Dietary protein and energy as determinants of food quality: trophic strategies compared
Stephen H. Bowen
INTRODUCTION
Fundamental differences in food quality are evident when major food resource categories are compared. Protein and energy are two nutrients of particular interest to ecologists that show these differences clearly. Protein and energy are two “macronutrients” required for animal metabolism and growth. In contrast to micronutrients like vitamins, minerals, and specific lipids, protein and substrates catabolized for energy must comprise most of the digestible matter in animal diets. Foods differ considerably in protein and energy content, both within and among food categories. Published data for food resources in aquatic environments provide examples [ILLUSTRATION FOR FIGURE 1 OMITTED]. Invertebrate prey are high in both protein and energy (Yurkowski and Tabachek 1979) [ILLUSTRATION FOR FIGURE 1 OMITTED]. Plant tissues are lower in energy since the majority of species use lower energy carbohydrates for both structural elements and energy storage (Boyd 1968, Platt and Irwin 1973). Algae contain more protein than macrophytes, presumably because macrophyte structure requires more carbohydrate fiber. The processes that produce organic detritus appear to consume both protein and energy relative to more refractory humic materials (Bowen 1979a, b, 1987a). These differences in protein and energy contents are ecologically significant inasmuch as consumer growth rate is expected to be directly proportional to nutrient level both within and among the ranges shown for food categories in Fig. 1 (Bowen 1984a, Hepher 1988, Halver 1989).
To better understand the relationship between consumers and their trophic resources, it would be useful to be able to predict consumer growth from protein and energy contents of the diet (Sinclair et al. 1981, Tenore 1981, Horn et al. 1986, Schroeder 1986, Fris and Horn 1993). The extant literature on dietary protein and energy has limited use in predicting growth of wild populations. With the goal of optimizing feeding practices in animal husbandry, typical experimental diets have been formulated to contain only the higher nutrient levels and do not represent diets of many omnivores, herbivores, and detritivores. In addition, most studies have treated protein and energy as independent variables, but it is unlikely that their effects are independent. Protein can be catabolized for energy, and energy can be used to synthesize about one-half the 21 amino acids used in growth and metabolism. In development of a model for predicting growth from dietary protein and energy, the possible effects of protein-energy interaction must be assessed. Finally, most experimental protocols have controlled energy intake by fixing the quantity of food supplied to experimental animals. This does not allow for appetite-based, compensatory adjustments in ingestion rate that can be expected in nature. The work reported here was intended to assess the effects of dietary protein and energy and their interaction on ingestion, assimilation, and growth in Tilapia aurea, an omnivorous fish (Spataru and Zorn 1978), as a model for predicting how these nutrients may affect the performance of fishes and other poikilotherms in the wild. Further, we hoped to be able to compare the significance of dietary protein and energy and their interaction as constraints to carnivory, herbivory, detritivory, and omnivory.
MATERIALS AND METHODS
Diet formulation. – We chose the randomized block factorial design to be analyzed by two-way analysis of variance (ANOVA) as a sensitive and efficient experimental design for assessing main effects of two variables and their interaction (Snedecor and Cochran 1980: Chapter 16). Sixteen artificial diets were prepared that contained all unique combinations of four levels of metabolizable energy (3. l, 6.7, 10.5, 14.1 kJ/g) and four levels of protein (3.0, 13.2, 23.2, 33.4 mg/ kJ ME). Metabolizable energy was used in the sense of “potential energy” (Jobling 1983:691) to formulate diets at each of four protein levels that provided consumers with the same potential energy per gram ingested. In making these calculations, we assumed assimilation efficiencies of 95, 95, and 75% (Hepher 1988: 308-309), and energy yield on catabolism of 17.3, 38.9, and 16.9 kJ/g (Brett and Groves 1979) for protein, lipid, and carbohydrate, respectively. Because protein, carbohydrate, and lipid differ considerably in the energy they provide a consumer, metabolizable energy units are necessary to achieve even intervals between treatments required for testing interaction. Protein levels are expressed in terms of the protein to energy ratio as has become standard practice (Hepher 1988).
