5 Performance of Early Juvenile Giant River ( rosenbergii) Fed Fish, Soybean, and Four Insect Based Diets While Under Low Temperature Stress Malcolm L. McCallum School of Agriculture and Applied Sciences, Langston University, Langston, Oklahoma 73050 Samad D. Weston Department of Agriculture and Natural Resources, Langston University, Langston, Oklahoma 73050 Yonathan Tilahun School of Agriculture and Applied Sciences, Langston University, Langston, Oklahoma 73050

Abstract: Current guidelines for Macrobrachium rosenbergii advise introduction into outdoor ponds when water is > 16⁰ C. However, little is known about possible interactions between diet quality and temperature tolerance. We examined use of seven rations for prawns raised at suboptimal temperatures. Juvenile prawns readily consumed all seven rations presented. Growth and survivorship were best on shrimp- and silkworm-based rations; whereas, the poorest growth was on fishmeal- and Black Soldier Fly larvae meal (BSFLM)-based rations. Soybean-, cricket-, mealworm-, and fishmeal-based diets had similar survivorship. Mortality occurred within 24 hr after each feeding of the BSFLM-based diet, possibly related to antimicrobial compounds produced by BSFL. Prawns raised at lower temperatures may require better quality feed compared to guidelines based on previous studies at ideal temperatures. Producers must determine whether it is better to stock prawns at higher rates or feed more expensive rations to manage survivorship of juvenile at lower temperatures.

and surrounding Islands (New 1990; New Introduction 2002; New 2005). Temperatures of 26 – 31⁰C (Sabdifer and Smith 1985) or 25 - 32⁰C Ectotherms face continuous challenges (Zimmermann 1998) are considered ideal for imparted by interactions between the kinetics of growth (New 1990; Satapornvanit 2006). The their physiology and the quality of their diets. critical thermal minima for this species when The rates at which stress response, pathogen acclimated to temperatures of 20 - 30⁰C are defense, digestion, and growth ensue are 10 – 16.24⁰C for postlarvae and 10.5 – 16.98⁰C directly tied to ambient temperature. This is for juveniles (Herrera et al. 1998; Manush et a problem for outdoor production of the Giant al. 2004). Food consumption is significantly River (Macrobrachium rosenbergii) in reduced when temperatures fall below 25⁰C temperate regions. This is a tropical species (Newman et al. 1982). Prawns start to manifest of significant commercial importance that is a physiologically compromised state with acute native to rivers of the East Asian continent or slow changes in temperature below 15⁰C and Proc. Okla. Acad. Sci. 100: pp 5 - 15 (2020) 6 Prawn Diet Performance Under at Suboptimal Temperatures are severely compromised with acute drop from set up a laboratory experiment comparing 20⁰C to 10⁰C (Chung et al. 2012). Prawns raised performance of juvenile freshwater prawns for seven days under exposure to Lactococcus fed seven different diets comprising corn meal garvieae at 20⁰C demonstrate low phagocytic and selected protein feedstuffs. The study was activity, tolerance to ammonia and salinity conducted at temperatures comparable to those (Cheng et al. 2003) and impeded immunological observed in surface waters in Oklahoma in responses due to a sudden drop in temperature late April through early May to help formulate from their thermal ideal (28⁰C) to 22⁰C (Chang guidelines for outdoor pond culture of prawns et al. 2015). Mortality is substantially elevated for Oklahoma producers and to test potential as temperatures fall below 12⁰C (Satapornvanit interactions between temperature, stress and 2006). Urea-N excretion is minimal at 17⁰C diet. We hypothesized that prawns would and rises with temperature (Chen and Kou grow slower at cooler temperatures and have 1996). Growth nearly doubles for every 5⁰C lower survivorship than typically expected increase in temperature from 20 to 36⁰C, without at higher temperatures, and that prawns may an appreciable change in conversion ratio perform better on - and - (Faranfarmaian and Moore 1978). However, based protein sources than on soybean or growth is more erratic at lower temperatures fishmeal diets. We predicted that growth (Whangchai et al. 2007). Guidelines suggest and survivorship would be higher when fed cultivation temperatures should be above 16⁰C arthropod- and crustacean-based protein sources (Herrera et al. 1998; New 2002). However, than on fishmeal or soybean meal. observations in research settings generally demonstrate higher survivorship than actually Materials and Methods observed in commercial settings (Tidwell et al. 2005). Prawns were obtained from Stickfin’s Fish Farm (St. Augustine, Florida) and housed Diets resulting in higher survival and communally for one week after arrival in growth also tend to impart better responses to aerated 40-L aquaria containing moderately hard stressors (Racotta et al. 2003). Research with synthetic freshwater made with reagent grade prawns has related temperature stress effects on chemicals (U.S. E.P.A. 2002). Following that neuroendocrine responses (Chang et al. 2015), week, 105 prawns were individually housed in oxygen consumption (Farmanfarmaian and 125 ml Pyrex Erlenmeyer flasks containing 100 Moore 1978; Chen and Kou 1996; Niu et al. ml of synthetic freshwater. An inverted Pyrex 25 2003; Manush et al. 2004), nitrogen excretion ml flask was inserted into the neck of each larger (Chen and Kou 1996), pH and ion balance flask to prevent contamination from airborne (Cheng et al. 2003), food consumption (Niu et particulate. Each prawn was placed in a weigh al. 2003), growth (Farmanfarmaian and Moore dish and excess water removed using a transfer 1978; Niu et al. 2003), and survivorship (Herrera pipette and then weighed on an electronic et al. 1998; Chung et al. 2012; Manush et al. analytical balance to the nearest 0.001 g. Next, 2004). Additional nutritional studies with the M. each prawn was then placed in its flask where it rosenbergii are numerous; however, little work resided for the duration of the study (28 days). has approached the currently growing interest in more sustainable replacements such as Water quality was monitored weekly and insect meal. water was changed if it became cloudy or otherwise fouled. The pH (7.4 – 7.8), hardness

