TY - JOUR
AU - Esmail, Michael Y
AB - Abstract Feed plays a central role in the physiological development of terrestrial and aquatic animals. Historically, the feeding practice of aquatic research species derived from aquaculture, farmed, or ornamental trades. These diets are highly variable, with limited quality control, and have been typically selected to provide the fastest growth or highest fecundity. These variations of quality and composition of diets may affect animal/colony health and can introduce confounding experimental variables into animal-based studies that impact research reproducibility. aquatic models, aquatic animal nutrition, cephalopods, xenopus, zebrafish INTRODUCTION The use of aquatic animals in society extends back centuries, with fish husbandry first appearing as early as 4000 years ago in China [1]. The need to develop and maintain fish for growth, maintenance, and reproduction has driven nutrition studies and nutrient analysis. Only in the past several decades have zebrafish (Danio rerio) become the most popular aquatic animal model in biomedical research. In addition to zebrafish, other aquatic species used in biomedical research include medaka (Oryzias latipes), 3-spined sticklebacks (Gasterosteus aculeatus), African Clawed Frogs (Xenopus laevis), Western Clawed Frogs [Xenopus (Silurana) tropicalis], Axolotl (Ambystoma mexicanum), and multiple cephalopod species. Despite the popularity these species have in research, the influence of diet and nutrition on research goes largely unstudied. However, over the past decade, a movement has developed to establish species-specific “standardized” diets for aquatic animals involved in research. Proponents describe the creation of diets for research rodents (eg, AIN-76A) started in the 1960s as precedent [2, 3]. This review will survey the current state of aquatic research animal nutrient requirements and diet formulations, feed management, sources of experimental variation from diets, and specific areas of research affected by the diet. Given the nature of species utilized in biomedical research, much of the review will focus on zebrafish and X. laevis. With that said, this review will also incorporate references from a much larger body of literature that describes the impacts of diet on a variety of fish in aquaculture. Overview of Current State of Nutritional Requirements for Aquatic Species Establishment of Requirements As previously described, there has been a growing call from within the research community, from internet blogs [4] to correspondence in Nature [5], to develop a standardized diet for zebrafish, emulating what was done with rodents starting in the 1960s [2, 6–8]. The use of a standard or defined reference diet is critical for any animal model, including zebrafish, African clawed frogs, axolotls, and cephalopods. While much has been published on the nutrient composition of diets fed to zebrafish and other aquatic species, there is no agreed-on set of requirements for these models used in biomedical research [2, 6, 7]. However, the body of literature on zebrafish nutrition is considerably more substantial than that for the aforementioned aquatic research models. Developing nutritional requirements for these species will likely, in part, rely on what has already been established for farmed fish, amphibians, and cephalopods. Readers are encouraged to review the reports and presentations of 2 recent NIH Office of Research Infrastructure Programs workshops on the establishment of nutritional requirements for zebrafish and the impact of diet on experimental reproducibility [2, 8]. Universal Factors Requiring Increased or Altered Nutritional Demands Nutrition significantly affects all life processes, including normal physiological processes like growth, reproduction, health, and senescence [9, 10]. Conversely, internal and external conditions will influence an individual’s dietary needs. These conditions vary extensively and include, but are not limited to, developmental stage, health status, environmental conditions, feeding strategies, ecological niche, and behavior [11–13]. Given the central role diet plays in biological and experimental processes, it is increasingly important to obtain a better understanding of required nutrition for experimental animal models. Growth Growing animals require nutrients to meet the needs of specific developmental stages (eg, embryo, larval, juvenile). Nutrients provide the basic building blocks to increase mass and size of structural tissues of the body [14]. From birth to sexual maturity, the rate of growth increases; however, it will progressively decrease as the animal ages. Growth rates vary by species, strain, environmental conditions, and health [10, 14]. When determining the nutritional requirements for aquatic species, one must take into consideration the developmental stage [6, 15, 16]. In general, the weight gain of younger animals principally consists of water, protein, and minerals required for growth of bone and muscle. As the animal matures, weight gain is due to higher proportions of fat [10]. An animal’s ability to develop at a species-typical growth rate is directly related to the nutrient intake and profile during development [10, 17]. Growth requires a large intake of energy-producing macronutrients, amino acids, fatty acids, vitamins, and minerals for development [14]. Reproduction Reproduction is conditioned by a long series of distinct but interrelated physiological events, involving not just the reproductive tissues but the whole organism. Nutritional factors play vital roles in the various events that occur in the attainment of sexual maturity and in the course of reproduction. In animals, undernutrition may delay sexual maturity and, if severe, may cause retrogressive changes in the sex organs after they are fully developed [11, 14]. Energy balance is likely the most important nutritional factor related to reproductive function; available energy is directed towards reproductive system development, gamete production, and specific behaviors during the breeding season [18, 19]. In fish, it has been demonstrated that decreased food availability or starvation causes gonad regression and a decrease in spawning or the number of eggs produced [20]. Moreover, low-protein diets have shown to increase maturation time and reduce reproductive performance, oocyte maturation, ovulation, egg production, and egg viability [21, 22]. The influence of nutrition on reproduction begins early in the animal’s life, with nutritional changes in reproductive organs influencing subsequent adult reproductive performance. A large body of literature demonstrates that an inadequate diet fed to mature animals, including zebrafish, Xenopus laevis, and Octopus vulgaris, can directly affect the production of ova, resulting in infertility or production of fewer offspring [6, 22–27]. Whereas females seem to invest energy in gametogenesis, in several species, male courtship is an energetically costly behavior involving swimming and/or fighting in most cases [15, 28–31]. Some species invest energy in parental care by preparing nests and guarding the eggs after spawning [21]. Many nutrients influence fertility and overall reproduction throughout the different phases or cycles; among the most important are lipids (essential fatty acids); proteins; vitamins A, E, and C; phosphorus; selenium; and trace elements like copper, molybdenum, iodine, manganese, and zinc [10, 14, 18, 32]. Disease Diets that supply inadequate or excess nutrients have the potential to directly and indirectly cause diseases, some of which are covered later in this review [33]. Deficiencies in essential limiting amino acids (lysine, methionine, tryptophan), essential fatty acids, phosphorus, iron, zinc, manganese, and selenium can cause disease in various species of farmed fish (eg, Cyprinus carpio, Oncorhynchus mykiss, Salmo salar) [34]. The level of protein, vitamin D3, and trace minerals influences reproductive success, larval growth, survival, and skeletal development in zebrafish [35–39]. Decreased vitamin A and obesity are reported as major nutrition-related problems in frogs [12, 40]. In addition, nutrition influences the immune system of nonnutritional diseases. Several dietary factors have been identified as affecting an animal’s response ability to resist infection by pathogenic agents [41, 42]. An adequate diet plays a critical role in the immune competence of aquatic species as the absence of essential amino acids, carotenoids, omega-3 and omega-6 fatty acids, vitamin A, folic acid, vitamin B6, vitamin B12, vitamin C, vitamin E, zinc, copper, iron, and selenium may affect immunity [41, 43, 44]. Senescence Aging progressively alters physiological systems and metabolic processes [45]. Senescence influences various aspects of digestive physiology, including microbiota, digestive hormones, gut morphology, nutrient digestibility, and immune characteristics [46]. In addition, senescent animals have different energy requirements, generally have decreased appetite, and utilize nutrients differently than younger animals [10]. Aged animals should be provided with a diet that will slow or prevent the progression of metabolic changes and minimize the effects of aging with the aim of prolonging lifespan and reducing age-associated diseases. These diets are often highly digestible and contain highly bioavailable nutrients to ensure appropriate nutrient