Interactive Effects of Temperature and Nutritional Condition on the Energy Budgets of the Sea Urchins Arbacia Punctulata And

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8-2006 Interactive Effects of Temperature and Nutritional Condition on the Energy Budgets of the Sea Urchins Arbacia Punctulata and Lytechinus Variegatus (Echinodermata : Echinoidea) Sophie K. Hill University of South Florida

John M. Lawrence University of South Florida, [email protected]

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Scholar Commons Citation Hill, Sophie K. and Lawrence, John M., "Interactive Effects of Temperature and Nutritional Condition on the Energy Budgets of the Sea Urchins Arbacia Punctulata and Lytechinus Variegatus (Echinodermata : Echinoidea)" (2006). Integrative Biology Faculty and Staff Publications. 17. https://scholarcommons.usf.edu/bin_facpub/17

This Article is brought to you for free and open access by the Integrative Biology at Scholar Commons. It has been accepted for inclusion in Integrative Biology Faculty and Staff ubP lications by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. J. Mar. Biol. Ass. U.K. (2006), 86, 783^790 Printed in the United Kingdom

Interactive e¡ects of temperature and nutritional condition on the energy budgets of the sea urchins Arbacia punctulata and Lytechinus variegatus (Echinodermata: Echinoidea)

OP Sophie K. Hill* and John M. Lawrence* *Department of Biology, University of South Florida, Tampa, 33620 Florida, USA 33620. O Present address: Department of Paediatrics, University of Oxford, John Radcli¡e Hospital, Headington, Oxford, OX3 9DU, UK. P Corresponding author, e-mail: [email protected]

Arbacia punctulata and Lytechinus variegatus are widely distributed echinoid species in shallow water in the western Atlantic Ocean, Caribbean Sea and Gulf of Mexico that seem to have di¡erent life history strategies. We evaluated the e¡ect of two types of stress (high temperature and starvation) on gonad production and scope for growth. We hypothesized that A. punctulata has a stress tolerant life strategy and would be more tolerant to stress and L. variegatus has a competitive^ruderal strategy and would be less tolerant to stress. Gonad production by A. punctulata was not as greatly a¡ected by temperature as L. variegatus, suggesting the hypothesis was correct. Arbacia punctulata had a signi¢cantly higher excretion rate indicating greater energy allocation to maintenance than production. Lytechinus variegatus had a signi¢cantly greater consumption rate but did not absorb signi¢cantly more energy. Arbacia punctulata compensated for its lower food consumption by a higher absorption e⁄ciency. Measured energy expenditure and calculated scope for growth did not di¡er. However, the percentage change in energy absorbed and energy expenditure was greater for L. variegatus than for A. punctulata with a change in temperature. Feeding had a greater e¡ect on production than temperature suggesting that the biotic stress of low food availability is more important than an abiotic stress such as temperature on energy budgets.

INTRODUCTION Scope for growth is an estimation of production calculated from the balanced energy equation of Winberg Arbacia punctulata (Lamarck) Philippi and Lytechinus (1960): variegatus (Lamarck) are widely distributed echinoid species in shallow water in the western Atlantic Ocean, CA ¼ R þ U þ P; P ¼ CA R U (1) Caribbean Sea and Gulf of Mexico. Water temperatures for L. variegatus are 15^318C and 9^318C for A. punctulata. where C is consumption, A is absorption e⁄ciency, R is On the Florida gulf-coast shelf, A. punctulata occurs alone respiration, U is excreta and P is production in energy on rubble bottoms and L. variegatus occurs alone on sand units. bottoms; they occur together in microhabitats on hetero- The e¡ect of temperature or food on scope for growth is geneous bottoms (Hill & Lawrence, 2003). The structure often measured but studies of the interactive e¡ects of of these two species is so di¡erent they belong to di¡erent temperature and food on scope for growth are less superorders (Smith, 1984).The lantern, teeth and ambula- common (e.g. Navarro et al., 2002). Scope for growth, cral plates of A. punctulata are more primitive than those of has been used to measure the physiological response of L. variegatus (Smith, 1984). Although experimental marine invertebrates to stress. evidence is meagre, the evolutionary changes in these The use of arti¢cial or natural food should have no structures seem associated with an increased capacity for e¡ect on the response to temperature. Arti¢cial food production (Lawrence & Bazhin, 1998). Life history char- eliminates variability in food quality. The diets of A. acteristics such as growth rate and longevity suggest punctulata and L. variegatus are extremely varied. Arbacia A. punctulata has a more stress-tolerant life history strategy punctulata is omnivorous and consumes a variety of items and L. variegatus a more competitive^ruderal one. including algae, sea grasses, sponges, dead ¢sh, sand Capacity for production is a major life history character- dollars, hydrozoans, mussels and bryozoans (Wahl & istic associated with life history strategies (Grime, 1977). Hay, 1995). The diet of L. variegatus consists of sea grass, Grime de¢ned stress as an environmental condition that algae and small crustaceans (Lowe & Lawrence, 1976). It decreases production. The response to stress, a decrease in would therefore be extremely di⁄cult to simulate their production, is a good criterion for distinguishing life natural diets in aquaria. In other studies on scope for history strategies. Because of a di¡erence in allocation of growth and energy budgets, both natural and arti¢cial resources, species with the stress-tolerant strategy should diets have been used. Many studies have used a monocul- be less productive than competitive^ruderal ones. ture which would not be typical of the organism’s diet in

