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Vegetarian Shrimp

Permanent Link: http://ncf.sobek.ufl.edu/NCFE004688/00001

Material Information

Title: Vegetarian Shrimp the Effects of Attractants in Alternative Plant-Based Diets on Growth Rates of Juvenile Pacific White Shrimp (Litopenaeus vannamei) (Boone, 1931)
Physical Description: Book
Language: English
Creator: White-Domain, Megan
Publisher: New College of Florida
Place of Publication: Sarasota, Fla.
Creation Date: 2012
Publication Date: 2012

Subjects

Subjects / Keywords: Sustainable Aquaculture
Pacific White Shrimp
Alternative Diets
Genre: bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Shrimp aquaculture is a growing industry with many related environmental impacts. One such impact is the harvest of wild fish stocks for the production of aquaculture feed ingredients (fish meal and fish oil) to feed shrimp raised in aquaculture systems. Alternative feeds are being developed using alternative plant-based protein and lipid sources. However, despite progress in reducing marine-based resources for the main protein source in alternative feeds, the requirement of attractants in the diets of Pacific white shrimp maintains dependence on wild fish stocks. The current research examines the role of attractants in plant-based diets by conducting growth trials with Pacific white shrimp to determine whether the presence of attractant effects growth rates. The results of the growth trials were inconclusive, with the experimental diet containing attractant out-performing the experimental diet without attractant in only one of the trials. Further research is needed in this area of aquaculture research to assist in reducing the dependence of the aquaculture industry on limited wild fish supplies.
Statement of Responsibility: by Megan White-Domain
Thesis: Thesis (B.A.) -- New College of Florida, 2012
Electronic Access: RESTRICTED TO NCF STUDENTS, STAFF, FACULTY, AND ON-CAMPUS USE
Bibliography: Includes bibliographical references.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The New College of Florida, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Local: Faculty Sponsor: Gilchrist, Sandra

Record Information

Source Institution: New College of Florida
Holding Location: New College of Florida
Rights Management: Applicable rights reserved.
Classification: local - S.T. 2012 W58
System ID: NCFE004688:00001

Permanent Link: http://ncf.sobek.ufl.edu/NCFE004688/00001

Material Information

Title: Vegetarian Shrimp the Effects of Attractants in Alternative Plant-Based Diets on Growth Rates of Juvenile Pacific White Shrimp (Litopenaeus vannamei) (Boone, 1931)
Physical Description: Book
Language: English
Creator: White-Domain, Megan
Publisher: New College of Florida
Place of Publication: Sarasota, Fla.
Creation Date: 2012
Publication Date: 2012

Subjects

Subjects / Keywords: Sustainable Aquaculture
Pacific White Shrimp
Alternative Diets
Genre: bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Shrimp aquaculture is a growing industry with many related environmental impacts. One such impact is the harvest of wild fish stocks for the production of aquaculture feed ingredients (fish meal and fish oil) to feed shrimp raised in aquaculture systems. Alternative feeds are being developed using alternative plant-based protein and lipid sources. However, despite progress in reducing marine-based resources for the main protein source in alternative feeds, the requirement of attractants in the diets of Pacific white shrimp maintains dependence on wild fish stocks. The current research examines the role of attractants in plant-based diets by conducting growth trials with Pacific white shrimp to determine whether the presence of attractant effects growth rates. The results of the growth trials were inconclusive, with the experimental diet containing attractant out-performing the experimental diet without attractant in only one of the trials. Further research is needed in this area of aquaculture research to assist in reducing the dependence of the aquaculture industry on limited wild fish supplies.
Statement of Responsibility: by Megan White-Domain
Thesis: Thesis (B.A.) -- New College of Florida, 2012
Electronic Access: RESTRICTED TO NCF STUDENTS, STAFF, FACULTY, AND ON-CAMPUS USE
Bibliography: Includes bibliographical references.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The New College of Florida, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Local: Faculty Sponsor: Gilchrist, Sandra

Record Information

Source Institution: New College of Florida
Holding Location: New College of Florida
Rights Management: Applicable rights reserved.
Classification: local - S.T. 2012 W58
System ID: NCFE004688:00001


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Vegetarian Shrimp: the Effects of A ttractants in A lternative Plant Based Diet s on Growth Rates of Juvenile Pacific White Shrimp ( Litopenaeus vannamei ) (Boone, 1931) By : Meagan White Domain A Thesis Submitted to the Division of Natural Sciences New College of Florida in partial fulfillment of the requirements for the degree Bachelor of Arts Under Sponsorship of Sandra Gilchrist Sarasota, Florida April, 2012

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ii For my father for always giving me the strength to carry on

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iii I would like to thank my committee members, Diana Weber, Leo Demski, and in particular my chair, Sandra Gilchrist, who donated her time to reading and editing this work while in progress. I would also like to thank Joel Beaver, Ian Schools, and Hannah Schotman, for their assistance in the lab. Final ly, I would like to thank New College of Florida for providing me lab space in the Pritzker Marine Biology Research Center and for funding my research through the Council of Academic Affairs Grant and the Research and Travel Grant.

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iv Table of Contents Dedication Acknowledgements Table of Contents An Introduction to the Aquaculture Industry and Its Practices The Growth and Practices of the Shrimp Aquaculture Industry The Dependence of Shrimp Aquaculture on Fish Meal and Fish Oil The Development of Potential Alternative Feeds Fish Meal and Its Potential Alternatives Fish Oil and Its Potential Alternatives Progress with Pa cific White Shrimp The Experimental Design Acclimation and Grow Out of Post Larval Shrimp The Control and Experimental Diets The Growth Trial Data, Analysis, and Results Discussion

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v List of Figures Figure 1 Distribution of aquaculture species among fresh, salt and brackish water by Figure 2 Distribution of global aquaculture production as of 2008.. Figure 3. The Pacific white shrimp ( Litopenaeus vannamei Figure 4. a. T he black tiger shrimp ( Penaeus monodon ). b. the Indian shrimp ( Penaeus indicus ). c. the banana shrimp ( Penaeus merguiensis ). d. the green tiger or bear shrimp ( Penaeus semisulcatus ). e. the o riental shrimp ( Penaeus chinensis ). f. the giant river prawn or the Malaysian prawn ( Macrobrachium rosenbergii ). g. the ginger prawn or the speckled shrimp ( Metapenaeus monoceros ). h. the yellow shrimp ( Metapenaeus brevicornis ............................................5 Figure 5. An oyster farm off the coast of Korea. Oysters are attached to ropes which hang down from the floats that ..................6 Figure 6. Salmon farms in Tasmania ..... ................................................. ........................... ..9 Figure 7. An in Figure 8. Collecting post larval shrimp from the wi ld with a fine mesh scissor net. Figure 9. Internal anatomy of shrimp, showing the luminal and serosal sides of the gut ............................................................................................................35 Figure 10. Grow out tank for post larval shrimp consisting of 100 gall ons of recirculating water. The dimensions of the tank are 21 x 82.5 inches with water 7 inches in depth Figure 11. Post larval shrimp in the grow out tank before the start of the growth trial Figure 12. One of the 65 gallon experimental tanks used for the growth trial. The water heater is shown at top right and the filter at bottom right Figure 13. A Pacific white shrimp from an experimental tank feeding on Experimental Diet 2. A second shrimp is approaching in the upper right corne r ..61 Figure 14. Graph of mean weight for each tank by week for Growth Trial 1. Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant. For mar gins of error refer to Table .64 Figure 15. Average weights for each diet by week for Growth Trial 1. For margins of error refer to Table 10

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vi Figure 16. Graph of mean weight for each tank by week Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant. For mar gins of error refer to Table 13. Figure 17. Average weights for each diet by week for Growth Trial 2. For margins of error refer to Table 14

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vii List of Tables Table 1. Statistics on the growth of the aquaculture industry Table 2. Details about the different systems of shrimp aquaculture. Table 3. Common shrimp aquaculture species that are raised in areas to which they are not indigenous Table 4. The net protein loss associated with f ed species in aquaculture Table 5. The optimal protein and lipid concentrations determined for various fish and invertebrate species Table 6. Apparent digestibility coefficients for a variety of feed ingred ients for Pacific white shrimp FM is fish meal; SBM is soybean meal; PM is peanut meal; WGM is wheat gluten meal; CGM is corn gluten meal; MBM is meat and bone meal; and PMM is poultry meat meal Table 7. The generalized life cycle for penaeid shrimp Table 8 Mean temperatures, salinities, and survival rates for Growth Trial 1 by tank Table 9 The mean weight (in grams) for each tank by week for Growth Trial 1. Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant Table 10 Average weights for each diet by week for Growth Trial 1 Table 1 1 Average daily growth coefficients and average specific growth rates of the three diets in Growth Trial 1 Table 12 Mean temperatures, salinities, and survival rates for Growth Trial 2 by tank. ..68 Table 1 3 The mean weight (in grams) for each tank by week for Growth Trial 2. Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant Table 14 Average weights for each diet by week for Growth Trial 2 Table 15 Average daily growth coefficients and average specifi c growth rates of the three diets in Growth Trial 2

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viii Vegetarian Shrimp: the Effects of A ttractants in A lternative Plant Based Diet s on Growth Rates of Juvenile Pacific White Shrimp ( Litopenaeus vannamei ) (Boone, 1931) M eagan White Domain New College of Florida Abstract Shrimp aquaculture is a growing industry with many related environmental impacts. One such impact is the harvest of wild fish stocks for the production of aquaculture feed ingredients (fish meal and fish oil) t o feed shrimp raised in aquaculture systems. Alternative feeds are being developed using alternative plant based protein and lipid sources. However, despite progress in reducing marine based resources for the main protein source in alternative feeds, the r equirement of attractants in the diets of Pacific white shrimp maintains dependence on wild fish stocks. The current research examines the role of attractants in plant based diets by conduct ing growth trial s with Pacific white shrimp to determine whether t he presence of attractant effects growth rates. The results of the growth trial s were inconclusive, with the experimental diet containing attractant out performing the experimental diet without attractant in only one of the trials. Further research is need ed in this area of aquaculture research to assist in reducing the dependence of the aquaculture industry on limited wild fish supplies. Dr. Sandra Gilchrist Division of Natural Sciences

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1 An Introduction to the Aquaculture Industry and Its Practices The Growth and Practices of the Shrimp Aquaculture Industry To feed the growing global population seafood production is continually rising, with an increasing amount of the total production being provided by the aquaculture sector (Table 1). Aquaculture consists of attaining juvenile fish, invertebrates, or plants either from the wild (capture based aquaculture) or from a hatchery (hatchery based aquaculture) and raising them to a marketable size (Aquaculture Development 6 FAO, 2011). The aquaculture sector encompasses aquatic plants and animals raised all over the world in fresh, brackish, or saltwater (Figures 1 and 2) (Jose and Jose, 2009). Wh ile the practice of aquaculture is thousands of years old with origins in China, global development and expansion of aquaculture began within the last 30 to 40 years to bridge the gap between the human demand for protein and the dwindling supplies of wild seafood species (De Silva et al., 2011). Aquaculture is now considered the fastest growing animal food sector (Allsopp et al., 2009) Shrimp aquaculture has become the fastest growing sector within aquaculture and is one of the highest value products in a quaculture (Shiau, 2008). Shrimp are one of the largest aquaculture products by volume, with only a few species such as carp and tilapia being produced at greater volumes (Stokstad 2010). This rapid growth in shrimp production is due to growing markets in countries like Japan and the United States, and the resulting export market and opportunities to earn foreign exchange among less economically advanced countries (Pillay and Kutty, 2005). Shrimp farming has been encouraged in many developing countries because of the high economic value of shrimp

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2 and the opportunity to obtain foreign excha nge (Veuthey and Gerber, 2011). G l obal shrimp production was 100,000 metric tons in 1980 (Stokstad 201 0) over 1 million tons in 2000, but almost 3.5 million tons by 2009 (FAO Yearbook 2009). Total Global Seafood Production (2008) 142 million tons Total Global Seafood Used for Human Consumption (2008) 115 million tons Average compounded rate of increase of seafood production from capture fisheries (wild caught) 1.4% per year since 1970 Average compounded rate of increase of seafood production from aquaculture sector (farm raised) 9.2% per year since 1970 Amount of se afood used for human consumption that came from aquaculture production (2000) Over 25% Amount of seafood used for human consumption that came from aquaculture production (2008) 46% Total Global Aquaculture Production (1950) Less than 1 million tons Total Global Aquaculture Production (2008) 52.5 million tons Table 1.Statistics on the growth of the aquaculture industry. From t he State of World Fisheries and Aquaculture 2010 ; Jose and Jose, 2009 ; Naylor et al., 2000 ).

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3 Figure 1. Distribution of aquaculture species among fresh, salt, and brackish water by weight. Data adapted from The State of World Fisheries and Aquaculture, 2010. Figure 2. Distribution of global aquaculture production as of 2008. Data adapted from The State of World Fisheries and Aquaculture, 2010.

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4 Common shrimp species raised in aquaculture systems include the Pacific white shrimp ( Litopenaeus vannamei ) (Figure 3), the black tiger shrimp ( Penaeus monodon ) (Figure 4a), the Indian shrimp ( Penaeus indicus ) (Figure 4b), the banana shrimp ( Penaeus merguiensis ) (Figure 4c), the green tiger or bear shrimp ( Penaeus semisulcatus ) (Figure 4d), the oriental shrimp ( Penaeus chinensis ) (Figure 4e), the giant river prawn or the Malaysian prawn ( Macrobrachium rosenbergii ) (Figure 4f), the ginger prawn or the speckled shrimp ( Metapenaeus monoceros ) (Figure 4g), and the yellow shrimp ( Metapenaeus brevicornis ) (Figure 4h) (Islam an d Haque, 2004; Pillay and Kutty, 2005). Figure 3. The Pacific white shrimp ( Litopenaeus vannamei ) (Pillay and Kutty, 2005).