Although protein and energy levels for experimental diets were chosen to simulate nutrient ranges in primary foods in the natural environment, prediction of growth in the wild requires careful choice of units. Assumptions required for estimation of metabolizable energy for artificial diets prepared from refined ingredients and fed under controlled conditions may not apply to natural diets obtained in the wild. Thus, comparison of the experimental diets to natural diets is more realistic if we use simpler terms involving fewer assumptions. We simplified description of experimental diets by using energy values for diet ingredients determined directly by bomb calorimetry. Accordingly, our experimental diets ranged from 2.7 to 26.5 mg protein per kilojoule assimilable energy, and from 4.1 to 18.7 kJ assimilable energy per gram where “assimilable energy” is the energy content of all diet ingredients that potentially can be digested, assimilated and used as an energy source by T. aurea (i.e., cellulose and mineral matter excluded (Stickney and Shumway 1974, Buddington 1979)). Described in these units, the ranges for experimental diets enclose the ranges for protein and gross energy found in natural primary food resources [ILLUSTRATION FOR FIGURE 1 OMITTED]. Most authors reporting energy values for natural foods from aquatic environments have not distinguished between gross and assimilable energy. Materials in natural diets that cannot be assimilated will reduce the range of assimilable energy values, and thus our experimental diets will similarly enclose the range of assimilable energy values that describe natural diets. Values for milligrams protein per kilojoule assimilable energy in natural foods will be greater than milligrams protein per kilojoule gross energy, but we expect the highest values for natural foods to fall well below the highest value in our experimental diets (26.5 mg/kJ assimilable energy) (Platt and Irwin 1973). Assumptions concerning the ability of T. aurea to assimilate nutrients from the diet were eliminated by measuring assimilation (ingestion minus egestion) directly.
Diet preparation. – Principal diet ingredients were purchased from U.S. Biochemical Corporation (USB) of Cleveland, Ohio. Vitamin free casein (USB number 12866) supplemented with 2% arginine (USB number 11490) was the protein source (all percentages by mass). The nonprotein energy source was 85% dextrin (USB number 14530) and 15% menhaden oil (USB number 34568). We calculated that the protein and non-protein source mixtures would both yield 16.5 kJ/g metabolizable energy. The protein to energy ratio was determined with combinations of the protein and energy mixtures that contained 5, 21.7, 38.3 and 55% protein. Assimilable energy was determined by addition of acid-washed cellulose (USB number 13293), which we expect not to be digested by T. aurea (Stickney and Shumway 1974, Buddington 1980) at 10, 33, 57, and 80% of total diet mass. “Vitamin Diet Supplements” (USB number 23431) and “AIN Mineral Mixture 76” (USB number 10664) added at 3.0 and 3.5% of the potentially assimilable ingredients, respectively, provided these nutrients at or above levels recommended for warmwater fishes (Post et al. 1977). Alganic acid (Sigma Chemical Corporation number A7128) was added at 1.5% as a binder. Preliminary tests showed this concentration produced diets that held together well, were readily ingested, and lost [less than]2% of potentially soluble ingredients in 8 h of exposure to water. Nearly all ingestion was accomplished in the first few hours following presentation of the food, with fish typically ingesting [greater than]50% of the food aliquot. Dissolution of diets may have affected ingestion estimates in that groups that ingested a smaller proportion of their food aliquot left more uneaten food exposed to leaching until the residue was recovered and dried at the end of 24 h. To the extent this was a factor, it would tend to reduce differences in ingestion reported below. Chromic oxide at 1% served as an undigested reference material for measurement of assimilation. Each diet was mixed with water to form a stiff dough, divided into aliquots for daily feeding, and frozen pending use.
Experiment protocol. – Juvenile T. aurea 1.1-4.8 g live mass were purchased from Lake Geneva Fisheries, Geneva, Alabama. After 7 d of acclimation to laboratory conditions, they were starved for 24 h to clear their guts, weighed, and assigned at random to 20-L aquaria at six per aquarium. This density appeared to minimize aggressive interactions. A total of 64 aquaria were used to provide four replicate groups for each of the 16 diets. A common recirculating water source supplied each of 64 aquaria, and water was passed through a series of two, 60-L gravel and sand filters 7 times each 24 h. A fine mesh net removed waste particles before water entered the filters. Biofilm was scraped from the aquaria weekly, and visible particles were siphoned from the bottom at 3- or 4-d intervals. Fluorescent lights provided a 14 h light, 10 h dark cycle. Daily temperature ranged from 20 [degrees] to 26 [degrees] C, with an average of 23.7 [degrees] C.