Journal of the Marine Biological Association of the United Kingdom (2006) 784 S.K. Hill and J.M. Lawrence Interaction of temperature and nutrition in sea urchins their natural environment. There has also been arti¢cial was siphoned into a biochemical oxygen demand bottle supplementation of the diet as in the studies of Navarro and the oxygen concentration measured with an oxygen et al. (2002) who supplemented the microalgae for their probe (Model YSI5000). The measurements on the ten scallops with lipid and carbohydrate. individuals were made simultaneously. The volume of If A. punctulata has a more stress tolerant life history each sea urchin was subtracted from the volume of the strategy and L. variegatus a more competitive^ruderal container to obtain the volume of water. Respiration rate strategy, the scope for growth of A. punctulata should be was calculated as the decrease in oxygen concentration less a¡ected by stress of high temperature and starvation. h71 g wet wt71. Ammonia is the primary excretory We tested this prediction by a study of the interactive product of sea urchins. The concentration of ammonia in e¡ects of high temperature and starvation on the scope the water sample was measured by the method of for growth of the two species. Solorzano (1969) and the excretion rate calculated as the increase in ammonia concentration h71 g wet wt71. For the feed, the energy equivalent was calculated using MATERIALS AND METHODS 17.16 J mg carbohydrate71, 29.55 J mg lipid71, and Seventy specimens each of Arbacia punctulata and 23.65 J mg protein71 (Crisp, 1984). For respiration, taking Lytechinus variegatus were collected from Caspersen into account the proximate composition of the feed, a 0 0 71 Beach, Florida (27807 N82827 W) by SCUBA diving on conversion of 13.61J mg O2 was used (Crisp, 1984). For 2 November 1998. Water temperature was 258C. Each excretion, a conversion of 0.025 J g ammonia71 was used individual was weighed (to the nearest 0.1 g) and its (Crisp, 1984). Scope for growth was calculated as the diameter measured (mm). The gonads of ten individuals energy equivalents of the organic matter absorbed (food were dissected out and weighed (wet weight). The gonad ingestedabsorption e⁄ciency) minus energy expended index of these individuals at the beginning of the experi- (oxygen consumption and ammonia production) (scope ment was calculated as: for growth¼A7(R+U)). Net growth e⁄ciency was calculated as (scope for growth/energy absorbed) (100). (g wet weight of gonad g wet body weight 1)(100): The two species could not be directly compared because (2) L. variegatus has a signi¢cantly larger test diameter than A. punctulata. Therefore the data were analysed separately The experiment was a 23 factorial design with two for each species for the e¡ect of food and temperature. species, two temperature levels and two nutritional condi- Whenever possible the data were analysed by one- and tions. The nutritional conditions were fed (ad libitum)a two-way analysis of variance (ANOVA) and Tukey’s prepared diet or starved. The prepared diet consisted of multiple comparison test. Whenever experimental data corn 24.89%, wheat middens 24.89%, soy £our 11.10%, were compared to initial data t-tests were used. However, ¢sh meal 12.00%, kelp meal 14.00%, sodium phosphate for some data it was not possible to successfully transform 1.33%, lecithin 1.00%, cholesterol 0.30%, ethoxyquin the data to meet requirements of normality and homoge- 0.20%, vitamin C 0.08%, vitamin/mineral mix 0.20%, neous variance. For these data, Kruskal^Wallis one-way potassium sorbate 0.30%, b-carotene 0.01%, ¢sh oil ANOVA on ranks and Dunn’s multiple comparison test 0.70%, glycerin 8.00% and phosphoric acid 1.00%. The were used. When experimental data were compared to temperatures were 238C and 318C. Lytechinus variegatus initial data and the data were not normal and could not does not survive 348C (Lawrence, 1975). be successfully transformed, the Mann^Whitney rank There were 12 individuals of each species in each treat- sum test was used. All data were analysed using the ment and the experiment was run for four weeks. The sea computer program Sigmastat. Sample sizes were between urchins were placed in an individual plastic container fed 8 and 12. by a submersible pump with a £ow rate of 398 36 ml min71. Each aquarium contained seawater with three individuals of each species. Consumption rates were measured daily. A known mass of feed (wet weight) was placed in containers daily and the Table 1. Arbacia punctulata and Lytechinus remaining feed left from the previous day was collected variegatus: test diameter (mm) and mass (g) at the beginning and weighed. Absorption e⁄ciency was calculated by the and end of the experiment. Mean SD. indirect method of Lowe & Lawrence (1976). The protein, carbohydrate and lipid concentrations of the feed and Te s t faeces was measured by the methods of Lowry et al. Species Treatment diameter Mass (1951), Dubois et al. (1956) and Folch et al. (1957) respectively to allow more accurate calculation of energy Arbacia punctulata Initial group 46.9 2.7 49.2 6.8 content. 238C, fed 44.7 1.6 46.9 5.7 Respiration and excretion rates were measured weekly 238C, starved 47.3 2.8 49.5 8.4 at the same hour before the sea urchins were fed (approxi- 318C, fed 41.9 6.0 42.5 12.6 mately 19 h after their previous feeding so measurements 318C, starved 39.4 5.1 32.7 11.1 for fed individuals would not include respiration associated Lytechnius variegatus Initial group 59.4 5.1 82.5 15.1 with speci¢c dynamic action). Ten individuals were placed 238C, fed 58.2 3.8 91.5 17.8 238C, starved 61.8 5.0 101.0 19.4 into separate containers (1050 ml volume) and an empty 318C, fed 58.2 5.9 86.2 23.2 container was run as a control. After one hour, the 318C, starved 57.4 4.2 72.5 23.0 containers were sealed. After two hours, a water sample

