Effect of Meal Type on Specific Dynamic Action in the Green Shore Crab, Carcinus Maenas

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Effect of meal type on specific dynamic action in the green shore crab, Carcinus maenas

Article in Journal of Comparative Physiology B · February 2014 DOI: 10.1007/s00360-014-0812-5 · Source: PubMed

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Iain J McGaw Chantelle M Penney Memorial University of Newfoundland Trent University

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Iain J. McGaw & Chantelle M. Penney

Journal of Comparative Physiology B Biochemical, Systems, and Environmental Physiology

ISSN 0174-1578 Volume 184 Number 4

J Comp Physiol B (2014) 184:425-436 DOI 10.1007/s00360-014-0812-5

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J Comp Physiol B (2014) 184:425–436 DOI 10.1007/s00360-014-0812-5

Original Paper

Effect of meal type on specific dynamic action in the green shore crab, Carcinus maenas

Iain J. McGaw · Chantelle M. Penney

Received: 14 December 2013 / Revised: 21 January 2014 / Accepted: 31 January 2014 / Published online: 15 February 2014 © Springer-Verlag Berlin Heidelberg 2014

Abstract The effect of meal type on specific dynamic a large variation in the amount of food eaten. The lack of action was investigated in the green shore crab, Carci- significant differences in the SDA response as a function nus maenas. When the crabs were offered a meal of fish, of nutrient content was likely due to differences in amount shrimp, or mussel of 3 % of their body mass the duration of food eaten, which is a major factor determining the SDA of the SDA response and thus the resultant SDA was lower response. The differences in SDA when consuming natural for the mussel, compared with the shrimp or fish meals. In food items were likely due to a combination of the costs of feeding behaviour experiments the crabs consumed almost mechanical digestion, variation in nutrient content and food twice as much mussel compared with fish or shrimp. When preference: determining how each of these factors contrib- the animals were allowed to feed on each meal until sati- utes to the overall SDA budget remains a pressing question ated, the differences in the SDA response were abolished. for comparative physiologists. The mussel was much softer (compression test) than the fish or shrimp meal, and meal texture is known to affect Keywords Carcinus maenas · Crab · Digestion · the SDA response in amphibians and reptiles. When the Feeding · Respiration · Specific dynamic action crabs were offered a meal of homogenized fish muscle or whole fish muscle, the SDA for the homogenized meal was approximately 35 % lower. This suggested that a sig- Introduction nificant portion of the SDA budget in decapod crustaceans may be related to mechanical digestion. This is not unex- The specific dynamic action of food or SDA describes a pected since the foregut is supplied by over forty muscles postprandial increase in metabolism. This increase in met- which control the cutting and grinding movements of the abolic rate, which is usually measured as an increase in gastric mill apparatus. There were slight, but significant oxygen consumption, represents the sum of activities asso- differences in protein, lipid, moisture and total energy con- ciated with the processing of the food, ingestion, mechani- tent of each meal type. Three prepared meals that were cal breakdown in the gut and the subsequent transport and high in either protein, lipid or carbohydrate were offered intracellular digestion of the nutrients (Mente 2003; Secor to the crabs to determine if the nutrient content was also a 2009). The characteristics of the SDA response meas- contributing factor to the observed differences in the SDA. ured include the time to reach peak oxygen consumption, The crabs did not eat the prepared meals as readily as the the peak oxygen consumption and/or the scope of oxygen natural food items and as they are messy feeders there was uptake (difference between resting and peak metabolism), and the duration that the postprandial metabolism remains elevated. The SDA or energy equivalent of the metabolic Communicated by I.D. Hume. response is most often used to quantify energy expenditure. It represents the accumulated energy expended above the * I. J. McGaw ( ) · C. M. Penney baseline for the duration of the SDA response (Secor 2009). Department of Ocean Sciences, Memorial University, 0 Marine Lab Road, St John’s, NL A1C 5S7, Canada When the meal size and environmental temperature are e-mail: [email protected] controlled, the nutrient content of the meal and the type