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5 Figure 4. a. T he black tiger shrimp ( Penaeus monodon ). b. the Indian shrimp ( Penaeus indicus ). c. the banana shrimp ( Penaeus merguiensis ). d. the green tiger or bear shrimp ( Penaeus semisulcatus ). e. the oriental shrimp ( Penaeus chinensis ). f. the giant river prawn or the Malaysian prawn ( Macrobrachium rosenbergii ). g. the ginger prawn or the speckled shrimp ( Metapenaeus monoceros ). h. the yellow shrimp ( Metapenaeus brevicornis ) (Pillay and Kutty, 2005; http://www.tnenvis.nic.in/bio_faunalgallery.htm ; www.sea lifebase.org/Summary/speciesSummary.php?ID=25244&genusname=M etapenaeus&sp eciesname=monoceros ; http://fishdb.sinica.edu.tw/chi/importpic.php?id=ZB17 ; http://www.biosearch.in/publicOrganismPage.php?id=2185 ). a h g f e d c b

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6 Pacific white shrimp, Litopenaeus vannamei are one of the most common types of aquaculture shrimp and are currently raised on farms in the Belize, Brazil, China, Colombia, Costa Rica, Cuba, Ecuador, Indonesia, Mexico, Nicaragua, Panama, Peru, Thailand, the United States, Venezuela, and Vietnam (F AO Yearbook, 2009). While they are smaller than some aquaculture shrimp species, such as the black tiger shrimp, Pacific white shrimp are reported to have fewer issues with disease, which makes them a very attractive farming species (Jose and Jose, 2009). In 2004, the main countries producing Pacific white shrimp were China (700,000 tons), Thailand ( 400,000 tons), Indonesia (300,000 tons), and Vietnam (50,000 tons) ( http://www.fao.org/fishery/culturedspecies/Litopenaeus_vannamei/en#tcNA00ED ). Thailand, whi ch produced mostly the black tiger shrimp until 2001 when it switched to the Pacific white shrimp (Wyban, 2007), is now one of the largest producers of Pacific white shrimp along with China (FAO Yearbook, 2009). Figure 5 An oyster farm off the coast of Korea. Oysters are attached to ropes which hang down from the floats that are visible abov e water ( http://www.lib.noaa.gov/retiredsites/korea/korean_aquaculture/history.htm ).

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7 There are three classifications of aquaculture based on nutrient input: extensiv e aquaculture involves little nutrient input by fish farmers and is done with organisms that get most of their nutritional requirements from the environment such as filter feeding mollusks (Figure 5); semi intensive aquaculture describes systems in which n utrients present in the environment are supplemented by the addition of food and/or fertilizers; and intensive aquaculture describes systems in which all nutrients are added to the system in the form of food and/or fertilizer, which is commonly done for ca rnivorous species ( Feng et al. 2004; Naylor et al. 2000; Roy et al. 2009a; Roy et al. 2009b). In addition, fish farmers in many areas continue to use traditional methods, such as the use of ghers in Bangladesh, in which rice is raised during the winter and shrimp are raised during the summer (Islam et al., 2005). Shrimp farms can be maintained as extensive, semi intensive, or intensive systems (Table 2) (Jose and Jose, 2009; Mazid and Banu, 2002). Some sources report stocking densities in intensive shri mp ponds to be as high as 200 250 fry per m 2 producing yields of up to 28 tons per hectare per year (Pillay and Kutty, 2005).

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8 System Type: Extensive Semi Intensive Intensive Pond Size: 1 5 hectares 2 3 hectares with 1 1.5 m depth 0.05 0.5 hectares with 0.8 1.5 m depth Stocking Density: 2 3 post larvae per m 2 10 25 post larvae per m 2 25 100 post larvae per m 2 Seed Source: Wild caught or hatchery Wild caught or hatchery Wild caught or hatchery Water Info: Depend on tides to replenish water and remove waste Daily water exchange of 25 30% Daily water exchange of 30 300% Use of Additives: Fertilizers or manures Fertilizers or manures Fertilizers or manures Feed Info: Natural food supplemented with low protein pelleted food Use of high protein pelleted food Use of high protein pelleted food Culture Period: 3 4 months 4 5 months 4 5 months Environmental Impact: Minimal Nutrient loading can cause eutrophication; High stocking densities increase risk of disease Nutrient loading can cause eutrophication; High stocking densities increase risk of disease Table 2. Details about the different systems of shrimp aquaculture. Information adapted from Mazid and Banu, 2002 and from details on Indian shrimp farms in Jose and Jose, 2009. There are also a number of setups for aquaculture farms. Inland systems invo lve raising organisms in inland ponds, tanks, or raceways. Ponds are maintained by adding water to counteract seepage and evaporation, which in some places is done by providing a continuous water flow (Stickney, 2005). Raceways are essentially circular or linear

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9 tanks that have continuous water flow. Coastal setups consist of ponds, net pens, or cages that are in direct contact with oceanic waters. Coastal ponds can be maintained by taking advantage of tides or through the use of pumps for water exchange (J ose and Jose, 2009). Net pens, sometimes called sea cages, are enclosed except for an opening at the top the sea floor, and allow a free exchange of water with the e nvironment (Figure 6) (Frazer, 2008). Shrimp are typically raised to market size in coastal or inland ponds. Hatcheries that raise juvenile (post larval) shrimp to sell to shrimp farms often use tanks, raceways, ponds, net pens, and floating cages during t he nursery phase of raising the post larval shrimp (Figure 7) (Creswell, 2011). Figure 6. Salmon farms in Tasmania. ( http://www.tasmania attractions.com/strahan.html ).

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10 Figure 7. An indoor shrimp hatchery in Hawaii (Pillay and Kutty, 2005). Aquacult The rapid growth of shrimp aquaculture can be attributed both to the creation of more ponds and to the intensification of existing pond setups by increasing stocking densities (Hardy, 2008). The intensification of existing shrimp farms can be estimated by the amount of shrimp production that uses complete commercial feeds In 1995, only 75% of shrimp production was dependent on commercial feeds and by 2008 93% of shrimp production was dependent on commercial feeds (Tacon et al. 2011). Both the creation of new ponds and intensification of shrimp production, as well as several other practice s associated with shrimp aquaculture, are related to environmental issues that need to be addressed to ensure long term sustainability of shrimp aquac ulture. Habitat modification is a topic of concern with coastal shrimp aquaculture systems. In areas where these systems are prevalent, shrimp are raised in converted coastline where

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11 mangroves and other vegetation have been destroyed to create ponds (Allso pp et al., 2009). When shrimp aquaculture became popular, unregulated expansion of shrimp farms through the destruction of mangrove forests was common in many countries. In the 1980s, the clearing of mangrove forests was even encouraged by some government s due to a lack of space for the creation of new shrimp farms (Stokstad, 2010). In Bangladesh during 1980 less than 20,000 hectares were devoted to shrimp farms and by 1995, 140,000 hectares contained shrimp farms (Deb, 1998). In Thailand and Indonesia the creation of farms for aquaculture accounts for 41% and 63% of mangrove deforestation respectively (Giri et al., 2008). In the Philippines, over 250,000 hectares of mangrove forest have been cleared for the construction of aquaculture farms, 60% of which w ent to shrimp and milkfish farms (Jose and Jose, 2009). It is estimated that 1 to 1.5 million hectares of global coastlines are dedicated to shrimp farms (Berlanga Robles et al., 2011). Shrimp aquaculture in particular requires continued creation of new ponds because of the short lifespan of ponds used for intensive production. Pollution causes shrimp ponds to be abandoned after only 5 to 10 years of use, after which point the land is too polluted to be used for agriculture (Anantanasuwong, 2003). Addit ionally, low soil pH (as low as 3.0) associated with mangrove areas can cause pond water to become acidic, further decreasing the lifespan of the ponds (Jose and Jose, 2009). The conversion of mangrove forests to aquaculture farms is so common that aquacul ture has become one of the largest causes of mangrove depletion (Battcock, 2009).

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12 This destruction is problematic because mangroves perform many functions in coastal areas including acting as nursery grounds for juvenile fish, preventing flooding and sedi ment erosion, providing coastal protection, facilitating water treatment, and providing fuel and building materials to local communities (Battcock, 2009; Giri et al., 2008). While it is worth noting that the harvest of mangroves by local peoples for fuel a nd building materials also causes some mangrove destruction, this impact is small compared to the large scale and continual clearing of mangroves for the creation of ponds for shrimp aquaculture. The large scale destruction of mangroves results in more vul nerable coastlines and negatively impacts wild fish populations through the loss of nursery grounds. Increased erosion due to mangrove clearing can damage nearby coral reefs by increasing sedimentation rates (Jose and Jose, 2009). While the destruction of mangroves to create shrimp farms is very common, other types of wetland areas may also be used for shrimp farms. In some areas of Mexico, saltmarshes are most often converted to shrimp farms because of advantages such as already established water supply a nd drainage, easier accessibility, and low economic value assigned to saltmarshes (Berlanga Robles et al., 2011). Rice paddies have also been converted into shrimp farms in some areas of Bangladesh because of the higher profits associated with shrimp (Ali, 2006). However, this can lead to issues of food security for humans and livestock. A compromise has been found through the practice of raising shrimp and salt tolerant rice together, which is a common practice in Bangladesh and India (Chowdhury et al., 20 11; Pillay and Kutty, 2005). This maximizes land use and uses the shrimp waste to increase rice production.

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13 Another response to the destruction on mangroves for shrimp ponds has been the development of integrated mangrove forest shrimp farms (Gautier, 20 02). Research into using mangroves as a biofilter for effluents from shrimp farms suggests that surrounding shrimp farms with mangroves may decrease environmental impacts of shrimp farms (Gautier et al., 2001). In such systems, the waste from the shrimp is filtered by the mangroves and encourages higher productivity of the mangroves (Gautier, 2002). Vietnam has begun using integrated mangrove shrimp systems (Primavera, 2009). Integrated mangrove shrimp setups can be done in either of two ways: (1) the mangr oves can be adjacent to intensive shrimp farms; and (2) mangroves can be included within the shrimp ponds, so that they also provide shade and some food (Bush et al., 2007). In areas where habitat modification in the form of mangrove clearing for shrimp aq uaculture continues, the detrimental effects to nearby ecosystems and communities will likely be long lasting. Environmental c oncerns associated with shrimp aquaculture practices include shortages and salinization of local freshwater sources. Intensive in land shrimp aquaculture systems use low salinity waters created by diluting hyper saline water that is trucked inland with the locally available freshwater (Szuster, 2003). This system has allowed shrimp farms along freshwater rivers. This method is common among shrimp farms and hatcheries in Thailand (Pillay and Kutty, 2005). Locally available freshwater sources may include groundwater (wells or springs), surface water (streams, rivers, or reservoirs), or miscellaneous water sources such as rain water (Jos e and Jose, 2009). Diluting hyper saline water requires that large volumes of freshwater be pumped from the local groundwater or other sources, which lowers the water table and can cause

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14 salinization of the freshwater, drying of wells, and shortages of dri nking water (Islam, 2003). This is also common in Central and South America, where they use diesel pumps to retrieve groundwater for shrimp ponds (Pillay and Kutty, 2005). In intensive farms in India, the practice of pumping groundwater to fill and exchang e water in shrimp ponds is also common (Bhattacharya and Ninan, 2011). Previously, in such systems 30 to 40% of the pond water was flushed and replaced daily to counteract the effects of evaporation and seepage, putting a high demand on both fresh and seaw ater resources (Flaherty et al., 2000). In addition, compensation for excessive evaporation in the summer and seepage with local freshwater sources can cause dramatic water shortages that affect both humans and livestock (Jose and Jose, 2009). Some countri es have begun using artificial seawater to reduce dependence on seawater trucked inland (Pillay and Kutty, 2005). However, artificial seawater must be mixed with freshwater, and therefore does not reduce dependence on local freshwater sources ( www.aquatice co.com/pages/full_width/78/Mixing Artificial Seawater ). Research shows limited water exchange or no water exchange does not negatively impact the shrimp, as long as the water is kept clean (Samocha, 2009). Recently, intensive shrimp aquaculture systems tha t require no water exchange are being developed (Vinatea et al., 2010). However, the availability of this technology in some areas where shrimp aquaculture is popular may hinder efforts to reduce dependence on local water sources. Until these technologies reach all areas, issues associated with older techniques will continue to contribute to shortages of local drinking water. For species that can tolerate a range of salinities, low saline ponds may be used. For example, Pacific white shrimp, which toler ate salinities in the range of 1ppt to 40ppt,

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15 is raised in low salinity waters in Brazil, China, Ecuador, Mexico, Thailand, the United States, and Vietnam ( Roy and Davis 2010; Davis et al. 2004 ). However, depending on the source of the water used, shrimp pon ds can have a large variation in the ionic profiles (Boyd and Thunjai, 2003). In Thailand, low salinity ponds are created by diluting hyper saline water from coastal seawater evaporation ponds with local freshwater sources (Davis et al., 2004). Low salinit y water can contain low levels of trace minerals such as potassium, magnesium, sodium, and chlorine necessary for osmoregulation in shrimp, often leading to moult related mortalities (Roy and Davis, 2010; Gong et al., 2004). To counteract this, fertilizers are added to low salinity ponds to increase potassium and magnesium concentrations (Roy et al., 2009a; Roy et al., 2009b; Roy and Davis, 2010). However, fertilizers can contribute to nutrient pollution and eutrophication, as discussed below. Dependence of shrimp aquaculture systems on freshwater sources can lead to conflicts over water use. Salinization of land in areas near aquaculture farms can occur. The presence of shrimp farms can affect nearby soil in the following ways: increased soil acidity, incr eased soil salinity, depletion of organic carbon, decline of calcium, magnesium, and potassium, and increases of nitrogen, phosphorus, and sulfur from the addition of fertilizers (Ali, 2006). In addition, dumping of saline waste into nearby freshwater reso urces that are used for irrigation by local farmers can result in salinization of soil (Flaherty et al., 2000). Recently, it has been suggested that effluents from low salinity shrimp farms may be used directly as irrigation. In Brazil some crops, such as melon, are found to perform just as well when receiving irrigation from effluents of low salinity shrimp farms a s when they received freshwater for irrigation (Miranda et al., 2008).

