Specific dynamic action: A century of investigation

Comparative Biochemistry and Physiology, Part A 144 (2006) 381 – 394 www.elsevier.com/locate/cbpa

Review

Specific dynamic action: A century of investigation M.D. McCue ⁎ Department of Biology, University of Arkansas, 601 Science Engineering, Fayetteville, AR, 72701, USA Received 2 December 2005; received in revised form 15 March 2006; accepted 21 March 2006 Available online 30 March 2006

Abstract Specific dynamic action (SDA) is the term used to refer to the increased metabolic expenditure that occurs in postprandial animals. Postprandial increases in metabolism were first documented in animals over two hundred years ago, and have since been observed in every species thus far examined. Ironically, the ubiquity of this physiological response to feeding understates its complex nature. This review is designed to summarize both classical and modern hypotheses regarding the causality of SDA as well as to review important findings from the past century of scientific research into SDA. A secondary aim of this work is to emphasize the importance of carefully designed experiments and systematic hypothesis testing to make more rapid progress in understanding the physiological processes that contribute to SDA. I also identify three areas in SDA research that deserve more detailed investigation. The first area is identification of the causality of SDA in ‘model’ organisms. The second area is characterization of SDA responses in novel species. The third area is exploration of the ecological and potential evolutionary significance of SDA in energy budgets of animals. © 2006 Elsevier Inc. All rights reserved. Keywords: Calorigenesis; Diet; Digestive energetics; Feeding costs; Gut-upregulation; Metabolic increment; Nutrition; Postprandial metabolism; SDA; Temperature

Contents 1. Introduction . . . . . . . . . . 2. History of SDA investigation . 3. Characterizing SDA . . . . . 4. Recent studies of SDA . . . . 5. Conclusion . . . . . . . . . . Acknowledgments . . . . . . . . . References . . . . . . . . . . . . .

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1. Introduction Specific dynamic action (SDA) refers to the increased metabolic rate an animal experiences following ingestion of a meal. The physiological causality of this phenomenon has a long history in comparative nutritional and physiological research. Over the past one-hundred years dozens of hypotheses have been advanced to explain the physiological processes that ac⁎ Tel.: +1 479 575 2963. E-mail address: [email protected]. 1095-6433/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2006.03.011

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count for SDA. These hypotheses can be grossly categorized into three groups (preabsorptive, absorptive, and postabsorptive physiological processes). Preabsorptive explanations of SDA involve the energetic costs of meal heating (Wilson and Culik, 1991), gut peristalsis (Borsook, 1936; Tandler and Beamish, 1979), enzyme secretion (Gawecki and Jeszka, 1978; Coulson and Hernandez, 1979; Owen, 2001), protein catabolism (Iwata, 1970; Pierce and Wissing, 1974; Coulson and Hernandez, 1979; Houlihan, 1991), acid secretion (Secor, 2003), intestinal remodeling (Secor and Diamond, 1995; Wang et al., 2001; Secor and Faulkner, 2002),

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and blood pH regulation (Secor and Diamond, 1995; Owen, 2001). Absorptive explanations of SDA typically involve energetic costs related to intestinal absorption (Secor et al., 1994; Secor, 2003; McCue et al., 2005) and nutrient transport across extradigestive membranes (Beamish, 1974; Soofiani and Hawkins, 1982), or imply that hormone secretions directly induce increased postprandial metabolism (Baumann and Hunt, 1925). Postabsorptive explanations of SDA are thought to involve costs of protein synthesis (Grisolia and Kennedy, 1965; Garrow and Hawes, 1972; Coulson and Hernandez, 1979; Brown and Cameron, 1991a,b; Houlihan, 1991; Whiteley et al., 2001; McCue et al., 2005), ketogenesis (Borsook, 1935, 1936), amino acid deamination and/or oxidation (Lusk, 1922; Chambers and Lusk, 1930; Wilhelmj, 1934; Borsook, 1936; Kriss, 1941; Coulson and Hernandez, 1979), glycogen production (Adams, 1926; Wilson and Lewis, 1930; Wilhelmj, 1935), urea production (Terroine and Bonnet, 1929; Borsook and Keighley, 1933; Brody, 1945), renal excretion (Wishart, 1928; Borsook and Winegarden, 1931; Dock, 1934; Borsook, 1935; Brody, 1945; Hoar, 1983; Kalarani and Davies, 1994), and general costs of growth (Brody, 1945; Ashworth, 1969; Krieger, 1978; Vahl, 1984; Carter and Brafield, 1992). The multitude of physiological processes that apparently contribute to SDA is potentially overwhelming to many researchers in this field. After decades of research arguably the most prolific investigator of SDA, Graham Lusk, eventually realized that, “A complete analyses of all the factors which meter into the specific dynamic action of protein is quite impossible, but their way of discovery appears open.” (Lusk, 1931) It should be noted that many of the pre- and postabsorptive physiological processes are inevitably linked to one another, and thus the energetic costs associated with each are difficult to isolate in vivo. For example, rates of renal excretion are highly dependent on rates of urea formation, which are dependent on rates of amino acid deamination, which are in turn dependent on the balance between protein catabolism and anabolism. Many of

these physiological processes are also difficult to isolate temporally and spatially within an animal (Fig. 1). For example, the liver might be a primary site for amino acid deamination and urea formation, but is also the primary site for ketogenesis and glycogenesis. Similarly, intestinal tissues may incur the distinct costs of tissue remodeling, peristalsis, and absorption. Since Lusk's time, researchers investigating SDA have made great progress in understanding how various endogenous and exogenous factors influence SDA in different species. However, our ability to identify the fundamental energetic processes underlying SDA is scarcely better now than it was in the first quarter of the twentieth century. Modern researchers investigating SDA may find it surprising that the rates of scientific development for most other physiological phenomena consistently outpace the progress toward understanding the causality of SDA; it is certainly not a result of a lack of effort (see below). In his classic paper on strong inference, Platt (1964) recognizes the fact that some areas of science are experiencing limited rates of progression. As previously described research into SDA physiology clearly falls into this category. In his manuscript Platt notes, “Anyone who looks at the matter closely will agree that some fields of science are moving forward very much faster than others, perhaps by an order of magnitude, if numbers could be put on such estimates.” Platt's solution to apparent scientific stagnation involves a rigorous battery of hypothesis testing. He further states, “We praise the ‘lifetime of study,’ but in dozens of cases, in every field, what was needed was not a lifetime but rather a few short months or weeks of analytical inductive inference. We should try, like Pasteur, to see whether we can reach strong inferences that encyclopedism could not discern.” Forthcoming investigations of SDA should not overlook this traditional yet effective approach to problem solving in science. As a result, this review is designed to summarize the existing ‘encyclopedic’ knowledge of SDA as well as to provoke testing of critical hypotheses that will hopefully allow researchers to make more rapid progress in understanding SDA. Peristalsis