uptake, especially if less food is consumed [45]. Diet plays an important role as a modulator of longevity and prevention of diseases associated with nutrient utilization [47]. For example, dietary caloric restriction extends life span and retards age-related diseases in a variety of species [48–50]. In the short-lived (lifespan of 4–9 months) African turquoise killifish (Nothobranchius furzeri), dietary restriction prevents the expression of aging markers in the liver and the brain, consistent with beneficial effects observed in rodent models [51]. A Brief Overview of Unique Dietary Requirements for Specific Laboratory Animal Species Follows Zebrafish (Danio rerio) In nature, zebrafish are observed to be omnivorous, consuming zooplankton, insects, phytoplankton, algae, and plant material [52, 53]. In the laboratory setting, they are known to feed throughout the water column, including surface and bottom feeding [15]. Live or formulated feeds can be used exclusively in culturing zebrafish at any life stage, though many facilities use a combination of the two [15, 54]. Exogenous feeding begins around 5–6 days postfertilization (dpf) [55] when larva are reared at 28.5°C. The size of the feed particle or pellet is one of the multiple factors that determines the success of a diet for zebrafish at various life stages. Prior to exogenous feeding, zebrafish larvae subsist on the yolk sac while the digestive system develops [15]. At the time exogenous feeding begins, the mouth gape of zebrafish is approximately 100 μm [55], thus limiting the size of feed it can consume. The nutrition of first feeding in fish is a complex process that involves multiple feed factors relating to the feed, including its color, smell, visual appearance, digestibility, position in the water column, and motility [56]. For example, the use of live foods appears to stimulate hunter/prey behavior in zebrafish larvae [57, 58]. Adult zebrafish have been known to thrive on diets as small as rotifers (approximately 250 μm) and pelleted diets as large as 1 mm [15, 57]. The specific nutritional requirements of zebrafish have yet to be established, but the topic is under active discussion within the research community [2, 8]. Nutritional requirements of other cyprinids may be used to help develop a standard diet and nutritional requirements [6]. For example, comparative studies show some similarities in diet composition and nutritional genomics between zebrafish and the common carp (Cyprinus carpio), also a stomach-less, warm-water cyprinid [59, 60]. Readers interested in the establishment of zebrafish nutritional requirements are encouraged to review the presentations on the topic delivered at a recent NIH Office of Research Infrastructure Programs workshop on zebrafish nutrition [2]. African Clawed Frog (Xenopus laevis) Xenopus laevis, an anuran, has long been utilized in laboratory research and teaching given they are relatively easy to maintain, are resistant to diseases, have a relatively short life cycle, and can produce large external clutches [61, 62]. Food is first detected primarily by the extremely sensitive lateral line organs distributed over the head and trunk and is then grasped with the frog’s forelimbs [63, 64]. There is little information regarding recommendations for feeding laboratory X. laevis, and nutrient requirements are not well specified [65]. Anurans are obligate carnivores as adults, typically opportunistic generalist predators of invertebrates and/or small vertebrates, and are monogastric with a very short and simple gastrointestinal tract [66, 67]. In strict carnivores, amino acids are catabolized to provide the substrates for the citric acid cycle and gluconeogenesis to generate utilizable energy [10]. Aerobic and anaerobic metabolism provide energy to allow frogs to display natural behaviors, including foraging, ambulation, resting, courtship, and aggression [68]. Adult anuran prey diets are typically high in protein, moderate in fat, and low in carbohydrates [69]. This nutritional profile is the case for the majority of invertebrate food sources utilized by anurans, with many invertebrate species containing approximately 60% crude protein (dry matter basis), substantial variations in the lipid content (4.6–64% dry matter), and a very low carbohydrate content (0.5–7% dry matter) [70–72]. Strict carnivores have high protein requirements due to high endogenous nitrogen losses and increased amino acid catabolism in liver and kidney [73]. The glucose needed to meet the carnivore’s demands is obtained via gluconeogenesis, preferentially obtained from high-protein feeding sources [74]. Fats also provide fuel for energy in carnivores [75]. In frogs, it has been proposed that fat acts as the substrate that supports activity during fasting periods (ie, dormancy or the breeding season) [68] and is mobilized for reproduction during the breeding season [18]. Studies in free-ranging frogs have demonstrated that blood glucose and plasma protein levels are positively associated [76]; moreover, 2 main forces (proteinogenic and lipogenic) are proposed as drivers of energy metabolism in captive X. laevis and free-range frog species [73, 77]. Pelleted diets developed for adult X. laevis available from commercial sources consist of a variety of nutrient sources, including animal protein from pigs, shrimp, poultry, and fish; plant protein such as soybean meal; and mineral-vitamin supplements. The published nutritional analyses of these diets consist of 92% dry matter (DM), 40% crude protein (CP), 10% crude fat (CF), 12% ash, 1.7% calcium (Ca), 1.3% phosphorus [78] and 44% CP, 6% CF, 3.7% Ca, 2.2% phosphorus [79]. These diets provide between 2800 and 3000 kcal/kg food. Frogs have been maintained on a variety of experimental diets, including 90.1% dry matter, 38.0% CP, 11.2% CF, 18.6% ash, 2.2% lysine, 7.6% methionine, 3.0% leucine, and 4228 kcal/kg food [73]. At the moment, little is known regarding feeding regimes for X. laevis and nutrient requirements are not specified. Aside from commercial feed, organ meat and live prey are utilized, but special attention is required in their use as there is a risk of contamination [62, 80]. Axolotl (Ambyostoma mexicanum) Axolotls are neotenic salamanders that are relatively easy to maintain in captivity and have been used as models in aging and regeneration [81]. Like X. laevis, A. mexicanum is a carnivore with a simple gastrointestinal tract. Food items commonly used in diets for adult axolotls are earthworms, small fishes, bloodworms, Daphnia sp., several arthropods, and commercial diets (pellets) [82]. During feeding, most salamanders lunge towards the prey, the buccal cavity is expanded, and, almost simultaneously, the weak jaws are opened [67]. Nutritional requirements of axolotls are not established; however, it is recommended to utilize ingredients high in protein and fat [81]. As in the case of frogs, dietary amino acids may be metabolized by gluconeogenesis to supply the needs of the brain and other glucose-requiring tissues [83]. and also provide substrates for energy production [84]. Diets should be balanced to avoid nutritional diseases, such as metabolic bone disease (imbalance between calcium, phosphorus, and vitamin D3), hypovitaminosis A, and corneal lipidosis (excess of dietary fats) [85]. In general, recommendations for salamanders include 30–60% crude protein, 40–70% fat [86], low carbohydrates and fiber, as well as adequate levels of vitamins B1, A, E, and D3 [87]. At the Ambystoma Genetic Stock Center, larvae are first raised on brine shrimp (Artemia sp.). Once larvae reach 3 cm, they are transitioned to California blackworms (Lumbriculus variegatus) to increase their growth rate and facilitate the transition from live to pelleted food. Also at the Ambystoma Genetic Stock Center, adult axolotls are fed aged, soft, moist pelleted food manufactured for salmon by Rangen, Inc., consisting of 44% crude protein, 18% crude fat, <5% fiber, and <8% ash [88–90]. Axolotls are also maintained on earthworms as well as diets of beef muscle and organ meat supplemented with vitamins and minerals. However, raw meat carries a risk of microbial contamination [80]. Cephalopods The use of cephalopods in research, including in behavior, cognition, genetics, and neuroscience/biology, as well as consideration of their welfare [91] has increased over the past 2 decades. Cephalopods used in scientific research and education have become regulated in the European Union; the regulations include all “live cephalopods” (approximately 700 species) at all life stages after hatching [92]. AAALAC International will evaluate “higher level invertebrates such as lobsters, squid, or octopi” at an institution that utilizes them. Therefore, with increasing use of cephalopods in research and increasing oversight, it is important to advance the understanding of the dietary requirements for captive species. Scientists and animal care professionals who are caring for cephalopods should consult the Guidelines for the Care and Welfare of Cephalopods in Research for husbandry, application of the 3R principles, and other related topics [93]. Reviewed in Sykes et al [94], much of the research on cephalopod digestive physiology has been focused on the European common cuttlefish (Sepia officinalis) [95–101], the common octopus (Octupus vulgaris) [96, 97, 102, 103], the Mexican four-eyed octopus (Octupus maya) [104–109], the European