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426 J Comp Physiol B (2014) 184:425–436 of meal also affect some of the characteristics of the SDA due to the cost of transport of stomach acids and digestive response. The general pattern is that meals high in protein enzymes to break down the intact meal, rather than energy generate larger SDAs than those that have a higher lipid required for mechanical breakdown by peristaltic contraction or carbohydrate content (reviewed in McCue 2006; Secor of the stomach muscles (Secor 2003; Boback et al. 2007). 2009). In the fish Oncorhynchus mykiss, Cyprinus car- Different diets have been evaluated for commercially pio, Oreochromis niloticus and Silurus meridionalis, an important species of shrimp and lobster; however, these increase in the percentage of protein leads to an increase articles tend to concentrate on short-term changes in oxy- in the SDA (LeGrow and Beamish 1986; Chakraborty et al. gen consumption (1–6 h) and feed conversion efficiency 1992; Ross et al. 1992; Fu et al. 2005). However, this pat- ratios, rather than the SDA (Nelson et al. 1977, 1985; Rosas tern is not universal, for example, increased protein content et al. 1995, 1996; Brito et al. 2000; Crear et al. 2002; Perera does not produce an observable change in the SDA of the et al. 2005; Huang et al. 2008; Díaz-Iglesias et al. 2011). blue gill, Lepomis machrochirus, sea bass, Dicentrarchus The general trend is metabolic rate increases with increas- labrax or horned frog, Ceratophrys cranwelli (Schalle and ing protein content of the meal; however, the exact pattern Wissing 1976; Peres and Oliva-Teles 2001; Grayson et al. is dependent on the species and the quality of both proteins 2005). The SDA is also influenced by the relative propor- and lipids. Other works have investigated the longer-term tions of lipids and proteins, and meals with a higher lipid effects of diet on metabolism: The isopod Ligia pallasii to protein ration evoke larger SDAs because the lipids may exhibits higher oxygen consumption rates after 30 days of have a protein sparing effect (LeGrow and Beamish 1986; feeding on brown algae compared with green or red algae Chakraborty et al. 1992; Fu et al. 2005; Luo and Xie 2008). (Carefoot 1987), whereas Ligia exotica exhibits higher The nutrient type is also important, digestion of complex oxygen uptake rates when fed a mixed diet of algae and proteins produces SDA’s of greater magnitude compared diatoms compared to either red or green algae (Carefoot with simple proteins or those lacking specific amino acid 1989). Very few papers have directly addressed the effects residues (McCue et al. 2005). of meal type on the SDA of crustaceans. The copepod There is comparatively less information on the SDA Acartia tonsa has a higher SDA coefficient when feeding responses of organisms consuming natural prey items. In on the flagellate Tetraselmis impellucida versus Dunaliella the tortoise Kinixys spekii the highest SDA occurs after eat- tertiolecta, which is associated with high protein assimila- ing millipedes, while lower SDAs are measured when they tion at the tissue level (Thor et al. 2002). The scope and consume leaves or fungi; this is related to the higher protein magnitude of the SDA in Ligia pallasii are higher after a content of millipedes (Hailey 1998). In the skink Eumeces meal of brown algae compared to green algae. However, chinensis the SDA peak and magnitude are greater for a high they ate twice as much brown algae (Carefoot 1989) and protein meat meal compared with meal worms that have this, rather than diet likely accounted for the difference lower protein content (Pan et al. 2005). A similar pattern is (Carefoot 1989; McGaw and Curtis 2013a). observed for the ascidian Ciona intestinalis which exhibits The species chosen for this study, the green crab Carcinus a significantly higher SDA after feeding on flagellates com- maenas, is an important invasive species in temperate marine pared to detritus (Sigsgaard et al. 2003). However, the nutri- environments; it occurs in the shallow subtidal and intertidal ent content of a natural meal is not the only factor to affect zones as well as in estuaries. As such it is an opportunistic the SDA. Consumption of vertebrate prey results in larger predator on a wide variety of both fresh and decaying mate- SDA’s in the garter snake Thamnopis sirtalis compared to rial including, but not limited to, bivalves, worms, crusta- consumption of soft bodied invertebrate prey (Bessler et al. ceans, carrion, detritus and algae (Behrens-Yamada 2001). 2010). The gila monster Heloderma suspectum, exhibits a Therefore, the aim of the present study was to investigate lower SDA when feeding on chicken eggs compared to an feeding behaviour on natural prey items and to determine equal sized meal of juvenile rats (Christel et al. 2007). Like- how consumption of these may affect the characteristics of wise, for a variety of anuran and salamander species fed hard the SDA response. The nutrient content of the meal was also bodied superworms, meal worms and crickets both the dura- manipulated to determine if this would also affect feeding tion and the magnitude of the SDA response are higher than behaviour and the SDA response of Carcinus maenas. when these species consume soft bodied red worms, beetle larva or neonatal rodents (Secor and Faulkner 2002; Secor and Boehm 2006; Secor et al. 2007). These authors sug- Materials and methods gested that it takes more energy to break down and assimilate the hard-bodied prey items (Secor 2009). Related to this, the Animal collection and housing physical state of the meal can influence the SDA response. Indian pythons, Python molurus, expend more energy to Adult intermoult male green crabs, Carcinus maenas (65– digest a whole rat versus a ground rat. This is primarily 100 g), were collected from North Harbour, Newfoundland

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J Comp Physiol B (2014) 184:425–436 427 and maintained at 30–32 ‰ and 14–16 °C at the Depart- were surrounded by black plastic sheeting to avoid visual ment of Ocean Sciences, Memorial University. They were disturbance to the animal. The resting metabolic rate (post- acclimated to laboratory conditions for at least 7 days, and absorptive, minimal activity) was recorded for a 3-h control all experiments were carried out at the holding tempera- period. The animals were then fed the test meal; any ani- ture and salinity. The animals were fed fish twice a week mals that did not eat all the food offered were not used in and allowed to eat until satiated, but were isolated from the the analyses. All the crabs had finished feeding by the time general population and fasted for 3–6 days prior to experi- the first postprandial oxygen consumption reading (0.5 h) mentation. This time period allowed all food to be evacu- was completed. Oxygen consumption was recorded until ated from the digestive system, but avoided large-scale it returned to pre-feeding levels. For each experiment the physiological changes associated with starvation (Wallace following parameters were calculated: (a) the time to reach 1973). peak oxygen consumption following feeding, (b) The scope of the SDA response—peak oxygen consumption divided Behaviour by the basal pre-feeding rates (RMR) (c) the duration of the SDA response—until oxygen dropped back to pre-feeding The feeding behaviour was assessed to determine how levels and (d) the SDA of each animal was calculated from much of each meal type a crab would consume. The food the total increase in oxygen uptake above baseline levels was soaked in seawater overnight to minimize any osmotic and standardized to kJ using the conversion factor of 1 mg gain or loss of water and was patted dry in paper towels O 14 J (Secor 2009). Differences in parameters were 2 = before being weighed. During feeding individual crabs compared using one-way ANOVAs or Student t tests. Data were held in plastic boxes of 25 cm 15 cm 10 cm showing a significant effect were further analysed with a × × depth with 1 mm mesh screen on the sides. Fifteen crabs Fisher LSD post hoc test. Data that were not normally dis- were offered an excess of either mussel, fish, or shrimp. tributed were analysed with a Kruskal–Wallis non-paramet- The animals were allowed to consume the food and when ric ANOVA on ranks followed by a Dunn post hoc test or they had ceased feeding for 1 h the experiment was termi- two samples were analysed with Wilcoxon rank sum tests. nated. The remaining food was collected with forceps, pat- In the first series of experiments the animals (n 10–11 = ted dry and weighed to calculate the wet mass consumed separate animals per meal type) were offered three natu- and was expressed as percent body weight eaten. The feed- ral prey items. The crabs were fed of 3 % of their body ing experiment was then repeated with three prepared diets weight (wet mass) of mussel flesh (Mytilus edulis), fish (high protein, fat or carbohydrate). Control samples of food muscle (sole), or shrimp muscle. The experiment was were also placed in empty mesh cages, the samples were then repeated, allowing the animals to feed ad libitum on weighed at the start and end of the experiment and any each meal; any excess was removed after they had finished weight gain or loss of the samples was adjusted for in the feeding for 1 h. A second series of experiments were car- final calculation of mass of food eaten. ried out to determine if the meal texture would affect the SDA. The crabs (n 13) were fed 2.5–3.0 % of their body = Oxygen consumption mass of sole flesh. The flesh was broken down to a paste- like texture with a tissue homogenizer and either com-