Deamination Ketogenesis Glycogenesis Urea production Protein catabolism

Esophagus

Enzyme production/secretion Liver Pancreas

Enzyme production/secretion Acid secretion Mechanical digestion Stomach

Peristalsis Gut remodeling Absorption

Excretion

Kidney

Anabolism New growth

Kidney

Peristalsis Absorption

Fig. 1. Schematic illustrating some of the physiological processes that have been hypothesized to be contributing factors to specific dynamic action.

M.D. McCue / Comparative Biochemistry and Physiology, Part A 144 (2006) 381–394

The concept of SDA is commonly introduced in textbooks of physiological nutrition (DuBios, 1936; White et al., 1964; Blaxter, 1989; Whitney and Rolfes, 1996; Randall et al., 1997), however most of these sources devote only one or two paragraphs to SDA. These brief overviews of SDA fail to emphasize multiplicity of physiological processes that underlie SDA and imply that this phenomenon is fully understood by scientists. A text published by the American Medical Association even laments SDA stating, “In our opinion, the importance of SDA in human nutrition has been misunderstood and overrated” (Bradfield and Jourdan, 1973). Such an attitude discounts both the enigmatic nature and the biological significance of SDA. Texts on clinical nutrition similarly suggest that the costs of SDA are negligible to digestive energetics (Taylor and Pye, 1966; Kreutler, 1980; Whitney and Rolfes, 1996), but this is clearly not the case in animals generally. While accounting for 6–17% of the energy budget in humans (Taylor and Pye, 1966), SDA accounts for approximately one third of the ingested energy in several nonhuman animals (Pierce and Wissing, 1974; Hailey and Davies, 1987; Secor and Phillips, 1997; Hailey, 1998; McCue and Lillywhite, 2002; McCue et al., 2005), and thus should not be ignored by biologists. Some studies of SDA even demonstrate that animals may demonstrate behavioral or physiological adaptations to minimize energy devoted to SDA (Taylor and Pye, 1966; Wilson and Culik, 1991; Boyce and Clarke, 1997; Radford et al., 2004; Fu et al., 2005; Jordan and Steffensen, 2005). These studies suggest that energy not appropriated to costs of digestion may then be spent on growth and activity of the organism (Kalarani and Davies, 1994; Alsop and Wood, 1997; Owen, 2001), however, no studies have yet investigated the potential influence of SDA costs on dietary choices and ultimately on the foraging behaviors of animals. Because SDA can account for a potentially large, albeit variable, fraction of animal energy budgets, a better understanding of SDA related energy expenditure promises to increase our general understanding of ecological and evolutionary bioenergetics. 2. History of SDA investigation Specific dynamic action has been described by several names in literature including ‘Darmarbeit’ (von Mering and Zuntz, 1877; Zuntz and von Mering, 1883), ‘metabolism of plethora’ (Lusk, 1922; Mason et al., 1927), ‘generic dynamic action’ (Wilhelmj, 1935), ‘secondary dynamic action’ (Wishart, 1928), ‘thermic energy’ (Brody and Procter, 1933) ‘thermic effect of food,’ (Whitney and Rolfes, 1996) ‘diet-induced thermogenesis’ (Newsholme and Leech, 1983), ‘heat increment’ (Blaxter, 1989),‘postprandial calorigenesis’ (McCue et al., 2002a; McCue, 2003) ‘calorigenic effect’ (Pike and Brown, 1984), as well as ‘SDA’. Each of the aforementioned terms were chosen by various researchers for its respective explanatory power, however the multiple nomenclature used to refer to this enigmatic phenomenon is indicative of its complex physiological nature. The most commonly used term specific dynamic action (and the initialism SDA) was adapted from the German phrase (specifisch-dynamische wirkung) coined by Max Rubner in the 1890s. Although in its native language this phrase referred to

383

specific physiological changes induced by food processing, its English translation is misleading (Pike and Brown, 1984). For example, it was a result of the disconnect between this term and its physiological significance that one study erroneously referred to specific dynamic action as ‘secondary dynamic action’ (Wishart, 1928). Whether related to its antiquity or its translation from its native tongue, the term specific dynamic action is somewhat confusing and does little to communicate any relationship between metabolism and feeding. Nevertheless SDA remains the most historically common term to refer to this phenomenon and thus will be employed throughout the remainder of this review. Most textbook descriptions of SDA still rely exclusively on Rubner's turn of the century metabolic measurements on postprandial dogs consuming lipid, carbohydrate or protein meals (White et al., 1964; Newsholme and Leech, 1983; Blaxter, 1989; Whitney and Rolfes, 1996). While Rubner's work was critical to the early characterization of specific dynamic action in animals, it was certainly not the first; the earliest observations of postprandially elevated metabolism were made by Lavoisier in 1780, Pettenkpfer and Voit in 1862, and Bidder and Schmidt in 1852 (see Borsook, 1936; Taylor and Pye, 1966). While Rubner's measurements of SDA on dogs clearly provided an initial framework on which to base hypothesis regarding the physiological processes underlying specific dynamic action, it is important to note that these conclusions may not apply to SDA in other animals. With the exception of Benedict's (1932) investigation into SDA of ectotherms, virtually all of the investigations of SDA prior to the 1940s employed endothermic animals as research subjects (most frequently dogs and rats). Regular investigations of SDA in ectotherms were not conducted until paramagnetic oxygen analyzers became widely available in the 1950s. Modern studies of SDA now embrace the use of ectothermic animals for several reasons (see below). As previously discussed, there are at least as many contributing factors to SDA as there are names for this phenomenon. Perhaps the earliest hypothesis to explain the source of increased postprandial metabolism was associated with the physiological costs associated with alimentary peristalsis, glandular secretion and mechanical digestion of a meal (see Borsook, 1936). Late in the nineteenth century Rubner's contemporary, Zuntz termed these collective costs ‘darmarbeit’ (von Mering and Zuntz, 1877; Zuntz and von Mering, 1883). However, the darmarbeit hypothesis was not supported by a series of studies where various nonnutritive meals were fed to dogs (Lusk, 1922; Mason et al., 1927). Despite additional comparative evidence against the darmarbeithypothesis (Lusk, 1912–1913b, 1915; Rapport, 1924; Coulson and Hernandez, 1979; McCue et al., 2005), some researchers have not completely abandoned this theory to explain the causality of SDA (Pierce and Wissing, 1974; Gawecki and Jeszka, 1978; Secor and Diamond, 1995). Prior to the past decade the richest period of inquiry into SDA occurred between 1910 and 1940, and attracted a diverse group of scientists including clinical physicians, biochemists, and comparative physiologists. In this early period, most of the scientific discourse on the subject was published in the Journal of Biological Chemistry and the Journal of Nutrition. Many of