Oklahoma has never had a prawn industry (160 – 180 CaCO3/L), and alkalinity (57 – 64 in the state despite apparent suitability of its CaCO3/L) never exceeded the typical range climate and unique infrastructure for moderately hard synthetic freshwater (U.S. characteristics (McCallum and Tilahun [In E.P.A. 2002). Temperature was maintained at Press]). Guidelines for earliest dates to 21⁰C throughout the study. stock ponds in Oklahoma are lacking. We Proc. Okla. Acad. Sci. 100: pp 5 - 15 (2020) M.L. McCallum, S.D. Weston, and Y. Tilahun 7

We obtained commercial fish meal and Daily observations of molting and mortality soybean meal from a local feed store (Stillwater were recorded. At the end of the study, all Milling Company, Stillwater, Oklahoma). Dried remaining prawns were weighed. Growth silkworm pupae (Bombyx mori), mealworm data were tested for normality using an larvae (Tenbrio molitor), “river” shrimp from Anderson-Darling test. We compared the Chubby Mealworms (Las Vegas, Nevada) and weight gain between treatments using a one- dried crickets (Acheta domesticus) came from way ANOVA with a Tukey means comparison Fluker Farms (Port Allen, Louisiana). Dried test. Survivorship and molting frequency was black soldier fly larvae (Hermetia illucens) compared between groups using Chi Square. came from Enviroflight, LLC (Yellow Springs, We used an alpha = 0.05 to assess significance. Ohio). Feedstuffs were ground and mixed with a household coffee grinder. Rations were Results balanced on a 35% protein basis (Table 1; New 2002; although even higher protein levels are In all cases, prawns readily consumed food effective [Millikin et al. 1980]) using bakery when presented and could be seen feeding on grade yellow corn meal (Quaker Oats Company, remaining food particles until the next feeding.

Chicago, Illinois). Prawns (ntotal = 105 prawns, None of the prawns consumed 100% of the food n = 15 prawns/treatment) were fed one of each offered after 24 hrs, with obvious remnants of ration (n = 7 treatments) ad libitum throughout food typically remaining for days. Prawns the study, although the quantity varied according did not perform equally well on all rations.