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16 Increased soil salinity can be detrimental to nearby land devoted to agricultural practices (Hoq, 2007). This occurs in Thailand and Vietnam where rice paddies are often close to aqua culture ponds (Lebel et al., 2002). Due to the high salinity in the soil after aquacultural use, abandoned ponds cannot be used for agricultural purposes for 5 to 7 years (Anantanasuwong, 2003). Efforts to mediate the salinization of soil near shrimp farms have explored the possibility of plants that may be able to reduce salinity in the soil. One study found that soybean crops have potential to reduce soil salinity in areas near shrimp farms (Boonsaner and Hawker, 2012). Salinization of local freshwater an d agricultural land occurs through the lowering of the water table due to overuse of freshwater for inland aquaculture systems, dumping of saline waste water into local freshwater resources, and seepage of saline waters from aquaculture farms. In some aqu aculture systems, shrimp are raised in parts of the world where they are not indigenous (Table 3). This trend has the potential to introduce non indigenous or invasive organisms and diseases. The introduction of non indigenous organisms can occur via escap e from aquaculture systems (Allsopp et al., 2009). Non indigenous organisms are more likely to become established when there are repetitive occurrences of escapes (Naylor et al., 2005). Hatchery raised escapees can compete with the wild population for reso urces and interbreeding can alter the genetic composition of the wild population (Allsopp et al., 2009). The introduction of non indigenous or genetically modified species into ecosystems can be catastrophic if the introduced organisms thrive at the expens e of indigenous species.

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17 Species Indigenous Areas Raised for Aquaculture (Non indigenous Areas) Reference Pacific white shrimp ( Litopenaeus vannamei ) Pacific coast of South and Central America Thailand; Indonesia; USA: Vietnam; India FAO Yearbook 2009; www.galvbayinvasives .org Giant river prawn or Malaysian prawn ( Macrobrachium rosenbergii ), Asia and Oceania inland waters; Philippines; Australia; Sri Lanka; Tahiti Brazil; Paraguay; Peru; Puerto Rico; USA; FAO Yearbook 2009; www.sealifebase.org Table 3. Common shrimp aquaculture species that are raised in areas to which they are not indigenous. The presence of non indigenous organisms can also facilitate the spread of pathogens, even without the escape of the host organisms. Examples of this are the Whitespot Virus (WSV) and the Taura Syndrome Virus (TSV) that commonly plague shrimp farms (Naylor et al., 2000). WSV and TSV were originally spread through the shipping of post larval and brood stock shrimp. WSV has been observed to spread from one a ffected farm to other nearby farms and to wild populations when there is a shared water dumping site (Jose and Jose, 2009). A free exchange of water with the ocean allows bacteria and other pathogens to pass between farmed and wild organisms in systems lik e net pens (Frazer, 2008). The spread and introduction of diseases that are caused by viral infection are of particular concern because these cannot be treated with antibiotics, a practice that is commonly done for bacterial diseases. While stocks and mort alities affected by viral diseases should be destroyed and not dumped into the surrounding areas with the waste, it is unclear how often such measures are taken (Jose

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18 and Jose, 2009). The dumping of infected stocks as waste may further facilitate the sprea d of diseases. The spread of diseases has been somewhat discouraged by the use of hatchery raised shrimp, as discussed below. Another environmental concern is the practice of stocking shrimp farms with wild caught, instead of hatchery raised, juveniles kn own as post larvae (Primavera, 2006). In the past, shrimp aquaculture has relied heavily on wild caught post larvae, which required the removal of young from wild populations (Islam and Haque, 2004). Post larval shrimp are typically caught in nets made of fine mesh, which results in a high amount of bycatch (Figure 8) (Ronnback et al., 2002). In India and Bangladesh, where wild caught post larval giant tiger shrimp have been used to stock shrimp farms, the amount of bycatch can be as high as over 500 post l arval non target shrimp, over 150 post larval finfish, and over 1,500 other macro zooplankton for a single post larval black tiger shrimp (Hoq et al., 2001). More recent estimates of bycatch levels found a target post larvae to bycatch ratio of 1:942 (Ahme d and Troell, 2010). Removing juveniles can cause a reduction in the adult population in both target and bycatch species in following years (Hoq, 2007). In the 1970s and the 1980s the shrimp industry in Ecuador relied heavily on wild caught post larvae but a decrease in the availability of wild post larvae and the advancement of technology has led to an increase in the use of hatchery raised shrimp to stock shrimp farms (Aquaculture Development 6 FAO, 2011). This trend has been seen in many countries with shrimp aquaculture.

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19 Figure 8. Collecting post larval shrimp from the wild with a fine mesh scissor net (Pillay and Kutty, 2005). Hatchery techniques have been developed for the main commercially important species of shrimp (Pillay and Kutty, 2005). Originally, hatcheries collected gravid females and while some hatcheries still prefer this method, shortages of gravid females in the wild and advancements in technology have led to the use of induced gonad development and spawning in captive adult shrimp (Creswell, 2011). There has been success with mating of most important aquaculture shrimp species in captivity (Pillay and Kutty, 2005). Many hatcheries maintain closed broodstock populations for many generations (Perez Enriquez et al., 2009). Now, there are shrimp hatcheries in China, Thailand, Vietnam, the Philippines, Indonesia, Malaysia, and India (Briggs et al., 2004). In Mexico, the shrimp aquaculture industry depends on 14 hatcheries that produce over 9 billion past larvae per year (Perez Enriquez e t al., 2009). In Japan and Taiwan, hatchery

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20 production is able to meet the demands for post larvae needed for aquaculture (Pillay and Kutty, 2005). However, because many hatcheries manage closed broodstock populations, in which new individuals are not intr oduced, there are often concerns of low genetic diversity which can increase inbreeding (Perez Enriquez et al., 2009). This problem could be avoided through the exchange of broodstock individuals between hatcheries to increase the variety within breeding g ene pools. Regardless, hatchery production in many countries does not entirely meet the demands, which results in wild caught post larvae being used to supplement the post larvae provided by the hatcheries (Pillay and Kutty, 2005). Due to the negative envi ronmental impacts of shrimp post larvae collection, Bangladesh and India issued bans on wild collection in 2000 and 1999, respectively (Ahmed and Troell, 2010). However, in Bangladesh collection of wild post larval shrimp continues despite the ban (Aquacul ture Development 6 FAO, 2011). In addition to reducing the collection of wild post larvae to stock farms, the use of hatchery raised post larvae has helped to reduce the spread of diseases through increasing the availability of disease free and disease resistant post larval shrimp (Stokstad, 2010). The U.S. Marine Shrimp Farming Program and several other programs have successfully established breeding programs for Pacific white shrimp that produces individuals that, in addition to being resistant to the Taura Syndrome Virus (TSV), are also fast growing, and specific pathogen free (SPF) (Wyban, 2007). The SPF specification means that they are guaranteed to be free of certain pathogens at the time of sale, but not that they are resistant to those specific p athogens (Arce et al., 2000). The SPF certification allows post larval shrimp, or other SPF species, to be sold and shipped to areas to which they are not indigenous without the danger that they will introduce a new disease to this area.

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21 Hatchery produced SPF shrimp certified to be without Whitespot Virus (WSV), Taura Syndrome Virus (TSV), Yellow Head Virus (YHV), and Infectious Hypodermal and Haematopoietic Necrosis Virus (IHHNV) are now being raised in Thailand (Lebel et al., 2010). Despite advances in ha tchery technology and the increasing information on raising specific pathogen free shrimp, the only SPF shrimp species commercially available at a large scale is Pacific white shrimp (Moss et al., 2012). The practice of using hatchery raised post larvae sh ould be encouraged to prevent spread of diseases and decrease collection from the wild. The use of antibiotics and other chemicals in aquaculture systems is a common practice especially in intensive aquaculture setups, in which antibiotics and other chemic als are used to fight and prevent disease, parasitism, and to improve water and pond conditions. Besides being used to treat bacterial diseases, antibiotics are often used as a preventative or prophylactic; this means the antibiotics are added to the water regularly and not necessarily only when needed, i.e. when disease is noticed (Holmstrom et al., 2003). Common bacterial diseases that affect aquaculture shrimp species include Luminous vibriosis (caused by the bacteria Vibrio harveyi and Vibrio splendidus ), shell disease (caused by the bacteria Vibrio Aeromonas and Pseudomonas ), and filamentous bacterial disease (caused by Leucothrix sp .) (Jose and Jose, 2009). In net pens antibiotics are administered through the feed and the uneaten food and feces sink beneath the pen, introducing antibiotics to the environment (Naylor and Burke, 2005). A study on antibiotic use in Thai shrimp farms fo und that 74% of the shrimp farmers interviewed used antibiotics in their farms, of which 86% used them as a preventative measure in addition to treatment once disease is seen and 14% used a daily

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22 administration of antibiotics (Holmstrom et al., 2003). Anot her study on antibiotic and chemical use in Thai shrimp farms conducted in 2000 found that all of the farmers interviewed used chemicals for soil and water treatment, the most common of which were liming agents (Graslund et al., 2003). Liming agents are us ed to improve water quality by optimizing alkalinity and pH levels of the water (Pillay and Kutty, 2005). Of the interviewed farmers, 63% used fertilizers to increase the algal growth for a food source for the shrimp, 96% used at least one type of disinfec tant or pesticide, 76% used at least one type of antibiotic given in the food to treat disease, 86% used products containing microorganisms either in the feed to improve digestion or into the pond system to increase decomposition and outcompete pathogenic bacteria, and 76% used vitamins to improve growth and fight disease (Graslund et al., 2003). This same study found that some farmers said they used antibiotics to treat both bacterial and viral diseases. However, viral diseases are not treatable through th e use of antibiotics or any other chemicals (Jose and Jose, 2009). A study on the use of antibiotics in Bangladesh shrimp hatcheries conducted in 2002 03 found that Chloramphenicol, Erythromycin, Oxytetracycline, and Prefuran are commonly used as broad sp ectrum antibiotics, formalin and malachite green are used to control parasites and protozoans, and Treflan and malachite green are used as antifungal agents (Uddin and Kader, 2006). In another study on antibiotic use in hatcheries in Bangladesh, Aftabuddin and colleagues (2009) found that 70% of surveyed hatcheries used formalin to treat broodstock, 30% of surveyed hatcheries used malachite green to treat broodstock, 30% of surveyed hatcheries used Chloramphenicol to treat broodstock, 15% of surveryed hatch eries used Erythromycin to treat broodstock, 5% of surveyed

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23 hatcheries used Oxytetracycline to treat broodstock, and 10% of surveyed hatcheries used Prefuran to treat broodstock. Chloramphenicol and Nitrofuans (such as Prefuran) are banned for use in food production worldwide due to their serious side effects (Commission Regulation EU 37/2010). It is clear that antibiotic use is common in systems that have both open and limited water exchange with the environment, which can lead to environmental impacts as well as concerns related to human health for consumers of this seafood. There are concerns that the heavy use of antibiotics and other chemicals in aquaculture may lead to residues present in the surrounding environment, residual levels in seafood, and th e development of antibiotic resistant bacterial strains which can be harmful to human health (Sapkota et al., 2008; Cabello, 2006). In Vietnam, Thailand, and the Philippines there have been instances of bacteria in and around shrimp farms that are resistan t to antibiotics used in those farms (Allsopp et al., 2009). Additional antibiotics can be added to the system through the use of fertilizers such as manure from farm animals that are fed antibiotics and this can lead to populations of bacteria that are re sistant to the antibiotics found in the manure (Petersen and Dalsgaard, 2003). Like fertilizers, manures from animals (including chickens, cows, pigs, ducks, and in some places humans) are often added to ponds to encourage growth of heterotrophic bacteria (Pillay and Kutty, 2005). Studies conducted in Vietnam found that residues of the antibiotics trimethoprim (TMP), sulfamethoxazole (SMX), norfloxacin (NFXC), and oxolinic acid (OXLA) as well as bacteria that had developed resistance to those antibiotics we re found in the water and sediments of shrimp farms and surrounding areas (Le and Munekage, 2004; Le et al., 2005). Additional chemicals used in shrimp farms

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24 include copper based chemicals that are used to deter fouling organisms (Sapkota et al., 2008), an d piscicides and molluscicides which are used in shrimp farms in Thailand to get rid of competitors and predators before filling the ponds with shrimp (Szuster, 2003). Additionally, another common practice used to remove unwanted aquatic plants from aquacu lture setups is the use of weedicides including the following: 2,4 dichlorophenoxyacetate, which is used against floating and emergent weeds; Diquat, which is used against floating, emergent, and submerged weeds; and copper sulfate, which is the most widel y used (Pillay and Kutty, 2005). Due to the nature of these chemicals piscicides, molluscicides, and weedicides are designed to kill fish, mollusks, and weeds/plants, respectively their release into nearby ecosystems can be devastating. The environmental a nd health issues associated with the widespread use of antibiotics and other chemicals are compounded by problems such as a lack of education of farmers on proper usage, as illustrated by the use of chemicals that have been banned in food production and th e use of antibiotics to treat viral diseases. In addition to antibiotics, aquaculture waste can also consist of organic material, feces, uneaten food, mortalities, and dissolved materials such as nitrogen and ammonia, fertilizers, and microbes, all of whi ch can be harmful to local ecosystems where waste is discharged (Islam, 2003; Szuster, 2003; Naylor and Burke, 2005; Cabello, 2006). Waste is of particular concern with systems such as net pens and ponds, in which waste goes directly into the seawater or t he nearby environment (Allsopp et al., 2009). In systems in which waste is released with saline water into freshwater areas, the salinity difference can also impact nearby crops and indigenous species (Szuster, 2003). In shrimp farms, fertilizers are often added to ponds before stocking to encourage algal blooms that serve