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these early publications contain scientific debates regarding the causality of SDA that are virtually identical to those found in modern literature (see below). Interestingly, these perspectives are rarely cited by current researchers of SDA. According to an elegant literature review by Wilhelmj (1935), three observations regarding SDA of proteins were consistently noted among endotherms. The first was that SDAwas not a result of direct ‘combustion’ of amino acids. This pattern has been later confirmed in studies of ectotherms. Coulson and Hernandez (1979) and McCue et al. (2005) found no correlation between the energy content of amino acids and resulting SDA in alligators and pythons respectively. The second observation was that SDA was not a result of direct stimulation of metabolism as a result of increased amino acid levels in tissues (but see Rapport and Katz, 1927). This observation was further supported in modern experiments on rodents (McNurlan et al., 1982) and several ectotherms. For example, Brown and Cameron (1991a,b) failed to observe SDA in catfish previously treated with cycloheximide, a chemical to inhibit protein synthesis, before being injected with several different amino acid solutions. Similar results with cycloheximide were observed in pythons (McCue et al., 2005). Wilhelmj's third observation was that SDA could not be fully explained by work of the digestive glands, intestinal movements, or nutrient absorption. This observation is also supported by data obtained from diverse ectothermic species. For example, Coulson et al. (1978) reported that the processes of absorption and transport are dominantly passive co-transport processes in alligators and caimans consuming complete, balanced protein meals. Tandler and Beamish (1979) also concluded that the mechanical component of SDA in bass fed cellulose was only a small fraction of total SDA. The 1950s and 1960s marked a relatively quiescent period in investigations of SDA. Although a few reports of SDA in ectotherms were published in these decades (e.g. Roberts, 1968), comparative studies of digestion did not emphasize SDA. However, in the 1970s Herbert Coulson's research into the digestive physiology of ectothermic tetrapods marked a renaissance for investigations into the causality of SDA (Coulson and Hernandez, 1968, 1970, 1979; Herbert and Coulson, 1975, 1976). In an apparent response to Coulson's ideas about SDA in ectotherms, aquacultural researchers charged with maximizing growth rates of fishes developed an obvious appreciation for SDA. By the 1980s SDA research was dominated by studies involving commercially raised fishes (see Jobling, 1981, 1983; Machida, 1981; Belokopytin, 2004). In the past decade, Secor and Diamond conducted experiments revealing that pythons exhibited comparatively large metabolic responses to feeding (Secor and Diamond, 1995). The ease in measuring SDA in pythons has allowed them and related snake species to become popular organisms for current studies of SDA (Secor and Diamond, 1998); however, the specialized diets of these animals preclude them from being the ideal model organism for all SDA investigations. Moreover, like much of the early research into SDA, modern interpretations of SDA are not without controversy. Secor and Diamond's work frequently stated that costs of gut upregulation accounted for the majority of SDA in pythons. However, recent experiments by Starck pre-

sented data that failed to support this hypothesis (Starck, 1999; Starck and Beese, 2001; Overgaard et al., 2002; Starck et al., 2004). Other studies conducting repeated feedings in fishes and turtles also concluded that gut upregulation was not a significant component of SDA (Owen, 2001; Pan et al., 2005b). Although early SDA research regularly employed endotherms, recent researchers tend to focus on the SDA of ectothermic species, particularly fishes and reptiles. Unfortunately, because of the specialized digestive physiology, morphology, and diet of many ectotherms, conclusions drawn from studies involving highly specialized species may not apply to many taxa. Current understanding of SDA of animals in general would certainly benefit from renewed research of SDA in endothermic animals. Patterns uncovered from such experiments would complement the ongoing investigations involving ectotherms and expand physiological understanding of SDA in animals generally. 3. Characterizing SDA Several methods are used to characterize the meal size in SDA trials; some of these methods more readily lend themselves to hypothesis testing than others. Early studies generally describe SDA response as a function of the absolute mass ingested (Lusk, 1912–1913a,b, 1915; Wilhelmj and Bollman, 1928; Wilhelmj et al., 1931), or as a function of the caloric value of the meal (Lusk, 1910, 1922; Kriss et al., 1934; Kriss, 1938; Kriss and Marcy, 1940). Many modern studies of tetrapods characterize SDA as a function of relative prey mass (Muir and Niimi, 1972; Janes and Chappell, 1995; Secor and Phillips, 1997; Hopkins et al., 1999; Overgaard et al., 1999; Busk et al., 2000; Hicks et al., 2000; Secor, 2003; Roe et al., 2004), and studies on fishes often describe SDA as a function of the percent of protein in the diet (Hamada and Maeda, 1983; Chakraborty et al., 1992). It is important to realize that the best characterization of a meal in SDA trials is not necessarily the one that is most frequently used in literature, but the one that most appropriately suits the phenomenon being evaluated. In many cases measurements of relative prey mass are among the least informative measures of meal size because such metrics are invariably confounded by animal size and fail to characterize meals at a molecular level. Like many physiological variables, SDA responses are wellknown to vary allometrically with an animal's body mass (Carter and Brafield, 1992; Beaupre et al., 1993; Boyce and Clarke, 1997; Clarke and Prothero-Thomas, 1997; Secor and Faulkner, 2002; Toledo et al., 2003; Beaupre, 2005; Fu et al., 2005). Interpretations of SDA that neglect to account for the allometric nature of the response could be misleading since a 1 kg animal consuming a 0.1 kg meal might be viewed identically to a 10 kg animal consuming a 1 kg meal. Consequently, SDA responses from these two situations can only be directly compared if SDA is known to scale linearly with meal size or if the allometric relationship between animal mass and SDA responses to a given meal type is known. Thus, the practice of describing meals based on their relative prey mass is only valid when dealing with conspecifics of a given age/size that are consuming identical meals. Although individual studies of SDA generally compare

