The U.S. broiler, egg and swine industries consume around 22 million t of SBM annually (United Soybean Board, 2012). With an anticipated replacement of 20 to 50% of SBM by microalgae in the diets, it would spare 4.4 to 11 million t of SBM annually for human consumption. Table 1 predicts the potential saving of corn and soybean meal and harvestable land in the U.S. if microalgal biomass is added into swine and poultry diets at 5 to 20%. To improve our understanding of the environmental impact of microalgae as a feedstuff, further research should closely examine the fecal and urinary excreta from animals fed the microalgal biomass. Pigs fed 15% DFA (on an as fed basis) had greater levels of fecal Cr, Ni, Pb, S, Si, Sr, and Ti at wk 6 than the control group, which may be indicative of a risk for microalgae’s trace mineral composition to contribute to heavy metal accumulation or runoff. To alleviate animal agriculture’s impact on environment, it’s pertinent that we closely monitor and supply animals with the precise amount of nutrients. Despite this, the implementation of a biofuel by-product as a feedstuff inherently provides an eco-friendly, value-added commodity that would otherwise be considered a leftover industrial waste product. The cultivation of microalgae for biofuel production ultimately harnesses energy while lowering greenhouse gas emissions by replacing fossil fuels and sequestering atmospheric CO2. Feed production contributes to 54 to 73% of total greenhouse gases derived from pork production (Basset-Mens and Van Der Werf, 2005). Because SBM and microalgae produce 721 and 135 g of CO2 eq. per

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kg (Dalgaard et al., 2008; Sander and Mruthy, 2010), respectively, replacement of SBM with microalgae could not only save food for human consumption but also cut down greenhouse effect of animal agriculture. To date, the production of microalgae for biofuel does not appear to be cost-effective, albeit it is seemingly advantageous. Based on predicted annual oil yields of cultivated algae, the approximate cost per barrel would amount to $20 (Demirbas, 2009), whereas the average U.S. barrel of oil is selling for over $100 per barrel (Demirbas and Fatih Demirbas, 2011). However, oil yields from microalgae cultivation have yet to reach this estimated price (Patil et al., 2005). In the current systems, both the need for water and nitrogen fertilizer in algaculture, and the energy expenditure required to process and extract lipids still amount to extensive costs (Pimentel et al., 2004; Pimentel, 2008). Both past research and our recent findings in swine and poultry have revealed that the microalgal biomass may indeed serve as a viable and health-value-added feedstuff. Future research will be required to quantify the energy and nutrient bioavailability of various defatted microalgal biomass from the biofuel production and to elucidate biochemical and molecular mechanisms for their nutritional and metabolic functions (Figure 2). Feeding the defatted microalgae biomass from biofuel production to poultry and swine will reduce the dependency of the animal industry on corn and SBM, potentially sparing these ingredients and(or) their used acreage for alternative applications and lowering greenhouse gas production from animal agriculture.

LITERATURE CITED Abril, J., W. Barclay, and P. G. Abril. 1999. Safe use of microalgae (DHA GOLD) in laying hen feed for the production of DHA-enriched eggs. In: J. S. Sim, S. Nakai, and W. Guenter, 16 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