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25 as a food source during the early post larval stages, as a liming agent for the water and soil, or to adjust the ionic profiles of low salinity ponds (Roy and Davis, 2010; Paul and Vogl, 2011). Often, commercial agriculture fertilizers are used for this practice (Pillay and Kutty, 2005). When fertilizers are released as waste into the surrounding waters, the excessive nitrogen causes nutrient pollution (eutrophication) (Craig and Helfrich, 2009). Eutrophication which can cause algal blooms, phytoplankton blooms, decreased dissolved oxygen concentrations, and eventually make an area un livable for fish and invertebrate species is more common in areas that have intensive farms, with more wast e being released into the surrounding environment (Jose and Jose, 2009). Aquaculture waste can introduce deadly chemicals, antibiotics, diseases, and excessive nutrients to nearby ecosystems, all of which have a devastating effect. Another topic of concer n is the harvest of wild fish stocks to produce aquaculture feeds. There are many types of food that are used in aquaculture systems. Supplementary feeds, which do not include all nutritional requirements of the aquaculture species, can be used in addition to natural foods in extensive and semi intensive aquaculture setups (Jose and Jose, 2009). In semi intensive systems the supplementary feed may consist of kitchen wastes, mill and brewery wastes, slaughterhouse wastes, poultry wastes, silkworm pupae, and unprocessed trash fish (the use of which may facilitate the spread of diseases) (Pillay and Kutty, 2005). In intensive systems, all of the nutritional requirements are fulfilled by the addition of fertilizers and feeds by farmers (Allsopp et al., 2009). In intensive systems using complete feeds, which include all nutritional requirements, feeding expenses account for 40 60% of total production costs (Pillay and Kutty, 2005). The major

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26 component of complete feeds is protein; other important components includ e lipids, carbohydrates, and non nutrient vitamins and minerals (Jose and Jose, 2009). Fish meal and fish oil from wild caught fish account for the main protein and lipid sources in marine based aquaculture feeds (Tacon et al., 2011). Fish meal is made by reducing whole fish through cooking, press drying, and milling the product into meal; fish oil is a byproduct in the production of fish meal (Aquaculture Development 5 FAO, 2011). On average, 100 kg of raw material in the form of fresh fish is reduced into about 20 kg of fish meal and 5 kg of fish oil (De Silva et al., 2011). All aquaculture finfish and crustaceans require some amount of protein, but raising carnivorous species, which requires an intensive system and complete food, typically results in a net loss in protein because the biomass input is greater than the biomass output due to protein requirements of the species. While some suggest that omnivores and herbivores actually require less protein than carnivores (Craig and Helfrich, 2009), others believe that it is the fact that carnivores tend to not digest carbohydrates as well as omnivores and herbivores (Pillay and Kutty, 2005). The inability of carnivores to process carbohydrates as well as other species could contribute to the more limited s uccess of fish meal replacement in carnivore diets compared to the success in herbivore and omnivore diets. Protein requirements also vary by the aquaculture setup, the stocking density, size of the organism, and water temperature and quality (Craig and He lfrich, 2009). While omnivores typically have fish meal present in low quantities in their diets to provide necessary amino acids (Naylor et al., 2000), carnivorous finfish and crustaceans, especially marine shrimp, are highly dependent on fish meal and fi sh oil, with carnivorous species requiring a biomass input 2.5 to 5 times greater than the biomass

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27 output (Tacon et al., 2006). Because of the net loss of protein associated with raising carnivores in aquaculture systems and the continued growth of the aqu aculture industry, a term that refers to any fish, crustaceans, and other invertebrates that are of low economic value from which fish meal and fish oil are made (Edwards et al., 2004). The removal of large amounts of fish for reduction into fish meal and fish oil for shrimp feeds can impact ocean food webs. The disruption of the food web occurs when small pelagic fish used in the production of fish meal for aquac ulture feed are caught and removed from the wild populations. The small pelagic fish used for fish meal tend to be lower trophic level fish that feed larger marine predators including carnivorous fish, which are typically targeted by fisheries for human co nsumption (Tacon and Metian, 2009a). These low trophic level fish function as the main means of energy transfer between plankton and large marine predators such as large carnivorous fish, marine mammals, and seabirds (Alder et al., 2008). The reduction of the wild food available to these high trophic level predators has the potential to reduce wild populations of higher trophic level species including carnivorous fish, marine mammals, and seabirds (Smith et al., 2011). The removal of small pelagic fish for fish meal and fish oil production in order to feed aquaculture species such as shrimp effects the food web by altering predator prey interactions on multiple trophic levels.

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28 The Dependence of Shrimp Aquaculture on Fish Meal and Fish Oil Although shrimp a re benthic omnivores (Jose and Jose 2009), 28% of the total fish meal used in aquaculture feeds goes to use in shrimp farming (Stokstad 2010). In 2008, an estimated 5.1 million tonnes of commercial marine shrimp feed were produced, accounting for 17.3% of total aquaculture feeds, second only to the 30% accounted for by carp feeds (Tacon et al. 2011). With the current trend in the growth of the aquaculture industry, it is imperative that more sustainable practices be developed and adopted. One of the main steps towards sustainability in the shrimp aquaculture industry is the reduction of the use of fish meal and fish oil in feeds. Fish me al and fish oil come from wild fish st ocks, which are continuing to decline. While the percentage of fully exploited stocks has remained at a constant 50% over the past 40 years the stocks classified as overexploited, depleted or recovering has increased from 10% in 1974 to 32% in 2008 (The State of World Fisheries and Aquaculture, 2010). As aquaculture grows so does the demand for fish meal and fish oil for feed. In 2002, 33 million tons of fish (whole fish and fish scraps) were reduced for fish meal and fish oils and in 2003, global production of fish meal and fish oil were 5.52 million and 0.92 million tons, respectively (Tacon et al., 2006). In 2008, 31.5 million tons of farm raised fish and crustaceans (46.1% of the total global aquaculture production ) were dependent on nutrient input in the form of fresh, farm made, or commercial aquaculture feeds (Tacon et al., 2011). In 2008 o f the 19% of captured fish that did not go directly toward human consumption, 67% went towards the production of fish meal a nd fish oil (The State of World Fisheries and Aquaculture, 2010). Due to the net loss of protein necessary to raise some aquaculture species, there is an overall net loss of protein

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29 species that require a nutrient input in the form of feeds (Table 4) (Tacon et al., 2011). Most aquaculture species have higher protein requirements than that mammals that are raised as livestock, making the net loss of protein a more pressing matter within the aquaculture industry (Miller, 2002). Thailan d was previously a major exporter of fish meal, but since becoming one of the largest p roducers of aquaculture shrimp, has increased its dependency on imports of fish meal to fuel its aquaculture production (Deutsch et al. 2007). Year Total Fed Species Produced (million tons) Total Feeds Used (million tons) Net Protein Loss (million tons) 1995 4.028 7.612 3.584 2000 7.684 14.150 6.466 2005 13.048 22.585 9.537 2007 16.126 26.950 10.824 2008 17.476 29.194 11.718 Table 4. The net protein loss associated with fed species in aquaculture. Table adapted from Tacon et al., 2011. Fish caught for the production of fish meal and fish oil come from two sources: industrial fisheries that target small pelagic (open ocean) fish and fisheries with other ta rget fish that catch trash fish as bycatch (Allsopp et al., 2009; Edwards et al., 2004). Fish meal and fish oil production involves the at sea or onshore processing of fish or fish parts into dry meals and oils and the nutritional value can be variable dep ending on the species of fish processed and the processing and storage methods (Tacon et al., 2006).

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30 The fish used for reduction are typically fatty fish, with a fat content of 8% or higher (De Silva et al., 2011). While the species used varies by region a nd fishing method, common species used as trash fish include anchovy, pony fish, lizardfish, herrings, sardines, sprat, capelin, blue whiting, sandeel, menhaden, and Alaskan pollack (Edwards et al., 2004; State of World Aquaculture, 2006). In many areas, t he use of these small, lower trophic level fish can be problematic because they are also used for human consumption (Aquaculture Development 5 FAO, 2011). Typically lower income communities are more reliant on low trophic value fish than higher income co mmunities, meaning the increased use of these species in fish meal production and the resulting decrease in availability of these species for human consumption may have the greatest impact in low income areas (Dey et al., 2005). In addition to their use fo r human consumption and to make aquaculture feeds, trash fish are used to make feed for livestock (Edwards et al., 2004). By 2003, the aquaculture industry used 53% of the global fish meal production and 87% of the global fish oil production to feed salmon ids, marine fish, and shrimp (State of World Aquaculture, 2006). Within shrimp aquaculture alone between 1992 and 2003, the total fish meal used rose from 232,000 to 670,000 tons and the total fish oil used rose from 27,800 to 58,300 tons ( Tacon et al. 20 06 ). The increasing demand from the aquaculture industry and the limited supply of fish meal and fish oil has led to increasing prices of these commodities (Lim et al., 2008). Increasing prices on trash fish in the face of the increasing aquaculture indust ry and demand for fish meal and fish oil can lead to food security concerns in areas, especially lower income communities, where these small pelagic fish are an important protein source (Alder et al., 2008). While subsistence fishing for these low value fi sh still exists in areas of the Asia Pacific, a

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31 significant amount of catch from marine fisheries is sold in local markets or exported (Funge Smith et al., 2005). In the Sub Saharan region of Africa, where fish can contribute up to 60% of the total animal protein supply, these low value fish are caught locally or imported (Tacon and Metian, 2009b). While artisanal fisheries are common in Peru, where small pelagic constitute the main species used for direct consumption, the catch from these fisheries may be used to sell raw materials as well as providing food for direct human consumption (Durand and Seminario, 2009). The dependence of aquaculture on trash fish for fish meal and fish oil is problematic for many reasons including the continued pressure on wild fish stocks and the competition with humans in communities where trash fish are a protein source. Another issue with the use of fish meal and fish oil in aquaculture feeds is the bioaccumulation of contaminants which can affect human health (Browdy et al. 2006). Fish oil can have contaminants including persistent organic pollutants (POPs) such as chlorinated dioxins (polychlorinated dibenzo p dioxin (PCDD) and polychlorinated dibenzofurans (PCDF)) polychlorinated biphenyls (PCBs), and polybrominated diph enyl ethers (PBDEs) that can be a human health concern (Berntssen et al., 2005; Hites et al., 2004; Allsopp et al., 2009). Additionally, organochlorine pesticides can act as contaminants and accumulate in fish oils as well (Pickova et al., 2011). POPs bioa ccumulate within the lipids in fish tissues and are extracted with the fish oil during the extraction process (De Silva et al., 2011). PCDDs and PCDFs are byproducts of industrial and combustion processes (White and Birnbaum, 2009). PCDDs and PCDFs have ne ver been intentionally produced and there are no known uses (World Health Organization, 2010). P CBs are used in electrical transformers, heat exchange fluids,

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32 hydraulic oils, and plastic manufacturing (Bell et al., 2005). PCBs are of concern for human heal th because they are known to cause cancer and to affect reproductive health (De Silva et al., 2011). Exposure to PCDDs, PCDFs, and PCBs has been found to cause toxic effects such as immunotoxicity, developmental and neurodevelopmental effects, hormone chan ges, and changes in reproductive function in humans (World Health Organization, 2010). PBDEs are a class of flame retardants that are used in textiles, carpets, polyurethane foam, television sets, electronic cables, and computers (Costa and Giordano, 2007) PBDEs are additives that are not chemically bonded to the polymers to which they are added, a situation which allows them to easily leach into the environment (Costa et al., 2008). More research is required on the impact of PBDEs on human health, but cur rently, they are considered potential developmental neurotoxins and endocrine disrupters (Costa et al., 2008). The bioaccumulation of harmful POPs in wild caught fish can be detrimental to humans when fish oil is used in feeds for aquaculture species. The Development of Potential Alternative Feeds When developing alternative feeds there are several factors that must be considered: the new diet must meet the protein, lipid, and other nutritional requirements of the species; the alternative ingredients must be ingestible and digestible by that species ; and the benefits of alternative ingredients must outweigh the detriments. To meet nutritional requirements, research must be done into the optimal protein and lipid levels for each aquaculture species of interest. Determination of the optimal lipid and p rotein levels is typically done by developing several diets all based on the same protein source that each have a different percent composition of either lipids or protein. These diets are then tested on the species to determine which percent composition y ielded the best

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33 growth. Knowledge of the optimal protein required for a species is important because feeding at optimal protein levels provides good growth and feed conversion (Pillay and Kutty, 2005). Adherence to optimal lipid levels is important because excessive dietary lipids have been found to result in fatty livers in aquaculture species (Pillay and Kutty, 2005). Species Optimal Protein Level Optimal Lipid Level Reference Southern Rock Lobster 29 31% 5 9% Ward et al. 2003 Pacific White Shrimp ~32% 75 g per kg Kureshy and Davis 2000; Hu et al. 2008 Black Tiger Shrimp 35 39% 7% Pillay and Kutty 2005; Chuntapa et al. 1999 Indian shrimp 43% X Pillay and Kutty 2005 Mud or Mangrove Crab 32 40% 6 12% Catacutan, 2002 Table 5. The optimal protein and lipid concentrations determined for various fish and invertebrate species. The optimal protein and lipid concentrations have been determined for multiple species (Table 5). In addition to determining the optimal protein and lipid levels, the vitamin, mineral, and other requirements must be considered. For example, post larval Pacific white shrimp require the presence of astaxanthin in their diets (Niu et al., 2009). For speci es raised in intensive setups, in which all nutrients come from complete feeds, it

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34 is important that these feeds provide all necessary vitamins and minerals (Pillay and Kutty, 2005). Mineral deficiencies are discussed below in association with raising Paci fic white shrimp at low salinity. In the development of alternative feeds, the digestibility of alternative proteins, lipids, and other ingredients must be determined Digestibility is a measure of how much of the energy is digested (Pillay and Kutty, 200 5). Specifically, it refers to the amount of ingested materials that pass from the luminal to the serosal side of the gut (Bell and Koppe, 2011) (Figure 9). Digestibility can be measured either directly, by monitoring the feed input and feces output, or in directly this measurement is called the apparent digestibility by adding an indigestible marker to the diet and monitoring the amount that returns in the feces (Glencross et al., 2007). Most natural proteins and lipids have a digestibility in the range of 80 90% (Pillay and Kutty, 2005). In terms of apparent protein digestibility, plant protein sources are similar to those for fish meal (Hardy, 2008). Digestibility varies by species and specific ingredient. The apparent digestibility has been determined for Pacific white shrimp for a number of protein sources (Table 6) (Yang et al., 2009).