Journal of the Marine Biological Association of the United Kingdom (2006) Interaction of temperature and nutrition in sea urchins S.K. Hill and J.M. Lawrence 785

Figure 1. Gonad indices for Arbacia punctulata and Lytechinus variegatus. ***, denotes statistically signi¢cant di¡erence compared to initial group (P50.001). Arb-initial, A. punctulata at the start of the experiment; A23F, fed A. punctulata at 238C; A23S, starved A. punctulata at 238C; A31F, fed A. punctulata at 318C; A31S, starved A. punctulata at 318C; Lyt-initial, L. variegatus at the start of the experiment;L23F,fedL. variegatus at 238C; L23S, starved L. variegatus at 238C; L31F, fed L. variegatus at 318C; L31S, starved L. variegatus at 318C.

Figure 2. Rate of food consumption for Arbacia punctulata and Lytechinus variegatus at 238Cand318C. Mean SD.

RESULTS punctulata were smaller than Lytechinus variegatus. The body sizes did not change signi¢cantly in the short-term experi- Body size and gonad index ments. Average diameter and mass of individuals in the Gonad indices are given in Figure 1. The mean gonad di¡erent treatments are given in Table 1. The individuals index of A. punctulata was 1.5 and did not change signi¢- of each species collected were similar in size. Arbacia cantly from the initial value in any treatment. The gonad

Journal of the Marine Biological Association of the United Kingdom (2006) 786 S.K. Hill and J.M. Lawrence Interaction of temperature and nutrition in sea urchins

Table 2. Arbacia punctulata and Lytechinus variegatus: absorption e⁄ciency. Mean SD.