editors, Egg Nutrition and Biotechnology. CABI Publishing. Wallingford. United Kingdom. p. 197-202. Albert, C. M., C. H. Hennekens, C. J. O'Donnell, U. A. Ajani, V. J. Carey, W. C. Willett. J. N. Ruskin, and J. E. Manson. 1998. Fish consumption and risk of sudden cardiac death. JAMA 279:23-28. Austic, R. E., A. Mustafa, B. Jung, S. Gatrell, and X. G. Lei. 2013. Potential and limitation of a new defatted diatom microalgal biomass in replacing soybean meal and corn in diets for broiler chickens. J. Agric. Food Chem. 61:7341-7348. Barclay, W., K. Meager, and J. Abril. 1994. Heterotrophic production of long chain omega-3 fatty acids utilizing algae and algae-like microorganisms. J. Appl. Phycol. 6:123-129. Basset-Mens, C., and H. M. G.Van Der Werf. 2005. Scenario-based environmental assessment of farming systems: The case of pig production in France. Agri. Ecosyst. Environ. 105:127144. Becker, E. W. 2004. Microalgae in Human and Animal Nutrition.In: A. Richmond, editor, Handbook of Microalgal Culture: Biotechnology and Applied Phycology. Blackwell Science Ltd, Oxford, United Kingdom. p. 312. Becker, E. W. 2007. Micro-algae as a source of protein. Biotechnol. Adv. 25:207-210. Belay, A., T. Kato, and Y. Ota. 1996. Spirulina (arthrospira): Potential application as an animal feed supplement. J. Appl. Phycol. 8:303-311. Bell, D. J., W. M. McIndoe, and D. Gross. 1959. Tissue components of the domestic fowl. 3. the non-protein nitrogen of plasma and erythrocytes. Biochem. J. 71:355-364. Bourgeois, L. 2012. A discounted threat: Environmental impacts of the livestock industry. Earth Common Journal. 2(1).

17 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

Https://Journals.Macewan.Ca/Index.Php/Earthcommon/Article/View/56/83.(Accessed 11 October 2013.) Brown, L. R. 2004. Outgrowing the earth: The food security challenge in an age of falling water tables and rising temperatures. WW Norton & Company. New York, NY. Bruinsma, J. 2003. World agriculture: Towards 2015/2030; an FAO perspective. Earthscan. http://www.fao.org/docrep/005/y4252e/y4252e00.htm. (Accessed August 15, 2013.) Brune, D., T. Lundquist, and J. Benemann. 2009. Microalgal biomass for greenhouse gas reductions: Potential for replacement of fossil fuels and animal feeds. J. Environ. Eng. 135:1136-1144. Burkholder, J., B. Libra, P. Weyer, S. Heathcote, D. Kolpin, P. S. Thorne, and W. Michael. 2007. Impacts of waste from concentrated animal feeding operations on water quality. Environ. Health Perspect. 115:308-312. Chisti, Y. 2007. Biodiesel from microalgae. Biotechnol. Adv. 25:294-306. Christaki, E., P. Florou-Paneri, and E. Bonos. 2011. Microalgae: a novel ingredient in nutrition. Int. J. Food Sci. Nutr. 62:794-799. Combs, G. F. 1952. Algae (chlorella) as a source of nutrients for the chick. Science. 116:453-454. Dalgaard, R., J. Schmidt, N. Halberg, P. Christensen, M. Thrane, and W. A. Pengue. 2008. LCA of soybean meal. Int. J. Life Cycle Assess. 13:240–254. Daviglus, M. L., J. Stamler, A. J. Orencia, A. R. Dyer, K. Liu, P. Greenland, M. K. Walsh, D. Morris, and R. B. Shekelle. 1997. Fish consumption and the 30-year risk of fatal myocardial infarction. N. Engl. J. Med. 336:1046-1053. Demirbas, A., and M. Fatih Demirbas. 2011. Importance of algae oil as a source of biodiesel. Energ. Convers. Manage. 52:163-170.