squid (Loligo vulgaris) [97, 110], and the chambered nautilus (Nautilus pompilius) [111–115]. The majority of cephalopods are carnivorous, with many being predators that capture live food. However, some cephalopods are scavengers, such as N. pompilius. What is known about cephalopod diet in the wild is limited; however, captive cephalopods generally adapt well to prey such as small fish, crustaceans, and mussels when provided in the laboratory [93, 116]. A review of the micronutrients required for cephalopods can be found in Navarro et al [117]. Feed Management of Aquatic Species Frequency Within the zebrafish community, it is common to feed fish 1 to 3 times per day [6, 54]. However, select facilities are known to feed 5 or more times per day with the intent of achieving faster growth and higher fecundity. Rapid growth may be important for researchers who need fish to reach adulthood quickly whether it be for tissue harvest or breeding; however, if the fish are simply used to maintain the strain, it may not be necessary. For moderate to large facilities, achieving 5 or more feedings per day requires significant personnel resources (multiple and/or dedicated staff) or may be done with automated feeders. These can cost hundreds of thousands of dollars because the technology is relatively new and still developing [118]. Resources such as labor and infrastructure weigh heavily on the feeding regime chosen for each facility [119, 120]. Life stage is also a factor in determining the frequency of feeding. Larval and juvenile fish are often fed more frequently than adult fish to facilitate increased survival and growth. Ad libitum feeding is a term used when feed is available to an animal at all times. With terrestrial animals, this type of feeding is relatively easy but is near impossible for zebrafish and some other aquatic animals due to the fact that water is constantly flowing through the tank and washing food out. Ad libitum feeding can be achieved with larval fish by polyculture, where fish are fed a sufficient quantity of live feed (such as rotifers or paramecia) that may continue to replicate while water flow is restricted such that it is stagnant or low enough to facilitate perpetual prey availability. Feeding rates are not well studied in amphibians. Feeding patterns and digestion are influenced by the passage rate, that is, the time required for food to pass through the digestive tract. In frogs, food passage rates have been reported using different methodologies based on measuring the time from feeding to defecation at several temperatures [121], analyzing stomach contents [122], and measuring the passage of a specific marker consumed in the food [123]. Adult X. laevis fed a pelleted diet exhibit a passage rate of approximately 96 hours (A.B.-S. personal observations and unpublished data). Digestibility has been studied in X. laevis, where digestibility is defined as the proportion of food that is not excreted in the feces and hence presumed to have been absorbed by the animal [10]. Digestibility changes with physiological state and diet content. The use of digestibility data has become important to demonstrate the true availability of nutrients for animals [124]. In X. laevis, apparent digestibility values reported are 78.3% dry matter, 45% crude protein, and 81.3% crude fat, with direct association with food intake as the driver of nutrient utilization [73]. A digestion rate of 24 hours was reported for A. texanum fed 13 different species of invertebrates [125]. Food passage rates and the efficiency with which energy is assimilated have been directly related to temperature in other salamanders [68]. Cephalopods in research are fed either ad libitum or intermittently; however, reports of ad libitum feeding in the literature are inconsistent in its definition. Intermittent feeding varies by cephalopod species, with feeding shrimp as frequent as twice a day to O. vulgaris [126] to twice a week feeding of crab to S. officinalis [94, 127]. Additional studies are needed on cephalopods’ nutritional requirements, which would be expected to influence the feeding rate. There exists anecdotal evidence that it is impossible to overfeed cephalopods as they will reject excess food [94]. Ration The ration provided to zebrafish may depend on the number of fish in a tank, age and strain, and frequency of feeding. In aquaculture, it is common to feed based on percent body weight: 1–5% for adults and up to 300% for juveniles per day [15, 128, 129]. Obtaining an accurate estimate of total body mass in hundreds (or thousands) of zebrafish tanks, each with varying ages of fish, is difficult to achieve and track. For this reason, many facilities feed a known quantity based on tank size that is observed to meet the zebrafish’s needs. Often, this is based on the amount that the fish consume in 3 to 5 minutes and thus achieve satiation [6, 54, 128]. X. laevis may be fed 2 or 3 times per week, although infrequent feedings of a week or longer have been reported [81, 130]. Food intake is controlled by several neural, metabolic, and endocrine mechanisms [131]. The amount of food eaten by an adult X. laevis has a direct role in controlling metabolism and digestibility, including activating malonyl-CoA, an intermediate substrate activated in glucogenic diets [73]. In addition, malonyl-CoA signals fatty acid metabolism in free-range frogs [77]. Under experimental conditions of feeding 3 times a day for 20 min/d, adult X. laevis consume 7.2 ± 4.0 g/kg of metabolic body weight, as defined as total mass of metabolically active tissues [73]. Axolotl digestion and metabolism are relatively slow, so food can be offered from 2 to 4 times per week; they often regurgitate if overfed [132]. In the case of A. mexicanum, average food intakes of 500 mg per individual (as fed) were reported in animals eating diets containing blood worms and Daphnia sp [133]. The amount of feed provided to individual cephalopods will depend on their life stage, species fed, types of food (eg, shrimp vs crabs, live vs frozen), and water temperature [94, 134]. Systematic studies of nutritional requirements have been performed for O. vulgaris [135], Octopus tetricus [136], and S. officinalis [137]. The amount of food provided is usually represented as a percent of body weight, with a range of 5–8% being reported [94]. Sources of Experimental Variation From Diets The variability in the types of feeds, feeding regimes, feed ingredients, and nutritional value of feeds that are exhibited within the aquatic research animal community [54, 57] is of concern as it could affect experimental outcomes. These factors have been shown to affect numerous physiological aspects of zebrafish physiology, including inflammatory response, skeletal anomalies, incidence of neoplasia, obesity, gut structure, fatty acid content of embryos, survival, growth, reproductive output, gut microbiota, and fat content [11, 138–147]. The degree to which these factors may affect research outcomes has not been ascertained. Formulated and Live Diets The variability in the nutritional content of zebrafish feeds could be a leading factor in the issue of reproducibility of research results. Dietary products commonly used in zebrafish culture have been documented to contain protein levels ranging between 24% and 61% (% dry weight) [148, 149], lipids between 8.6% and 25.4% (% dry weight) [148], and omega-3 fatty acids from 4.4% to 39.6% (% of total lipids) [149, 150]. Potential sources of the nutritional variation include the variety of live diets used (Artemia, copepods, rotifers, Paramecia), enrichment protocols used to culture live diets, differences in feed formulations, and storage conditions of feeds. Published nutritional data on formulated feeds are limited. The nutrient content of formulated feeds supplied by some manufacturers is often vague data regarding terms such as “protein no less than 53%” or “crude fat no less than 16%,” but the actual nutritional content of those feeds is not given. This variability, however, is understandable as most of these diets are manufactured for the aquaculture industry, which is less concerned about specific levels of nutrients as opposed to exceeding an animal’s specific nutritional requirements [6]. Live and formulated feeds each have positive and negative aspects. As an example, once placed in water, the nutrients in pelleted food begin to leach out and become unavailable to the animal [6]. Thus, a pellet that is consumed at the end of a feeding episode, sometimes minutes later, will have fewer water-soluble vitamins such as vitamin C, choline, folic acid, and vitamin B6 than one that is consumed initially [151, 152]. Within the same time frame, the nutrient content in live feeds remains consistent. However, some formulated feeds are subject to microencapsulation during manufacturing to limit leaching. Microencapsulated feeds have an outer layer that surrounds each pellet, which eliminates or reduces nutrient leaching [152]. Therefore, the degree of leaching is quite variable between feed types. Though a known quantity of feed is administered to a tank of animals, not all of it may be consumed. Feed characteristics and tank design can determine how long the feed remains available to the animal. Formulated feed comes in floating or sinking forms and, depending on the water flow characteristics of a tank, can be washed out before animals have a chance to consume