Diets were assigned to aquaria at random with four replicate aquaria per diet. Starting at [approximately equal to]0900, uneaten food from the previous day was removed and dried at 50 [degrees] C. An aliquot of diet that had thawed under refrigeration during the previous day was weighed and then immersed in Ca[Cl.sub.2] solution to activate the binding capacity of alganic acid. Diets were supplied in excess of fish consumption.
The fish were fed daily for 42 d. Animals that died were weighed and replaced with individuals of known mass. Those that replaced fish that died within the first 10 d were treated the same as members of the starting group. Those that died after the first 10 d were replaced by fish marked with a fin clip, and these were excluded in subsequent performance measures. The total mortality rate of 12% at the end of 42 d was due in part to aggressive behavior.
Feces were collected daily from each aquarium during the last week of the experiment, and dried at 50 [degrees] C. On day 43, individual fish were weighed, and then lyophilized to determine water content. Lipid content was determined gravimetrically by extraction with hexanes, and the residue was homogenized by grinding in a Wiley mill. Ash content was determined as residue after combustion of a subsample at 550 [degrees] C to constant mass. Protein content was estimated as fresh mass minus the masses of water, lipid, and ash. Chromic oxide in diets and feces was measured calorimetrically and assimilation calculated as described by Furukawa and Tsukahara (1966). Energy content of the diet and feces was determined in triplicate using a Phillipson type micro-bomb calorimeter calibrated with benzoic acid. Protein in feces was measured using the Lowery assay (Kaushik and Hynes 1968).
Growth was expressed as the specific growth rate (SGR),
SGR = (ln [M.sub.t42] – ln [M.sub.t0])[multiplied by]42 [d.sup.-1],
where [M.sub.t0] and [M.sub.t42] are mass at the start and the end of the 42-d growth period, respectively (Ricker 1979). When multiplied by 100, SGR is equivalent to percent mass gain per day. Daily ingestion was calculated as mass eaten each day per mass of fish, with fish mass estimated for each experiment day from the group starting mass ([M.sub.t0]), SGR, and any changes in group mass that may have resulted from replacement of dead fish.
Statistical analyses were conducted using Statgraphics Version 5 (STSC, Rockville, Maryland), and response surfaces were fitted using Surfer, Version 4 (Golden Software, Golden, Colorado). Results are presented using two sets of units. For statistical analyses, diet formulation values defined protein and energy treatment levels in two-way ANOVA using Type I sums of squares (Table 1) and Tukey’s Honestly Significant Difference multiple range analyses (hsd, 95% confidence level). For comparisons to diets of fish in the wild, cell means [+ or -] 95% confidence intervals are plotted as a function of assimilable (noncellulose) energy (kilojoules per gram dry mass) and protein per assimilable energy (milligrams per kilojoule) as discussed above.
RESULTS
Components of consumer response
Ingestion rate for individual groups ranged from 0.009 to 0.131 g dry mass of diet per gram fish live mass per day. Protein level, metabolizable energy level, and their interaction all affected ingestion (Table 1). For all protein levels, ingestion increased with decreasing energy level [ILLUSTRATION FOR FIGURE 2 OMITTED]. The principal effect of protein level was that ingestion was much reduced at the lowest protein level.
The ingestion response to diet quality largely compensated [TABULAR DATA FOR TABLE 1 OMITTED] for differences in diet energy. Energy assimilation rate varied little across the four energy levels (Table 1, [ILLUSTRATION FOR FIGURE 3a OMITTED]). Tukey’s hsd multiple range analysis by protein level showed energy assimilation rate for the lowest energy diets and for the highest energy diets in the same homogeneous group. In contrast, ingestion did not compensate for diet protein level [ILLUSTRATION FOR FIGURE 3b OMITTED]. Protein assimilation rate was directly proportional to protein level in the diet within each energy level. Of the response variables studied, protein assimilation rate was most significantly affected by protein-energy interaction (Table 1). At 26.5 mg/kJ, protein assimilation decreased with decreasing energy level. In contrast, at 11.1 mg/kJ, protein assimilation increased with decreasing energy level until the lowest level.