Oxygen consumption (mg O2 kg/h) was measured using a pacted pieces of paste or whole pieces of fish were offered L-DAQ intermittent flow respirometry system (Loligo sys- to the crabs. In a final series of experiments the effects tems, Copenhagen, Denmark). This fully automated system of meals high in protein, lipids or carbohydrates on the is equipped with two pumps: the first pump continually SDA response were investigated. The crabs (n 10) were = flushes seawater through the chamber while it is open. The offered prepared meals of 3 % of their body weight. The chamber is sealed for measurements and a second pump re- high-protein diet consisted of ground sole (70 % wet mass) circulates the water through the chamber at a rate of 10 L/ in gelatin (30 % wet mass) and had an energetic content min ensuring that oxygen gradients do not build up within of 4.35 0.15 kcal/g dry weight, the high lipid diet con- ± the chamber. During experiments the animals were held in sisted of sole (45 % wet mass) blended with lard (15 % wet cylindrical chambers (20 cm diameter 12 cm depth) and mass) and menhaden oil (10 % wet mass) in gelatin (30 % × allowed to settle for 12 h. Oxygen consumption was cal- wet mass) with an energetic content of 7.05 0.13 kcal/g ± culated during a 20-min decline in oxygen levels while the and the high-carbohydrate diet consisted of sole (45 % chamber was sealed; then the chamber was continuously wet mass), blended with potato starch paste (25 % wet flushed for 10 min between readings. Data was recorded on mass) in agar (30 % wet mass) with an energetic content a Loligo data acquisition system (Copenhagen, Denmark). of 4.15 0.05 kcal/g. A small amount of commercial crab ± The experiments were carried out in constant dim light, attractant (Pautzke crab ‘n’ shrimp fuel®) was also added to which helped reduce any diurnal rhythms and the apparatus each meal.