to bodyweight. Guidelines suggest prawns Growth (F6, 104 = 4.69, P < 0.001) varied among should be fed 10-20% of the total bodyweight treatments (Table 2, 3). Growth data were not (New 2002), but this is based on bulk weights, normally distributed (A2 =16.56, P < 0.001) so not individual measures. Because of this, it was we transformed these data using the normalize impractical to feed such small quantities at the function in MiniTab 13.0. Prawns gained weight onset of the study. Each prawn received 15% of better on shrimp (-0.060, -1.708) and silkworm its last measured bodyweight. If food remained pupae (-0.040, -1.688) than on fishmeal. They after 24 hr, we would reduce the quantity by also gained better on shrimp (-0.303, -1.9506) 10% as fed on the next feeding. If food was and silkworm pupae (-0.283, -1.931) than on consumed after 24 hr, we increased the feeding black soldier fly larvae. No other significant rate by 10% as fed, and added the additional differences in growth were observed. quantity to the flask. Food was delivered by sprinkling the dried meal on the water surface. There were marginal differences in survivorship (ꭓ2 = 10.81, df = 6, P = 0.094) If food settled on the bottom began to mold, among treatments. Prawns survived equally we siphoned it off with a transfer pipette for well when fed fish meal, soybean meal, ground disposal. mealworms and ground crickets (ꭓ2 = 4.42, df Table 1. Nutritional breakdown on an as fed basis of the eight ingredients used to formulate diets for juvenile freshwater prawns (Macrobrachium roosenbergii). Black Fish Soybean Shrimp Cricket Silkworm Mealworm Corn Soldier meal meal meal meal pupae meal meal meal Fly meal DM % 90.12 91.26 92.40 93.0 95.7 94.0 94.8 88.0 Protein % 70 40 50 64 37 45 53.6 7.4 Fat % 14.82 18.48 13.13 19.0* 14.2* 29% 29.2 1.8 Gross energy 21.9 19.7 19.1 21.8* 23.8 25.8** 24.4** 13.8 MJ/KG DM Crude Fiber % 2.22% 7.10% 1.2% 8.5 7.0% 6% 18.5 7.4% *Finke 2002 **http://feedipedia.org Proc. Okla. Acad. Sci. 100: pp 5 - 15 (2020) 8 Prawn Diet Performance Under at Suboptimal Temperatures Table 2. Performance of juvenile Giant Freshwater Prawns (Macrobrachium rosenbergii) on seven diets at the lower threshold of thermal tolerance.

Ending BM* Starting BM (g) Growth* (g) Molts Survivorship Protein source (g) Mean (SE) Mean (SE) (n) (%) Mean (SE) Fish meal 0.020 (0.002) 0.022 (0.002) 0.002 (0.001) 4 6.7 Soybean meal 0.020 (0.002) 0.028 (0.004) 0.008 (0.004) 4 33 Shrimp 0.025 (0.002) 0.039 (0.004) 0.015 (0.003) 8 86.7 Silkworm 0.018 (0.001) 0.033 (0.006) 0.016 (0.006) 10 66 Mealworm 0.030 (0.002) 0.035 (0.003) 0.014 (0.009) 6 40 Cricket 0.023 (0.002) 0.025 (0.003) 0.003 (0.001) 13 40 Black Soldier 0.026 (0.002) 0.027 (0.002) 0.0003 (0.0003) 3 6.7 Fly Overall 0.023 (0.001) 0.030 (0.001) 0.008 (0.002) 48 42 *Ending body mass (BM) and growth are the averages for those that survived to the end of the study; whereas, starting BM includes the entire starting population.

Table 3. ANOVA table for the response of growth to different foods.

Source DF SS MS F P Food type 6 15.778 2.630 4.69 < 0.001 Error 98 54.997 0.561 Total 104 70.775