Species Absorption e⁄ciency Treatment Week 1 Week 2 Week 3 Week 4

Arbacia punctulata total organic 238C, fed 84.80 4.17 82.71 6.26 82.35 5.27 81.62 7.24 soluble protein 85.13 6.69 80.53 8.40 76.12 9.06 80.82 7.71 lipid 78.55 8.40 70.10 13.94 74.60 9.91 71.58 1.31 carbohydrate 91.60 5.17 92.95 2.94 92.48 4.86 * insoluble protein 84.14 1.49 83.13 5.42 86.58 2.31 * total organic 318C, fed 82.28 5.73 82.89 5.27 83.27 4.18 90.34 1.80 soluble protein 81.31 7.67 78.74 5.34 76.47 7.93 89.16 3.26 lipid 73.19 12.83 74.34 8.89 76.48 7.62 89.59 4.47 carbohydrate 90.59 3.02 93.92 2.33 94.17 2.64 97.60 0.23 insoluble protein 81.66 5.80 84.52 5.12 87.26 2.82 88.95 0.73 Lytechinus variegatus* total organic 238C, fed 80.69 5.71 78.52 5.82 73.02 8.45 protein 75.62 8.56 68.38 7.81 62.30 14.56 lipid 68.75 10.23 61.00 11.20 51.86 22.28 carbohydrate 89.50 5.71 91.10 3.91 75.93 3.46 insoluble protein 84.01 3.53 84.51 5.46 65.93 7.51 total organic 318C, fed 83.00 3.17 76.91 2.69 62.38 8.13 protein 80.54 5.05 67.55 6.92 lipid 73.25 6.94 61.33 6.86 carbohydrate 90.27 2.07 91.72 2.61 insoluble protein 83.69 2.88 83.69 3.53

*, faeces for Lytechinus variegatus were insu⁄cient to measure carbohydrate and insoluble protein concentrations in week 3 and for all proximate constituents in week 4.

Figure 3. The e¡ect of temperature and nutritional condition on rate of respiration in Arbacia punctulata and Lytechinus variegatus 71 71 (mM O2 gwetweight h ). Mean SD.

index of L. variegatus was also low (3.8). The gonad index Consumption of starved L. variegatus did not change signi¢cantly from The rates of food consumption are given in Figure 2. the initial value in either temperature treatment. The The rate of food consumption in L. variegatus was always gonad index of fed individuals increased by 111% at greater than that of A. punctulata. Temperature had no 238C (a signi¢cant increase at P50.001) and by 47% at signi¢cant e¡ect on the food consumption rate of 318C. A. punctulata but at 238C, the food consumption rate did

Journal of the Marine Biological Association of the United Kingdom (2006) Interaction of temperature and nutrition in sea urchins S.K. Hill and J.M. Lawrence 787

Figure 4. The e¡ect of temperature and nutritional condition on rate of excretion in Arbacia punctulata and Lytechinus variegatus 71 71 (mgNH3 g wet weight h ). Mean SD. change signi¢cantly over time (P50.001). Temperature similar. For both A. punctulata and L. variegatus the respira- and time had a signi¢cant e¡ect on the food consumption tion rate was similar for all treatments in Week 1. Subse- rate of L. variegatus when consumption was signi¢cantly quently, the respiration rate was signi¢cantly less in higher at 238C than at 318C(P¼0.027). starved individuals than fed individuals (P50.001). Temperature had no signi¢cant e¡ect on the respiration Absorption e⁄ciencies rate of A. punctulata or L. variegatus. Absorption e⁄ciencies are given in Table 2. Absorption e⁄ciencies for A. punctulata were higher than those for Excretion L. variegatus. Absorption e⁄ciencies were variable for all Excretion rates are given in Figure 4. The rate of ammo- proximate constituents and di¡erences were not consistent. nium excretion per unit weight of L. variegatus was less than Temperature had no signi¢cant e¡ect on the absorption that of A. punctulata. Excretion rates were very variable e⁄ciency of A. punctulata. Temperature and time had a within treatments and over time. Excretion rates were signi¢cant interaction for organic, lipid and carbohydrate signi¢cantly lower in fed A. punctulata than starved ones e⁄ciencies in L. variegatus (P50.01) but not for (P50.001) with a mean decrease of 20%. Arbacia punctulata A. punctulata. Again, the di¡erences were not consistent. had a signi¢cantly higher excretion rate (mean increase of 52%) at 318C than at 238C(P¼0.001).Temperature did not Respiration have a signi¢cant e¡ect on the excretion rate of L. variegatus. Respiration rates are given in Figure 3. The respiration Fed individuals had a signi¢cantly lower excretion rate rates per unit weight of L. variegatus and A. punctulata were (P50.001) with a mean decrease of 37%.

Table 3. Arbacia punctulata and Lytechinus variegatus: energy absorbed, energy expended and scope for growth (J g wet weight71 d71) and net growth e⁄ciency (%). Mean SD of average weekly values. N¼4.