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Digestion constant weight. The caloric energy value of the dried sam- ples (0.1 g) was measured using a bomb calorimeter (Parr The clearance rates of the foregut were investigated using Instruments, SemiMicro, Moline, IL). Digestive efficiency a serial slaughter technique (Hill 1976; Choy 1986). The was calculated using the equation outlined in Romero crabs were fed mussel, shrimp or fish of approximately et al. (2006): AE [EC food dry mass (g) EC fae- = × − 3 % of the body mass and allowed 1 h to consume the food. ces dry mass (g)/EC food dry mass (g)] 100, where × × × Six crabs were removed from each feeding treatment at set AE assimilation efficiency andE C energetic content. = = intervals and immersed in iced seawater for 5 min to induce Differences in assimilation efficiencies were tested with a a chill coma and to halt the digestive processes. They were one-way ANOVA followed by Fishers LSD post hoc tests. then frozen and stored at 20 °C. For analysis the animals − were thawed, the foregut was dissected and the digesta was Proximate analysis of food rinsed out with distilled water. These contents were dried to constant weight at 60 °C. A foregut clearance index was Samples of the meals were processed by the Centre for derived by multiplying the dry mass of the digesta by the Aquaculture and Seafood Development at the Marine Insti- reciprocal of the carapace width to standardize for size tute, Memorial University. Moisture content was calcu- (Simon 2009). Regression lines were fitted to the data and lated by drying the sample to constant weight in an oven the slopes of the lines compared (Zar 1984). at 60 °C. The ash-free dry weight of the samples were In order to determine if there was any correlation between determined by placing 3 g of dried sample in a crucible the characteristics of the SDA and digestion, the transit time and heating to 550 °C in a muffle furnace for 15 h. The of a radio-opaque meal was followed through the digestive remaining inorganic material was weighed and percentage system. The crabs were fed a radio-opaque meal consisting ash calculated. Fat was extracted from the dry samples by of electrolytic iron powder (10 % by mass) and gelatin (15 % acid hydrolysis and the lipid content in each of the samples by mass) added to whole pieces of mussel, fish or shrimp was calculated using a modified Soxhlet method (Booij and (McGaw 2006). During experiments the animals (n 8 per van den Berg 1994). The protein content of the samples = food item) were housed in individual chambers where they was measured using the Kjeldahl method: this measures the were allowed to settle for 3 h before initiation of the experi- total amount of nitrogen in the sample; the results therefore ment. The animals were offered the food and allowed 15 min represent the crude protein content of the sample because to eat the meal; those that did not eat the entire meal were some nitrogen may have come from non-protein compo- not used in the analysis. For X-ray analysis a plastic box was nents (Bradstreet 1954). Carbohydrate levels were calcu- submerged in the chamber and the animals were coaxed into lated as the remaining percentage difference from totals the box. The box was then placed in under a LIXI PS500 of moisture, ash free weight, lipid and protein levels. The OS, X-ray system with LIXI image processing software. A caloric energy value of 0.1 g dried sample was measured still image of the gut system was captured at hourly intervals using a semi-micro bomb calorimeter (Parr Instruments). for the first 12 h and then at 3–12 h intervals following this The compressibility of each food item was measured using period. Technical specifications for X-ray were 35 kV tube a TA-XT Plus analyzer (Stable Micro Systems Ltd, Surrey, voltage and 155 μA tube current with a 5 cm focal window. UK). Tests were performed using a flat cylindrical 9.5 mm The movement of the digesta and marker was followed until it probe using a 50 % compression test. Differences in param- had been voided in the faeces and the time of emptying of the eters were compared using one-way ANOVAs. Data show- foregut, midgut and hindgut regions was calculated (McGaw ing a significant effect were further analysed with a Fisher 2006). Differences in transit rates as a function of meal type LSD post hoc test. Data that were not normally distrib- were analysed using a 2-way repeated measures ANOVA. uted were analysed with a Kruskal–Wallis non-parametric The digestive efficiency was assessed following the ANOVA on ranks followed by a Dunn post hoc test. consumption of a mussel, fish or shrimp meal. During feeding the crabs (n 6 per treatment) were held in plas- = tic boxes of 25 cm 15 cm 10 cm depth with 1 mm Results × × mesh screen on the sides and were offered a pre-weighed meal of mussel, fish or shrimp. The animals were allowed Feeding behaviour to consume the food and when they had ceased feeding for 1 h the remaining food was collected with forceps, patted When the crabs were allowed to feed ad libitum on mussel, dry and weighed to calculate the mass consumed. At daily fish or shrimp flesh they had all stopped feeding within 1 h. intervals (for a total of 3 days) faeces were removed and The crabs consumed on average 6.91 0.6 % of their body ± washed with distilled water to prevent salt crystallization. mass of mussel flesh; this was significantly greater than The faeces and samples of the food were dried at 60 °C to the 3.39 0.55 % body mass of fish or the 4.34 0.3 % ± ± 1 3 Author's personal copy

J Comp Physiol B (2014) 184:425–436 429 body mass of shrimp flesh eaten (ANOVA, F 13.34, = P < 0.001). When crabs were offered three artificial diets high in either protein, fat or carbohydrates all feeding had ceased within 45 min. The crabs consumed 3.31 0.43 % ± of their body mass of the protein meal, 2.83 0.53 % body ± mass of the fat meal and 4.37 0.72 % body mass of the ± carbohydrate meal; there were no significant differences between these values (ANOVA, F 1.86, P 0.173). = = Oxygen consumption

Carcinus maenas exhibited a sharp increase in oxygen con- sumption immediately following feeding with a slower sus- tained decrease to pre-feeding levels over the subsequent 48 h (Fig. 1). In some cases there was a significant variation in resting metabolic rate (RMR), not only between individ- ual treatments, but also within individual animals over time (Tables 1, 3). When the crabs were fed a meal of 3 % of their body mass, the duration of the SDA response for crabs consum- ing mussels was approximately half of that of animals that ate a meal of fish or shrimp (Table 1). The increased duration for fish and shrimp meals resulted in significantly higher SDAs compared with the mussel meal. The SDA coefficient of the shrimp meal was significantly higher than that calculated for the mussel meal or the fish meal which were not significantly different from one another (Table 1). When the animals were allowed to feed on each of the three food items ad libitum there was no significant difference in any of the characteristics of the SDA response (Table 1). When the crabs ate an homogenized meal of fish, they reached peak oxygen consumption at a faster rate com- pared with crabs that were offered whole pieces of fish (Table 2). Although there was no significant difference in the scope or the duration of the SDA response, oxygen consumption declined more sharply following ingestion of the homogenized meal (Fig. 2), resulting in an SDA that was approximately 35 % lower. The SDA coefficient of the Fig. 1 a Changes in oxygen consumption for the green shore crab homogenized meal was also less than half that measured Carcinus maenas following consumption of a meal of either fish, for consumption of whole pieces of fish (Table 2). mussel or shrimp totaling 3 % of their body mass. b The experiment When the crabs were offered prepared meals (3 % of body was repeated with separate animals allowing them to consume fish, mussel, or shrimp until satiated. The data represent mean SEM of mass) high in protein, fat or carbohydrates there was a large 10–11 individuals ± variation in the amount of food consumed. The time to reach peak oxygen consumption was most rapid for the fat meal and slowest for the protein meal (Fig. 3; Table 3). There were were in the 30 to 50 mm3 range; larger pieces were tubu- no significant differences in any of the other characteristics of lar in shape and were up to 650 mm3 in size. The average the SDA response for each of the three prepared meal types. sizes of large pieces of the fish, 162.5 35.5 mm3, mussel ± 121.6 21 mm3 and shrimp, 178.5 50.9 mm3, in the gut ± ± Digestion were not significantly different from one another (ANOVA, F 0.54, P 0.59). Fine pieces of shrimp and mussel were = = The clearance of food from the foregut was followed also found in the midgut region 1 h after feeding, but no fish between 1 and 12 h after feeding (Fig. 4). At 1 h pieces of was evident at this time. By 12 h after feeding the foregut food were easily recognisable in the foregut the majority region contained less than 10 % of each of the original meals