= 4, P = 0.352). They performed just as well temperatures. Wild prawns feed on aquatic when fed ground shrimp or silkworm pupae (ꭓ2 invertebrates, detritus and algae (Balaz and Ross = 0.196, df = 1, P = 0.158). Prawns had higher 1976). Previous studies on nutrition of prawns survivorship when fed shrimp meal or silkworm were conducted within the thermal optima for pupae meal than when fed black soldier fly or fish this species and largely determine fishmeal meal (ꭓ2 =10.84, df = 3, P = 0.013). There were and soybean meal to be adequate protein feeds no observed differences in molting frequency (ꭓ2 (Hasanuzzaman et al. 2009; Gupta et al. 2007; = 5.64, df = 6, P = 0.464) among treatments. Koshio et al. 1992) although reports as low as 11% survivorship on fishmeal are known (Kumlu Within 24 hours of first feeding black soldier 1999). Addition of shrimp oil to a balanced diet fly larvae to prawns, 27% died; whereas, the doubled the final biomass of prawns (Sandifer other feeds had 93 – 100% survivorship after and Joseph 1976). Further, post-larvae fed 24-hr (Total 24-hr survivorship on other feeds entirely on Artemia nauplii perform well (Barros = 97.8%). Mortality rose to 40% by the fifth day and Valenti 2003; New 2002). In general, when fed the Black Soldier Fly larvae meal- prawns performed acceptably on proven protein based ration. After seven days, remaining food sources (shrimp meal, soybean meal) but particles (mostly corn meal) were removed from growth and survivorship on less suitable feeds all flasks, and new feed introduced. Then, 24-hr (fishmeal, Black Soldier Fly larvae meal) was after being again fed the Black Soldier Fly larvae less impressive. Arginine, one of three key meal-based ration, another 47% of prawns died, amino acids thought to be important to prawns with a total mortality of 93.3% in this treatment. (e.g., Methionine, Lysine [D’Ambramo and The single remaining prawn survived until the Sheen 1994]) is generally more abundant in end of the study, but its growth was negligible. soybean and shrimp meals than fish meal (Watts 1968); however, amino acid requirements have Discussion been difficult to elucidate (Reed and D’Abramo 1989). Temperature and nutritional stress manifest in physiological trade-offs for ectotherms, and Differences in survivorship and growth may our results provide evidence that when raised be explained by changes in feeding behavior, at suboptimal temperatures freshwater prawns more efficient digestion, and more effective appear to become more sensitive to food quality stress responses when temperatures are warm compared to previous studies performed at ideal compared to suboptimal. The time prawns spend Proc. Okla. Acad. Sci. 100: pp 5 - 15 (2020) M.L. McCallum, S.D. Weston, and Y. Tilahun 9 feeding is known to decline with temperature of other dipterids (Bradley and Sheppard 1984). (Niu et al. 2003). Consequently, when at optimal This insect has been fed successfully to poultry temperatures, prawns may increase consumption (Cullere et al. 2016; Elwert et al. 2010; Dluokun sufficiently to overcome the minor inadequacies 2000), livestock (Veldkamp and Bosch 2015; of amino acid composition. However, when Veldkamp et al. 2012), dogs and cats (Bosch et housed at sub-optimal temperatures, feeding al. 2014), and fish (Shakil Rana et al. 2015; Tran behavior is suppressed and they cannot fully et al. 2015; Sealey et al. 2011; St-Hilaire et al. accommodate for reduced limiting nutrient 2007). supply, leading to poorer performance. Further work is needed to elucidate amino Previous studies of black soldier fly acid needs of prawns (Mukhopadhyay et al. larvae meal for decapod diets exist, though 2003; D’Ambramo and Sheen 1994) so that not for M. roosenbergii. Growth of juvenile informed supplementation with imperfect feeds white shrimp (Litopenaeus vannamei) was is possible. increasingly suppressed as black soldier fly larvae meal became a higher proportion of Physiological processes in all ectotherms are the diet (Cummins et al. 2017). Weight gain, tied to the ambient temperature (Wilmer et al. final body weight, feed conversion ratio, and 2004; Manush et al. 2004; Manush et al. 2006), specific growth rate of shrimp became less including digestion in prawns (Kumlu 1995; acceptable as the dietary component of black Newman et al. 1982). Each of these ingredients soldier fly larvae meal increased. Survivorship require different residency times and enzyme of these shrimp was much higher than in our assemblages to digest and absorb, and each study (~91% vs. 6.7%). Other than the species enzyme operates in an ideal temperature range. It involved, the primary differences in these two is likely that digestive enzyme activity in prawns studies is that ours involved much younger/ was suppressed by lower temperatures, leading smaller (initial prawn BW = 0.023 g to inefficient digestion of less perfect feeds. +/- 0.001 vs. initial shrimp BW = 1.24 +/- 0.01 Further, as a kinetically controlled biochemical g), diets with a much larger component of black process, production of non-essential amino acids soldier fly meal, smaller housing (100 ml vs. is altered at lower temperatures. Combined with 110 L), individualized housing (vs. communal), feeding behavior, digestion and biochemical and we maintained a lower temperature (21⁰C processes could explain why prawns fed fish, vs 29.5⁰C). These differences provide several soybean and shrimp meal perform well at avenues for the vastly different survivorship optimal temperatures; whereas, survival and levels. The younger prawns may have less growth is much reduced at cooler temperatures. developed functional immune/stress response systems. Stress and immune responses are Unlike other ingredients in this