M.D. McCue / Comparative Biochemistry and Physiology, Part A 144 (2006) 381–394

Resting metabolic rate Duration

Fig. 2. Schematic illustrating the difficulty in precisely identifying the terminus of the SDA response in animals that exhibit strong diel fluctuations in resting metabolic rates (Based on Roe et al., 2004).

Time to peak metabolic rate

SMR

Duration of increased metabolism

Increase in metabolic rate

Highest recorded metabolic rate

similar age/size classes within a species, comparisons of results from other studies using identical species can be precluded when a different size class is used. Some studies of SDA control for relative meal size, but they do not account for the differences in energy content of meals (Tandler and Beamish, 1979; Hamada and Maeda, 1983; Chakraborty et al., 1992; McGaw and Reiber, 2000; Grayson et al., 2005; Pan et al., 2005a). Like comparisons involving different relative meal sizes, the results of these studies should be interpreted with caution since two identical rations might have drastically different caloric content and induce differential SDA responses. For example, a pure lipid meal of a given mass has a smaller volume, but a caloric value much greater than that of a hydrated carbohydrate meal. Comparisons of SDA responses from isoenergetic meals of a given physiological fuel should also be interpreted with caution. For example protein meals consisting of gelatin and casein are subject to differential physiological processing because of their dramatically different amino acid composition; casein can be readily converted to new tissue growth whereas gelatin contains a very incomplete mixture of amino acids and cannot be used to support extensive protein synthesis (Coulson and Hernandez, 1979; McCue et al., 2002b, 2005). Similar results are expected from comparisons of lipid or carbohydrate meals if they differ greatly in their molecular composition. Because SDA is an increase in metabolic expenditure following feeding, it is important that researchers develop uniform methods for characterizing the pre- and postfeeding metabolic rates in various animals. Many animals are known to demonstrate diel fluctuation in metabolic rates; these fluctuating metabolic rates must be subtracted from the postprandial metabolic expenditure to determine actual energy devoted to SDA. Some studies have ignored diel fluctuations in metabolic rates and used the lowest metabolic measurement made during a 24 h period to characterize postabsorptive metabolic expenditure (Beaupre, 2005). This technique will not only overestimate the magnitude and duration of the SDA response in postprandial animals, but will also yield an apparent SDA response in postabsorptive animals! A recent study outlines criteria for identifying SDA in animals that exhibit strong diel fluctuations in metabolic rate. Roe et al. (2004) suggest defining the SDA response in animals that exhibit diel variation in resting metabolic rates by subtracting the dynamic postabsorptive metabolic rate from dynamic prefeeding values. They also recommend defining the terminus of

the SDA response in animals as the point in time when postprandial metabolic rates return to the upper 25% of prefeeding metabolic rates for a given time of day (Fig. 2). This technique of course requires detailed information about pre-feeding metabolic rates, but allows researchers to precisely determine the terminus of SDA. Unfortunately this method may not be useful for some animal species that consume very large meals. Some animals that consume relatively large meals (i.e. pythons, starfish, or nemerteans) are able to convert the majority of ingested matter into biologically active tissue during the course of digestion; thus the metabolic rate of the animal would never return to its original value, ultimately obscuring the terminus of the actual SDA response. Although no technique has been proposed to standardize SDA measurements in such animals, a method that allows for inter-species comparisons of SDA responses is desirable. Because SDA is an increase in energy expenditure following feeding, it can also be characterized using several metrics (Fig. 3). Numerous metrics for quantifying SDA have been developed presumably because they offer insight into the various physiological processes underlying SDA (see Jobling, 1981; Guinea and Fernandez, 1997). Most accounts of SDA utilize multiple measurements to characterize postprandial metabolic responses. Some investigations of SDA emphasize the duration of elevated metabolism (Hamada and Maeda, 1983; Kalarani and Davies, 1994; Guinea and Fernandez, 1997; Roberts and Thompson, 2000), or an animal's absolute increase in metabolic rate (Overgaard et al., 1999; Somanath et al., 2000). Other studies emphasize the duration following feeding at which peak postprandial metabolism occurs (Machida, 1981; Hamada and Maeda, 1983; Ross et al., 1992; Janes and Chappell, 1995; Roberts and Thompson, 2000). This latter measure allows dominant physiological processes during SDA to be temporally categorized into early or late SDA responses. Measures of SDA duration vary widely among taxa compared to other measures, and thus often preclude meaningful interspecific comparisons. For example, while birds and mammals typically demonstrate SDA responses lasting only hours (Janes and Chappell, 1995), animals with very low metabolic rates may demonstrate responses

Metabolic rate

Metabolic rate

Diel fluction in RMR

385

Time Fig. 3. Schematic illustrating several of the metrics used typically used to quantify the SDA response (modified from McCue, 2003).

