Abstract
Energy budget is one of the most studied parameters in aquatic animals under environmental challenge. To examine how prolonged starvation would affect their energy budget, respiration rate (RR), ammonia excretion rate (ER), oxygen consumption to ammonia–nitrogen excretion (O:N) ratio and scope for growth (SfG) representing the balance between energy intake and metabolic output, two Asian horseshoe crab species, Tachypleus tridentatus and Carcinoscorpius rotundicauda, were investigated in two feeding regimes (fed and starved) over a period of 7 weeks. No significant effects of species and time course, as well as their interaction, on absorption efficiency were observed in the fed treatments. For both species, RR and ER of the starved treatments significantly decreased, while their O:N ratio significantly increased during the experiment. However, such values for the fed treatments remained relatively stable over the study period. A rapid reduction in SfG was only apparent in the first week of the starved treatments for both species; thereafter, their SfG remained relatively constant. In the fed treatments, SfG of T. tridentatus was significantly lower than that of C. rotundicauda throughout the experiment. In general, C. rotundicauda showed a greater decrease in SfG under starvation than T. tridentatus, suggesting that they may have a more competitive life-history strategy for adjusting to poor nutritional conditions.
Similar content being viewed by others
References
Bayne BL, Newell RC (1983) Physiological energetics of marine mollusks. In: Saleuddin ASM, Wilbur KM (eds) The mollusca, vol 4. Academic Press, New York, pp 407–515
Bayne BL, Widdows J (1978) The physiological ecology of two populations of Mytilus edulis L. Oecologia 37:137–162
Bayne BL, Brown DA, Burns K, Dixon DR, Ivanovici A, Livingstone DR, Lowe DM, Moore MN, Stebbing ARD, Widdows J (1985) The effects of stress and pollution on marine animals. Praegar, New York, pp 315–320
Beiras R, Camacho AP, Albentosa M (1994) Comparison of the scope for growth with the growth performance of Ostrea edulis seed reared at different food concentrations in an open-low system. Mar Biol 119:227–233
Botton ML (1984) Diet and food preferences of the adult horseshoe crab Limulus Polyphemus in Delaware Bay, New Jersey, USA. Mar Biol 81:199–207
Botton ML, Shuster NCJ, Keinath AJ (2003) Horseshoe crab in a food web: who eats whom? In: Shuster NCJ, Barlow BR, Brockmann HJ (eds) The American horseshoe crab. Harvard University Press, London, pp 133–153
Brockington S, Clarke A (2001) The relative influence of temperature and food on the metabolism of a marine invertebrate. J Exp Mar Biol Ecol 258:87–99
Carmichael RH, Rutecki D, Annett B, Gaines E, Valiela I (2004) Position of horseshoe crabs in estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition. J Exp Mar Biol Ecol 299:231–253
Chatterji A (1994) The horseshoe crab—a living fossil. A Project Swarajya Publication, Orissa
Chatterji A, Mishra JK, Parulekar AH (1992) Feeding behaviour and food selection in the horseshoe crab, Tachypleus gigas (Müller). Hydrobiologia 246:41–48
Chen JC, Lin CY (1995) Responses of oxygen consumption, ammonia–N excretion and urea–N excretion of Penaeus chinensis exposed to ambient ammonia at different salinity and pH levels. Aquaculture 136:243–255
Chiu HMC, Morton B (2003) The morphological differentiation of two horseshoe crab species, Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura), in Hong Kong and a regional Asian comparison of them. J Nat Hist 37:19–26
Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Biochem Phys B 90:461–473
Comoglio LI, Gaxiola G, Roque A, Cuzon G, Amin O (2004) The effect of starvation on refeeding, digestive enzyme activity, oxygen consumption, and ammonia excretion in juvenile white shrimp Litopenaeus vannamei. J Shellfish Res 23:243–249
Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11:338–354
Dall W, Smith DM (1986) Oxygen consumption and ammonia–N excretion in fed and starved tiger prawns, Penaeus esculentus Haswell. Aquaculture 55:23–33
Elliott JM, Davison W (1975) Energy equivalents of oxygen consumption in animals energetics. Oecologia 19:195–201
Grably S, Piery Y (1981) Weight and tissue changes in long-term starved frogs Rana esculenta. Comp Biochem Physiol A 69:683–688
Hagerman L, Szaniawska A (1994) Hemolymph nitrogen compounds and ammonia efflux rates under anoxia in the brackish water isopod Saduria entomon. Mar Ecol Prog Ser 103:285–289
Helson JG, Gardner JPA (2007) Variation in scope for growth: a test of food limitation among intertidal mussels. Hydrobiologia 586:373–392
Hervant F, Renault D (2002) Long-term fasting and realimentation in hypogean and epigean isopods: a proposed adaptive strategy for groundwater organisms. J Exp Biol 205:2079–2087
Hervant F, Mathieu J, Barre H, Simon K, Pinon C (1997) Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comp Biochem Physiol A 118:1277–1283
Hill SK, Lawrence JM (2006) Interactive effects of temperature and nutritional condition on the energy budgets of the sea urchins Arbacia punctulata and Lytechinus variegatus (Echinodermata: Echinoidea). J Mar Biol Assoc UK 86:783–790
Hirata H, Yamasaki S (1987) Effect of feeding on the respiration rate of the rotifer Brachionus plicatilis. Hydrobiologia 147:283–288
Hu MH, Wang YJ, Chen Y, Shin PKS, Cheung SG, Li QZ (2009) Summer distribution and abundance of juvenile Chinese horseshoe crab (Tachypleus tridentatus) along an intertidal zone of Beibu gulf, Southern China. Aquat Biol 7:107–112
Hu MH, Wang YJ, Tsang ST, Cheung SG, Shin PKS (2010) Effect of prolonged starvation on body weight and blood-chemistry in two horseshoe crab species: Tachypleus tridentatus and Carcinoscorpius rotundicauda (Chelicerata: Xiphosura, Limulidae). J Exp Mar Biol Ecol 395:112–119
Ivlev VS (1934) Eine Micromethode zur Bestimmung des Kaloriengehalts von Na¨hrstoffen. Biochem Z 6:49–55
Kesarcodi-Watson A, Klumpp DW, Lucas JS (2001) Comparative feeding and physiological energetics in diploid and triploid Sydney rock oysters (Saccostrea commercialis)–II. Influences of food concentration and tissue energy distribution. Aquaculture 203:195–216
Lopez GR, Levinton JS (1987) Ecology of deposit feeding animals in marine sediments. Q Rev Biol 62:235–260
Mayzaud P, Conover RJ (1988) O–N atomic ratio as a tool to describe zooplankton metabolism. Mar Ecol Prog Ser 45:289–302
McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Phys A 156:1–18
Mikkelsen T (1988) The secret in the blue blood. Science Press, Beijing
Nagashima K, Nakai S, Matsue K, Konishi M, Tanaka M, Kanosue K (2003) Effects of fasting on thermoregulatory processes and the daily oscillations in rats. Am J Physiol-Reg I 284:1486–1493
Nakaoka M (1992) Spatial and seasonal variation in growth rate and secondary production of Yoldia notabilis in Otsuchi Bay, Japan, with reference to the influence of food supply from the water column. Mar Ecol Prog Ser 88:215–223
Navarro JM, Leiva GE, Gallardo CS, Varela C (2002) Influence of diet and temperature on physiological energetics of Chorus giganteus (Gastropoda: Muricidae) during reproductive conditioning. New Zeal J Mar Freshw Res 36:321–332
Norkko J, Pilditch CA, Thrush SF, Wells RMG (2005) Effects of food availability and hypoxia on bivalves: the value of using multiple parameters to measure bivalve condition in environmental studies. Mar Ecol Prog Ser 298:205–218
Patil JS, Anil AC (2000) Epibiotic community of the horseshoe crab Tachypleus gigas. Mar Biol 136:699–713
Pedrosa MAC, Lima AMJ, Duarte DPF, Da-Costa CP (2002) The effect of feeding on the respiratory activity of the sloth. Braz J Med Biol Res 35:851–854
Qvarnstrom A, Wiley C, Svedin N, Vallin N (2009) Life-history divergence facilitates regional coexistence of competing Ficedula flycatchers. Ecology 90:1948–1957