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Table 1 Characteristics of the Meal type SDA response of two groups of Carcinus maenas Fish Mussel Shrimp Statistics

Meal Fixed = Body mass (g) 84.1 4.4 82.8 4.3 74.8 5.1 F 1.18, P 0.324 ± a ± b ± a = = RMR (mg O2 kg/h) 53.2 1.49 66.4 1.51 57.3 1.38 H 37.3, P < 0.001* The first group of crabs were ± ± ± = Peak VO2 (mg O2 kg/h) 181.96 13.91 196.00 8.84 171.49 9.33 F 1.26, P 0.296 fed a meal of fish, mussel or ± ± ± = = Time to peak (h) 5.04 1.24 3.67 0.53 3.46 0.84 H 1.33, P 0.52 shrimp of 3 % of their body ± ± ± = = mass (n 10). The second Scope (peak MO2/RMR) 3.34 0.26 3.00 0.22 3.09 0.17 F 0.65, P 0.53 = ± ± ± = = group were (n 10–11) fed the Duration (h) 39.31 3.79a 19.83 2.21b 40.5 2.74a H 16.70, P < 0.001* = ± ± ± = same meals but were allowed SDA (kJ) 1.81 0.20a 0.77 0.08b 1.58 0.15a H 19.19, P < 0.001* to eat until satiated. Values ± ± ± = SDA (kJ/kg) 22.10 2.40a 9.81 0.81b 22.67 3.58a H 21.46, P < 0.001* represent the mean SEM. ± ± ± = Data were analysed± with student SDA coefficient (%) 14.02 1.30a 12.53 1.82a 21.72 1.79b H 11.61, P 0.003* ± ± ± = = t tests, or Mann–Whitney U Meal Satiation tests and significance reported = Body mass (g) 81.6 4.3 78.9 2.9 81.6 2.3 H 0.17, P 0.92 at the P < 0.05 level. Like ± ± ± = = RMR (mg O kg/h) 47.8 1.18a 50.0 1.86ab 52.6 1.15b H 8.26, P < 0.016* letters are not significantly 2 ± ± ± = different from one another. Peak VO (mg O kg/h) 201.89 20.84 209.82 18.56 169.09 8.05 F 1.80, P 0.118 2 2 ± ± ± = = Asterisk denotes significance at Time to peak (h) 3.50 0.90 1.70 0.48 3.50 0.81 H 4.18, P 0.13 the P < 0.05 level ± ± ± = = Scope (peak MO /RMR) 4.22 0.38 4.42 0.56 3.20 0.17 F 2.92, P 0.071 a These values were calculated 2 ± ± ± = = Duration (h) 45.65 4.16 47.85 5.32 49.18 7.57 F 0.09, P 0.915 using the mean mass of each ± ± ± = = food item consumed from the SDA (kJ) 2.35 0.28 2.29 0.29 2.04 0.36 F 0.27, P 0.765 ± ± ± = = feeding behaviour experiments SDA (kJ/kg) 29.74 4.07 29.44 4.09 24.54 3.95 F 0.54, P 0.588 ± ± ± = = and therefore represent an esti- SDA coefficient (%)a 18.94 2.59 14.53 2.02 18.32 2.95 F 0.84, P 0.444 mate only ± ± ± = =

Table 2 Characteristics of the SDA response of two groups of Carcinus maenas Whole food Ground food Statistics

Body mass (g) 78.23 4.26 83.67 3.28 t 1.02, P 0.325 ± ± = − = RMR (mg O kg/h) 44.74 3.11 43.49 2.85 U 113, P 0.571 2 ± ± = = Peak VO (mg O kg/h) 151.88 10.25 144.75 12.99 t 0.43, P 0.672 2 2 ± ± = − = Time to peak (h) 6.05 1.44 1.75 0.75 U 66.5, ± ± P= − 0.004* = Scope (peak MO /RMR) 3.41 0.18 3.34 0.20 t 0.27, P 0.790 2 ± ± = − = Duration (h) 52.05 4.10 46.10 5.09 t 0.91, P 0 .375 ± ± = = SDA (kJ) 1.73 0.21 1.10 0.21 t 2.12, P 0.048* ± ± = = SDA (kJ/kg) 21.93 2.00 13.13 2.33 t 2.87, P 0.010* ± ± = = SDA coefficient (%) 21.76 1.98 10.70 1.93 t 3.99, P < 0.001* ± ± = The first group of crabs was fed a meal of whole fish muscle, while the second group was offered a fish muscle that had been broken down in a tissue homogenizer (n 13). Values represent the mean SEM. Data were analysed with student t tests, or Mann–Whitney U tests and signifi- cance reported at the P= < 0.05 level. Like letters are not± significantly different from one another. Asterisk denotes significance at the P < 0.05 level which consisted of very fine particles suspended in a liquid. entered the midgut and hindgut before the fish meal, although The slopes of the regression were compared and there was this trend was not statistically significant (Kruskal-Wallis; no difference in the rate of foregut clearance between fish H 1.86, P 0.500 and H 1.76, P 0.414, respectively). = = = = and mussel (t 0.69, P 0.495), fish and shrimp (t 0.86, Due to large inter-individual variation there were no differ- = = = P 0.393) or mussel and shrimp (t 0.18, P 0.861). ences in emptying times of the foregut (ANOVA, F 0.018, = = = = A fluoroscope was used to follow the movement of digesta P 0.982), midgut (ANOVA, F 0.439, P 0.652) or = = = into the midgut and hindgut regions and clearance of mate- hindgut regions (ANOVA, F 2.058, P 0.167). = = rial from the foregut, midgut and hindgut region (Fig. 5). In The crabs used in the digestive efficiency experiments line with the foregut evacuation results, shrimp and mussel consumed significantly more mussel tissue (dry mass)