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Table 1a Overview of SDA responses in amphibians, fishes, and invertebrates Animal

Meal

CSDA (%)

Aves Penguin (chick)

Krill

10

10

Mammals Dog Dog Dog Dog (large meal) Dog (small meal) Dog Human Human Human Human Rat Rat Rat Rat Rat Rat

Glucose Water Olive oil Beef Beef Beef Protein Protein Glucose Fat Beef heart a Gelatina Caseina Olive oila Starcha Casein

5 n/a 19 50 32 45 17 17 4 4 7 8 13 4 4

Reptiles House snake (large meal) House snake (small meal) Alligator Alligator Alligator Alligator Black racer Boa (large meal) Boa (small meal) Brown forest skink Caiman Chinese skink Chinese skink Colubrid snake Colubrid snake Corn snake Cottonmouth Gopher snake Gopher snake King snake Lizard Monitor Monitor Monitor Monitor Python Python Python Python Python Python Python Python Python Python Python Python (20 C) Python (35 C) Rattlesnake (large meal) Rattlesnake (large meal) Rattlesnake (small meal) Rattlesnake (small meal)

Mouse Mouse Casein b Fishb Gelatinb Rodents Mouse Mouse Mouse Mealworm Rodents Frog heart Mealworm Guinea pig Mouse Mouse Mouse Mouse Mouse Mouse Mealworm Hardboiled egg Rat Turkey/snails Rodents Mouse Rat Chicken Mouse Mouse (puree) Lard Glucose Amino acids Starch Gelatin Casein Mouse Mouse Mouse Mouse Mouse Mouse

15 17 21 28 3

Duration (h)

Time to peak

Reference

1.2

1

Janes and Chappell (1995)

5

1.3 1.0 1.2

3 n/a 3

22 10

1.9 2.0 1.2 1.2 1.1 1.2 1.2 1.3 1.1 1.3 1.6

8

Lusk, 1912, 1915 Lusk, 1912; Rapport, 1924 Lusk (1912) Weiss and Rapport (1924) Weiss and Rapport (1924) Williams et al. (1912) Bradfield and Jourdan (1973) Mason et al. (1927) Mason et al. (1927) Mason et al. (1927) Kriss (1938) Kriss (1938) Kriss et al., 1934; Kriss, 1938 Kriss et al. (1934) Kriss et al. (1934) Gawecki and Jeszka (1978)

b24 b24 b24 b24 b24

Scope

5.3 3.2 130 80 36

4.0

15 14 12

96 210 58 38

17 9 26 28

60 70

3.3 5.4 8.1 2.5 1.6 1.6 2.0 1.5

48 216 120 72 96 48 72 90 60

2.4 5.5 8.0 2.7 7.0 1.9 6.7 9.9 10.4

24 96 56 56 0 85 40 0 0 100 432 240 170 360 62 110

17.0 5.4 3.4 5.2 0.0 3.4 3.8 0.0 0.0 3.1 6.2 5.7 7.3 10.4 3.7 3.9

33 14 17 14 24 23 17 27 32 32 15 20 0 32 0 0 18 25 28 18 13

3 3 4

1 2 2 0

24 24 12 12 8 36 38 14 13 19 14

12 60 16 4 24 27 27 24 40 360 36 24 18 n/a 40 9 n/a n/a 76 216 36 33 36 15 24

Roe et al. (2004) Roe et al. (2004) Coulson and Hernandez (1979) Coulson and Hernandez (1979) Coulson and Hernandez (1979) Busk et al. (2000) Secor and Diamond (2000) Toledo et al. (2003) Toledo et al. (2003) Lu et al. (2004) Gatten (1980) Pan et al. (2005a) Pan et al. (2005a) Benedict (1932) Hailey and Davies (1987) McCue, unpublished data McCue and Lillywhite (2002) Secor and Diamond, 2000 McCue (2002) Secor and Diamond (2000) Roberts and Thompson (2000) Secor and Phillips (1997) Secor and Phillips (1997) Secor and Phillips (1997) Hicks et al. (2000) Overgaard et al. (2002) Secor and Diamond (1995) McCue et al., 2005; 2002b McCue et al., 2005; 2002b McCue et al. (2005) McCue et al. (2005) McCue et al. (2005) McCue et al. (2002a) McCue et al. (2005) McCue et al. (2005) McCue et al. (2005) Wang et al. (2003) Wang et al. (2003) Andrade et al. (1997) Zaidan and Beaupre (2003) Andrade et al. (1997) Zaidan and Beaupre (2003)

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Table 1a (continued) Animal

Meal

Reptiles Red-eared slider turtle Red-eared slider turtle Stripe-necked turtle Stripe-necked turtle Tortoise Tortoise Tortoise Turtles Water skink Water snake Water snake

Mealworm Shrimp Mealworm Shrimp Fungi Leaves Insects Beef Mealworm Unknown Fish

CSDA (%)

Duration (h)

Scope

55 45 72 72 144 72 72 120 48 83

11 13 14 16 23 20 8

1.5 1.5 1.8 1.4 2.2 1.6 2.7 1.9 5.0 3.2

Time to peak

Reference

18 14 13 12

Pan et al. (2004) Pan et al. (2004) Pan et al. (2005b) Pan et al. (2005b) Hailey (1998) Hailey (1998) Hailey (1998) Secor and Diamond (1999) Iglesias et al. (2003) Hopkins et al. (1999) Sievert and Andreadis (1999)

36 25 22 18

CSDA refers to SDA coefficient (see text), scope refers to the maximal metabolic rate during digestion divided by the standard or basal metabolic rate of the animal, and time to peak refers to the time period after feeding at which the SDA response reaches a peak level. a Corrected for basal ration (5.5 g calf meal; approx. 98.9 kJ). b Estimated for 1 kg alligator.

on the order of several days (Andrade et al., 1997; Boyce and Clarke, 1997; Clarke and Prothero-Thomas, 1997; Secor and Diamond, 1997; Hopkins et al., 1999; McCue and Lillywhite, 2002). One starfish has even been reported to increase postprandial metabolism for up to 42 days (Vahl, 1984). Other studies report factorial increase in metabolism (occasionally referred to as ‘scope’ or ‘factorial scope’) resulting from SDA (Secor and Diamond, 1995, 1997; Hailey, 1998; Hopkins et al., 1999). SDA scope is calculated as the maximal postprandial metabolic rate divided by the standard or basal metabolic rate. The SDA scope is important because it can be compared to maximal

metabolic scope of an animal in order to estimate the residual capacity for activity during digestion. Guinea and Fernandez (1997) provide quantitative descriptions of some of the aforementioned metrics (Fig. 3). Some measures of SDA demonstrate more bioenergetic relevance compared to others. Since the energy devoted to SDA generally increases with ration and meal size (Hamada and Maeda, 1983; Wilson et al., 1985; Chakraborty et al., 1992; Andrade et al., 1997; Boyce and Clarke, 1997; Secor and Diamond, 1997; Secor and Phillips, 1997; Hailey, 1998; Toledo et al., 2003; Fu et al., 2005), the most informative measures of