study, freeze known to undergo ontogenetic changes as an dried black soldier fly larvae appear unsuitable organism grows (Manning and Turner 1976). for feeding prawns, at least at suboptimal The larger soldier fly component in the feed temperatures. Significant mortality occurred should deliver a larger dose of antimicrobial within 24 hours of feeding fly meal to the chemicals. The larger housing and resultant prawns. Black soldier flies are known to harbor larger water volume used with white shrimp may compounds with antimicrobial properties be sufficient to dilute feed-borne compounds (i.e., defensin-like peptide4, a 40 amino acid in the water column to non-toxic levels. The AMP; Elhag et al. 2017; Park et al. 2015) differences in temperature may also be a sufficiently powerful to suppress growth of significant factor. Prawns were already under Escherichia coli, Salmonella spp., antibiotic thermal and potentially nutritional stress. These resistant Staphylococcus aureus, and gram two stressors are known to participate in a trade- positive Pseudomonas aeruginosa (Lalander off system that provides added risk to additional et al. 2015; Liu et al. 2008). Their excretions stressors (Padmanabha et al. 2011; Cotter et al. are also known to inhibit growth in the larvae 2011; Karasov et al. 2007). Considering that Proc. Okla. Acad. Sci. 100: pp 5 - 15 (2020) 10 Prawn Diet Performance Under at Suboptimal Temperatures as an ectotherm, all physiological processes et al. 1999). Using soybean meal eliminates are bound to thermal optima (Wilmer et al. dependence on wild stocks for protein and 2004), the stress response of prawns may be reduces the contaminant problem, but brings an compromised by low temperature making them array of other environmental issues connected to more susceptible to chemical stressors like those crop farming such as pesticide use (van Meter et produced by soldier fly larvae. A confounding al. 2018; Mitsch et al. 2001; Pimentel et al. 1993). element to these results is that we did not Soybean meal also contains phytoestrogens provide perches for molting behavior. This may (Coward et al. 1993), which may adversely have provided across-the-board higher mortality impact invertebrate reproductive potential, (McCallum et al. 2018). growth and development (Jefferson et al. 2005; Ryokkynen and Kukkonen 2006; McCallum et Black soldier fly has also been proposed for al. 2013). Hence, there are good reasons to desire use in human diets (Wang and Shelomi 2017; alternatives to these two products, especially in Dossey and Morales-Ramos 2016; van Huis aquaculture and , the latter of which et al. 2015; Boland et al. 2013). The recent prides itself on being sustainable (Forchino et al. findings above suggest that incorporation of 2017; Konig et al. 2016; Goddek et al. 2015). If black soldier fly meal into the human food chain the freshwater prawn industry is positioned as a should be done with great consideration. The sustainable alternative to wild-caught shrimp, it compounds black soldier fly larvae produce can carve a larger place in the market and likely could lead to new strains of microbes afflicting draw higher prices. Abandoning less-sustainable humans and animals that are highly resistant to feed ingredients is an important step to reaching antibiotics. Further, there has been no testing this goal (Sánchez-Muros et al. 2014). Although to determine if these compounds have long-term in its infancy, carefully selected and prepared health effects for the organisms ingesting them, insect meals may serve this purpose (Rumpold or if these compounds could be transferred from and Schlüter 2013). food animals to humans. Until such studies are undertaken, it seems prudent to avoid using this The performance of prawns at temperatures protein source for humans or animals intended similar to those in April – May in Oklahoma for human consumption. Other insects in this suggest that if producers intend to stock ponds study do not appear to hold such risks. Thus far, that early, they will need to feed very high we have found little evidence that the scientific quality feeds or stock ponds at higher levels than community has considered the risks associated typically recommended to ensure a harvestable with antimicrobial compounds in black soldier product. Alternatively, producers could cover flies. It has been more focused on heavy small ponds with greenhouse structures to metal accumulation in the larvae, microbial extend the season (Pillai et al. 1999), restrict decontamination prior to processing, and food production to indoor recirculating or aquaponics allergies (Rouge and Barre 2017; Wang and facilities, or wait until later in the year when Shelomi 2017). water temperatures are more suitable to stock ponds with juvenile prawns. Fish, shrimp, and soybean meals are among the most commonly used protein sources in Acknowledgments feeds, including prawns (Hasanuzzaman et al. 2009; Koshio et al. 1992). Fish and shrimp Many thanks to Steve Hart, Arthur Goetsch, meal continue to be sourced from wild Ali Hussein, Roger Merkel, Zaisen Wang, and are increasingly expensive (Carter and Tilahun Sahlu, and Walter Meshaka, Jr. for Hauler 2000), thus discounting the sustainability feedback and discussions about this research. of aquaculture operations (Love et al. 2014; The research was funded through the USDA Gatlin et al. 2007). Further, they can harbor Evans Allen Program, Project Number USDA- contaminants from the wild environment (Costa NIFA-OKLUMCCALLUM2017 and was 2007; Dorea 2006; Hardy 2002; Galindo-Reyes conducted under accordance with the Federal Proc. Okla. Acad. Sci. 100: pp 5 - 15 (2020) M.L. McCallum, S.D. Weston, and Y. Tilahun 11

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