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35 Figure 9. Internal anatomy of shrimp, showing the luminal and serosal sides of the gut. Adapted from http://shrimp culture.blogspot.com/2010/09/morphology anatomy and p hysiology of.html Table 6. Apparent digestibility coefficients for a variety of feed ingredients for Pacific white shrimp (adapted from Yang et al., 2009). FM is fish meal; SBM is soybean meal; PM is peanut meal; WGM is wheat gluten meal; CGM is corn g luten meal; MBM is meat and bone meal; and PMM is poultry meat meal. The negative effects of alternative ingredients should not outweigh the benefits. Detriments of alternative diets are often in the form of anti nutritional factors present in alternative protein or lipid sources. Anti nutritional factors are chemicals present that may inhibit growth of the fish or invertebrates that are fed the diet (Reigh, 2008). Anti nutritional factors have the potential to inhibit growth of both fish and shrimp when i n

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36 sufficient levels within their diets (Tacon, 1987). Anti nutritional factors can be divided into four groups: (1) those that affect protein utilization and digestion, such as p rotease inhibitors, lectins and tannins; (2) those that affect mineral utiliz ation, such as phytates, glucosinolates, and gossypol pigments; (3) antivitamins; and (4) miscellaneous factors, such as saponins, and phytoestrogens (Francis et al., 2001) Once an alternative feed has been developed, growth trials are conducted to determine the effect of the feed on the success of the species in an aquaculture setting. The success is usually measured in survival rates, feed efficiency, and growth rates. The survival rate is reported as a percentage of the number of individuals that survived the entire trial over the number of individuals at the beginning of the trial (Glencross et al., 2007). The efficiency with which an animal uses feeds is often given as one of two measurements: the feed efficiency (FE) (given by weight gained over feed consumed) or feed conversion ratio (FCR) (given by feed consumed over weight gained) (Craig and Helfrich, 2009). Conversion efficiency is defined as the weight gained over the feed intake, all times 100 (Pillay and Kutty, 2005). Growth rates are typi cally reported as daily gain (live weight gain over the time, given in grams per day), daily growth coefficient (DGC) (Equation 1; given below), specific growth rate (SGR) (Equation 2; given below), or thermal growth coefficient (TGC) (Equation 3; given be low), where is the final weight, is the initial weight, and is the time (Glencross et al., 2007).

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37 Fish Meal and Its Potential Alternatives Alternative feeds are being developed to replace fish meal in feeds partially or completely. Animal based protein sources have been tested in aquaculture feeds including the following: blood meal, poultry byproduct meal, meat and bone meal, and feather meal (Tacon et al., 2006). Blood meal is made from slaughtered fa rmed poultry or livestock (Tacon et al., 2011). It is made from fresh animal blood and may be prepared by spray drying, crooker drying, or flash drying (Li et al., 2008). Blood meal, in combination with meat and bone meal, poultry byproduct meal, and corn gluten meal, has been successfully tested as a partial replacement for fish meal in the diets of Pacific white shrimp (Ye et al., 2011). Poultry byproduct meal is made from slaughtered farmed poultry (Tacon et al., 2011). It has been tested as a partial fi sh meal replacement in diets of the Pacific white shrimp without adverse effects on weight gain (Markey et al., 2010; Samocha et al., 2004). One experiment looked at fish meal replacement with a mix of poultry byproduct meal (PBM), corn gluten meal, soybea n meal, and squid meal in Pacific white shrimp (Markey et al., 2010). In both pond and tank trials, there were no significant differences between survival rates, final weights, and feed conversion ratios between shrimp fed the fish meal based diets and tho se fed the experimental diets with comparable protein and lipid concentrations. Partial replacement of menhaden fish meal

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38 protein with co extruded soybean poultry byproduct meal (CEPM) in the diets of Pacific white shrimp resulted in equivalent weight gain by percentage, final weight, and feed efficiency and an increase in protein conversion efficiency with diets containing higher percentages of CEPM protein (Davis and Arnold, 2000). Within the same study, partial replacement of menhaden fish meal with flas h dried poultry byproduct meal (FD PBM) in the diets of Pacific white shrimp resulted in a significant increase in weight gain and feeding efficiency and a small, non significant increase in protein conversion efficiency with diets higher in FD PBM protein s (Davis and Arnold, 2000). Additionally, there has been success in pond conditions with the complete replacement of fish meal in the diets of the Pacific white shrimp with a mix of soybean meal, corn gluten meal, and poultry byproduct meal (Amaya et al., 2006; Amaya et al., 2007). Meat and bone meal is made from products from mammalian tissues, typically cows, pigs, and lambs (Li et al., 2008). Meat and bone meal composed of a mixture of beef, pork, and poultry has been tested as a partial replacement for fish meal in the diets of Pacific white shrimp with negligible effects on growth rates at levels of 25% replacement (Forster et al., 2003). Hydrolyzed feather meal partially replaced fish meal in the diets of Pacific white shrimp without adverse effects on weight gain (Mendoza et al., 2001). Pacific white shrimp experience no significant differences between growth rates or feed efficiencies when fed diets with partial replacement of fish meal protein with protein from steam processed feather meal (SPFM) and enzymatically hydrolyzed feathers (EHF) (Mendoza et al., 2001). While meals made from byproducts of the meatpacking industry may be lower in protein quality than fish meal, inclusion in small amounts in diets with alternative protein source may help balan ce the amino acid profiles of these diets (Li et al., 2008).

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39 Another alternative is to make fish meal using the byproducts of fish (trimmings, bone, viscera, heads, skins, and gonads) that are processed for human consumption, including fish from both capt ure fisheries and aquaculture (Forster, 2008). Certain fish hydrolysates and fish meals made from byproducts of the Alaskan fishing industry have been successfully tested as partial replacements for menhaden meal in the diets of Pacific white shrimp withou t significant effects on final weight or growth (Forster et al., 2011). Fisheries byproducts have also been used in crustacean diets, including shrimp meal (which is made from the byproducts of shrimp processing, namely heads and shells), squid meal (which is made from squid waste during processing of squid for human consumption and it typically consists of viscera, head, tentacles, fin, skin, and pen), crab meal and crab protein concentrate (which are made from the waste from crab processing and/or whole c rab), krill meal (which is made of krill and has high levels of carotenoid pigments important for many crustaceans), and mollusk products (which can be made from mussels, oysters, clams, and/or scallops) (Shiau, 2008). Plant based protein alternatives tha t have been tested in aquaculture feeds include the following: corn gluten meal, cottonseed meal, peanut (groundnut) meal, leaf meals, leaf protein concentrate, lupin meal, pea meal, potato protein concentrate, canola meal, canola protein concentration, ra peseed meal, rapeseed protein concentrate, rice protein concentrate, soybean meal, soybean protein concentrate, sunflower seed meal, and wheat gluten (Tacon et al., 2006; Pillay and Kutty, 2005; Venero et al., 2008; Reigh, 2008; Oujifard et al., 2012). Cor n gluten meal is made from the remnants of corn after the starch, bran, and germ have been removed and it is a good source of methionine (Venero et al., 2008). Cottonseed meal has been successfully tested as a partial fish meal

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40 replacement in diets of Paci fic white shrimp and has been shown to have no adverse effects on weight gain with replacement levels up to 40% (Lim, 1996). The use of cottonseed meal to replace fish meal is hindered due to the low concentrations of certain essential amino acids includin g lysine, methionine, and cysteine (Lim et al., 2008). Peanut meal is a byproduct in the production of peanut oil (Costa et al., 2001). Peanut meal has high protein content and a good amino acid profile for aquatic feeds (Reigh, 2008). Peanut meal has been successfully tested as a partial fish meal replacement in diets of Pacific white shrimp, showing no adverse effects on weight gain with 10% replacement (Lim, 1997). Peanut meal was also successful as a partial replacement for fish meal when used in combin ation with soybean meal (Yue et al., 2011). Leaf meals are commonly made from leucaena and alfalfa, the latter of which has been used in aquatic feeds, despite having the anti nutritional factor of containing trypsin inhibitors (Venero et al., 2008). Leaf meal made from leucaena contains mimosine, which is a toxic amino acid that is used as an insecticide and may act as an anti nutritional factor (Reigh, 2008). Leaf protein concentrate (LPC) is made by extracting juice from plants and coagulating the protei ns (Pillay and Kutty, 2005). Meal made from lupins, which are seeds from leguminous plants in the bean and pea family, are a good option because they are not typically consumed by humans, and therefore there is less competition for this resource (Smith et al., 2008). Pea meal has been successfully tested as an alternative protein source in the diets of juvenile tiger shrimp, showing no adverse effects on weight gain, feed intake, and feed conversion ratios when it accounted for up to 25% of the total prote in (Bautistia Teruel et al., 2003).

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41 Potato protein concentrate is a byproduct in the production of potato starch (Refstie and Tiekstra, 2003). Potato protein concentrate has a high protein content that can be as high as 83% by weight (Lokra et al., 2008). Despite its good amino acid profile, potato protein concentrate also contains an anti nutritional factor called solanine, which can reduce shrimp growth when present in high levels (Reigh, 2008). Canola and rapeseed refer to varieties of plants within th e same genus; canola refers to varieties that yield oil containing less than 2% erucic acid and meal containing less than 30 micromoles per gram of glucosinolates (Enami, 2011). As much as 80% of fish meal protein can be replaced with soybean and canola me al protein without negative impacts on Pacific white shrimp (Suarez et al., 2009). Canola protein concentrate typically contains the same protein levels as fish meal, is high in lysine and methionine, and has low levels of glucosinolates (Enami, 2011). Rap eseed meal is produced after the oil has been extracted from the seeds. It contains about 40% protein by weight and is high in the amino acids methionine and cysteine (Burel and Kaushik, 2008). Both canola and rapeseed meal are very inexpensive less than half the cost of fish meal (Enami, 2011; Burel and Kaushik, 2008). However, use of rapeseed meal in aquaculture diets is limited due to the presence of anti nutritional factors (Turchini and Mailer, 2011). Anti nutritional factors in rapeseed meal include : glucosinolates (which are biologically inactive, but whose products which are catalyzed in the body can have detrimental effects), phytics acids (which can decrease growth, protein utilization, survival, and thyroid function), tannins (which can lead to lower feeding efficiency), sinapine (which can decrease palatability and can affect nutrient absorption), and fiber (which may affect nutrient absorption) (Burel and Kaushik, 2008). Testing of inclusion rates of rice protein

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42 concentrate has suggested t hat it could be used to replacement up to 50% of fish meal in the diets of Pacific white shrimp (Oujifard et al., 2012). Soybean meal contains limiting anti nutritional factors such as trypsin inhibitors, which are proteins that bind with trypsin and chymo trypsin and block these enzymes (which function in the breakdown of protein in the gastrointestinal (GI) tract) from working, lectins, which cause clotting of the red blood cells, saponins, which are thought to be involved with binding to carbohydrates in the GI tract, and phytoestrogens, whose hydrolyzed forms are similar in form to estrogen and have estrogenic activity, the effects of which are not entirely clear in aquaculture species, and low concentrations of lysine, methionine, and threonine (Brown et al. 2008). These anti nutritional factors, which can affect fish and shrimp, can potentially limit the inclusion rates of soybean meal in aquaculture diets. Many of these anti nutritional factors are destroyed by heat, making soybean meal still a viable option for an alternative protein source (Jose and Jose 2009). However, heat also denatures proteins (Bauman, 2011), which may alter the effectiveness of soybean meal as a protein source. Soybean meal has been successfully tested as a partial fish meal re placement in the diets of speckled shrimp, demonstrating no adverse effects on growth when replacing up to 40% of fish meal (Rahman et al., 2010). Sookying and Davis (2012) found that soybean protein concentrate can be used at inclusion rates of up to 12% in soybean based diets for Pacific white shrimp without causing adverse effects on growth rates, feed conversion, and survival. Sunflower seed meal, which is made from the residue that remains after the oil has been extracted from sunflower seeds, has a high protein content and good amino acid profile for aquatic feeds (Reigh 2008). Dayal and colleagues (2011) found that s unflower

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43 seed meal can be used as a partial fish meal replacement in diets of black tiger shrimp, replacing up to 20% fish meal Wheat gluten is often used in shrimp diets because it is a good binding agent and is a good source of methionine (Venero et al. 2008). Additional underu se d plant based protein sources include safflower seed meal, sesame seed meal, linseed meal, and mustard se ed meal, all of which are produced from the residues remaining after the oil has been extracted from their respective seeds, and fababean seed meal, lentil seed meal, pea seed meal, and palm kernel meal (Reigh 2008). Research on raising Pacific white shri mp using microbial floc meal showed that the test diets consisting of microbial floc meal were not only successful but actually outperformed the control diets in terms of growth rates (Kuhn et al., 2009). Co culturing Pacific white shrimp with green seawe ed results in shrimp with improved growth rates, lower lipid levels within the shrimp, and higher levels of carotenoids and astaxanthine (important for pigmentation) in the shrimp (Cruz Suarez et al., 2010). Another source of protein is single cell protein s (SCPs), which include yeast SCP, bacterial SCP, and algal meal, which have been tested for shrimp (Tacon et al., 2006). Other alternative protein sources that come from neither plants nor animals include byproduct of alcoholic beverage of the brewery industry (Webster et al., meal replacement in the diets of Pacific white shrimp without adverse effects on growth rates (Roy and Davis, 2009).