Growth responses to diets can be summarized in three groups. For animals fed protein levels [greater than or equal to] 11.1 mg/kJ and energy levels [greater than or equal to]8.4 kJ/g (group 1), growth rate was relatively high. For animals fed the lowest protein level (group 2), growth was very low in all cases. For those fed the lowest energy level (group 3), growth was intermediate and proportional to protein content. Increased ingestion was adequate to compensate for lower energy density at values [greater than or equal to]8.4 kJ/g (group 1), but not at the lowest energy density. Responses were similar, whether growth was measured in units of energy [ILLUSTRATION FOR FIGURE 3c OMITTED], protein [ILLUSTRATION FOR FIGURE 3d OMITTED], or live mass [ILLUSTRATION FOR FIGURE 3e OMITTED]. Within-treatment variation made it difficult to distinguish effects of dietary protein and energy within group 1, but body lipid concentrations show that both protein and energy affect to some extent the material deposited in growth (Table 1, [ILLUSTRATION FOR FIGURE 3f OMITTED]).
DISCUSSION
Ingestion compensates for low dietary energy, but not for low dietary protein
Biologists have often observed an inverse relationship between diet energy density and ingestion rate, and generally have concluded that ingestion is regulated to meet the consumers’ need for energy (Rozin 1961, Harper 1976). However, the physiological mechanism by which ingestion is regulated remains unclear (Fletcher 1984, Pi-Sunyer 1990). Inasmuch as protein content is frequently correlated with energy density, some authors have viewed ingestion rate as a response to dietary protein level in both physiological (Matty and Lone 1985) and behavioral (Taghon and Greene 1990) terms. The factorial design of our experiment allows separation of the effects of dietary protein and energy. The results show that ingestion rate does compensate for low energy density to maintain energy assimilation rate, but there is no compensatory response to low protein levels. Within the range of protein levels that support significant growth, protein assimilation rate depends on the ratio of assimilable protein to assimilable energy.
Tilapia aurea in this experiment did respond to the lowest dietary protein level with very low ingestion rates, relative to other diets. Similar responses were reported for Tilapia zilli (Teshima et al. 1978) and rats (Harper 1976). Since there is a protein cost of feeding in terms of digestive enzymes and gut wall cell debris (metabolic fecal nitrogen), this response has been interpreted as being protective of the consumers’ protein reserves (Harper 1976).
Growth predicted from dietary. energy and protein
Our results provide a basis for prediction of growth from measures of dietary protein and energy. Because animals differ considerably in abilities to ingest, digest, and assimilate various foods, a more general model for prediction of growth can be based on assimilated protein and energy. For our data, multiple linear regression of the second-order polynomial describing growth in live mass in terms of energy assimilation rate and the ratio of protein to energy in the material assimilated accounted for 91% (adjusted [R.sup.2]) of the variation in growth [ILLUSTRATION FOR FIGURE 4a OMITTED]. To the extent to which efficiency in the use of assimilated protein and energy is relatively conservative across taxa (Bowen 1987b), Fig. 4a may serve as a first approximation model for prediction of growth in other poikilotherms.
Prediction of growth from direct measures of protein and energy in the diet integrates the effects of adaptations for feeding, digestion, and assimilation, and thus provides a model more specific to the particular consumer on which it is based. Although a multiple linear regression of the second-order polynomial describing growth in live mass in terms of kilojoules assimilable energy per gram diet and milligrams protein per assimilable kilojoule accounted for 81% of the variation in growth, the form of the regression implied counterintuitive trends at the margins of the plot. A more useful model was produced by Kriging interpolation to construct a response surface [ILLUSTRATION FOR FIGURE 4b OMITTED].