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Fig. 2 Changes in oxygen consumption for two groups of Carcinus Fig. 3 Changes in oxygen consumption for in the green shore crab maenas fed a meal of fish muscle (2.5–3 % of their body mass) that Carcinus maenas fed a prepared meal of 3 % of their body mass was either whole or had been reduced to a paste with a tissue homog- that was high in protein, carbohydrate or lipid. The data represent enizer The data represent mean SEM of 11–13 individuals mean SEM of 10 individuals for each treatment ± ± compared with either fish or shrimp. The dry mass of fae- resting metabolic levels and can remain elevated for ces produced was linked to the amount of food consumed, between 12 and 48 h, depending on the species and the size with more faeces produced by crabs consuming the greatest of the meal (McGaw and Curtis 2013a). The characteristics amount of food (Table 4). Digestive efficiency was high for of the SDA response obtained here for Carcinus maenas each meal (>98 %) and there was no significant difference were similar to those recorded for other species (Houlihan between each of the three meals (Table 4). et al. 1990; McGaw 2006; Curtis and McGaw 2010; McGaw and Curtis 2013a); however, unlike many of the other spe- Proximate analysis cies there was a significant variation in oxygen uptake rates between and within individual animals. The crabs exhib- There were a number of significant differences in nutrient ited spontaneous periods of activity which appeared to be content of the three meals (Table 5). The caloric energy unrelated to endogenous rhythms or exogenous cues; such content of 1 g of dry mass of the fish meal was higher than behaviour is common for this species and likely accounted that of the shrimp, which in turn was higher than that of for differences in resting metabolic rate between groups mussel. The fish also had a slightly higher protein and fat (Reid and Naylor 1990; Warman et al. 1993). content and a lower ash and moisture content than either When Carcinus maenas was allowed to feed ad libitum the mussel or shrimp. When the caloric content of the three on the three natural prey items they consumed more mussel meals was calculated taking into account the differences in flesh (almost 7 % BW) than shrimp or fish. This species moisture and ash content, the meals were still in the same has a broad diet ranging from small fish to algae and detri- order with fish having 1.1 kcal/g, shrimp 0.74 kcal/g, and tus (Behrens-Yamada 2001), which would tend to argue mussel having an energetic content of 0.69 kcal/g per 1 g of against a simple preference (Kittaka and Booth 2000). wet flesh. The compressibility values (softness) of the fish The mussel flesh had the lowest protein and energy con- and shrimp flesh were both significantly higher than that of tent and the highest moisture content and there was a rela- the mussel (Table 5). tionship between energy content and amount of food eaten, with more of the lower energy food consumed. A number of other invertebrate species can select meals of different Discussion nutritional quality depending on their metabolic needs (Loo and Bitterman 1992; Behmer et al. 2005; Behmer 2009; The postprandial increase in oxygen consumption in deca- Lee et al. 2012). However, when the crabs were offered pod crustaceans typically peaks at 1.5- to threefold above artificial foods with more pronounced differences in

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Table 3 Characteristics of the SDA response of Carcinus maenas Meal type Protein Fat Carbohydrate Statistics

Meal Fixed = Body mass (g) 78.6 3.1 78.9 4.8 78.8 1.1 F 0.21, P 0.998 ± ± ± = = RMR (mg O kg/h) 48.11 1.34a 42.87 1.29b 45.82 1.50ab F 3.76, P 0.026* 2 ± ± ± = = Peak VO (mg O kg/h) 136.39 9.06 143.27 13.55 139.81 10.22 F 0.10, P 0.909 2 2 ± ± ± = = Time to peak (h) 5.25 1.25a 1.65 0.57b 3.1 0.75ab F 4.20, P 0.03* ± ± ± = = Scope (peak MO /RMR) 2.88 0.24 3.43 0.33 3.18 0.34 F 0.82, P 0.45 2 ± ± ± = = Duration (h) 42.7 5.77 42.60 3.73 32.9 4.05 F 1.49, P 0.243 ± ± ± = = SDA (kJ) 1.09 0.18 1.39 0.35 0.71 0.12 F 2.06, P 0.147 ± ± ± = = SDA (kJ/kg) 13.85 2.16 17.52 4.09 9.20 1.61 H 2.82, P 0.244 ± ± ± = = The crabs (n 10 per treatment) were offered prepared meals of 3 % of their body mass that were high in carbohydrate, lipid or protein. Values represent the =mean SEM. Data were analysed with student t tests, or Mann–Whitney U tests and significance reported at theP < 0.05 level. Like letters are not significantly± different from one another. The SDA coefficients were not calculated here because the amount of food ingested (and thus the energetic content) could not be reliably measured for animals in the apparatus. Asterisk denotes significance at the P < 0.05 level nutrient and energy content there was no difference in con- suggesting a simple volume constraint limiting the amount sumption rates, which would tend to argue against a prefer- of fish and shrimp that could be ingested at any one time. ence based on the nutritional quality of the meal. Decapod When fed an equal amount of each meal, the postpran- crustaceans will typically feed until the foregut is full and dial oxygen uptake rates of crabs that consumed the mussel need to empty the foregut before they can take in extra food declined to pre-feeding levels before those that consumed (Condrey et al. 1972). A large meal for a decapod crusta- shrimp or fish; this resulted in a lower SDA for the mus- cean is typically 3–5 % of their body weight (Simon 2009; sel meal (Fig. 1; Table 1). The magnitude of the SDA in Curtis et al. 2010), and the consumption levels of shrimp and fish fell within this range. The mussel flesh was softer and thus much more compressible than the fish or shrimp,