Table 1b Overview of SDA responses in birds, mammals and reptiles Animal

Meal

Amphibians Horned frog Horned frog Horned frog Horned frog Salamander Toad Toad Toad Toad Toad Toad Toad

Pinky mouse Earthworm Amino acids Mice Fly larvae Small rat Large rat Earthworm Superworm Rodent (20 °C) Rodent (35 °C) Insects

Fishes Aholehole (small meal) Aholehole (large meal) Bass Bass Bluegill Bluegill Bluegill Carp Carp Carp Carp Carp Carp

Fish Fish Fish Fish Mayfly nymphs Fish Earthworm High carb diet High lipid diet High protein diet Plants Low protein High protein

CSDA (%)

15 13 13 23 37 21 16 17

16 16 14 13

15 21 23 7 9 16

Duration (h)

Scope

Time to peak

66 69 33 51 11 2 6 4 7 9 2.5 7

4.2 4.4

20 16

3.5 1.8 2.9 6.4 4.2 4.2 3.8 4.2 1.7

24 24 34 48 18 48 96 20 3

60 42 16 30

2.6 1.9 1.4

14 14

1.8 1.6 1.7

16 16 10 10 18 13 9

20 24

2.0 2.9

6 8

Reference Grayson et al. (2005) Grayson et al. (2005) Powell et al. (1999) Powell et al. (1999) Feder (1984) Secor and Faulkner (2002) Secor and Faulkner (2002) Secor and Faulkner (2002) Secor and Faulkner (2002) Secor and Faulkner (2002) Secor and Faulkner (2002) Sievert and Bailey (2000)

Muir and Niimi (1972) Muir and Niimi (1972) Machida (1981) Beamish (1974) Pierce and Wissing (1974) Machida (1981) Machida (1981) Carter and Brafield (1992) Carter and Brafield (1992) Carter and Brafield (1992) Carter and Brafield (1992) Chakraborty et al. (1992) Chakraborty et al. (1992) (continued on next page)

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Table 1b (continued) Animal

Meal

Fishes Carp Catfish Catfish (large meal) Catfish (small meal) Cichlid Hawkfish Plunder Fish (large ration) Plunder Fish (small ration) Sculpin Shark Sleeper Sparus Tilapia Walleye

Pellets Amino acids Loach Loach Pellets Shrimp/squid Krill muscle Krill muscle Shrimp/squid Fish Fish Pellets Fish meal Fish

Invertebrates Blue crab Copepod Copepod Flea Leech Lobster (day fed) Lobster (night fed) Mosquito Nemertean Prawn Starfish

Fish and clams Algae (A) Algae (B) Blood T. tubifex Mussels Mussels Blood Limpet Pellets Mussels

CSDA (%)

14 13 15 10 56 17

18 10

Duration (h)

Scope

Time to peak

15

1.5

52 16 6 36 390 324 160 12 18 38 10 36

4.1 1.5 2.4 2.2 2.4 2.5 2.4 2.3 2.7 2.6 2.4 4.0

4 3 22 4 3 12 36 6 48 9 12 3 8 10

2.6

4

Hamada and Maeda (1983) Brown and Cameron (1991b) Fu et al. (2005) Fu et al. (2005) Somanath et al. (2000) Johnston and Battram (1993) Boyce and Clarke (1997) Boyce and Clarke (1997) Johnston and Battram (1993) Ferry-Graham and Gibb (2001) Machida (1981) Guinea and Fernandez (1997) Ross et al. (1992) Tarby (1981)

McGaw and Reiber (2000) Thor et al., 2002 Thor et al., 2002 Fielden et al. (2004) Kalarani and Davies (1994) Radford et al. (2004) Radford et al. (2004) Gray and Bradley (2003) Clarke and Prothero-Thomas (1997) Gonzalez-Pena and da Gloria Blumer Soares Moreira (2003) Vahl (1984)

19 6

29 38 2

8 30 36 55 720 36 1200

1.8 1.2 1.6 1.8 1.5 1.7 2.0 2.3

Reference

4 18 3 10,30 6 336

CSDA refers to SDA coefficient (see text), scope refers to the maximal metabolic rate during digestion divided by the standard or basal metabolic rate of the animal, and time to peak refers to the time period after feeding at which the SDA response reaches a peak level.

Because of the nonlinearity of SDA responses resulting from variable meal sizes or different animal masses (see Beaupre, 2005 and references therein), CSDA can only be reliably compared within similar sized conspecifics ingesting identical meals unless allometric relationships between meal size, meal type, and animal size are known. Unfortunately, such relationships are rarely known. Therefore, in the absence of such information CSDA can be used to broadly compare results among studies that vary by species, body masses, and meal sizes and type. CSDA is similar to the variable ‘apparent specific dynamic action coefficient’ (ASDAC) and ‘SDA coefficient’ described by Guinea and Fernandez (1997) and Ross et al. (1992) respectively. The tables below presents CSDA, and other metrics of SDA responses reported in studies of animals ingesting various meals (Tables 1a and b). Some of these values were not implicitly presented in primary literature and had to be calculated from other information provided in the text. While this table is not intended to include all studies reporting CSDA, it does embody the SDA responses of a

Ac

tivi

ty

A

SD

SDA

CSDA ¼ ðESDA =Emeal Þ⁎100

diverse collection of animals consuming a variety of diets. It should again be mentioned that measures of CSDA are not always linear and are often subject to allometric constraints, particularly when animals consume unusually small or unusually large meals. In some cases CSDA is reported to increase exponentially with meal size (Lusk, 1912–1913b, 1922; Weiss and Rapport, 1924; Carter and Brafield, 1992), whereas in other studies CSDA is differentially reduced as meal size increases (Toledo et al., 2003; Fu et al., 2005). Although CSDA is an ideal measure for comparing SDA in some situations, it is not beneficial for testing all hypotheses about SDA. This is especially true when comparing the postprandial calorigenic effects of individual amino acids or other mixtures of purified physiological fuels. In cases where animals are ingesting various mixtures, it is more helpful to quantify SDA using molar quantities (Lusk, 1912;

Activity

SDA are those that correlate the energetic content of a meal with the total energy devoted to SDA. This is most commonly accomplished by calculating the SDA coefficient (CSDA). CSDA is traditionally calculated by dividing the energy devoted to SDA (ESDA) by the energy contained in the meal (Emeal). Sometimes, this divisor is corrected to reflect only the metabolizable energy in a meal. It is expressed using the following formula.