Differences in the forms of models in Fig. 4a, b are due to T. aurea’s compensatingly high ingestion rate at lower energy levels. On most of the surface outside the upper left quadrant of Fig. 4b, growth isopleths are essentially parallel to the assimilable energy axis, indicating this variable has little effect on growth in mass for the nutrient ranges studied. T. aurea is one of the tilapia group of fishes that is adapted for feeding on algae, aquatic macrophytes, and organic detritus. They have the ability to process relatively large quantities of food (Spataru and Zorn 1978, Buddington 1979, Drenner 1987). For animals less adapted to vegetable diets than T. aurea, we would expect differences in these two models to be less.
Food quality constraints and consumer adaptations compared for food categories
The model in Fig. 4a offers a basis for comparing the roles of dietary protein and energy in the trophic strategies of carnivores, herbivores, detritivores, and omnivores. Major categories of food resources can be mapped onto the figure using published data on protein and energy contents [ILLUSTRATION FOR FIGURE 1 OMITTED], and on the extent to which these can be assimilated. Taken from the literature on fishes, representative assimilation efficiencies (quantity assimilated as a percentage of the quantity ingested) are: invertebrate protein and energy, 80% (Persson 1983); algal protein, 85% and energy, 70% (Moriarty 1973, Kitchell et al. 1978, Wessel et al. 1982, Teferra 1988); macrophyte protein, 70% and energy, 45% (Hickling 1966, Buddington 1979, De Silva and Perera 1983); detritus protein, 77% and energy, 63% (Bowen 1979b, 1981). For the sake of comparison, energy intake was calculated for each food type as if a hypothetical consumer ingested an amount equivalent to 5% of body mass per day. Given this assumption, the resultant Fig. 5 indicates the relative value of various food categories for growth of fishes adapted to their use.
Invertebrate prey clearly provide the highest food quality in terms of both protein and energy compared to the primary food resources of algae, macrophytes, and detritus. However, the quantity of prey available is typically a constraint. It is not uncommon for fish to ingest well below 5% of body mass per day when feeding on invertebrate prey (Lane et al. 1979, Wooton 1992). This is consistent with the interpretation that the morphology and behavior of fishes that feed extensively on invertebrates are adapted to optimize energy gain (Werner 1977, inter alia).
Algae, aquatic macrophytes, and detritus are all inferior to aquatic invertebrates as sources of protein and energy. The relative importance of protein and energy as limiting nutrients is indicated by the slope of gradient vectors for the regression model [ILLUSTRATION FOR FIGURE 4A OMITTED] evaluated at mean protein and energy values for each food category [ILLUSTRATION FOR FIGURE 5 OMITTED]. Protein is most important as a constraint for detritivores: the gradient vector is nearly parallel to the protein axis, indicating that for a detritivore feeding at random, an increase in diet protein content will affect growth rate much more than an equivalent increase (as proportion of model range) in energy assimilation rate. By this same analysis, protein and energy are equally important as constraints for herbivores feeding at random on macrophytes and energy is somewhat more important for those feeding on algae.
From the results presented above, we expect a consumer to respond differently to limited protein and limited energy. The energy constraint can be reduced by increased ingestion rate. Fishes that feed on primary foods generally have long digestive tracts adapted to process large quantities of food per day (Horn and Messer 1992, Wooton 1992), and detritivores typically have the longest guts reaching 22 times the total fish length (Kapoor et al. 1975, Fange and Grove 1979). Primary foods are often available in quantities that exceed the consumers’ ability to consume them in the short term. Thus, the compensatory response to low energy content shown by T. aurea in the present study can be expected from other fishes feeding on primary food resources. We would expect fishes feeding on algae, macrophytes, or detritus to ingest larger quantities of food to compensate for the food’s low energy density.
We expect consumer responses to low protein content to take a different form. For detritus and aquatic macrophytes, the two food categories in which protein is most important as a constraint, there is a wide range of protein values. The higher values are characteristic of foods found at predictable locations (Boyd 1968, Bowen 1987a) and fishes feeding on detritus and macrophytes show a high degree of selectivity, preferentially ingesting the most protein-rich material (Bowen 1987a; M. S. Caulton, personal communication). Taken together, increased ingestion and selection for higher protein foods have the potential to compensate for low protein and energy levels in primary foods. The effectiveness of these responses is shown by the fact that some of the highest growth rates reported for freshwater fishes are for herbivorous/detritivorous species (Lowe-McConnell 1975).