Scope for growth Species Treatment Energy absorbed Energy expended (production) Net growth e⁄ciency

Arbacia punctulata 238C, fed 175.4 49.2 11.6 2.1 163.7 47.2 92.4 1.3 238C, starved 5.8 2.2 75.8 2.2 318C, fed 203.8 48.1 11.5 1.5 192.2 48.7 318C starved 7.2 1.7 77.1 1.7 92.4 4.2 Lytechinus variegatus 238C, fed 192.9 34.7 11.0 1.0 181.7 34.8 238C, starved 4.6 0.8 74.6 0.8 93.8 1.5 318C, fed 185.1 39.3 9.6 0.8 175.5 40.1 318C, starved 5.3 0.8 74.3 2.6 94.1 1.9

Journal of the Marine Biological Association of the United Kingdom (2006) 788 S.K. Hill and J.M. Lawrence Interaction of temperature and nutrition in sea urchins

Table 4. Arbacia punctulata and Lytechinus variegatus: percentage change in energy absorbed, energy expended, scope for growth, and net growth e⁄ciency for individuals at 238 or 318C, starved/fed and for fed or starved individuals, 318C/238Ccalculated from mean values in Table 3. Percentage change in energy absorbed, scope for growth and net growth e⁄ciency was calculated only for fed individuals.

Scope for growth (calculated Net growth Species Percentage change Energy absorbed Energy expended production) e⁄ciency

Arbacia punctulata 238C fed/starved 750 7104 318C fed/starved 737 7104 fed 238C/318C 16 71 17 0 starved 238C/318C 24 722 Lytechinus variegatus 238C fed/starved 758 7103 318C fed/starved 745 7102 fed 238C/318C 74 713 73 0 starved 238C/318C 15 7

Scope for growth and net growth e⁄ciency In sea urchins, major short-term changes in production The calculated scope for growth and net growth e⁄- involve non-gametogenic nutritive phagocytes in the ciencies are given in Table 3. Scope for growth (produc- gonads that consequently have the role of nutrient storage tion) was negative for starved individuals as energy was organs (Walker et al., 2001). An increase in gonad index expended but not absorbed. Temperature had no signi¢- would indicate production and storage of nutrients; a cant e¡ect on the energy absorbed by A. punctulata. Conse- decrease would indicate use of nutrients. Stress-tolerant quently, the scope for growth and net growth e⁄ciency species should show relatively less change in gonad index were similar at both temperatures for fed individuals. Fed with conditions. Non-signi¢cant decreases in the gonad individuals at 238Cand318C had signi¢cantly higher index of starved Arbacia punctulata occurred at both 238C energy expenditure than starved individuals at 238C and and 318C. The gonad index was small at this time and the 318C respectively (P50.001). Starved individuals at 318C potential for a decrease would have been small. However, also had signi¢cantly higher energy expenditure than as predicted for a stress-tolerant species, non-signi¢cant starved individuals at 238C(P¼0.003). The percentage increases occurred in the gonad index of fed individuals decrease in energy expended by starved A. punctulata at at both temperatures. 238C was 50% compared to 37% at 318C. Scope for The gonad index of Lytechinus variegatus did not decrease growth was 17% greater at 238C than at 318C for fed greatly with starvation at both temperatures. Again, as individuals. with A. punctulata, the gonad index was small at this time For L. variegatus, energy absorbed, energy expended and (3.8) and would have had little potential for decrease. In scope for growth did not di¡er signi¢cantly at 238C and contrast to A. punctulata, the gonad index of fed L. variegatus 318C. Fed individuals had signi¢cantly higher energy increased signi¢cantly as predicted for competitive or expenditure than starved individuals as seen for ruderal species. The increase in gonad index was greater A. punctulata (P50.001). Energy expenditure decreased by at the lower temperature (111%) than at the higher 58% at 238C and 45% at 318C for starved individuals. temperature (47%) indicating a sensitivity of production The e¡ect of temperature on percentage change in to temperature. energy absorbed and expended was greater in L. variegatus Consumption rates and absorption e⁄ciencies of stress- than in A. punctulata (Table 4). Temperature had no e¡ect tolerant species should be a¡ected less than those of on calculated net growth e⁄ciency in either species. competitive or ruderal species. We found the consumption rates and absorption e⁄ciencies of A. punctulata and L. variegatus did not di¡er signi¢cantly at 238Cor318C. DISCUSSION In contrast, Moore & McPherson (1965) reported almost Life history strategies should re£ect the environmental no consumption by L. variegatus at 208C and a maximum conditions under which species evolved. Grime (1977) consumption rate at 308C. They found no feeding at 348C. suggested two environmental variables that a¡ect ener- Klinger et al. (1986) reported a lower consumption rate getics are important: stress and disturbance. Species and absorption e⁄ciency of L. variegatus at 168C than at adapted to stress, either extreme physical variables or low 238C. The feeding rates we obtained were similar to, or resource availability, have less capacity for production and greater than those in the literature. Hay et al. (1986) greater capacity for maintenance than competitive or reported feeding rates of 0.174^0.216 g algae/urchin/24 h ruderal species. If so, it should be possible to distinguish for A. punctulata. Our rates of 0.47^0.69 g urchin/day were species with di¡erent strategies by subjecting them to well above this. Moore et al. (1963) reported a feeding rate stress and measuring the e¡ect on the di¡erent compo- of 1.33 g d71 wet weight of grass for L. variegatus. The nents of the energy budget. Production should be a¡ected feeding rates in our study were 0.88^1.20 g/urchin/ less in stress-tolerant species than competitive or ruderal day. Therefore the use of a commercial feed did not species.

