Skip to main content

Advertisement

Log in

Effect of starvation on the energy budget of two Asian horseshoe crab species: Tachypleus tridentatus and Carcinoscorpius rotundicauda (Chelicerata: Xiphosura)

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Google Scholar 

  • Bayne BL, Widdows J (1978) The physiological ecology of two populations of Mytilus edulis L. Oecologia 37:137–162

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chatterji A (1994) The horseshoe crab—a living fossil. A Project Swarajya Publication, Orissa

    Google Scholar 

  • Chatterji A, Mishra JK, Parulekar AH (1992) Feeding behaviour and food selection in the horseshoe crab, Tachypleus gigas (Müller). Hydrobiologia 246:41–48

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Biochem Phys B 90:461–473

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11:338–354

    Article  Google Scholar 

  • Dall W, Smith DM (1986) Oxygen consumption and ammonia–N excretion in fed and starved tiger prawns, Penaeus esculentus Haswell. Aquaculture 55:23–33

    Article  CAS  Google Scholar 

  • Elliott JM, Davison W (1975) Energy equivalents of oxygen consumption in animals energetics. Oecologia 19:195–201

    Article  CAS  Google Scholar 

  • Grably S, Piery Y (1981) Weight and tissue changes in long-term starved frogs Rana esculenta. Comp Biochem Physiol A 69:683–688

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Helson JG, Gardner JPA (2007) Variation in scope for growth: a test of food limitation among intertidal mussels. Hydrobiologia 586:373–392

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hirata H, Yamasaki S (1987) Effect of feeding on the respiration rate of the rotifer Brachionus plicatilis. Hydrobiologia 147:283–288

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ivlev VS (1934) Eine Micromethode zur Bestimmung des Kaloriengehalts von Na¨hrstoffen. Biochem Z 6:49–55

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Lopez GR, Levinton JS (1987) Ecology of deposit feeding animals in marine sediments. Q Rev Biol 62:235–260

    Article  Google Scholar 

  • Mayzaud P, Conover RJ (1988) O–N atomic ratio as a tool to describe zooplankton metabolism. Mar Ecol Prog Ser 45:289–302

    Article  CAS  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Phys A 156:1–18

    Article  Google Scholar 

  • Mikkelsen T (1988) The secret in the blue blood. Science Press, Beijing

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Patil JS, Anil AC (2000) Epibiotic community of the horseshoe crab Tachypleus gigas. Mar Biol 136:699–713

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Qvarnstrom A, Wiley C, Svedin N, Vallin N (2009) Life-history divergence facilitates regional coexistence of competing Ficedula flycatchers. Ecology 90:1948–1957

    Article  Google Scholar 

  • Regnault M (1987) Nitrogen excretion in marine and fresh water crustacea. Biol Rev 62:1–24

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sekiguchi K (1988) Ecology. In: Sekiguchi K (ed) Biology of horseshoe crabs. Science House Co. Ltd., Tokyo, pp 50–68

    Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Smith SA, Berkson J (2005) Laboratory culture and maintenance of the horseshoe crab (Limulus polyphemus). Lab Animal 34:27–34

    Article  Google Scholar 

  • Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  CAS  Google Scholar 

  • Stead RA, Thompson RJ (2003) Physiological energetics of the protobranch bivalve Yoldia hyperborea in a cold ocean environment. Polar Biol 26:71–78

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Taghon GL, Greene RR (1992) Utilization of deposited and suspended particulate matter by benthic interface feeders. Limnol Oceanogr 37:1370–1391

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wassmann P (1991) Dynamics of primary production and sedimentation in shallow fjords and polls of Western Norway. Oceanogr Mar Biol 29:87–154

    Google Scholar 

  • 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

    Google Scholar 

  • 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)

    Google Scholar 

  • 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)

    Google Scholar 

  • Westerterp K (1977) How rats economize energy loss in starvation. Physiol Zool 50:331–362

    Article  Google Scholar 

  • Widdows J (1973) Effect of temperature and food on heart beat, ventilation rate and oxygen uptake of Mytilusedulis. Mar Biol 20:269–276

    Article  Google Scholar 

  • Widdows J (1985) Physiological procedures. In: Bayne BL (ed) The effects of stress and pollution on marine animals. Praegar, New York, pp 161–178

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Paul K. S. Shin.

Additional information

Communicated by H. O. Pörtner.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1672-0

Keywords

Navigation