These results help to explain why optimal foraging theory has met with limited success in efforts to explain diet selection by primary consumers. Various studies found primary consumers were selective in choosing their diets, but this selection appeared not to optimize energy intake (Paine and Vadas 1969, Larson et al. 1980). Evidence is accumulating to show that protein is frequently the principal constraint to the growth, fecundity, and survival of invertebrate and vertebrate primary consumers in aquatic, marine, and terrestrial habitats, and that diet selection by these animals generally maximizes diet protein:energy ratio (Zimmerman and Wissing 1979, Tenore 1981, Smock and Harlowe 1983, Steinwachser and Travis 1983, Bowen 1984b, Valett and Stanford 1987, Duffy and Hay 1991).
Omnivory is a common feeding strategy in which consumers complement protein from invertebrate prey with energy from more abundant primary foods (Ahlgren 1990). Among fishes, some feed as omnivores throughout an annual cycle, whereas others turn to omnivory as an alternative only when invertebrate prey are rare (Lowe-McConnell 1975). Members of the latter group are generally not adapted to the use of primary foods and may actually lose mass during this period, but at a slower rate than expected if they were to rely solely on the few invertebrate prey they can capture (Kitchell and Windell 1970). Omnivory appears to be equally important to many freshwater invertebrates. Although it was originally thought that net-spinning caddisflies are detritivores, the finding that a small proportion of invertebrate prey in the diet is essential to the growth of most species establishes these consumers as omnivores (Benke and Wallace 1980, Anderson and Cargill 1987). Only those species that fed on the finest particles, those relatively rich in protein, depended entirely on organic detritus for their nutrition (Benke and Wallace 1980). Similar conclusions have been reached for other macroinvertebrate taxa (Anderson and Cargill 1987).
Extension of this approach to understanding protein and energy nutrition of consumers in the wild will require more detailed investigation of the characteristic trophic abilities of specific consumers. Individual species have considerable potential to adapt to feeding opportunities offered by a complex menu of food resources in natural environments. Growth responses may also depend on the consumer’s physiological status and physical environment. For any particular situation, more precise knowledge of the effects of dietary protein and energy will require direct assessment for the conditions and consumers of interest.
ACKNOWLEDGMENTS
We thank Paul Dey and Lisa Jipping for assistance in the laboratory, Tom Drummer and Bob Keen for assistance with statistics, and Chris Passerello for help with gradient vectors. Development of the research plan benefited from related work by MTU Master’s degree candidate T. Kinery. Preliminary work on diet formulation was conducted by S. H. Bowen while on sabbatical leave at the Instituto de Acuiculture Torre de la Sal, Castellon, Spain. This work was supported in part by a grant from the Conservation, Food and Health Foundation of Boston, Massachusetts.
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COPYRIGHT 1995 Ecological Society of AmericaThe effects of dietary protein and energy on ingestion and growth were determined for nutrient ranges that correspond to primary foods in freshwaters: algae, aquatic macrophytes and organic detritus. Sixteen diets containing four levels of metabolizable energy (ME) (3.1, 6.7, 10.5, 14.1 kJ/g) and four levels of protein (3.0, 13.2, 23.2, 33.4 mg/kJ ME) were each fed ad libitum to four replicate groups of juvenile Tilapia aurea for 42 d. Protein, energy, and protein-energy interaction affected both ingestion and growth (two-way ANOVA, all P [less than] 0.01 ). Increased ingestion largely compensated for lower energy levels within each protein level. Growth was proportional to diet protein content, and ingestion did not compensate for protein limitation. A second-order polynomial for growth as a function of diet protein content and energy assimilation rate fitted by linear regression accounts for 91% of variation in growth, and provides a model for comparison of the relative importance of protein and energy as nutritional constraints for animals feeding on invertebrate prey, algae, aquatic macrophytes, and organic detritus. Protein appears to be the primary constraint to food value of macrophytes, and detritus, and we predict from our results that consumers of these materials will increase growth most by feeding selectively on the most protein-rich material available, as has been observed. In contrast, growth of animals feeding on algae will be increased most by increased ingestion. Omnivory is interpreted as a compromise strategy in which protein from scarce animal prey is complemented by energy from abundant primary foods.
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