Journal of the Marine Biological Association of the United Kingdom (2006) Interaction of temperature and nutrition in sea urchins S.K. Hill and J.M. Lawrence 789 appear to have an adverse e¡ect on the urchins’ maintenance and may enhance survival and delay senes- feeding rates. cence (Hawkins, 1991). If A. punctulata has a more stress- Energy allocated to respiration is used for anabolism tolerant life history strategy, it should prioritize mainte- (production) and maintenance. We predicted stress would nance over growth and reproduction. a¡ect the percentage change in energy allocated to anabo- There was no signi¢cant di¡erence in the amount of lism and maintenance less in A. punctulata than in energy absorbed by A. punctulata and L. variegatus.If L. variegatus. Temperature did not have a signi¢cant e¡ect L. variegatus is a competitive species, it would be expected on respiration of either species. Moore & McPherson to absorb more energy under favourable conditions than (1965) reported an increase in respiration of L. variegatus the stress-tolerant A. punctulata. As expected, L. variegatus from 208C to a peak at 33^358C. The e¡ect of starvation had a signi¢cantly higher consumption rate. Arbacia on respiration was not apparent until the second week of punctulata had a signi¢cantly higher absorption e⁄ciency the experiments. Fed individuals of both species had that compensated for the lower amount of energy ingested. similar signi¢cantly higher respiration rates than starved Fed individuals had signi¢cantly higher energy expendi- individuals at both temperatures. The higher respiration ture than starved individuals at each temperature. The rate of fed animals could have resulted from speci¢c e¡ect of food can be explained by the signi¢cantly higher dynamic action, the increase in respiration associated respiration rates at the higher temperature to produce with anabolism of products of digestion, or higher meta- energy for anabolism of digestive products. Respiration bolic activity associated with well-fed animals. The contributed a much larger proportion to energy expendi- respiratory rate of the sea urchins Strongylocentrotus ture than excretion, an average 7^8 J (range 1^22 J) and droebachiensis increased after feeding (Lilly, 1979). It 0.3^0.7 J (range 0^6 J), respectively. Therefore, changes in should be noted that the contribution of anaerobic meta- respiration had a much larger impact on energy expendi- bolism for energy was not measured. Shick (1983) pointed ture than changes in excretion. This is similar to the parti- out that echinoderms are basically aerobic organisms but tioning of energy found in other studies although the noted that anaerobic metabolism may be prominent in percentage of energy allocated to respiration in this study gonads when they are large. In our experiments this must was very low (4^12%). be considered in the production of large gonads with Arbacia punctulata had signi¢cantly higher energy expen- feeding in L. variegatus. diture than L. variegatus. Arbacia punctulata should have It was expected that either L. variegatus would have a higher maintenance costs while L. variegatus should have greater respiration rate than A. punctulata or that they higher respiration costs. Ebert (1975) calculated that would be equal. If L. variegatus is a competitive species it consumption, respiration, and excretion rates were should be absorbing more energy and allocating this similar in a slow-growing species (Strongylocentrotus droeba- energy to production. This should be re£ected in higher chiensis) and two fast-growing species (Lytechinus variegatus, respiration rates. It is also possible that both species could Tripneustes ventricosus) and concluded that di¡erences in have equal respiration rates but that L. variegatus allocated energy allocation were responsible for di¡erences in life the energy to production while A. punctulata allocated the history characteristics. Energy expenditure by A. punctulata energy to maintenance. If A. punctulata is a stress-tolerant (the stress-tolerant species) should be less a¡ected by stress species, its respiratory rate should be less a¡ected by than L. variegatus (the competitive^ruderal species). temperature or starvation than that of L. variegatus. Ho¡mann & Parsons (1991) stated that an organism may Respiration rates were not signi¢cantly di¡erent for the increase its tolerance to stress by reducing its metabolic two species indicating that the absolute level of energy rate, resulting in a lower energy demand. Therefore, the metabolism in the two species was similar. response seen does not support the idea that A. punctulata As with respiration, ammonium excretion can be is a stress-tolerant species. a¡ected by both maintenance and anabolism. Breakdown It was expected that L. variegatus would have a signi¢- of proteins for maintenance would increase ammonium cantly higher scope for growth than A. punctulata.If excretion while amination of metabolites with production L. variegatus has a competitive life history strategy, it would decrease it. In contrast to respiration rates, should have a very high capacity for production when temperature signi¢cantly increased excretion rates in conditions are favourable and should be able to absorb A. punctulata. This suggests increased catabolism of proteins and allocate more energy than the more stress-tolerant and nucleic acids although increased metabolism was not A. punctulata. It was expected that L. variegatus would have evident in the respiration rate. Temperature would have a greater decrease in scope for growth under stress than less e¡ect if proteins were catabolized instead of lipids or A. punctulata. This prediction was not borne out by these carbohydrates. The respiratory quotient of proteins is only results as no signi¢cant di¡erences were found for scope about 0.79 while that of carbohydrates is 1.00 (Burggren & for growth between the two species. One reason for this Roberts, 1991) and catabolism of proteins would have less could have been that measurements of respiration did not e¡ect on respiration than catabolism of carbohydrates. include speci¢c dynamic action, the energy allocated to Starved A. punctulata had a signi¢cantly higher excretion anabolism. rate than fed individuals. Despite the decrease in respira- In addition to the correlation of rate of metabolism with tion rate, starved L. variegatus had a signi¢cantly higher life history strategy, percentage change in rate of metabo- excretion rate than fed individuals. lism with stress should be very indicative of strategy and Arbacia punctulata had signi¢cantly higher excretion rates show which physiological processes are susceptible. Our than L. variegatus. This could be a result of increased data indicate that the percentage change in energy protein catabolism or turnover in A. punctulata. Although absorbed and energy expended was a¡ected more for protein turnover is energetically costly, it increases L. variegatus than A. punctulata.