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44 Alternative proteins have the following considerations to succeed: price, protein leve l, amino acid profile, anti nutritional factors, and other factors that may limit substitution into diets (Hardy, 2008). In the development and use of alternative protein sources, whether plant or animal based, the feeds must maintain the amino acid prof iles required by the shrimp. There are 10 essential amino acids that cannot be synthesized by shrimp methionine, arginine, threonine, tryptophan, histidine, isoleucine, lysine, leucine, valine, and phenylalanine and therefore these must be present in the d iet (Craig and Helfrich, 2009; Tacon, 1987). A reduction in dietary crude protein in the diets of Pacific white shrimp is possible as long as the essential amino acids are provided through supplementation (Huai et al., 2010). Many plant based proteins are deficient in these essential amino acids. For example soy derived proteins are lacking in methionine, corn derived proteins are lacking in lysine, and small grains are lacking in arginine and threonine (Hardy, 2008). Given advances in genetic engineering, it may become possible to engineer plants to produce all of the necessary amino acids, making them better replacements for fish meal. However, a high percentage of protein replacement with plant based proteins is possible with supplementation of amino aci ds (Lunger et al., 2007) or with low inclusion levels with alternative proteins such as byproducts of the meatpacking industry, as discussed above, to balance amino acid profiles (Li et al., 2008) Research into the inclusion of probiotics suggests plant b ased diets may be improved through the use of probiotics in such diets for Pacific white shrimp (Olmos et al., 2011). With increased substitution of fish meal proteins for plant based proteins, many diets require the addition of palatability enhancers, st imulants, or attractants to counteract the reduced palatability sometimes associated with the substitution of marine proteins

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45 (Gatlin and Li, 2008). Such enhancers, typically used in low percentages, may include fish and invertebrate meals that are rich in amino acids and nucleotide bases, for example menhaden fish solubles, shrimp head meal, meat and bone meal, squid meal, and krill meal (Gatlin and Li, 2008). There is support for the research and use of more unconventional protein sources that are locally available as this would decrease dependence on one or two large crops worldwide and it would reduce the costs due to importing (Reigh, 2008). Fish Oil and Its Potential Alternatives Fish oil is an important ingredient in aquaculture feeds because it is a good source of the amino acids and polyunsaturated fatty acids (PUFAs) required by shrimp (Naylor et al., 2000). Polyunsaturated fatty acids are divided into three families: n 9, n 6, and n 3 (Pillay and Kutty, 2005). Shrimp require fatty acids in the n 3 (also known as the omega 3) family (Craig and Helfrich, 2009). Commercially raised shrimp typically get these fatty acids from the fish oil included in their diets (Browdy et al., 2006). Marine oils have high levels of n 3 polyunsaturated fatty acids (Olse n et al., 2011). In particular, fish oil contains high levels of the n 3 fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) (De Silva et al., 2011). In addition to being important for 3 fatty acids are very import ant for human health and therefore are acids DHA and EPA are important for the health of the shrimp and for the health of human consumers of shrimp (Sidhu, 2003; Bro wdy et al., 2006). Plant based oils tend to have lower concentrations of n 3 fatty acids and higher concentrations of n 6 fatty acids (Jose and Jose, 2009). Fish oils typically consist of 17.4 33.4% n 3 fatty acids and 2.1

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46 5.1% n 6 fatty acids, while plant oils typically consist of 0.4 55.6% n 3 fatty acids and 10.2 52.2% n 6 fatty acids (Bell and Koppe, 2011). This means many plant based oils tend to have lower concentrations of EPA and DHA (De Silva et al., 2011). Therefore replacement of fish oil with pl ant based oils may result in reduced concentrations of n 3 fatty acids in the tissues of aquaculture species and potentially could lead to essential fatty acid deficiency, unless supplementation of fatty acids is accomplished (Gatlin and Li, 2008). Because many plant based oils tend to have lower concentrations of n 3 fatty acids and higher concentrations of n 6 fatty acids (Jose and Jose, 2009), creating shrimp feeds that maintain the proper fatty acid composition is imperative. There are multiple animal b ased sources that are being explored as a replacement for fish oil, including marine resources such as marine invertebrates and mesopelagic fish, and byproducts from the livestock and fishery industries. Some have suggested the use of underu s ed marine sour ces of lipids that may serve to be good substitutes for fish oil in aquaculture feeds, including resources such as marine invertebrates like copepods, euphausiids, and amphipods, as well as mesopelagic fish and other marine organisms (Olsen et al. 2011). Copepods are a group of small planktonic crustaceans that are very abundant and widespread ( Garrison, 2007 ). Copepods feed on low lipid phytoplankton and are high lipid food sources for higher trophic levels (Kattner and Hagen, 2009). In this way they play a very important role in marine food webs as a link between primary production and carnivores (Nybakken and Bertness, 2005). Copepods can have a total lipid content as high as 50 70% of the body dry weight (Olsen et al. 2011). This high lipid content sug gests they may provide a source of marine oil in the future. Euphausiids, more commonly referred to as krill, are a group of crustaceans that can be herbivorous or

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47 carnivorous (Nybakken and Bertness, 2005). They have a lipid content of 24 68% dry weight du ring peak seasonal times (Olsen et al. 2011). Fisheries already exist for krill in the Antarctic and off the coast of Japan (Nicol and Endo, 1997). High levels of EPA and DHA in krill oil make it a promising substitution for fish oil (Gunstone 2011). Amp hipods are another group of planktonic crustaceans ( Garrison, 2007 ). Amphipods can have a lipid content as high as 40% dry weight (Olsen et al. 2011). The mesopelagic zone consists of intermediate depths of the pelagic, aphotic zone and it is inhabited by small fish, crustaceans, jellyfishes, and cephalopods (Nybakken and Bertness, 2005). D epending on the species they can have lipid content s in the range of 29 73% dry weight (Olsen et al. 2011). Despite the fact that there appears to be a lot of unuse d b iomass lower trophic level organisms. It is likely that the true impact of such large scale fishing initiatives will affect the food web in ways that may not be immediate ly evident. Additional sources of animal based oils that have been tested in aquaculture feeds include tallow, lard, and poultry fat, which are produced as a byproduct of processing slaughtered meat for human consumption (Bureau and Meeker 2011). In addi tion, Zhong and colleagues (2011) found that the partial replacement of fish oil with conjugated linoleic acid in the diets of Pacific white shrimp may improve meat quality. It may also be possible to produce oils from byproducts of fish processing, including byproducts from aquaculture and from pelagic fisheries, which catch oil rich species such as salmon, herring, and mackerel (Olsen et al. 2011). In fish processing for human consumption, about 30% is not edible and therefore could be put towards the production of alternative oil sources (Miller et al. 2011). Additionally, for fatty species the lipid content of

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48 byproducts can be higher than the lipid content of the whole body (Olsen et al. 2011). Fish processing byproducts can yield fish meal and fish oil without producing any further byproducts (Gehring et al., 2011). However, there are legal regulations in place to prevent feeds from being fed to the same species from which they were made, to decrease the chance of intraspecies recycling of cont aminants and disease transfer (Olsen et al. 2011). There are several plant based oils that may be useful alternatives to fish oil and are already being produced large scale, including palm oil, soybean oil, rapeseed (canola) oil, sunflower seed oil, lins eed oil, coconut oil, and palm kernel oil (Gunstone 2011). Palm oil is extracted from the fruit of the oil palm tree (Ng 2002). Palm oil has both food and nonfood uses including being used as a frying oil, in biodiesel, and in animals and aquaculture fee ds (Gunstone 2011). Palm oil is one of the cheapest commodity oils because it has a very high yield in terms of oil per hectare per year and crops can produce oil continually for over two decades, making it a relatively reliable oil source (Ng and Gibon 2011). As is the case with many plant based oils, the lower concentrations of n 3 fatty acids in palm oil are likely to limit inclusion levels in aquaculture diets, unless there is a supplementation of nec essary fatty acids. Soybean oil production is the second largest of all types of vegetable oil globally (United States Department of Agriculture, 2010 ). Soybean oil has been successfully tested as a partial replacement for fish oil in the diets of Pacific white shrimp (Gonzalez Felix et al. 2010). Soybea n oil and soybean lecithin oil have also been successfully used as complete replacements for menhaden fish oil in the diets of Pacific white shrimp without adverse effects on weight gain (Hu et al., 2011). In 2008/09, rapeseed (canola) oil was third in ter ms of global production (United States

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49 Department of Agriculture, 2010 ). Rapeseed oil was first used as a lubricant before being used for food purposes such as a salad oil, cooking oil, and as an ingredient in margarines (Turchini and Mailer 2011). Rapese ed oil has also been tested as a fish oil replacement in the diets of Pacific white shrimp (Zhou et al. 2007). Rapeseed oil is a monounsaturated fatty acid rich oil therefore it may require the inclusion of low levels of fish oil in order to ensure the p roper fatty acid composition required by many aquaculture species (Turchini and Mailer 2011). By 2009, sunflower seed oil accounted for over 10% of global vegetable oil trade (United States Department of Agriculture, 2010 ). Linseed oil is considered the i ndustrial oil version of flax seed oil, which comes from the same plant but is prepared more carefully for human consumption (Gunstone 2011). Linseed, camelina, and perilla oils have high n 3 to n 6 fatty acid ratios and high oil contents (linseeds yield 35 44% oil; camelina seeds yields 37% oil; perilla seeds yield 35 45% oil ) (Tocher et al. 2011). Linseed oil has been tested as a fish oil replacement in the diets of several aquaculture species (Bell et al. 2004; Mourente et al. 2005 ; Ferreira et al., 2011 ). Camelina oil has been tested as a fish oil replacement in the diets of several aquaculture species (Morias et al., 2012; Johnson et al., 2005). Perilla oil has been tested as a substitution for fish oil in aquaculture feeds (Tocher et al., 2011). Co conut oil and palm kernel oil are often referred to as lauric oils due to the high amounts of short and medium chain fatty acids in both of these oils (Ng and Gibon 2011). Both have food and nonfood purposes, including use in aquaculture feeds (Gunstone 2011). Coconut oil corn oil, and safflower oil ha ve been tested in the diets of Pacific white shrimp as a fish oi l replacement (Lim et al., 199 7).

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50 Another promising source of n 3 PUFA especially EPA and DHA that has recently become available is from sin gle celled sources such as heterotrophic marine algae (Browdy et al. 2006; Gunstone et al. 2011). In the marine environment, single celled organisms such as thraustochytrids (marine protists), diatoms, microalgae, and some marine bacteria are the origina l source of n 3 PUFA that bioaccumulate within the food web (Miller et al. 2011). Browdy and colleagues (2006) tested diets of plant based proteins (from soybean meal, corn gluten meal, and pea meal) and DHA produced by heterotrophic marine algae and foun d no difference in feed conversion ratio, survival, or mean weight at harvest, when compared to the fish meal control diet of comparable protein and lipid concentrations. It should be noted that these plant based diets contained squid meal as an attractant Aquaculture species fed plant based oils may exhibit a reduction in n 3 fatty acids in their tissues (Gatlin and Li, 2008) To counteract this, finishing diets may be used to restore n 3 fatty acid levels. Finishing diets are typically high in n 3 fatty a cids, such as EPA and DHA, and are fed to aquaculture species for a short period before they are sent to market (Glencross and Turchini 2011). The high levels of n 3 fatty acids are often accomplished by using a finishing diet with an oil source of 100% fish oil (Mourente and Bell, 2006). This method restores the fatty acid content of the flesh so that human consumers receive the health b enefits associ ated with omega 3 fatty acids (Allsopp et al. 2009). There are potential benefits to the replacement of fish oil with plant oils, including the following: the presence of vitamin E (which affects the immune system, reproductive system, and o ther factors) in the form of tocopherols and/or tocotrienols in plant oils such as palm, linseed, rapeseed (canola), corn, and soy oils; and the presence of carotenoids

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51 (for example astaxanthin) which improve larval growth and survival, and broodstock, and immune system function (Pickova et al. 2011). Additionally, replacement of fish oil with vegetable oil may decrease the amount of fat soluble contaminants such as mercury and persistent organic pollutants (POPs) (Rosenlund et al. 2011). Progress with P acific White S hrimp The generalized life cycle for penaeid shrimp, such as Pacific white shrimp, involves several larval stages (including nauplius stages, protozoea stages, and mysis stages), a post larval stage, a juvenile stage, a sub adult stage, and a n adult stage ( Table 7 ) ( http://www.dnr.sc.gov/marine/pub/seascience/shrimpcycle.html ). Pacific white shrimp have a life cycle involving marine planktonic larval stages, estuarine post larval juveniles and sub adult stages and a marine adult stage that includes spawning ( Valles Jimenez et al., 2005 ). Growth in crustaceans including shrimp can seem discontinuous as it is generally dependent on the pattern of molts. After a molt, there is a period of growth before the new integument hardens and then there is a period during which no external growth occurs until the shrimp molt again (Bureau et al., 2000). Shrimp may have different protein requirements at different stages of their life cycle. Juvenile Pacific white shrimp have maintenance protein requirement s of 1.8 3.8 g dietary protein/kg of body weight/day while sub adult Pacific white shrimp have maintenance protein requirements of 1.5 2.1 g dietary protein/kg of body weight/day (Kureshy and Davis, 2002). The differences in protein requirements may be rel ated to differing rates of external growth at different life stages. Pacific white shrimp raised at 27C molt about every 10 12 days when in the stage of growing between 1 to 10 grams live weight and molt about every 15

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52 Egg Stage: Eggs sink to the bottom and spawning occurs in marine waters. Larval Stage Nauplius: There are several nauplius stages (typically five) and with each stage the larvae get larger. In these stages, larvae have limited swimming ability and are consider ed planktonic. Larval Stage Protozoea: There are several protozoea stages (typically three). In these stages, larvae have limited swimming ability and are considered planktonic. Mouth parts and abdomen begin to develop. Larval Stage Mysis: There are several mysis stages (typically three). In these stages, larvae have limited swimming ability and are considered planktonic. Legs and antennae begin to develop. Post Larva Stage: There can be several stages. Legs are developed and post larva are miniature adults. Juvenile: Rapid growth during this phase. Similar in appearance to adults, but typically have a longer rostrum. Sub Adult: Shrimp move into marine waters at the en d of this stage. Slower growth rates than seen in juveniles. Do not show signs of sexual maturity. Adult: Found in marine waters. Exhibit sexual maturity and reproductive behaviors. Table 7. The generalized life cycle for penaeid shrimp ( http://www.dnr.sc.gov/marine/pub/seascience/shrimpcycle.html ).