Regnault M (1987) Nitrogen excretion in marine and fresh water crustacea. Biol Rev 62:1–24
Schmitt ASC, Uglow RF (1997) Effects of ambient ammonia levels on blood ammonia, ammonia excretion and heart and scaphognathite rates of Nephrops norvegicus. Mar Biol 127:411–418
Sekiguchi K (1988) Ecology. In: Sekiguchi K (ed) Biology of horseshoe crabs. Science House Co. Ltd., Tokyo, pp 50–68
Shin PKS, Li HY, Cheung SG (2009) Horseshoe crabs in Hong Kong: current population status and human exploitation. In: Tanacredi JT, Botton ML, Smith DR (eds) Biology and conservation of horseshoe crabs. Springer, New York, pp 347–360
Smith SA, Berkson J (2005) Laboratory culture and maintenance of the horseshoe crab (Limulus polyphemus). Lab Animal 34:27–34
Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801
Stead RA, Thompson RJ (2003) Physiological energetics of the protobranch bivalve Yoldia hyperborea in a cold ocean environment. Polar Biol 26:71–78
Stead RA, Thompson RJ, Jaramillo JR (2003) Absorption efficiency, ingestion rate, gut passage time and scope for growth in suspension and deposit-feeding Yoldia hyperborea. Mar Ecol Prog Ser 252:159–172
Taghon GL, Greene RR (1992) Utilization of deposited and suspended particulate matter by benthic interface feeders. Limnol Oceanogr 37:1370–1391
van Dijk PLM, Staaks G, Hardewig I (2002) The effect of fasting and refeeding on temperature preference, activity and growth of roach, Rutilus rutilus. Oecologia 130:496–504
Wassmann P (1991) Dynamics of primary production and sedimentation in shallow fjords and polls of Western Norway. Oceanogr Mar Biol 29:87–154
Wei JG, Dai JG, Jin G, Huo GH (2007) Assay of amino acids of yellow connective tissue in mature horseshoe crab of China. Food and Drug 9:41–43
Weng ZH, Hong SG (2003) Ultrastructural observation on nutrient cell of yellow connective tissues in horseshoe crab (Tachypleus tridentatus). J Jimei Univ (Nat Sci) 8:134–138 (in Chinese)
Weng ZH, Xie YJ, Hong SG (2001) Study on yellow connective tissues in horseshoe crab (Tachypleus tridentatus Leach) I. Microstructural observation on the yellow connective tissues. J Jimei Univ (Nat Sci) 6:301–307 (in Chinese)
Westerterp K (1977) How rats economize energy loss in starvation. Physiol Zool 50:331–362
Widdows J (1973) Effect of temperature and food on heart beat, ventilation rate and oxygen uptake of Mytilusedulis. Mar Biol 20:269–276
Widdows J (1985) Physiological procedures. In: Bayne BL (ed) The effects of stress and pollution on marine animals. Praegar, New York, pp 161–178
Widdows J, Hawkins AJS (1989) Partitioning of rate of heat dissipation by Mytilus edulis into maintenance, feeding, and growth components. Physiol Zool 62:764–784
Wood CM (2001) Influence of feeding, exercise and temperature on nitrogen metabolism and excretion. In: Wright PA, Andersen PM (eds) Fish physiology. Vol. 20. Nitrogen excretion, vol 20. Academic Press, San Diego, pp 201–238
Acknowledgments
We gratefully acknowledge three anonymous reviewers for their constructive comments. We would also like to express our thanks to Raymond Chan and Amy Chong of the Department of Biology and Chemistry, City University of Hong Kong, for their technical assistance. The work described in this paper was fully supported by a Strategic Research Grant (Project No. 7002581) from City University of Hong Kong, Hong Kong.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. O. Pörtner.
Rights and permissions
About this article
Cite this article
Hu, M., Wang, Y., Tsang, S.T. et al. Effect of starvation on the energy budget of two Asian horseshoe crab species: Tachypleus tridentatus and Carcinoscorpius rotundicauda (Chelicerata: Xiphosura). Mar Biol 158, 1591–1600 (2011). https://doi.org/10.1007/s00227-011-1672-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-011-1672-0