Journal of the Marine Biological Association of the United Kingdom (2006) 790 S.K. Hill and J.M. Lawrence Interaction of temperature and nutrition in sea urchins

The relative changes in the gonad indexes with stress Hill, S.K. & Lawrence J.M., 2003. Habitats and characteristics support the suggestion that A. punctulata and L. variegatus of the sea urchins Lytechinus variegatus and Arbacia punctulata have di¡erent life history strategies. The results for the (Echinodermata) on the Florida gulf-coast shelf. P. S. Z. N. energy budget also give some support for this hypothesis; Marine Ecology, 24, 15^30. A. punctulata had a higher excretion rate indicating Ho¡mann, A.A. & Parsons, P.A., 1991. Evolutionary genetics and environmental stress. Oxford: Oxford University Press. increased protein catabolism than L. variegatus. Lytechinus Klinger, T.S., Hsieh, H.L., Pangallo, R.A., Chen, C.P. & variegatus had a greater consumption rate that was more Lawrence, J.M., 1986. The e¡ect of temperature on feeding, a¡ected by temperature, but did not absorb signi¢cantly digestion, and absorption of Lytechinus variegatus (Lamarck) more energy. (Echinodermata: Echinoidea). Physiological Zoology, 59, The results indicate the e¡ect of food availability had a 332^336. much greater e¡ect than temperature on the energy Lawrence, J.M., 1975. The e¡ect of temperature^salinity combi- budget of Arbacia punctulata and Lytechinus variegatus.A nations on the functional well-being of adult Lytechinus greater e¡ect of food than temperature on scope for variegatus (Lamarck) (Echinodermata: Echinoidea). Journal of growth has also been reported for the copepod Calanus Experimental Marine Biology and Ecology, 18, 271^275. chilensis (Escribano et al., 1997), the scallop Argopecten Lawrence, J.M. & Bazhin, A., 1998. Life-history strategies and Journal of Shell¢sh purpureus (Navarro et al., 2000) and the gastropod Chorus the potential of sea urchins for aquaculture. Research, 17,1515^1522. giganteus (Navarro et al., 2002). This suggests that the Lilly, G.R., 1979. The in£uence of diet on the oxygen uptake of biotic stress of low food availability is more important the sea urchins, Tripneustes ventricosus and Strongylocentrotus droe- than an abiotic stress such as temperature on energy bachiensis. Comparative Biochemistry and Physiology, 62A, 463^471. budgets. Lowe, E.F. & Lawrence, J.M., 1976. Absorption e⁄ciencies of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea) We thank A.L. Lawrence for formulating the feed and Wenger for selected marine plants. Journal of Experimental Marine Manufacturing, Inc. for providing the extruded feed. J.M. Biology and Ecology, 21, 223^234. Lawrence was supported by Florida SeaGrant no. R/LR-A-21. Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall R.J., 1951. We thank Erica Amato, Angela Belcher, Francisco Collazos, Protein measurement with the Folin phenol reagent. Journal of Einab Edenburg, Robert Gerczak, Mariana Goncalves, Joseph Biological Chemistry, 193,265^275. Green, Michael Kastura, Ray Martinez, Martin Montalvo, Moore, H.B., Jutare, T., Bauer, J.C. & Jones, J.A., 1963. The Adrienne Parlette, Amy Parsons, Larry Plank, Robert Sturgeon, biology of Lytechinus variegatus. Bulletin of Marine Science, 13, Chih-Yi Tan and Ti¡any Talbot for their