18 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

Demirbas, A. H. 2009. Inexpensive oil and fats feedstocks for production of biodiesel. Energy Education Science and Technology Part A-Energy Science and Research. 23:1-13. Dominguez-Bocanegra, A. R., I. Guerrero Legarreta, F. Martinez Jeronimo, and A. Tomasini Campocosio. 2004. Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis. Bioresour. Technol. 92:209-214. Donsbough, A. L., S. Powell, A. Waguespack, T. D. Bidner, and L. L. Southern. 2010. Uric acid, urea, and ammonia concentrations in serum and uric acid concentration in excreta as indicators of amino acid utilization in diets for broilers. Poult. Sci. 89:287-294. Février C. and B. Sève. 1975. Incorporation of a spiruline (Spirulina maxima) in swine food. Ann. Nutr. Aliment. 29:625-650. Fredriksson, S., K. Elwinger, and J. Pickova. 2006. Fatty acid and carotenoid composition of egg yolk as an effect of microalgae addition to feed formula for laying hens. Food Chem. 99:530-537. Gerster, H. 1998. Can adults adequately convert alpha-linolenic acid (18:3n-3) to eicosapentaenoic acid (20:5n-3) and docosahexaenoic acid (22:6n-3). Int. J. Vitam. Nutr. Res. 68:159-173. Grau, C. R., and N. W. Klein. 1957. Sewage-grown algae as a feedstuff for chicks. Poult. Sci. 36:1046-1051. Halle, I., P. Janczyk, G. Freyer, and W. Souffrant. 2009. Effect of microalgae Chlorella vulgaris on laying hen performance. Arch. Zootechnica. 12:5-13. He, M. L., W. Hollwich, and W. A. Rambeck. 2002. Supplementation of algae to the diet of pigs: A new possibility to improve the iodine content in the meat. J. Anim. Physiol. Anim. Nutr. (Berl.). 86:97-104.

19 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

Heederik, D., T. Sigsgaard, P. S. Thorne, J. N. Kline, R. Avery, J. H. Bønløkke, E. A. Chrischilles, J. A. Dosman,C. Duchaine, S. R. Kirkhorn, K. Kulhankova, and J. A. Merchant. 2007. Health effects of airborne exposures from concentrated animal feeding operations. Environ. Health Perspect. 115:298-302. Herber, S. M., and M. E. Van Elswyk. 1996. Dietary marine algae promotes efficient deposition of n-3 fatty acids for the production of enriched shell eggs. Poult. Sci. 75:1501-1507. Hernandez, F., M. Lopez, S. Martinez, M. D. Megias, P. Catala, and J. Madrid. 2012. Effect of low-protein diets and single sex on production performance, plasma metabolites, digestibility, and nitrogen excretion in 1- to 48-day-old broilers. Poult. Sci. 91:683-692. Hintz, H. F., and H. Heitman. 1967. Sewage-grown algae as a protein supplement for swine. Anim. Prod. 9:135-140. Isaacs, R., K. R. Roneker, M. Huntley, and X. G. Lei. 2011. A partial replacement of soybean meal by whole or defatted algal meal in diet for weanling pigs does not affect their plasma biochemical indicators. J. Anim. Sci. 89(Suppl. 1):723 (Abstr.) Jia, W., B. A. Slominski, W. Guenter, A. Humphreys, and O. Jones. 2008. The effect of enzyme supplementation on egg production parameters and omega-3 fatty acid deposition in laying hens fed flaxseed and canola seed. Poult. Sci. 87:2005-2014. Jiang, Z. R., D. U. Ahn, and J. S. Sim. 1991. Effects of feeding flax and two types of sunflower seeds on fatty acid compositions of yolk lipid classes. Poult. Sci. 70:2467-2475. Jung, B. Y., K. K. Lum, K. R. Roneker, and X. G. Lei. 2013. Supplemental fumaric acid restored growth performance of weanling pigs fed 10% full-fat diatom microalgae. J. Anim. Sci. 91(E-Suppl. 2):705. (Abstr.) Kalogeropoulos, N., A. Chiou, E. Gavala, M. Christea, and N. K. Andrikopoulos. 2010.