it. Sinking feed can be quickly removed if tank affluent exists at or near the bottom of the tank. This can be problematic as most zebrafish, X. laevis, and axolotl recirculating and flow-through commercial housing systems have a baffle or siphon designed to remove water from the bottom of the tank. Floating feed can be quickly removed if water leaves near the surface of the tank, as occurs when tank levels are high and water overflows through holes or slots. For example, the same quantity of feed delivered to tanks in 2 different facilities exhibit different quantities of consumption due to differences in tank hydrodynamics, type of feed, water flow rate, tank manufacturer, or cleanliness of the baffle. Live feeds can also be susceptible to quick removal. Once distributed, live feeds are generally thought to be free swimming and evenly distributed throughout the tank. However, Artemia and rotifers (Branchionus plicatilis) commonly fed to zebrafish are euryhaline organisms susceptible to physiological shock or death when placed immediately into a freshwater environment. When this occurs, live prey tends to stay on or near the bottom of the tank and is susceptible to quick removal as described for some formulated feeds. To avoid osmotic shock, it is recommended that rotifers be placed in 3–5 ppt water for 10–20 minutes before they are fed to zebrafish [153]. Anecdotally, it is worth noting that some zebrafish laboratories turn the water flow off during feeding to increase retention time of diets. Live diet can also impact study reproducibility and model consistency of aquatic animal models as their provision can result in (1) the transfer of the live diet microbiota to that of the model’s and (2) the inadvertent introduction of pathogens, including bacteria, nematodes, fungus, algae, and bryozoan species, to the environment and/or the animal. Aside from potentially significant morbidity and mortality caused by microbial contamination, study reproducibility is impacted by infections. Microbial infections have the potential to affect every host system and can have variable effects based on type and strain of microbe, the environment, and status of the host (life stage, stressed, etc.) [154, 155]. Artemia, Paramecium, and rotifers experimentally infected with Mycobacterium marinum and M. chelonae can transmit and establish infections in zebrafish provided these contaminated live feeds [156, 157]. Mycobacteria spp. have also been identified in rotifers during a mycobacteriosis outbreak in a research zebrafish facility [158] and in Artemia diets held in ornamental fish facilities [159]. In addition to the potential of causing significant clinical disease [160] and research variability, M. marinum is a zoonotic agent responsible for fish tank granuloma [161]. The microbiota of both Artemia and rotifers have been reported, and there is some evidence to suggest that some of these bacteria will colonize larval fish [162]. Vibrio spp. have been isolated from Artemia, with Vibrio alginolyticus, a fish pathogen, occurring in two-thirds of those isolated [163–165]. To mitigate these risks, researchers are actively pursuing prepared diets for zebrafish [2, 6, 73, 128, 166–168]. Amphibians are fed a variety of live and raw diets, including worms, insects, snails, young field mice, lizards, and small invertebrates. Historically, research Xenopus spp. have been fed organ meat. Raw meat and organs have been associated with Chlamydophila spp. outbreaks and may be contaminated with Salmonella. [80, 169–172]. In addition, Salmonella has been identified within and on the outside of lesser mealworm beetles (Alphitobius diaperinus) [173], although transmission to amphibians has not been documented. Research facilities utilizing live invertebrate diets for amphibians will often feed, or “gut load,” those invertebrates with a vitamin-mineral–rich diet [80, 174]. The diets fed to invertebrates can vary and may include mash for laying hens, rodent pellets, crushed dog food, fruits, vegetables, and/or commercially available gut-load diets used by hobbyists [80]. Some institutions sprinkle live diets with calcium powder, a practice intended to enrich insects, like crickets, that may be of poor nutritional quality. The variability in the nutrient value of invertebrates provided to an amphibian diet can contribute to experimental reproducibility. Recent studies reveal that crayfish (Procambarus spp. and Orconectes virilis) are natural hosts of and can be experimentally infected with Batrachochytrium dendrobatidis (Bd) fungus [175]. Chytridiomycosis caused by Bd is responsible for causing extreme population declines in wild amphibians [176]. The route of transmission for Bd is considered to be direct by shedding directly from infected animals or through motile waterborne zoospores [177]. There is some concern that infected crayfish, when used as feed for salamanders, may serve as a source of infection [175]; however, this possibility requires additional study [177]. Recommendations made by zoos for sourcing live diets include culturing live food on-site or utilizing commercial suppliers with clean facilities that use high-quality materials and that source diets reared indoors without exposure to pests [178]. In cephalopods, a digestive tract protozoal parasite, Aggregata octopiana, is considered to be the main epizootic agent of O. vulgaris in the wild and reared in the laboratory. A. octopiana-infected crustaceans used as live diets may inadvertently infect research cephalopods [179]. In infected O. vulgaris, A. octopiana is found in the esophagus, crop, intestine and cecum, gills, and mesentery of the digestive gland and gonads. In these tissues, cellular hypertrophy with inflammation, phagocytosis, ulceration, and destruction of organ architecture was noted [180]. Enzyme function studies indicate that a O. vulgaris infected with A. octopiana may suffer from malabsorption syndrome [181]. While it is unlikely crustaceans will be completely eliminated from the diets of all research cephalopods, the development of specific pathogen-free crustaceans would mitigate the risk of introduction of infectious agents and subsequent experimental variability resulting from infection [93, 182]. The impacts of microbiological contamination of live diets are summarized in Table 1. The effects of microorganisms on microbiota/microbiome research are covered later in this review. Table 1. Summary of Microbiological Contamination of Live Diets of Aquatic Species Microbiological Agent . Clinical Effect . Research Affect . Affected Species Documented . Mycobacteria spp [156–159] Subclinical/clinical disease; lethargy, decreased fecundity; zoonotic Death; documented impact on carcinogenicity, immunology, inflammation studies Zebrafish [1] [56–158]; ornamental fish [159] Vibrio alginolyticus [163–165] Opportunistic or pathogenic (species-dependent); septicemia, hemorrhage, dark skin, ulcers Death; possible impact on immunology studies Gilt-head sea bream (Sparus aurata), [163] juvenile turbot (Scophthalmus Maximus) [164, 165] Chlamydophila spp. (raw beef liver) [80, 169–172] Mass mortalities associated with C. psittaci; subclinical with C. suis and C abortus; pneumonia, sepsis, coelomic distention, red leg; zoonotic Death; possible impact on immunology and oncology studies Xenopus laevis, [171, 172] Western clawed frog (Silurana tropicalis) Salmonella spp [80, 169, 173] Subclinical or clinical disease; lethargy, anorexia, diarrhea, enteritis, septicemia; zoonotic Death and morbidity; possible impact on immunology, infectious studies Frogs, newts, toads Aggregata octopiana [179–181] Clinical disease; malabsorption syndrome, GI tract detrimentally impacted, loss of intestinal/cecal epithelium Death; possible impact on immunology, GI, nutrition studies Common octopus (Octopus vulgaris) Microbiological Agent . Clinical Effect . Research Affect . Affected Species Documented . Mycobacteria spp [156–159] Subclinical/clinical disease; lethargy, decreased fecundity; zoonotic Death; documented impact on carcinogenicity, immunology, inflammation studies Zebrafish [1] [56–158]; ornamental fish [159] Vibrio alginolyticus [163–165] Opportunistic or pathogenic (species-dependent); septicemia, hemorrhage, dark skin, ulcers Death; possible impact on immunology studies Gilt-head sea bream (Sparus aurata), [163] juvenile turbot (Scophthalmus Maximus) [164, 165] Chlamydophila spp. (raw beef liver) [80, 169–172] Mass mortalities associated with C. psittaci; subclinical with C. suis and C abortus; pneumonia, sepsis, coelomic distention, red leg; zoonotic Death; possible impact on immunology and oncology studies Xenopus laevis, [171, 172] Western clawed frog (Silurana tropicalis) Salmonella spp [80, 169, 173] Subclinical or clinical disease; lethargy, anorexia, diarrhea, enteritis, septicemia; zoonotic Death and morbidity; possible impact on immunology, infectious studies Frogs, newts, toads Aggregata octopiana [179–181] Clinical disease; malabsorption syndrome, GI tract detrimentally impacted, loss of intestinal/cecal epithelium Death; possible impact on immunology, GI, nutrition studies Common octopus (Octopus vulgaris) Open in new tab Table 1. Summary of Microbiological Contamination of Live Diets of Aquatic Species Microbiological Agent . Clinical Effect . Research Affect . Affected Species Documented . Mycobacteria spp [156–159] Subclinical/clinical disease; lethargy, decreased fecundity; zoonotic