Fig. 5 Transit times of food through regions of the digestive system of Carcinus maenas. The animals were fed a meal of chunks of fish, mussel or shrimp that were mixed with a radio-opaque marker (elec- trolytic iron powder) and gelatin. The passage of the digesta was fol- Fig. 4 Index of foregut clearance rates of Carcinus maenas fed lowed through the digestive tract until the meal had been completely a fish, shrimp or mussel meal of 3 % of their body weight, linear voided. Data represents the mean SEM of eight animals per treat- regression lines were fitted to each treatment ment ±

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Table 4 Digestive efficiency of the of fish, mussel and shrimp meals when animals were allowed to feed to satiation Fish Mussel Shrimp Statistics

Food consumed (g) 0.60 0.07a 1.07 1.12b 0.59 0.07a F 9.18, P 0.002* ± ± ± = = Food energy content (kcal/g) 5.51 0.03a 4.45 0.07b 4.89 0.02c F 127.33, P < 0.001* ± ± ± = Faeces produced (g) 0.016 0.004ab 0.023 0.001a 0.013 0.001b H 0.086, P 0.018* ± ± ± = = Feces energy content (kcal/g) 2.70 0.16a 3.47 0.06b 2.91 0.16a F 8.63, P 0.003* ± ± ± = = Assimilation efficiency (%) 98.74 0.22 98.22 0.22 98.62 0.19 F 1.66, P 0.224 ± ± ± = = Data represent mean SEM of six animals per treatment. Like letters are not significantly different from one another.Asterisk denotes signifi- cance at the P < 0.05 ±level

Table 5 Proximate analysis of the three meal types Fish Mussel Shrimp Statistics

Protein (%) 17.03 0.93a 13.54 0.92b 13.74 0.11b F 6.51, P 0.031* ± ± ± = = Fat (%) 1.57 0.04a 1.33 0.11b 0.05 0.03c F 136.76, P < 0.001* ± ± ± = Carbohydrate (%) 1.41 0.84 0.82 0.61 1.24 0.38 F 0.23, P 0.802 ± ± ± = = Moisture (%) 79.17 0.14a 82.54 0.41b 81.70 0.39ab H 5.96, P 0.025* ± ± ± = = Ash (%) 0.82 0.02a 1.77 0.06b 3.18 0.08c F 413.01, P < 0.001* ± ± ± = Energy content (kcal/g dry mass) 5.51 0.03a 4.45 0.07b 4.89 0.02c F 127.33, P < 0.001* ± ± ± = Compressibility (N) 6.68 0.34a 1.64 0.37b 7.97 0.77a F 45.15, P < 0.001* ± ± ± = Data represent mean SEM of 5–10 samples per treatment. Like letters are not significantly different from one another. Asterisk denotes significance at the P <± 0.05 level this and other species of crustaceans is primarily influenced into the midgut and hepatopancreas for further digestion by the duration of the SDA response (Houlihan et al. 1990; and absorption (Heinzel et al. 1993; McGaw and Cur- McGaw and Curtis 2013a). There was no difference in tis 2013a, b). In support of this assumption, the SDA for the scope of the SDA response for each meal; this is com- Carcinus maenas consuming homogenized fish paste was mon in crustaceans and suggests that a substantial amount approximately 35 % lower compared with whole pieces of of energy is required to upregulate the digestive system, fish pieces (which were still relatively large when bitten off irrespective of meal type or size (Boyce and Clarke 1997; with the mandibles and swallowed). In snakes the majority McGaw and Curtis 2013a). For crustaceans a large propor- of the difference in energy cost between homogenized and tion of the increase in postprandial metabolic rate has been whole meals is connected with HCl production and trans- attributed to intracellular protein synthesis (Mente 2003; port. Since crustaceans do not employ acid digestion it is Mente et al. 2003), while virtually no energy in copepods likely that the increase in energy expenditure was required (Kiorboe et al. 1985) and only 5–8 % of the total SDA for by the gastric mill to process the intact fish muscle. These isopods (Carefoot 1989, 1990) is expended as mechani- findings contradict those reported for lower order crusta- cal energy to move the meal through the gut. The foregut ceans (Kiorboe et al. 1985; Carefoot 1989, 1990). How- of copepods and isopods is much simpler and most of the ever, the gastric mill of decapod crustaceans is a large food processing takes place at the mandibles, whereas in complex organ; therefore, it might not be unexpected that decapod crustaceans the ingested food is processed by the mechanical processing in decapods could comprise a fairly gastric mill apparatus in the foregut (Ceccaldi 1997). The large portion of the SDA budget. foregut and gastric mill apparatus are innervated by the The mussel was much softer than the fish or shrimp sug- stomatogastric nervous system which synapses on over 40 gesting, like the homogenized fish paste, that it may have different skeletal muscles that control the movements of taken less energy for the gastric mill to process. Several spe- the gastric mill (cutting/grinding) and pyloric sac (filtration cies of amphibians and reptiles also exhibit differences in the of digesta) (Heinzel et al. 1993; Marder and Bucher 2007; characteristics of the SDA response as a function of meal Stein 2009). The gastric mill has a complex behavioural texture, with hard bodied prey items, or those with thicker repertoire and food may be processed in the foregut for exoskeletons requiring more time and energy to digest than 12–18 h (McGaw and Curtis 2013b). This suggests that a softer meals (Secor and Faulkner 2002; Secor 2003; Secor considerable portion of the energy could be associated with and Boehm 2006; Christel et al. 2007; Secor et al. 2007; mastication and preparation of the meal before it is passed Boback et al. 2007; Bessler et al. 2010). If the softer mussel