20 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

Nutritional evaluation and bioactive micoconstituents (carotenoids, tocopherols, sterols and squalene) of raw and roasted chicken fed on DHA-rich microalgae. Food Res. Int. 43:2006-2013. Kenyon, C. N. 1972. Fatty acid composition of unicellular strains of blue-green algae. J. Bacteriol. 109:827-834. Kotrbáček, V., M. Skřivan, J. Kopecký, O. Pěnkava, P. Hudečková, I. Uhríková, and J. Doubek. 2013. Retention of carotenoids in egg yolks of laying hens supplemented with heterotrophic chlorella. Czech J. Anim. Sci. 58:193-200. Lands, W. E. 2005. Dietary fat and health: The evidence and the politics of prevention: Careful use of dietary fats can improve life and prevent disease. Ann. N. Y. Acad. Sci. 1055:179192. Leng, X. J., H. N. Hsu, R. E. Austic, and X. G. Lei. 2012. Defatted algae biomass may replace one-third of soybean meal in diets for laying hens. J. Anim. Sci. 90(Suppl. 3):701. (Abstr.) Li, Y., M. Horsman, N. Wu, C. Q. Lan, and N. Dubois-Calero. 2008. Biofuels from microalgae. Biotechnol. Prog. 24:815-820. Lum, K. K., K. R. Roneker, and X. G. Lei. 2012. Effects of various replacements of corn and soy by defatted microalgal meal on growth performance and biochemical status of weanling pigs. J. Anim. Sci. 90(Suppl. 3):701. (Abstr.) Mallin, M. A., and L. B. Cahoon. 2003. Industrialized animal production: A major source of nutrient and microbial pollution to aquatic ecosystems. Popul. Environ. 24:369-385. Mokady, S., S. Yannai, P. Einav, and Z. Berk. 1979. Algae grown on wastewater as a source of protein for young chickens and rats. Nutr. Rep. Int. 9:383-390. Mostafa, S.S.M. 2012. Microalgal Biotechnology: Prospects and Applications. In: N.K. Dhal,

21 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

editor, Plant Science. http://www.intechopen.com/books/plant-science/microalgalbiotechnology-prospects-and-applications (Accessed 11 October 2013.) Patil, V., K. I. Reitan, G. Knutsen, L. M. Mortensen, T. Källqvist, E. Olsen, G. Vogt, and H. R. Gislerød. 2005. Microalgae as source of polyunsaturated fatty acids for aquaculture. Curr. T. Pl. Biol. 6:57-65. Pimentel, D. 2008. Biofuels, solar and wind as renewable energy systems: Benefits and risks. Springer-Verlag. Dordrecht, The Netherlands. Pimentel, D., B. Berger, D. Filiberto, M. Newton, B. Wolfe, E. Karabinakis, S. Clark, E. Poon, E. Abbett, and S. Nandagopal. 2004. Water resources: Agricultural and environmental issues. Bioscience 54:909-918. Ross, E., and W. Dominy. 1990. The nutritional value of dehydrated, blue-green algae (Spirulina plantensis) for poultry. Poult. Sci. 69:794-800. Sander K. and G. S.Murthy. 2010. Life cycle analysis of algae biodiesel. Int. J. Life Cycle Ass. 15:704-714. Schenk, P. M., S. R. Thomas-Hall, E. Stephens, U. C. Marx, J. H. Mussgnug, C. Posten et al. 2008. Second generation biofuels: High-efficiency microalgae for biodiesel production. Bioenergy Research 1:20-43. Secretariat, U. N. 2006. World population prospects: The 2006 revision. New York. http://www.un.org/esa/population/publications/wpp2006/wpp2006.htm. (Accessed 11 October 2013.) Shields, R. J., and I. Lupatsch. 2012. Algae for aquaculture and animal feeds. J. Anim. Sci. 21:23-37. Steinfeld, H., P. Gerber, T. Wassenaar, V. Castel, M. Rosales, and C. Haan. 2006. Livestock's