Meal Size Fig. 4. Schematic illustrating the potential tradeoff between activity scope and metabolic increment associated with SDA (modified from Owen, 2001).

P

e

rp

o bs

tiv

A SD

SDA

l dia

n

ra

tp os

389

25% RPM 20% RPM 15% RPM 10% RPM 5% RPM

SDA

Metabolic rate

M.D. McCue / Comparative Biochemistry and Physiology, Part A 144 (2006) 381–394

sta

Po

Meal Size

Duration

Running speed Fig. 5. Schematic illustrating the maximal aerobic metabolic rate of postprandial and postabsorptive lizards (modified from Hicks and Bennett 2004).

Wilhelmj, 1934; Herbert and Coulson, 1976; Coulson et al., 1978; Coulson and Hernandez, 1979; McCue et al., 2005). 4. Recent studies of SDA Recent studies investigating SDA can be divided into three major categories. Some of these studies are designed to investigate the specific physiological causality of SDA in species in which SDA is well characterized. Other studies focus on characterizing SDA responses in species in which it has not yet been quantified. A third group of studies seeks to understand the ecological and evolutionary significance of SDA in the context of natural history and energy budgets. These three lines of investigation are complementary to one another, and much has been learned from each of these approaches. The following section reviews some of the most recent advances in SDA research in these areas. Using an ecological approach, Alsop and Wood (1997) introduced the idea that animals devoting energy to SDA may not be able to devote maximal energy toward other activities such as locomotion. They concluded that postprandial trout exhibited lower maximal swimming speeds compared to postabsorptive cohorts. Similar observations have been made in Atlantic cod (Jordan and Steffensen, 2005). This concept of division of energy was later formalized by Owen (2001) who speculated that aerobic expenditure of an animal must be partitioned between the demands of SDA and those involved in ‘activity’ (Fig. 4). On the other hand, Hicks and Bennett (2004), examining the traditional concept of ‘maximal aerobic rate’ in varanid lizards

Fig. 7. Schematic illustrating the nonlinear relationship between relative meal size or relative prey mass (RPM) and SDA response typical in ectotherms.

running on a treadmill, found that postprandial lizards were able to achieve a new, higher ‘maximal aerobic rate’ compared to the maximal metabolic rates measured in postabsorptive lizards (Fig. 5). Interestingly, Hicks and Bennett's findings failed to support the ‘energy partitioning hypothesis’ advanced by Owen (2001), and concluded that the ability to separate cost of SDA and activity may vary among taxa. In light of these findings, these researchers speculated that the additive effect of metabolism devoted to locomotion and SDA in lizards was possible because these two physiological states utilized different tissue groups (i.e. viscera and locomotory muscles), and are thus not mutually exclusive. As a result of these findings, further examination of energetic partitioning between SDA and other energetic demands in additional species is recommended. Several studies have examined the influence of temperature on SDA. Most of these investigations reported that temperature had dramatic influence on the duration and peak metabolic rate during digestion, but had little influence on the total energy devoted to SDA and thus CSDA (Machida, 1981; Powell et al., 1999; Whiteley et al., 2001; Robertson et al., 2002; Secor and Faulkner, 2002; Wang et al., 2003; Zaidan and Beaupre, 2003). Although one study of SDA and temperature reported that energy devoted to SDA in boid snakes is slightly greater at digestion temperatures of 25 °C compared to 30 °C (Toledo et al., 2003), most studies investigating the relationships between

SDA

SDA

warmer temperatures

cooler temperatures

An

ima

Duration

Fig. 6. Schematic illustrating influence of digestion temperature on SDA in ectotherms (based on Wang et al., 2003).

lm

ass

ass

al m

Me

Fig. 8. Schematic illustrating the allometric relationship between animal body mass, meal size, and SDA increment (based on Beaupre, 2005).

M.D. McCue / Comparative Biochemistry and Physiology, Part A 144 (2006) 381–394

SDA and temperature employed larger sample sizes and thermal ranges greater than 5 °C than those described by Toledo et al. (2003). In a simultaneous investigation, Wang et al. (2003) found no thermal dependence of total energy devoted to SDA in pythons. The results of this study are indicative of most studies on thermal dependence of SDA, and are thus summarized in the following schematic (Fig. 6). Because of its dramatic effect on SDA, meal size is one of the most examined variables in SDA studies. Most recent investigations report that SDA is highly dependent on ration. However not all researchers arrive at this conclusion (Machida, 1981; Boyce and Clarke, 1997). As previously discussed, studies of endotherms typically conclude that energy devoted to SDA increases at a rate disproportionately greater than meal size, but most recent studies of ectotherms tend to suggest that increases in meal size result in disproportionately lower SDA responses (Andrade et al., 1997; Secor and Faulkner, 2002; Toledo et al., 2003; Zaidan and Beaupre, 2003; Fu et al., 2005) (Fig. 7). Variability among studies investigating the relationship between meal size and SDA has prompted Fu et al. (2005) to conclude, “More data about the effect of meal size on SDA in different kinds of animals should be documented….” Additional information about the effect of relative meal size is also required to further investigate the physiological basis for observed allometric relationships in SDA. Recent studies have uncovered the influence animal size has on SDA responses. Typically researchers consciously minimize the variance in the masses of the animals used in their studies, however studies investigating SDA in individuals of dramatically different size have revealed that SDA is dependent on animal mass (Secor and Faulkner, 2002; Zaidan and Beaupre, 2003; Beaupre, 2005). This observation was apparently first quantified by Beamish (1974) in feeding trials of bass. The figure below illustrates the generalized interaction between animal mass, meal mass and SDA (Fig. 8). Although many physiological responses associated with metabolism are well-known to scale with allometric exponents of 0.67 to 0.75 (Kleiber, 1932, 1947; Von Bertalanffy, 1957; Schmidt-Nielsen, 1970; Schmidt-Nielsen, 1975; West et al., 2000), little is known about why SDA responses are far less dependent on body mass. Only two physiological mechanisms have thus far been advanced to explain why SDA scales allometrically with body mass. The first hypothesis involves differential rates of intestinal tissue sloughing during digestion (Beamish, 1974), whereas the second hypothesis pertains to differential costs of upregulation of intestinal transporters (Secor and Faulkner, 2002). However because the costs involved in nutrient uptake are believed to be much less than the observed body-size related difference in SDA (McCue et al., 2005), additional hypotheses should be investigated. The energetic costs of gut upregulation on SDA have been debated in recent SDA literature, particularly in animals that undergo long periods of fasting between meals. This debate centers on the mechanism of gut upregulation exhibited by pythons (see Starck and Beese, 2001; Zaidan and Beaupre, 2003; McCue et al., 2002a,b; Overgaard et al., 2002). While the actual costs associated with gut remodeling in pythons still remain unknown, it is likely that the costs of gut upregulation in most