Death; documented impact on carcinogenicity, immunology, inflammation studies Zebrafish [1] [56–158]; ornamental fish [159] Vibrio alginolyticus [163–165] Opportunistic or pathogenic (species-dependent); septicemia, hemorrhage, dark skin, ulcers Death; possible impact on immunology studies Gilt-head sea bream (Sparus aurata), [163] juvenile turbot (Scophthalmus Maximus) [164, 165] Chlamydophila spp. (raw beef liver) [80, 169–172] Mass mortalities associated with C. psittaci; subclinical with C. suis and C abortus; pneumonia, sepsis, coelomic distention, red leg; zoonotic Death; possible impact on immunology and oncology studies Xenopus laevis, [171, 172] Western clawed frog (Silurana tropicalis) Salmonella spp [80, 169, 173] Subclinical or clinical disease; lethargy, anorexia, diarrhea, enteritis, septicemia; zoonotic Death and morbidity; possible impact on immunology, infectious studies Frogs, newts, toads Aggregata octopiana [179–181] Clinical disease; malabsorption syndrome, GI tract detrimentally impacted, loss of intestinal/cecal epithelium Death; possible impact on immunology, GI, nutrition studies Common octopus (Octopus vulgaris) Microbiological Agent . Clinical Effect . Research Affect . Affected Species Documented . Mycobacteria spp [156–159] Subclinical/clinical disease; lethargy, decreased fecundity; zoonotic Death; documented impact on carcinogenicity, immunology, inflammation studies Zebrafish [1] [56–158]; ornamental fish [159] Vibrio alginolyticus [163–165] Opportunistic or pathogenic (species-dependent); septicemia, hemorrhage, dark skin, ulcers Death; possible impact on immunology studies Gilt-head sea bream (Sparus aurata), [163] juvenile turbot (Scophthalmus Maximus) [164, 165] Chlamydophila spp. (raw beef liver) [80, 169–172] Mass mortalities associated with C. psittaci; subclinical with C. suis and C abortus; pneumonia, sepsis, coelomic distention, red leg; zoonotic Death; possible impact on immunology and oncology studies Xenopus laevis, [171, 172] Western clawed frog (Silurana tropicalis) Salmonella spp [80, 169, 173] Subclinical or clinical disease; lethargy, anorexia, diarrhea, enteritis, septicemia; zoonotic Death and morbidity; possible impact on immunology, infectious studies Frogs, newts, toads Aggregata octopiana [179–181] Clinical disease; malabsorption syndrome, GI tract detrimentally impacted, loss of intestinal/cecal epithelium Death; possible impact on immunology, GI, nutrition studies Common octopus (Octopus vulgaris) Open in new tab Contaminants in Feeds There is a legitimate concern that manufactured and live feeds could be contaminated with deleterious compounds that would affect animal health and research outcomes. Manufactured feeds have been known to contain deleterious compounds due to natural or human-sourced toxins via feed ingredients [129]. The impacts of chemical contamination of diets are summarized in Table 2. Table 2. Summary of Chemical Contaminants Found in Diets of and Its Effects on Aquatic Species Contaminants . Physiological Effect . Research Effect . Affected Species Documented . Heavy metals and persistent organic pollutants Chromium accumulation [183, 290] Clinical disease; documented 100% larval mortality and orange-colored embryos, reduction in fecundity Death; possible impact on oncology, embryonic development, toxicology, neurology studies Zebrafish [183], juvenile rock fish (Sebastes schlegelii) [290] Pesticides (glycophyosate, endosulfan, toxaphene) [184–187] Unknown clinical presentation, likely subclinical Possible impact on oncology and toxicology studies Rats Antimetabolites Trypsin inhibitors [188–190] Interferes with protein digestion, decreased growth Possible impact on nutrition, physiology studies Carp, channel catfish (Ictalurus punctatus), rainbow trout (Oncorhynchus mykiss), Phytic acids [188] Binds to calcium, magnesium, and zinc; suppresses growth; limits thyroid function; promotes cataracts Possible impact on nutrition, physiology, immunology, and ophthalmologic studies Salmonids, Chinook salmon (Oncorhynchus tshawytscha) Gossypol [193, 194] Binds to lysine, causes histological changes in liver and kidney, inhibits growth Possible impact on nutrition, physiology, metabolism, GI/renal studies Rainbow trout [193], young channel catfish [194] Endocrine disruption compounds in diets Genistein and daidzein in diet [197] Plasma vitellogenin levels increased, possible inhibition of testicular growth Possible impact to in vivo screening assays for endocrine disruptors, reproductive studies Goldfish (Carassius auratus) Estradiol in diet [198] Hypertrophic, hyperlipemic livers Possible impact on in vivo screening assays for endocrine disruptors, reproductive, metabolism studies Siberian sturgeon (Acipenser baeri) Genistein in water [199–202] Induces apoptosis, activates estrogen receptors, skews sex ratios, affects blood vessel formation, increases embryo malformation Possible impact on in vivo screening assays for endocrine disruptors, reproductive, developmental, metabolism studies Zebrafish Toxins Aspergillus flavus (Aflatoxin B1) [188, 203] Epizootic outbreak of liver cancer; hepatic necrosis, brachial edema, hemorrhage Death; possible impact on oncology, metabolism, physiology, immunology studies Rainbow trout Oxalate toxicity [205, 206] Urinary disease; renal calculi Possible impact on physiology, metabolism, nephrology studies American bullfrogs (Lithobates catesbeianus), [206] relict leopard frog (Rana onca) Shellfish toxins [94, 207–209] No clinical disease; toxin accumulation in digestive gland and brain Possible impact on neurology, behavior studies Common octopus (Octopus vulgaris) Nitrosamine (N-nitrosodiethylamine) [143, 258, 259] Hepatocellular carcinoma, spongiosis hepatitis, hepatic vacuoles Possible impact on oncology, nutrition, toxicology studies Medaka (Oryzias latipes) Contaminants . Physiological Effect . Research Effect . Affected Species Documented . Heavy metals and persistent organic pollutants Chromium accumulation [183, 290] Clinical disease; documented 100% larval mortality and orange-colored embryos, reduction in fecundity Death; possible impact on oncology, embryonic development, toxicology, neurology studies Zebrafish [183], juvenile rock fish (Sebastes schlegelii) [290] Pesticides (glycophyosate, endosulfan, toxaphene) [184–187] Unknown clinical presentation, likely subclinical Possible impact on oncology and toxicology studies Rats Antimetabolites Trypsin inhibitors [188–190] Interferes with protein digestion, decreased growth Possible impact on nutrition, physiology studies Carp, channel catfish (Ictalurus punctatus), rainbow trout (Oncorhynchus mykiss), Phytic acids [188] Binds to calcium, magnesium, and zinc; suppresses growth; limits thyroid function; promotes cataracts Possible impact on nutrition, physiology, immunology, and ophthalmologic studies Salmonids, Chinook salmon (Oncorhynchus tshawytscha) Gossypol [193, 194] Binds to lysine, causes histological changes in liver and kidney, inhibits growth Possible impact on nutrition, physiology, metabolism, GI/renal studies Rainbow trout [193], young channel catfish [194] Endocrine disruption compounds in diets Genistein and daidzein in diet [197] Plasma vitellogenin levels increased, possible inhibition of testicular growth Possible impact to in vivo screening assays for endocrine disruptors, reproductive studies Goldfish (Carassius auratus) Estradiol in diet [198] Hypertrophic, hyperlipemic livers Possible impact on in vivo screening assays for endocrine disruptors, reproductive, metabolism studies Siberian sturgeon (Acipenser baeri) Genistein in water [199–202] Induces apoptosis, activates estrogen receptors, skews sex ratios, affects blood vessel formation, increases embryo malformation Possible impact on in vivo screening assays for endocrine disruptors, reproductive, developmental, metabolism studies Zebrafish Toxins Aspergillus flavus (Aflatoxin B1) [188, 203] Epizootic outbreak of liver cancer; hepatic necrosis, brachial edema, hemorrhage Death; possible impact on oncology, metabolism, physiology, immunology studies Rainbow trout Oxalate toxicity [205, 206] Urinary disease; renal calculi Possible impact on physiology, metabolism, nephrology studies American bullfrogs (Lithobates catesbeianus), [206] relict leopard frog (Rana onca) Shellfish toxins [94, 207–209] No clinical disease; toxin accumulation in digestive gland and brain Possible impact on neurology, behavior studies Common octopus (Octopus vulgaris) Nitrosamine (N-nitrosodiethylamine) [143, 258, 259] Hepatocellular carcinoma, spongiosis hepatitis, hepatic vacuoles Possible impact on oncology, nutrition, toxicology studies Medaka (Oryzias latipes) GI, gastrointestinal. Open in new tab Table 2. Summary of Chemical Contaminants Found in Diets of and Its Effects on Aquatic Species Contaminants . Physiological Effect . Research Effect . Affected Species Documented . Heavy metals and persistent organic pollutants Chromium accumulation [183, 290] Clinical disease; documented 100% larval mortality and orange-colored embryos, reduction in fecundity Death; possible impact on oncology, embryonic development, toxicology, neurology studies Zebrafish [183], juvenile rock fish (Sebastes schlegelii) [290] Pesticides (glycophyosate, endosulfan, toxaphene) [184–187] Unknown clinical presentation, likely subclinical Possible impact on oncology and toxicology studies Rats Antimetabolites Trypsin