help in the laboratory 23^53. and ¢eld. Moore, H.B. & McPherson, B.F., 1965. A contribution to the study of the productivity of the urchins Tripneustes esculentus REFERENCES and Lytechinus variegatus. Bulletin of Marine Science, 15, 855^871. Navarro, J.M., Leiva, G.E., Martinez, G. & Aquilera, C., 2000. Burggren, W. & Roberts, J., 1991. Respiration and metabolism. Interactive e¡ects of diet and temperature on the scope for In Comparative animal physiology, 4th edn. Environmental and meta- growth of the scallop Argopecten purpuratus during reproductive bolic animal physiology (ed. C.L. Prosser), pp. 353^435. NewYork: conditioning. Journal of Experimental Marine Biology and Ecology, Wiley-Liss, Inc. 247, 67^83. Crisp, D.J., 1984. Energy £ow measurements. In Methods for the Navarro, J.M., Leiva, G.E., Gallardo, C.S. & Varela, C., 2002. study of the marine benthos. 2nd edn. (ed. N.A. Holme and A.D. In£uence of diet and temperature on physiological energetics McIntyre), pp. 284^372. Oxford: Blackwell Scienti¢c of Chorus giganteus (Gastropoda: Muricidae) during reproduc- Publications. tive conditioning. New Zealand Journal of Marine and Freshwater Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. & Smith, Research, 36, 321^332. F., 1956. Colorimetric method for determination of sugars and Shick, J.M., 1983. Respiratory gas exchange in echinoderms. In related substances. Analytical Chemistry, 28, 350^356. Echinoderm studies 1 (ed. M. Jangoux and J.M. Lawrence), Ebert, T.A., 1975. Growth and mortality of post-larval echinoids. pp. 67^110. Rotterdam: A.A. Balkema. American Zoologist, 15, 755^775. Smith, A., 1984. Echinoid palaeobiology. London: George Allen & Escribano, R., Irribarren, C. & Rodriguez, L., 1997. In£uence of Unwin. food quantity and temperature on development and growth of Solorzano, L., 1969. Determination of ammonia in natural waters the marine copepod Calanus chilensis from northern Chile. by the phenol hypochlorite method. Limnology and Oceanography, Marine Biology, 128, 281^288. 14, 799^801. Folch, J., Lees, M. & Sloane Stanley, G.H., 1957. A simple Wahl, M. & Hay, M.E., 1995. Associational resistance and method for the isolation and puri¢cation of total lipids from shared doom: e¡ects of epibiosis on herbivory. Oecologia, 102, animal tissues. Journal of Biological Chemistry, 226, 497^509. 329^340. Grime, J.P., 1977. Evidence for the existence of three primary Walker, C.W., Unuma, T., McGinn, N.A., Harrington, L.M. & strategies in plants and its relevance to ecological and evolu- Lesser, M.P., 2001. Reproduction of sea urchins. In Edible sea tionary theory. American Naturalist, 111,1169^1194. urchins: biology and ecology (ed. J.M. Lawrence), pp. 5^26. Hawkins, A.J.S., 1991. Protein turnover: a functional appraisal. Amsterdam: Elsevier Science Publishers B.V. Functional Ecology, 5, 222^233. Winberg, C.G., 1960. Rate of metabolism and food requirements Hay, M.E., Lee Jr, R.R. & Guieb, R.A., 1986. Food preference of ¢shes.Translated Series Fisheries Research Board Canada, 194. and chemotaxis in the sea urchin Arbacia punctulata (Lamarck) Philippi. Journal of Experimental Marine Biology and Ecology, 96, 147^153. Submitted 29 July 2005. Accepted 31 January 2006.

Journal of the Marine Biological Association of the United Kingdom (2006)