Metabolic rate

390

Duration Second feeding

Fig. 9. Schematic illustrating the additive response of the SDA response in pythons and turtles refed before metabolic rates returned to postabsorptive levels. The open circles represent the actual metabolic response to feeding on two meals, whereas the curves beneath the open circles represent the theoretical nonadditive SDA responses (based on data presented in Overgaard et al., 2002; Pan et al., 2005b).

animals are dramatically less than in pythons since most animals typically feed more frequently than pythons (Hailey, 1998). Two studies examining the costs of gut upregulation in pythons and turtles by refeeding postprandial animals before the terminus of the SDA response (Overgaard et al., 2002; Pan et al., 2005b) document an additive response between the end of the initial SDA response and the second SDA response (Fig. 9). Because these meals were fed so closely to one another gut atrophy (or gut-downregulation) could not occur, the results allowed the researchers to conclude that the cost of gut remodeling was negligible in this species. Additional research is required to determine if this pattern is exhibited in other animals. 5. Conclusion The energetic costs associated with SDA are the result of numerous preabsorptive, absorptive, and postabsorptive physiological processes. These costs vary with diet and might serve an important role in shaping natural history and foraging behavior in animal species. Although SDA responses can be easily detected in animals through indirect calorimetric measurements, accounts of SDA that rely exclusively on metabolic responses have demonstrated only limited promise in identifying the underlying causality of SDA. Several alternatives to simple measurements of metabolic rate show the greatest promise in identifying the dominant physiological processes responsible for SDA. One of the earliest experimental approaches to identify the specific tissues involved in SDA responses was made by William Dock. Dock (1931, 1934) ligated various organs in postprandial rats in order to identify how particular organs and tissues differentially contributed to SDA; he concluded that much of the energetic costs of physiological processing associated with SDA occurred in hepatic tissues. Modern experiments have been able to further expand this line of investigation. The use of chemicals that block particular processes (i.e. acid secretion and protein synthesis) have allowed researchers to develop estimates of the energetic contribution of specific physiological processes related to SDA. Forthcoming investigations might similarly involve drug use

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such as muscle relaxers to examine the energetic costs associated with peristalsis or hormone blockers to investigate the role of hormonal regulation of SDA. Other experimental approaches for investigating the causality of SDA might involve the use of artificial dialysis to examine the excretory costs associated with SDA, as well as technologies that allow measurements of blood flow, metabolism, and nutrient flux in various organs and tissues. The numbers of scientific studies investigating the phenomenon of SDA has grown dramatically over the past decade. This trend will likely continue as comparative researchers come to appreciate the interactions among SDA, whole animal energetics, and performance variables. I suggest we employ hypothesisdriven experiments that focus on three important areas of SDA research. The first area is identification of the causality of SDA in model organisms. The second area is characterization of SDA responses in novel species. The third area is exploration of the ecological and evolutionary significance of SDA in energy budgets of animals. Acknowledgments I wish to thank Drs. T.J. Bradley, A.F. Bennett, S.J. Beaupre, H. B. Lillywhite, K.E. McCue, and G. Huxel as well as R. Wittenberg for helpful comments on various phases of this manuscript. Constructive comments were also provided by two anonymous reviewers. I also wish to acknowledge funding provided by the National Science Foundation Predoctoral Fellowship and the Walton Distinguished Doctoral Fellowship awarded to MDM. References Adams, E.T., 1926. Specific dynamic action from the standpoint of the second and third laws of thermodynamics. J. Biol. Chem. 67, 21–22. Alsop, D., Wood, C., 1997. The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykis). J. Exp. Biol. 200, 2337–2346. Andrade, D.V., Cruz-Neto, A.P., Abe, A.S., 1997. Meal size and specific dynamic action in the rattlesnake Crotalus durissus (Serpentes: Viperidae). Herpetologica 53, 485–493. Ashworth, A., 1969. Metabolic rates during recovery from protein-calorie malnutrition: the need for a new concept of specific dynamic action. Nature 223, 407–409. Baumann, E.J., Hunt, L., 1925. On the relation of thyroid secretion to specific dynamic action. J. Biol. Chem. 64, 709–726. Beamish, F.W.H., 1974. Apparent specific dynamic action of largemouth bass, Micropterus salmonoides. J. Fish. Res. Board Can. 31, 1763–1769. Beaupre, S.J., 2005. Ratio representations of specific dynamic action (massspecific SDA and SDA coefficient) do not standardize for body mass and meal size. Physiol. Biochem. Zool. 78, 126–131. Beaupre, S.J., Dunham, A.E., Overall, K.L., 1993. Metabolism of a desert lizard: the effects of mass, sex, population of origin, temperature, time of day, and feeding on oxygen consumption of Sceloporus merriami. Physiol. Zool. 66, 128–147. Belokopytin, Y.S., 2004. Specific dynamic action of food and energy metabolism of fishes under experimental and natural conditions. Hydrobiol. J. 40, 68–75. Benedict, F.G., 1932. The Physiology of Large Reptiles. Carnegie Institution, Washington. Blaxter, K.L., 1989. Energy Metabolism in Animals and Man. Cambridge, New York. Borsook, H., 1935. The correlation between excess calories and excess urinary nitrogen in the specific dynamic action of protein in animals. Proc. Natl. Acad. Sci. U. S. A. 21, 492–498.

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