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53 21 days when in the stage of growing between 12 to 20 grams live weight (Bureau et al., 2000). As discussed above, numerous studies have been performed testing alternative protein and lipid s ources in the diets of Pacific white shrimp. Because a majority of Pacific white shrimp are raised in low salinity waters and due to the issues associated with low salinity farms, there is a growing body of research in water modification dedicated to count eracting the mineral deficiencies and supplementation of diets of Pacific white shrimp in low salinity waters (Saoud and Davis, 2005; Saoud et al., 2007; Gong et al., 2004; Roy and Davis, 2010; Roy et al., 2007a; Roy et al., 2007b; Roy et al., 2009b; Roy e t al., 2006). For example, the addition of dietary potassium increases the growth rates in low salinity environments (Roy et al., 2007a). However, the huge variation in ionic profiles depending on the source of the water limits the application of many stud ies to only the tested salinities and ionic profiles. While research on fish meal replacement in the diets of Pacific white shrimp is increasing, less research has been done in the area of fish meal replacement in their diets when they are raised at low sa linity (Roy et al., 2009a). The research that has been done at low salinity has accomplished solubles without negative impacts on growth rates (Roy and Davis, 2009). It should be noted that the diets that did not contain an animal based protein source included squid meal as an attractant.

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54 As mentioned above, many diets for Pacific white shrimp that were successful in either partial or complete fish meal replacement, inc luding those done at low salinity, contained squid meal as an attractant and fish oil to provide fatty acids and lipids (Amaya et al., 2006; Roy and Davis, 2009). Squid meal is commonly included in feeds for shrimp because it contributes important amino ac ids and also acts an as attractant (Tacon et al., 2006). While these attractants typically exist in low concentrations in the feed, they represent further dependence on marine resources for proteins. Samocha and colleagues (2004) looked at the role of attr actants by creating and comparing two diets with the same protein source 100% fish meal replacement with co extruded soybean poultry byproduct meal with egg supplement and with only one of the diets containing krill meal to act as an attractant. The lack o f a significantly different outcome suggests that the krill meal was not necessary to improve palatability or to attract shrimp to the diet. However, these diets contained animal based proteins which may have been acted as an attractant on their own. The Experimental Design Complete replacement of fish meal in the diets of Pacific white shrimp raised at low salinity has already been successful (Roy et al., 2009a; Roy and Davis, 2009). The use of squid meal as an attractant in diets with fish meal replaceme nt has been found to be unnecessary when the alternative protein source is animal based (Samocha et al., 2004). The current research focuses on the possibility of eliminating the attractant in diets with fish meal replacement in which the alternative prote in source is plant based. The experimental diets with plant based protein and lipid sources had 36% protein and 11% lipid, based on research that suggests the ideal protein concentration for Pacific white

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55 shrimp is slightly higher than 32% (Kureshy and Dav is, 2000) and the success of previous alternative diet studies with 35 36% protein and 8% lipid (Roy et al., 2009a; Roy et al., 2009b; Roy and Davis, 2009). As is common practice, shrimp were fed 10% of their body weight daily during the growth trials (Jos e and Jose, 2009). Furthermore, trials were conducted at a salinity of 4ppt because most Pacific white shrimp are raised in low salinity ponds. Because the ionic profile of a low salinity tank should mimic that of seawater diluted to the same salinity, an ideal ionic profile was accomplished for the current research by using seawater diluted with reverse osmosis water (Davis et al., 2004). The hypothesis of the current research is that there will not be a significant difference in growth rates between Paci fic white shrimp fed the experimental diets with and without the attractant. If this hypothesis is supported, it would suggest the possibility caught stocks even further by eliminating attractants i n plant based diets of Pacific white shrimp. Methods Acclimation and Grow Out of Post Larval Shrimp Two thousand post larval Pacific white shrimp were purchased from Miami Aquaculture which shipped a batch of only males ( h ttp://www.miami aquaculture.com). Upon arrival, they were acclimated to the grow out tank which consisted of a water table with a 60 gallon area for the shrimp and a 40 gallon sump, providing a system with 100 gallons of recirculating water (Figures 10 and 11). The grow out tank had a mix of sand and gravel as substrate and a heater that kept the water between 72F and 74F. At the

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56 time of acclimation, the salinity of the grow out tank was 35ppt. The grow out tank had a light regime of light from 9:00 am to 5:00 pm and dark from 5:00 pm to 9:00 am. During the grow out period the post larval shrimp were fed commercially available feed pellets from Zeigler Feeds containing 35% crude protein, 7% crude fats, and 4% crude fiber that were about 2mm in diameter (Ze igler Shrimp Grower L. vannamei product description). Because the shrimp were so small upon arrival, the pellets were ground to a powder with a mortar and pestle. At the time of acclimation, the salinity of the grow out tank was 35ppt and because the water in which the post larvae were shipped was 35ppt, salinity acclimation unnecessary. The temperature of the water in which post larvae was shipped was 71F. A drip line was used to acclimate the post larval shrimp to the temperature of the grow out tank. Th e drip line technique consisted of using thin aquarium tubing to transfer water from the grow out tank into the water in which they were shipped at a relatively slow al lowed for a rate of water of about 1 mL every 3 seconds. Because it is suggested to feed them immediately when received after shipping ( Davis et al. 2004 ), during the acclimation process the shrimp were fed the ground Zeigler food described above

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57 Figu re 10. Grow out tank for post larval shrimp consisting of 100 gallons of recirculating water. The dimensions of the tank are 21 x 82.5 inches with water 7 inches in depth. During the grow out period before the growth trials, they were fed ground Zeigler pellets two or three times a day. After a month in the grow out tank, the salinity was lowered from 36ppt to 4ppt by replacing the tank water with reverse osmosis (RO) water. The salinity of 4ppt was used because previous research on raising Pacific white shrimp on diets with alternative proteins has had success at this salinity (Roy et al., 2009a). The lowering of the salinity was done over a period of a week and at a rate that never exceeded the maximum salinity change of 4ppt per hour (Davis et al., 2004 ). Because shrimp can have a delayed reaction to salinity change, the salinity adjustments were completed a month before the start of the growth trials.

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58 Figure 11. Post larval shrimp in the grow out tank before the start of the growth trial. The Control and Experimental Diets The control diet was a commercially available pellet food from Zeigler that is specially designed for Pacific white shrimp. The di et contained marine animal proteins and consisted of 35% crude protein, 7% crude fats, and 4% crude fiber (Zeigler Shrimp Grower L. vannamei product description). The experimental diets were gel diets designed by Mazuri and produced by Smelt Feed. These di ets contained plant based proteins from dehulled soybean meal, dehydrated alfalfa meal, spirulina algae, spinach, carrot powder, dried kelp, wheat germ, and soy oil. The experimental diets consisted of 36% crude protein, 11% crude fats, and 7% crude fiber (Mazuri Custom Crustacean Gel Diet 5Z0N Appendix). One of the experimental diets contained a squid based attractant as is commonly used in feeds containing alternative protein sources and the other experimental diet contained no attractant. Because of th e relatively small size of the -------3 cm -------

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59 growth trial, gelatin based diets were used as the experimental diets because they could be ordered to specific qualifications without the requirement of a large order, as was the case for specialty pellet diets. The gelatin used by the production company was of bovine origin (personal communication with Mazuri nutritionist), so the presence of gelatin in the experimental diets prevents them from being free of all animal products. However, the diets were considered to contain negligible animal based proteins. The gelatin based diets are made by adding boiling water to dry product in equal proportions by weight. The gelatin is then allowed to set and the diet is refrigerated. To create the Experimental Diet 1, which was the die t with plant based proteins without squid attractant, dry product was mixed with boiling water in equal proportions. To create the Experimental Diet 2, which was the diet with plant based proteins with squid attractant, dried squid was boiled in water and then strained out. This water was then added to the dry product. Unlike the squid meal attractants that are used in commercial diets, this method would allow a test of the effectiveness of squid as an attractant, without the addition of animal proteins to the overall composition of the diet because the act of boiling served to destroy the proteins, which are known to be denatured (made inactive) by high temperatures (Bauman, 2011). The Growth Trial Six tanks were used for the growth trial, which allowed there to be two replicate tanks for each diet used: Control Diet, Experimental Diet 1, and Experimental Diet 2. Each tank was a 65 gallon tank with a heater, a sponge filter that encouraged aeration b y breaking up the surface tension of the top of the tanks, and a substrate of sand and gravel

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60 (Figure 12). Prior to the introduction of the shrimp to the experimental tanks, each tank was lowered to 4ppt by the dilution of seawater with reverse osmosis wat er. Figure 12. One of the 65 gallon experimental tanks used for the growth trial. The water heater is shown at top right and the filter at bottom right. Two four week growth trials were conducted and for each trial 25 shrimp were placed into each of t he six experimental tanks. Shrimp were weighed in groups of five at the beginning of each trial and once a week during the trial. An average weight was determined for each tank. Shrimp were fed twice daily, at 12pm and 7pm. Shrimp were fed 10% of their bod y weight daily, which for the gelatin based diets, was accomplished by feeding 20% of their body weight since the gelatin based diets are half water by weight. Each week, the amount of food was adjusted to be 5% and 10% of the new weights. Temperature and salinity was monitored daily and ammonia levels were checked

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61 and filters cleaned weekly. At the end of growth trial, shrimp were again weighed in groups of five. Survival rates were calculated for each tank. Data, Analysis, and Results During the growth trials, the shrimp fed Experimental Diets 1 and 2 were seen to approach the food shortly after its addition to the tank (Figure 13). Figure 13. A Pacific white shrimp from an experimental tank feeding on Experimental Diet 2. A second shrimp is approaching in the upper right corner. During Growth Trial 1, the temperatures and salinities of each tank were recorded daily. Means of the temperatures and salinities were d etermined for each tank (Table 8 ). The mean temperatures of each tank were compared using a one way ANOVA test to determine if there were significant differences between temperatures. Given that the critical F value was about 2.27 and the calculated value was F(5,168) = 7.76 with p = <.0001, it was determined that there were significant differences between mean -------3 cm -------

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62 temperatures of Tanks 1, 2, 3, and 4 were significantly different from the mean temperatures of Tanks 5 and 6 but not from one another. The mean temperatures of Tanks 5 and 6 were also not significantly different from one another. The mean salinities of each tank were compared using a one way ANOVA to determine if there were significant differences between salinities. Given that the critical F value was about 2.27 and the calculated value was F(5,168) = 4.80 with p = 0.0004, it was determined that there were significant differences between mean salinities. A test of least significant difference showed that the mean salinities of Tanks 1, 2, 3, and 4 were significantly different from the mean salinities of Tanks 5 and 6 but not from one another. The mean salinities of Tanks 5 and 6 were also not significantly different from one another Survival rates were no ted for all tanks in Growth Trial 2 (Table 8 ). Table 8 Mean temperatures, salinities, and survival rates for Growth Trial 1 by tank. The mean weight was determine d for each tank by week (Table 9 ; Figure 14). Then the replicate tanks for each diet were compared using an independent sample t test to determine if there were significant differences in weights between replicate tanks. This was done for the pre trial weights and the final weights. The mean pre trial weights of Tank 1 and 2 were compared with a two tailed t test with alpha = 0.025 on each tail and a

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63 critical t value of 2.306. Given that the calculated value was t (8) = 0.83 with p = 0.4314, there was no significant difference between the two means. The mean final weights of Tank 1 and 2 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 0.80 with p = 0.4457, there was no significant difference between the two means. Therefore, Tanks 1 and 2 were combined into a Control Diet group. The mean pre trial weights of Tank 3 and 4 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calc ulated value was t (8) = 0.26 with p = 0.8040, there was no significant difference between the two means. The mean final weights of Tank 3 and 4 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given th at the calculated value was t (8) = 0.29 with p = 0.7796, there was no significant difference between the two means. Therefore, Tank 3 and 4 were combined into an Experimental Diet with Attractant group. The mean pre trial weights of Tank 5 and 6 were compa red with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 1.22 with p = 0.2562, there was no significant difference between the two means. The mean final weights of Tank 5 and 6 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 1.02 with p = 0.3406, there were no significant differences between the two means. Therefore, Tank 5 and 6 were combined into an Experimental Diet without Attractant group.

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64 Table 9 The mean weight (in grams) for each tank by week for Growth Tri al 1 Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant. Figure 14 Graph of mean weight for each tank by week for Growth Trial 1. Tank 1 and 2 are th e control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant. For margins of erro r refer to Table 9. Mean weight was then determined for each diet by week (Table 10 ; Figure 15 ). The mean pre trial weights of the three diets were compared using a one way ANOVA to determine if the means were significantly different. Given tha t the critical F value was 3.35 and the calculated value was F(2,27) = 12.64 with p = 0.0001, and t he squared value was 0.483624, it was determined that there were significant differences between mean pre trial weights of the three diet groups. A homogeneity of variance test for this data yielded p = 0.1360. A test of least significant differences showed that the mean

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65 weight of the control diet group was significantly difference from the mean weights of both of the experimental diets but neither of the mean weights of the experimental diet groups was significantly different from one another. Th e mean final weights of the three diets were compared using a one way ANOVA to determine if the means were significantly different. Given that the critical F value was 3.37, with a calculated value of F(2,26) = 42.81 with p = <0.0001, and the squared value was 0.767069, it w as determined that there were significant differences between mean final weights of the three diet groups. A homogeneity of variance test yielded p = 0.1290. A test of least significant differences showed that the mean weight of the control diet group was significantly difference from the mean weights of both of the experimental diets but neither of the mean weights of the experimental diet groups w as significantly different from one another. Table 10 Average weights for each diet by week for Growth Tria l 1.