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434 J Comp Physiol B (2014) 184:425–436 took less energy to process it might be expected that it would 2005; Secor and Boehm 2006). Therefore, to further test for be evacuated from the foregut and transit through the gut the possible roles of different nutrient and energy levels on system at a faster rate. However, there was no difference in the SDA, artificial meals high in protein, lipid or carbohy- foregut evacuation rates or gut transit rates as a function of drate were offered to the crabs. These meals were not con- meal type (Figs. 4, 5). These results in themselves do not rule sumed as readily as the natural ones; Carefoot (1990) also out the original hypothesis that less energy was expended had difficulties getting isopods to eat prepared diets. Crabs to process the mussel. Evacuation and transit rates are very are messy feeders (Barker and Gibson 1977; Ahvenharju variable among individual crustaceans and use of this meth- and Ruohonen 2005) and they tended to tear the prepared odology is limited when trying to infer connections between meals apart while feeding, ingesting food then blowing par- the SDA responses and food passage (McGaw and Whiteley ticles back out of the mouth when it came into contact with 2012; McGaw and Curtis 2013a). The transit and evacuation the esophageal taste receptors (Aggio et al. 2012). Thus the rates do not give an indication of how much actual energy size of the meal consumed could only be approximated to was expended by the gastric mill. In addition, the foregut between 1 and 2.5 % of the crab’s body mass. This undoubt- is not only a site of mastication, enzymes are secreted from edly influenced the negative results for the artificial meals, the hepatopancreas into the foregut and chemical digestion since meal size is a major factor governing the characteris- begins here, so foregut evacuation rate is not solely con- tics of the SDA response not only in crustaceans, but also nected with mechanical processing (Hopkin and Nott 1980; across a wide range of taxa (Secor 2009; McGaw and Curtis Icely and Nott 1992; McGaw and Curtis 2013b). 2013a). It could be argued that messy feeding could account It is also likely that differences in nutrient and energy for the observed differences between the homogenized fish content contributed to the SDA responses for the natu- paste and whole fish muscle (Fig. 2; Table 2). However, ral meals. In a number of fish species an increase in the unlike the prepared meals, the crabs did not regurgitate food protein content of a meal by approximately 15 to 35 % once it was consumed and there no was evidence of pieces can affect the peak, duration and magnitude of the SDA left behind in the experimental chamber. In addition the response (LeGrow and Beamish 1986; Chakraborty et al. experiment was designed to compensate for any potential 1992; Ross et al. 1992), while for crustaceans a change loss that we did not notice, and 3 % BW of homogenized in protein content of 10–20 % results in an increase in the food was offered, versus 2.5 % BW for whole food. short-term oxygen uptake and ammonia excretion rates The physiological processes that account for the SDA (Rosas et al. 1995, 1996; Perera et al. 2005). Differences are difficult to isolate both temporally and spatially. The in energy expenditure occur when spiny lobsters Panulirus differences in the SDA response obtained for the three dif- interruptus consume meals of squid or mussel (Díaz-Igle- ferent natural meals are undoubtedly due to several fac- sias et al. 2011). It was suggested that postprandial oxygen tors, including the texture of the meal and thus the cost of consumption was higher for the squid meal because it was mechanical digestion and the nutrient content how these used entirely for catabolic processes, whereas the higher are used in the animal for catabolic or anabolic processes fat content of mussel (3 %) would have a protein sparing (Díaz-Iglesias et al. 2011). The partitioning of the indi- effect allowing energy to be channelled towards anabolic vidual components that comprise the SDA has not been processes (Díaz-Iglesias et al. 2011). In the present study worked out for any organism to date; but the results of the the variation in protein (<4 %) and fat (<1.5 %) content of present study do suggest that the decapods invest a signifi- the natural meals was low, so these were unlikely to have cant amount of the SDA budget in mechanical digestion. contributed much to the observed differences in the SDA. Determining the amount of energy that the individual com- There were more pronounced differences in energetic ponents contribute to the SDA represents a pressing chal- content of the three meals, and a trend existed between lenge for comparative physiologists. increasing energy content of the meal and an increase in the magnitude of the SDA response (Tables 1, 5). Other works Acknowledgments We would like to thank Dr. Stephen Secor for have shown that differences in energy content of a meal can helpful discussion. This work was supported by an NSERC Discovery grant to IJM. affect the SDA of fish and reptiles (LeGrow and Beamish 1986; McCue et al. 2005). The SDA coefficient gave a value for the SDA relative to the proportion of energy ingested and References it showed that lower amounts of energy were required for digestion and assimilation of the mussel; however, the SDA Aggio JF, Tieu R, Wei A, Derby CD (2012) Oesophageal chemore- coefficient for the fish and shrimp meal did not directly relate ceptors of blue crabs, Callinectes sapidus, sense chemical deter- to the observed differences in SDA. The use of the SDA rents and can block ingestion of food. J Exp Biol 215:1700–1710 Ahvenharju T, Ruohonen K (2005) Individual food intake measure- coefficient does have its limitations and researchers need to ment of freshwater crayfish (Pacifastacus leniusculus Dana) juve- be careful when inferring any adaptive significance (Beaupre niles. Aquac Res 36:1304–1312

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