inhibitors [188–190] Interferes with protein digestion, decreased growth Possible impact on nutrition, physiology studies Carp, channel catfish (Ictalurus punctatus), rainbow trout (Oncorhynchus mykiss), Phytic acids [188] Binds to calcium, magnesium, and zinc; suppresses growth; limits thyroid function; promotes cataracts Possible impact on nutrition, physiology, immunology, and ophthalmologic studies Salmonids, Chinook salmon (Oncorhynchus tshawytscha) Gossypol [193, 194] Binds to lysine, causes histological changes in liver and kidney, inhibits growth Possible impact on nutrition, physiology, metabolism, GI/renal studies Rainbow trout [193], young channel catfish [194] Endocrine disruption compounds in diets Genistein and daidzein in diet [197] Plasma vitellogenin levels increased, possible inhibition of testicular growth Possible impact to in vivo screening assays for endocrine disruptors, reproductive studies Goldfish (Carassius auratus) Estradiol in diet [198] Hypertrophic, hyperlipemic livers Possible impact on in vivo screening assays for endocrine disruptors, reproductive, metabolism studies Siberian sturgeon (Acipenser baeri) Genistein in water [199–202] Induces apoptosis, activates estrogen receptors, skews sex ratios, affects blood vessel formation, increases embryo malformation Possible impact on in vivo screening assays for endocrine disruptors, reproductive, developmental, metabolism studies Zebrafish Toxins Aspergillus flavus (Aflatoxin B1) [188, 203] Epizootic outbreak of liver cancer; hepatic necrosis, brachial edema, hemorrhage Death; possible impact on oncology, metabolism, physiology, immunology studies Rainbow trout Oxalate toxicity [205, 206] Urinary disease; renal calculi Possible impact on physiology, metabolism, nephrology studies American bullfrogs (Lithobates catesbeianus), [206] relict leopard frog (Rana onca) Shellfish toxins [94, 207–209] No clinical disease; toxin accumulation in digestive gland and brain Possible impact on neurology, behavior studies Common octopus (Octopus vulgaris) Nitrosamine (N-nitrosodiethylamine) [143, 258, 259] Hepatocellular carcinoma, spongiosis hepatitis, hepatic vacuoles Possible impact on oncology, nutrition, toxicology studies Medaka (Oryzias latipes) Contaminants . Physiological Effect . Research Effect . Affected Species Documented . Heavy metals and persistent organic pollutants Chromium accumulation [183, 290] Clinical disease; documented 100% larval mortality and orange-colored embryos, reduction in fecundity Death; possible impact on oncology, embryonic development, toxicology, neurology studies Zebrafish [183], juvenile rock fish (Sebastes schlegelii) [290] Pesticides (glycophyosate, endosulfan, toxaphene) [184–187] Unknown clinical presentation, likely subclinical Possible impact on oncology and toxicology studies Rats Antimetabolites Trypsin inhibitors [188–190] Interferes with protein digestion, decreased growth Possible impact on nutrition, physiology studies Carp, channel catfish (Ictalurus punctatus), rainbow trout (Oncorhynchus mykiss), Phytic acids [188] Binds to calcium, magnesium, and zinc; suppresses growth; limits thyroid function; promotes cataracts Possible impact on nutrition, physiology, immunology, and ophthalmologic studies Salmonids, Chinook salmon (Oncorhynchus tshawytscha) Gossypol [193, 194] Binds to lysine, causes histological changes in liver and kidney, inhibits growth Possible impact on nutrition, physiology, metabolism, GI/renal studies Rainbow trout [193], young channel catfish [194] Endocrine disruption compounds in diets Genistein and daidzein in diet [197] Plasma vitellogenin levels increased, possible inhibition of testicular growth Possible impact to in vivo screening assays for endocrine disruptors, reproductive studies Goldfish (Carassius auratus) Estradiol in diet [198] Hypertrophic, hyperlipemic livers Possible impact on in vivo screening assays for endocrine disruptors, reproductive, metabolism studies Siberian sturgeon (Acipenser baeri) Genistein in water [199–202] Induces apoptosis, activates estrogen receptors, skews sex ratios, affects blood vessel formation, increases embryo malformation Possible impact on in vivo screening assays for endocrine disruptors, reproductive, developmental, metabolism studies Zebrafish Toxins Aspergillus flavus (Aflatoxin B1) [188, 203] Epizootic outbreak of liver cancer; hepatic necrosis, brachial edema, hemorrhage Death; possible impact on oncology, metabolism, physiology, immunology studies Rainbow trout Oxalate toxicity [205, 206] Urinary disease; renal calculi Possible impact on physiology, metabolism, nephrology studies American bullfrogs (Lithobates catesbeianus), [206] relict leopard frog (Rana onca) Shellfish toxins [94, 207–209] No clinical disease; toxin accumulation in digestive gland and brain Possible impact on neurology, behavior studies Common octopus (Octopus vulgaris) Nitrosamine (N-nitrosodiethylamine) [143, 258, 259] Hepatocellular carcinoma, spongiosis hepatitis, hepatic vacuoles Possible impact on oncology, nutrition, toxicology studies Medaka (Oryzias latipes) GI, gastrointestinal. Open in new tab Heavy Metals and Persistent Organic Pollutants Live feeds are susceptible to bioaccumulation of heavy metals and other pollutants. A recent report described near 100% larval mortality and orange-colored embryos in zebrafish fed contaminated Artemia [183]. Incidents of feed contaminants resulting in lethality, although catastrophic, are relatively rare. However, contamination may be unknowingly common as most sublethal effects are not monitored, zebrafish feeds are not typically tested for contaminants, and the dietary concentrations of contaminants that result in sublethal effects are unknown. Although information regarding the effects of oral consumption of contaminants is limited, we know of some feed contaminants that could be present in animal feeds and are aware of the toxicological effects that those compounds can have on aquatic animals via waterborne exposure. Fish meal and oil are perhaps the most commonly used ingredients in fish feeds, the source of which is often pelagic marine fishes [129]. Persistent organic pollutants and heavy metals are known to accumulate in aquatic animals, and therefore both are potential contaminants in fish feeds. Persistent organic pollutants, including pesticides such as glyphosate, endosulfan, and toxaphene, have been detected in companion animal feeds, rodent chow, and fish feed [184–187]. In most incidences, the contamination level is well below what is considered acceptable for human consumption; however, it is unclear if these levels could affect certain research outcomes in aquatic laboratory animals. Within the food-fish industry, it is thought, likely incorrectly, that the risk of heavy metal exposure via feed consumption is relatively low [188]. Recent chromium contamination events at the University of Minnesota and the University of Utah [183] suggest this may not be the case for aquatic laboratory animals. Furthermore, heavy metal concentrations in fish feed may not affect growth or mortality in fish destined for human consumption but may be affecting aquatic laboratory animals in ways that taint research results. Antimetabolites Most manufactured fish feeds also contain plant-based ingredients. Many plant feedstuffs contain antimetabolites that interfere with various metabolic processes in fish. One group of antimetabolites are trypsin inhibitors, which are prevalent in soybeans and are known to interfere with protein digestion and have been reported to decrease growth in multiple fish species [188]. Fortunately, trypsin inhibitors can be inactivated with proper heating during the manufacturing process, but overheating can lower the nutritional value of the diet, particularly lysine levels [189, 190]. Thus, there is a fine balance between too little and too much heat, and the optimal heat treatment can vary between species [188]. Phytic acid, another antimetabolite, is found in most cereal products, including soybean, rapeseed, and cottonseed. Phytic acid can bind to minerals such as calcium, magnesium, and zinc, limiting bioavailability to fish and resulting in mineral deficiencies [188]. Studies in salmonids concluded that high levels of phytates suppress growth, limit thyroid function, and promote cataract formation in chinook salmon and rainbow trout [191, 192]. Gossypol is a yellow phenolic pigment prevalent in cottonseed that preferentially binds to lysine and has been found to cause histological changes in the liver and kidney in rainbow trout at a concentration as low as 95 ppm [193]. It was also found that growth was inhibited in catfish that were fed a diet containing gossypol levels above 0.09% [194]. Sensitivity to gossypol varies by species, [188] and the degree of sensitivity in zebrafish has yet to be determined. There are many other antimetabolites, including lectins, saponins, and other enzyme inhibitors, that could also be a source of experimental variation in aquatic laboratory animals. Phytoestrogen Compounds: Endocrine Disruptors Phytoestrogen compounds are known to be present in many common feedstuffs [195]. Examples of phytoestrogens include genistein, biochanin A, coumestrol, and daidzein. A study conducted by Matsumoto et al [196] showed the presence of estrogenic activity in several commercial fish feeds, including some that are fed to laboratory fish. The effects these phytoestrogen-containing