22 Downloaded from www.journalofanimalscience.org at Queen Mary, University of London on June 16, 2014

long shadow: Environmental issues and options. Rome, Food and Agriculture Organization of the United Nations (FAO). http://www.fao.org/docrep/010/a0701e/a0701e00.htm. (Accessed 11 October 2013.) Tilman, D., K. G. Cassman, P. A. Matson, R. Naylor, and S. Polasky. 2002. Agricultural sustainability and intensive production practices. Nature 418:671-677. Tokuşoglu, Ö, and M. Üunal. 2003. Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisis galbana. J. Food Sci. 68:1144-1148. Toyomizu, M., K. Sato, H. Taroda, T. Kato, and Y. Akiba. 2001. Effects of dietary Spirulina on meat color in muscle of broiler chickens. Br. Poult. Sci. 42:197-202. United Soybean Board. 2012. Animal agriculture economic analysis: National, 2001-2011. A Report for United Soybean Board. June 2012. Agralytica, Inc., Alexandria, VA. USDA Economic Research Service. 2006. Poultry Yearbook, Young Chicken: Per capita consumption, retail weight basis. www.ers.usda.gov/topics/animal-products/poultryeggs.aspx (Accessed on August 27, 2013.) Van Elswyk, M. E. 1997. Comparison of n-3 fatty acid sources in laying hen rations for improvement of whole egg nutritional quality: A review. Br. J. Nutr. 78:S61-S69. Yap, T. N., J. F. Wu, W. G. Pond, and L. Krook. 1982. Feasibility of feeding Spirulina maxima, Arthrospira platensis or Chlorella sp to pigs weaned to a dry diet at 4 to 8 days of age. Nutr. Rep. Int. 25:543-552. Zahroojian, N., H. Moravej, and M. Shivazad. 2011. Comparison of marine algae (Spirulina platensis) and synthetic pigment in enhancing egg yolk color of laying hens. Br. Poult. Sci. 52:584-588.

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Table 1. Potential saving of corn and soybean meal and harvestable land in the U.S. with microalgal inclusion into swine and poultry diets1

1

Dietary algae inclusion

Corn and soybean saved, thousand t

Land saved, thousand ha

5%

575

188-283

10%

1,150

375-567

20%

2,300

750-1,134

Calculations based on the 1997 and 1999 yields from Bruinsma et al., 2003.

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FIGURE CAPTIONS Figure 1. Comparisons of nutrient compositions of microalgal biomass with those of soybean meal and corn. All values are actually analyzed and normalized to the compared ingredient. Compared with those levels in soybean meal, the microalgal biomass had greater levels of EE, ADF, NDF, Ca, ash and Na. Compared with those levels in corn, levels of all nutrients in the microalgae biomass were greater. Abbreviations: DFA = de-fatted diatom microalgae biomass (Staurospira sp); WFA = whole fat diatom microalgae (Staurospira sp); DGA-1 = de-fatted green microalgae biomass species 1 (Desmodesmus sp); and DGA-2 = de-fatted green microalgae biomass species 2 (Desmodesmus sp.).

Figure 2. Preliminary overview of effects of microalgal biomass supplementation to diets of weanling pigs, broiler chicks, and laying hens. Data are summarized from Leng el at., 2012; Lum et al., 2012; Austic et al., 2013; and Jung et al., 2013. Abbreviations: DFA = de-fatted diatom microalgae biomass (Staurospira sp); WFA = whole fat diatom microalgae biomass; TRAP = tartrate resistant acid phosphatase.

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Figure 1

Percentage relative to soybean

1200

DFA WFA DGA-1 DGA-2

1000 800 600 400 200 0 DM

EE

ADF

NDF

Lys

Met

Thr

Trp

Met

Thr

Ca

P

Ash

DFA WFA DGA-1 DGA-2

1000 800 600 400 200 0

DM

Fold

Percentage relative to corn

1200

CP

1000 900 800 700 600 500 400 300 200 100 0

CP

EE

ADF

NDF

Lys

Trp

P

Ash

DFA WFA DGA-1 DGA-2

Na relative to soybean

Na relative to corn

Ca relative to corn

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Figure 2

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Nonruminant Nutrition Symposium: Potential of defatted microalgae from the biofuel industry as an ingredient to replace corn and soybean meal in swine and poultry diets.

While feeding food-producing animals with microalgae was investigated several decades ago, this research has been reactivated by the recent exploratio...
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