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66 Figure 15. Average weights for each diet by week for Growth Trial 1. For margins of error refer to Table 10 Using the mean weights for each of the three diets, the average weight gain was determined for each of the diets. The average weight gains for the control diet, the experimental diet with attractant, and the experimental diet without attractant were 230.6%, 129.2%, and 143.9%, respectively. The average daily growth coefficients (DGC) and average specific growth rates (SGR) were calculated fo r the th ree diets (Table 11 ). The daily growth coefficient and specific growth rate was largest for the control diet. The percent differences between the DGC and the SGR of the control diet and the experimental diet with attractant are 121.9% and 106.2%, r espectively. The percent differences between the DGC and the SGR of the control diet of the experimental diet without attractant are 104.9% and 78.7%, respectively. The percent differences between the DGC and the SGR of the experimental diet with attractan t and the experimental diet without attractant are 24.9% and 34.9%, respectively.

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67 Table 1 1 Average daily growth coefficients (DGC) and average specific growth rates (SGR) of the three diets in Growth Trial 1. During Growth Trial 2, the temperatures and salinities of each tank were recorded daily. Means of the temperatures and salinities were determined for each tank (Table 1 2 ). The mean temperatures of each tank were compared using a one way ANOVA to determine if there were significant differences be tween temperatures. Given that the critical F value was about 2.27 and the calculated value was F(5,168) = 21.17 with p = <.0001, it was determined that there were significant differences between mean temperatures. A test of least significant difference sh owed that Tank 5 was significantly different from all other tanks and Tank 6 was significantly different from all other tanks. The mean salinities of each tank were compared using a one way ANOVA to determine if there were significant differences between s alinities. Given that the critical F value was about 2.27 and the calculated value was F(5,168) = 1.71 with p = 0.1339, it was determined that there were no significant differences between mean salinities. Survival rates were noted for all t anks in Growth Trial 2 (Table 12 ).

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68 Table 1 2 Mean temperatures, salinities, and survival rates for Growth Trial 2 by tank. The mean weight was determined for each tank by week (Table 13 ; Figure 16 ). Then the replicate tanks for each diet were compared using an indep endent sample t test to determine if there were significant differences in weights between replicate tanks. This was done for the pre trial weights and the final weights. The mean pre trial weights of Tank 1 and 2 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 0.63 with p = 0.5438, there was no significant difference between the two means. The mean final weights of Tank 1 and 2 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 1.05 with p = 0.3245, there was no significant difference between the two means. Therefore, Tank 1 and 2 were combined into a Con trol Diet group. The mean pre trial weights of Tank 3 and 4 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 0.39 with p = 0.7063, there was no significant di fference between the two means. The mean final weights of Tank 3 and 4 were compared with a two tailed t test with alpha = 0.025 on each tail and a critical t value of 2.306. Given that the calculated value was t (8) = 0.41 with a p = 0.6895, there

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69 was no s ignificant difference between the two means. Therefore, Tank 3 and 4 were combined into an Experimental Diet with Attractant group. The mean pre trial weights of Tank 5 and 6 were compared with a two tailed t test with alpha = 0.025 on each tail and a crit ical t value of 2.306. Given that the calculated value was t (8) = 0.62 with p = 0.5504, there was no significant difference between the two means. The mean final weights of Tank 5 and 6 were compared with a two tailed t test with alpha = 0.025 on each tai l and a critical t value of 2.306. Given that the calculated value was t (8) = 0.28 with p = 0.7847, there were no significant differences between the two means. Therefore, Tank 5 and 6 were combined into an Experimental Diet without Attractant group. Ta ble 1 3 The mean weight (in grams) for each tank by week for Growth Trial 2 Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant. Mean weight was then determined for each diet by week (Table 1 4 ; Figure 17). The mean pre trial weights of the three diets were compared using a one way ANOVA to determine if the means were significantly different. Given that the critical F value was 3.35, the calculated value squared value was 0.030691, it was determined that there were no significant differences between mean pre trial weights of the three diet groups. Because a homogeneity of variance test for this data yield ed p = 0.0438, a Kruskal Wallis test was performed, which yielded p = 0.6825. This supported the original finding that there were no significant differences between the pre trial weights of the three diet groups.

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70 Figure 16 Graph of mean weight for each tank by week. Tank 1 and 2 are the control diet; Tank 3 and 4 are the experimental diet with attractant; and Tank 5 and 6 are the experimental diet without attractant. For m argins of error refer to Table 13 The mean final weights of the three diets were compared using a one way ANOVA to determine if the means were significantly different. Given that the critical F value was 3.35, the calculated value was F(2,27) = 59.80 with p = <0.0001, and that the square d value was 0.815826, it was determined that there were significant differences between mean final weights of the three diet groups. A homogeneity of variance test yielded p = 0.2046. A test of least significant differences showed that the mean weight of e ach of the three diets was significantly different from the mean weights of the other two diets.

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71 Table 1 4 Average weights for each diet by week for Growth Trial 2. Figure 17 Average weights for each diet by week for Growth Trial 2. For m argins of error refer to Table 14 Using the mean weights for each of the three diets, the average weight gain was determined for each of the diets. The average weight gains for the control diet, the experimental diet with attractant, and the experimental diet with out attractant were 300.3%, 218.0%, and 148.2%, respectively. The average daily growth coefficients and average specific growth rates were calculat ed for the three diets (Table 15 ). The daily growth coefficient and specific growth rate was largest for the control diet. The percent differences between the DGC and the SGR of the control diet and the experimental diet with attractant are 39.9% and 34.1%, respectively. The percent differences between the DGC and the SGR of the control diet

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72 of the experimental d iet without attractant are 105.1% and 94.6%, respectively. The percent differences between the DGC and the SGR of the experimental diet with attractant and the experimental diet without attractant are 72.9% and 65.8%, respectively. Table 15 Average dai ly growth coefficients (DGC) and average specific growth rates (SGR) of the three diets in Growth Trial 2. Discussion Within Growth Trial 1, the control diet out performed the experimental diet with attractant as well as the experimental diet without attractant based on the mean final weights and average weight gain. This outcome could have been due to better use of the c ontrol diet due its pellet form, better use of the marine based protein sources in the control diet, temperature differences between the tanks, salinity differences between the tanks, or a combination of these factors. The fact that the control diet was in pellet form and both experimental diets were gelatin based diets may have influenced growth rates because the gelatin diets were half water by weight and therefore may have been more energetically costly to digest. To gain the same amount of nutrients, th e shrimp must eat twice as much of a gelatin diet than a pellet diet, all other things being equal. To determine if the use of gelatin based diets affected the outcome, this experiment should be repeated using experimental diets that are also in the form o f dry pellets. Alternatively, if this research were continued, the pellets could be ground and mixed with gelatin, so that all of the diets were gelatin based. As mentioned above, the use of dry pellets was

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73 not possible for this study due to the requiremen t of large scale production to order pellet diets. The formulation of plant based proteins could have affected growth rates. It is possible that the plant proteins used were not as easily digested or utilized by the shrimp. This experiment should be repea ted using plant based experimental diets on that have already been tested and are known to not affect growth rates, such as the plant based diet used by Roy and colleagues (2009a). The lower temperatures and salinities in the tanks receiving the experiment al diet without attractant could have contributed to lower growth rates among the shrimp fed this diet. This is consistent with findings by Ponce Palafox and colleagues (1997) who found that Pacific white shrimp experience lower growth rates at lower temperatures The same study found that Pacific white shrimp exhibit lower growth rates at lower salinities. This trend of lower temperatures and salinities for shrimp fed alternative diets has not been observed in other studies, suggesting it was an artif act of the experimental setup. Mostly likely it was due to the location of these tanks in respect to the other four tanks. In terms of the survival rates, the highest two survival rates were for the tanks receiving the control diet and the lowest survival rates were for the tanks receiving the experimental diet without attractant. The lower survival rates seen in the tanks fed the experimental diets without attractant could have been attributed to the lower temperatures and salinities of these tanks through out the growth trial. Additionally, the lower survival rates may be due to the shrimp not finding the experimental diet without attractant palatable enough, which could have resulted in cannibalism within these tanks. However, the similar survival rates se en in Growth Trial 2, as discussed below, does not seem to support the occurrence of cannibalism.

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74 Within Growth Trial 2, the control diet group out performed the experimental diet with attractant and the experimental diet without attractant. Also within G rowth Trial 2, the experimental diet with attractant out performed the experimental diet without attractant. As discussed above, this outcome could have due to better use of the control diet due its pellet form, better use of the marine based protein sourc es in the control diet, temperature differences between the tanks, or a combination of these factors. The low temperatures in the tanks fed the experimental diet without attractant could have decreased the growth rates of the shrimp in these tanks. As ment ioned above this is supported by findings of low temperatures causing lower growth rates in Pacific white shrimp (Ponce Palafox et al., 1997). Again, lower temperatures for shrimp fed alternative diets was not been observed in other studies, suggesting it was an artifact of the experimental setup. Because Growth Trial 2 had more variables that were controlled throughout the trial pre trial weights, salinities, and survival rate this trial can be considered a better representation of the effects of the different diets on growth rates. The similar survival rates observed in Growth Trial 2 suggest that there was not an increased occurrence of cannibalism among the shrimp fed the experimental diets. The experimental diet with attractant outperformed the exp erimental diet without attractant in one of the two trials. The results suggest that the attractant may facilitate better weight gain. These results seem to support the idea that plant based diets require an attractant to improve the palatability of the di ets for aquaculture species. However, because the growth from the experimental diet with attractant was significantly different from growth from the experimental diet without attract in only one of the two trials, this research needs to be replicated for m ore accuracy. The short duration of these growth

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75 trials could have also not provided enough time for significant differences in growth between the experimental diet with attractant and experimental diet without attractant in the first growth trial. It is possible that trends were obscured by t he short duration of the growth trials. Because external growth in shrimp is dependent on the pattern of molts (Bureau et al., 2000) it is possible that the re were not enough period s of post molt growth included within the trials to show significant growth results Additionally, it is likely that shrimp experience varying growth rates at different life stages, based on the findings that shrimp have different maintenance protein requireme nts at different life stage s (Kureshy and Davis, 2002) and also different molt patterns at different stages of growth (Bureau et al., 2000) Therefore, t his research should be repeated using longer growth trial periods similar to the nine week growth trial used by Roy and Davis (200 9). In addition, more variables, such as pH and nitrates levels, should be monitored in future research to ensure that the shrimp in different tanks are receiving the same environmental conditions. In future research, fecal collection techniques should be used to determine the digestibility of diets with and without attractant as described by Glencross and colleagues (2007) Due to a lack of fecal collection during the current research, the only indication of ingestion of experimental diets with the color ation of feces noted to be the same green as the experimental diets. Despite progress in reducing fish meal in aquaculture feeds, shrimp aquaculture remains highly dependent on wild caught stocks for reduction into aquaculture feed ingredients. In additio n to replacing the major protein ingredients with more sustainable

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76 protein sources, the aquaculture industry needs to further reduce its dependence on wild stocks by eliminating marine based attractants whenever possible. Because this has already been dete rmined to be possible for alternative animal based diets (Samocha et a l., 2004 ) implementation of the removal of attractants in diets with animal based proteins would facilitate reduction in dependence on wild stocks of fish and invertebrate s However, continuation of the current research is necessary to determine if attractants can also be removed from diets with plant based proteins. Eliminating the reliance on wild caught fish and invertebrate stocks is only one of the steps towards sustai nability within the aquaculture industry. The issues discussed above, such as habitat destruction and the overuse of antibiotics in association with shrimp farms, also need to be addressed and remedied in order to ensure that the aquaculture industry is su stainable in the future.

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77 Appendix: Mazuri Custom Crustacean Gel Diet 5Z0N Mazuri Custom Crustacean Gel Diet Meagan White Domain New College, FL 5Z0N (Available at our TestDiet Unit (765)966 1885/testdiet@purinamills.com) Description Mazuri Custom Crustacean Gel Diet 5ZJ31 is designed based on the specification provided by Meagan White Domain of New College of Florida for a Nutritional Study looking at squid attractant in diets fed Pacific White Shrimp. This diet was base d on the Mazuri Herbivore Aquatic Gel Diet 5ZJ3, but the protein and fat levels were increased per Meagan to 36% and 11% respectively and animal based protein sources removed. Squid attractant has not been added to this diet and will be added at the time of this study. Features and Benefits Soft moist texture of gel Contains stabilized vitamin C Longer shelf life. Contains all vitamins and trace minerals known to be required by fish. Low starch formula more closely replicates wild type diets. Product Form Powder Crude fat 11.0% Crude fiber 7.0% Ingredients Dehulled soybean meal, dehydrated alfalfa meal, spirulina algae, gelatin, soy oil, dicalcium phosphate, spinach, carrot powder, s alt, dried kelp, wheat germ, vitamins and minerals. Feeding Directions Mix with an appropriate amount of hot water (over 200F). Blend with a spoon for one minute and pour into a flat pan to cool. Chill overnight in a refrigerator. Cut the gel by hand or with a food processor to obtain an appropriate size. Feed to herbivorous fish. The firmness of the gel is affected by the amount of water used. A good starting point is to use a ratio of 50:50 by weight of dry diet and water.

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78 Storage Directions The dry powder is shelf stable for at least six months. Once this product is mixed with water to form a gel, it should be handled like raw fish. It can be kept in the refrigerator for up to three days, if kept clean and sealed (wrapped). Similarly, it may be fr ozen like raw fish, and will last at least six months in the freezer. We recommend making batches that will last about a month, due to repeated entry into the container allowing the frozen gel to be exposed to oxygen. Average Feed Weights (note that aver age feed weights may vary due to method of measuring) Measurement g of Diet cup

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