diets have on species are unknown. However, there is some information regarding dietary phytoestrogen effects on other fish species. Plasma vitellogenin levels in goldfish (Carassius auratus), a species in the same family as zebrafish, were shown to increase when fish were fed diets containing phytoestrogens [197]. Siberian sturgeon (Acipenser baeri) exhibited hypertrophic and hyperlipidemic livers when fed commercial diets containing estradiol [198]. Although there is no information regarding dietary phytoestrogen exposure to zebrafish, there are several studies involving waterborne phytoestrogen exposure. As an example, genistein has been known to induce apoptosis, activate estrogen receptors, skew sex ratios, affect blood vessel formation, and increase incidences of malformation in zebrafish embryos [199–202]. Toxins Mycotoxins are secondary metabolites produced by various fungi that can contaminate feed ingredients or formulated feeds. Fungal contamination is often due to improper storage, particularly when ingredients or feeds are stored in areas with high heat and humidity [6]. The metabolites produced are potentially toxic and can cause severe health problems in fish [129]. The most well-studied mycotoxin is aflatoxin B1 (AFB1). AFB1 was first described in the 1960s when an epizootic outbreak of liver cancer occurred in rainbow trout (Oncorhynchus mykiss). Cottonseed meal contaminated with Aspergillus flavus was shown to be the source of this outbreak. Aspergillus contamination can also occur in other common fish feedstuffs such as corn, wheat, and rice [188]. Sensitivity to AFB1 varies between species, and zebrafish are reported to be more sensitive than others, with an LD50 (lethal dose, 50%) between 0.44 and 0.58 mg/kg [188]. Other acute toxic effects of AFB1 include hepatic necrosis, brachial edema, and hemorrhage [203]. The outbreak in rainbow trout has led to proactive monitoring of AFB1 in ingredients used for fish food [188]. Other mycotoxins of concern include aflatoxin B2, ochratoxin B1, and aflatoxin G1. Amphibians may be adversely affected by mycotoxin-contaminated insects, which are relatively resistant to the effects of this toxin [12, 204]. Oxalate toxicity has been observed in captive tadpoles and adult frogs when provided with crickets fed oxalate-rich plants, like spinach or kale [205, 206], resulting in renal calculi and urinary disease. As previously described, cephalopods are commonly fed live diets, including bivalve mollusks. Bivalves feed on phytoplankton, which may produce shellfish toxins. In particular, mammals ingesting shellfish may develop amnesic or paralytic shellfish poisoning, which manifests with neurological and gastrointestinal signs, respectively [94, 207–209]. Currently, there are no observed clinical effects of experimentally induced accumulation of shellfish toxins in cephalopod species. Damoic acid (DA) accumulates in the digestive gland and brains of O. vulgaris [208, 209]. DA acts as an analog of glutamate, an excitatory neurotransmitter. Further studies are needed to determine if cephalopods are neurologically or behaviorally impaired by DA and therefore would interfere with research aims using cephalopod animal models. Feed Additives Antioxidants Fish feeds often contain high levels of polyunsaturated fatty acids, which can be oxidized into aldehydes, ketones, and free radicals. These oxidized lipid products can lead to deficiencies in antioxidant vitamins such as carotenoids, vitamin C, and vitamin E [129]. Deficiencies in these vitamins have been known to result in liver degeneration, anemia, and abnormalities of the spleen [210]. In zebrafish, vitamin E-deficient diets have been shown to decrease the startle response, increase embryo mortality and deformities, and alter over 900 RNA transcripts in zebrafish embryos [211, 212]. Antioxidants are often added to oils or diets to limit oxidation [129, 152]; however, the quantity of antioxidants needed in the diet varies depending on species and quality of lipid used [188]. Synthetic Hormones Synthetic hormones have been used in aquaculture for the induction of spawning, increasing growth, and establishment of monosex populations. The US Food and Drug Administration does not allow their use in diets fed to fish cultured for human consumption [129]. However, regulations regarding feeds used for aquarium fish are less stringent. Hormones are often added to aquarium fish feeds to enhance the breeding colors or induce breeding of certain species. The effects these dietarily sourced hormones have on zebrafish are unknown. Research Areas Affected by Diet Aquatic animal models have been utilized in virtually every area of the biomedical research discipline. The following overview details the impacts that diet and nutrition may have on select research areas where aquatic models have been used. Digestive Physiology The digestive system comes in direct contact with and is the first system impacted by the animal’s diet. Across fish and amphibians, there are considerable differences in digestive tract anatomy and physiology. However, as with other areas of research, the development of the digestive tract in fish and amphibians is sufficiently similar to that occurring in other vertebrates, making then valuable models. Aquatic organisms have been used in a variety of studies involving the investigation of digestive physiology, ranging from comparative studies [213], nonalcoholic fatty liver disease [214], nutritional genomics [215–218], intestinal immunity [219–221], and developmental biology [222–225]. Gut morphology and physiology can be influenced directly by the diet, depending especially on the protein content and source. The morphology of the gut can vary considerably among fish species, those with or without stomachs, and those who develop stomachs as they age. Generally speaking, and not without exceptions, herbivorous fish have longer guts than those of omnivores and carnivores [226–228]. These trends are not only specific to the ontogeny of the species but also to the diet injected [229]. In a review of 32 cichlid species in Lake Tanganyika, an African Great Lake, investigators determined that intestine length was predicted by its trophic position or its position in the food chain [230]. In another study utilizing 4 different species of prickleback, fish native to the central California coast, there was evidence to support phenotypic plasticity in some species of prickleback that had increased relative gut length when placed on high-protein diets compared with natural herbivorous diets. Investigators also demonstrated evidence that ontogeny plays a greater role in gut size [226]. In a recent study, zebrafish were provided 1 of 4 isocaloric diets (ancestral, carnivore, omnivore, or herbivore) for 5 months. The diets varied primarily by protein and fiber contents. Zebrafish on a herbivorous diet had the longest gut, most intestinal epithelial surface area, and largest enterocyte volume as a result of hypertrophy (as opposed to hyperplasia). Zebrafish on the carnivorous diet were significantly heavier and longer than fish on other diets. Amylase activities in the gut were higher in fish fed omnivorous and herbivorous diets. Fish fed the omnivorous diet had significantly higher maltase and trypsin intestinal activity [147]. The development of novel transgenic LipoGlo zebrafish, which labels atherogenic lipoproteins (apolipoprotein-B) with luciferase, has demonstrated the influence of content on intestinal physiology [231]. Atherogenesis is stimulated in LipoGlo zebrafish larvae fed a high-lipid diet containing 4% (w/w) cholesterol. By 15 dpf, macrophages are recruited to the vasculature-stimulated inflammatory responses in larvae fed high-fat diets [221, 231, 232]. While there exists a substantial body of literature on the changes to digestive physiology during amphibian metamorphosis, [233] there is a dearth of research on digestive changes associated with diets [225, 234]. Two studies suggest that digestive physiology after metamorphosis is relatively resistant to change because dietary chemistries and sugar/amino acid transporter activity do not change in the face of dietary changes in Lithobates catesbeianus [235] and Bufo spinulosis [236]. Nonetheless, some studies have demonstrated that changes in diet, frequency of intake, and seasonality might impact the enzymatic activity as well as the morphology of the digestive tract [234, 236]. Cancer Zebrafish have been used extensively in cancer research and in the drug discovery process. Letrado et al (2018) found 355 case studies in which zebrafish were employed in cancer drug discovery, including investigating drugs targeting breast cancer, leukemia, lung cancer, melanoma, glioblastoma, colorectal cancer, and hepatocarcinoma, among others. Multiple strategies exist to generate zebrafish models of cancer, including mutagenesis (irradiation, chemical, and insertional) and transplant assays (allograft, xenograft, and orthograft) [154, 237–239]. Examples of mutant/transgenic zebrafish cancer models include melanoma [240, 241], hepatocellular carcinoma [242, 243], a variety of intestinal cancers [244], and brain tumors [245, 246]. The influence of diet on cancer risk has been long established in a variety of vertebrates [48, 247] and invertebrates [248, 249]. This relationship was recently demonstrated in a systematic study of melanoma-prone p53/BRAF zebrafish exposed to 1×, 2×, or 4× daily feeding of 60 mg of pelleted diet from 42 dpf. Diet was provided precisely by an automatic robot feeder system, and the fish number per tank remained constant throughout the study. Fish fed 4× daily had significantly increased rates of melanoma incidence, and tumors developed earlier than in fish fed 2× or 1× daily [250]. This result mimics the findings between obesity and melanoma formation/aggressiveness in humans and mouse models [251]. While the aforementioned studies describe the important relationship between calories consumed over the animal’s lifespan, diet composition can directly or indirectly affect neoplastic processes. In farmed carnivorous Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) at 4 different Norwegian farms studied over 3 years, investigators documented increased rates of intestinal tumors in fish fed plant-based commercial diet compared with non-plant–based diets [252]. While this study lacked strict controls and did not adequately account for dietary carcinogens, the investigators suggest that providing carnivorous salmonids a soy-based commercial diet is more likely to induce chronic intestinal inflammation that could lead to dysplasia and eventually carcinogenesis [253, 254]. There is evidence to suggest that saponin present in soybean meal is more likely to cause enteritis in Atlantic salmon than rainbow trout or zebrafish [255–257]. However, zebrafish larvae fed soybean meal do develop intestinal inflammation characterized by significantly increased neutrophil recruitment. In evaluations of both soy protein and soy saponin, soy saponin is associated with more inflammation [256]. Nitrosamines and nitrosamides contained within commercial fish foods are a plausible natural carcinogen. There are a variety of nitrosamines found in food. Exposure of Medaka (Oryzias latipes) to the nitrosamine N-nitrosodiethylamine led to concentration-dependent increases in spongiosis hepatitis, hepatic vacuoles, and, after 3 and 6 months, a significant increase in hepatocellular carcinoma [143, 258, 259]. To minimize the risk posed by nitrosamines to their carcinogenesis bioassays, scientists at the Gulf Coast Research Laboratory, Ocean Springs, Mississippi, arrange pretest fish meal to ensure acceptable levels of nitrosamines. A maximum level of 100 ppb is the limit for the most commonly occurring nitrosamine in fish meal (W. Hawkins, R. Overstreet, personal communication). In one retrospective analysis on 12 years of diagnostic zebrafish cases, spontaneous intestinal neoplasia prevalence was examined and tumors classified. During this period, increasing prevalence of intestinal neoplasia and associated pathology was noted, with the majority having subclinical preneoplastic or neoplastic changes. In the same study, investigators sought to replicate similar intestinal lesions by using the same diet that was fed by a laboratory with high rates of cancer. However, after 6 months of feeding, there were no preneoplastic or neoplastic intestinal changes, suggesting that other factors likely contributed to these lesions [260]. Host Microbiome Over the past decade with an increasing availability of molecular identification techniques, there has been a renaissance of research studying the trillion organisms making up the microbiome [261] to better understand its relationship with the development and maintenance of normal physiological functions such as digestion, immunity, and growth. In addition, its disruption has been associated with diseases like inflammatory bowel disease, diabetes, and obesity [261–263]. Amphibians and fish are colonized following hatching by microorganisms found on the chorion and in the water [262, 264–266]. Microbiome investigation has been reported in a wide range of fish and amphibian species such as rainbow trout, Atlantic salmon, Arctic charr (Salvelinus alpinus), Northern leopard frog (Lithobates pipiens) [267], X. laevis, and zebrafish [267–269]. The advent of the germ-free zebrafish has allowed for controlled studies of the effects of the microbiota and microbiome on the development of zebrafish larvae [270–273]. For example, germ-free zebrafish, compared with conventionally reared zebrafish, are significantly less able to absorb dietary fatty acids and form lipid droplets in intestinal epithelium and liver [274]. The amount of fat in the diet plays a significant role in the microbiota of the zebrafish. On one study, investigators fed high-fat (24%), low-fat (6%), and control diets (15%) to 5–70 dpf zebrafish. Using 16s rRNA sequencing, zebrafish intestinal microbiota rapidly diverged after feeding various diets and became increasingly different as zebrafish continued to grow, eventually resulting in distinct gut microbiota between groups [145]. In pet store-derived adult fish fed low-fat (8%) and high-fat (24%) diets for 8 weeks, differences in the microbiota composition emerged and were also sex dependent [275]. The protein and fat sources play an important role in influencing the intestinal microbiota. Rainbow trout fed either animal-sourced or plant-sourced diets demonstrated significant differences in the predominant phylum found in the intestinal tract. Fish provided carnivorous diets became Proteobacteria phylum-dominant vs those provided herbivorous diets, which had Firmicutes phylum-dominant intestinal tracts [276–278]. While dietary source plays a role in the microbial intestinal distribution, the species also determines microbiota diversity. In another study with 4 different naturally herbivorous, omnivorous, and carnivorous bream and carp species reared in the same environment and provided dried distillers grain, herbivorous fish possessed more bacterial species than the others [279]. Dietary carotenoids are utilized in some species of frogs to confer red, orange, and yellow colorations [280]. In addition, carotenoids are precursors to vitamin A and act as an antioxidant [281]. Captive red-eyed tree frogs (Agalychnis callidryas) fed carotenoid-enriched diets had significantly higher diversity and abundance of skin-associated bacteria [282]. This finding was also demonstrated in the Australian southern corroboree frog (Pseudophyrne corroboree), where frogs receiving dietary carotenoid supplementation had increased skin microbiota diversity and abundance. The mechanism for carotenoid-enhanced microbiota diversity has not been determined, but it has been suggested that carotenoids may enhance production of mucous in dermal mucous glands or alter the skin, making it more hospitable to bacteria. Aerobic bacteria may also directly utilize carotenoids for its antioxidant activity as a defense to the damaging effects of oxidative stress [283]. Future Considerations: Recommendations to Reduce Experimental Variability While this review describes the many sources of variability in the diets of aquatic species, momentum is building for the establishment of a standardized, open-formulated diet for zebrafish, although less so for other aquatic models. Establishing a standardized or defined reference diet for each species and each life stage requires significant investment of time and resources by the research community [6]. The “ideal” standardized diet [284] has been described as a diet that (1) provides the daily nutritional requirements, (2) promotes healthy growth, (3) promotes good egg production and viability, (4) contains defined ingredients that are consistent in quality, (5) produces animals that are consistent in metabolic profiles, and (6) does not induce morbidity. Experimental variability can be further reduced by making open formula diets (purified, semipurified, practical, etc.) for aquatic species available to researchers. These diets will allow researchers to carefully assess the influence of the dietary composition on their research model. As discussed in other articles of this journal series, reproducibility will be increased when investigators can directly compare their results with others in the field with the same model and with previous experiments. Similarly, journals must require full disclosure of diet composition provided to reported aquatic animal models. There exist a number of established reporting guidelines and checklists, including ARRIVE (Animal Research: Reporting of In Vivo Experiments) [285, 286], PREPARE (Planning Research and Experimental Procedures on Animals: Recommendations for Excellence) [287], and the GSPC (Gold Standard Publication Checklist) [288]. Recently, the International Council for Laboratory Animal Science compiled multiple guidelines to assemble a consensus guideline called the Harmonized Animal Research Reporting Principles [289]. However, in regards to the diet provided to animal models, these guidelines require type of diet to be described. Therefore, these guidelines can be further improved to require additional information in regards to nutrition in research animals. Ultimately, establishing reporting standards will promote scientific rigor and experimental reproducibility. 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TI - The Role of Feed in Aquatic Laboratory Animal Nutrition and the Potential Impact on Animal Models and Study Reproducibility
JF - ILAR Journal
DO - 10.1093/ilar/ilaa006
DA - 2019-12-31
UR - https://www.deepdyve.com/lp/oxford-university-press/the-role-of-feed-in-aquatic-laboratory-animal-nutrition-and-the-1g0u7fFi0f
SP - 197
EP - 215
VL - 60
IS - 2
DP - DeepDyve
ER -