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Marine Biology

, Volume 156, Issue 8, pp 1547–1558 | Cite as

How size relates to oxygen consumption, ammonia excretion, and ingestion rates in cold (Enteroctopus megalocyathus) and tropical (Octopus maya) octopus species

  • Ana Farías
  • Iker Uriarte
  • Jorge Hernández
  • Soledad Pino
  • Cristina Pascual
  • Claudia Caamal
  • Pedro Domíngues
  • Carlos Rosas
Original Paper

Abstract

The scaling of metabolic rates with body mass is one of the best known and most studied characteristics of aquatic animals. Herein, we studied how size is related to oxygen consumption, ammonia excretion, and ingestion rates in tropical (Octopus maya) and cold-water (Enteroctopus megalocyathus) cephalopod species in an attempt to understand how size affects their metabolism. We also looked at how cephalopod metabolisms are modulated by temperature by constructing the relationship between metabolism and temperature for some benthic octopod species. Finally, we estimated the energy balance for O. maya and E. megalocyathus in order to validate the use of this information for aquaculture or fisheries management. In both species, oxygen consumption and ammonia excretion increased allometrically with increasing body weight (BW) expressed as Y = aBWb. For oxygen consumption, b was 0.71 and 0.69 for E. megalocyathus and O. maya, respectively, and for ammonia excretion it was 0.37 and 0.43. Both species had low O/N ratios, indicating an apparent dependence on protein energy. The mean ingestion rates for E. megalocyathus (3.1 ± 0.2% its BW day−1) and O. maya (2.9 ± 0.5% its BW day−1) indicate that voracity, which is characteristic of cephalopods, could be independent of species. The scope for growth (P = I − (H + U + R) estimated for E. megalocyathus was 28% higher than that observed in O. maya (320 vs. 249 kJ day−1 kg−1). Thus, cold-water cephalopod species could be more efficient than tropical species. The protein and respiratory metabolisms of O. maya, E. megalocyathus, and other octopod species are directly dependent on temperature. Our results offer complementary evidence that, as Clarke (2004) stated, the metabolic response (R and U) cannot be determined mechanistically by temperature, as previously proposed (Gillooly et al. 2002).

Keywords

Oxygen Consumption Metabolic Rate Live Weight Oxygen Consumption Rate Ammonia Excretion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The study on Enteroctopus megalocyathus was financed by FONDECYT 1070800 and FONDEF D04 I1401. The study of O. maya was financed by DGAPA-UNAM project No. IN 216006-3 and CONACYT-Básico 2007-24743. We thank the Programa Bicentenario de Ciencia y Tecnología of CONICYT project ACI-34 for contributing to the collaborative work between Chilean and Mexican teams. We finally thank Ms. Jessica Dörner of HIM-UACH and Mr. Juan Carlos Rojas of UNAM for their valuable technical assistance. Thanks are given to anonymous referees that helped us improve the original manuscript.

References

  1. Aguado-Giménez F, García-García B (2003) Growth and food intake models in Octopus vulgaris Cuvier (1797): influence of body weight, temperature, sex and diet. Aquac Int 10:361–377. doi: https://doi.org/10.1023/A:1023335024053 CrossRefGoogle Scholar
  2. Aguila J, Cuzon G, Pascual C, Domingues P, Gaxiola G, Sánchez A, Maldonado T, Rosas C (2007) The effects of fish hydrolysate (CPSP) level on Octopus maya (Voss and Solis) diet: digestive enzyme activity, blood metabolites, and energy balance. Aquaculture 273:641–655. doi: https://doi.org/10.1016/j.aquaculture.2007.07.010 CrossRefGoogle Scholar
  3. APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DCGoogle Scholar
  4. Bayne BL, Brown DA, Burns K, Ivanovici A, Livingstone DR, Lowe DM, Moore MN, Stebbing ARD, Widdows J (1985) The effect of stress and pollution on marine animals (Praeger special studies). Praeger Scientific, WestportGoogle Scholar
  5. Borer KT, Lane CE (1971) Oxygen requirements of Octopus briareus Robson at different temperatures and oxygen concentrations. J Exp Mar Biol Ecol 7:263–269. doi: https://doi.org/10.1016/0022-0981(71)90009-8 CrossRefGoogle Scholar
  6. Boucaud-Camou E, Boucher-Rodoni R (1983) Feeding and digestion in cephalopods. In: Saleuddin ASM, Wilbur KM (eds) The mollusca. Academic Press, New York, pp 149–187CrossRefGoogle Scholar
  7. Boucher-Rodoni R, Mangold K (1985) Ammonia excretion during feeding and starvation in Octopus vulgaris. Mar Biol (Berl) 86:193–197. doi: https://doi.org/10.1007/BF00399026 CrossRefGoogle Scholar
  8. Cerezo-Valverde J, Garcia-Garcia B (2005) Suitable dissolved oxygen levels for common octopus (Octopus vulgaris cuvier, 1797) at different weights and temperatures: analysis of respiratory behaviour. Aquaculture 244:303–314. doi: https://doi.org/10.1016/j.aquaculture.2004.09.036 CrossRefGoogle Scholar
  9. Cerezo-Valverde J, García-García B (2004) Influence of body weight and temperature on post-prandial oxygen consumption of common octopus (Octopus vulgaris). Aquaculture 233:599–613. doi: https://doi.org/10.1016/j.aquaculture.2003.11.025 CrossRefGoogle Scholar
  10. 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. doi: https://doi.org/10.1016/0044-8486(95)01060-2 CrossRefGoogle Scholar
  11. Clarke A (2004) Is the universal temperature dependence of metabolism? Funct Ecol 18:252–256. doi: https://doi.org/10.1111/j.0269-8463.2004.00842.x CrossRefGoogle Scholar
  12. Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature? Funct Ecol 18:243–251. doi: https://doi.org/10.1111/j.0269-8463.2004.00841.x CrossRefGoogle Scholar
  13. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905. doi: https://doi.org/10.1046/j.1365-2656.1999.00337.x CrossRefGoogle Scholar
  14. Colvin LB, Brand CW (1977) The protein requirement of penaeid shrimp at various life cycle stages in controlled environmental systems. Proc. World. Maricul. Soc 8:821–840CrossRefGoogle Scholar
  15. Conover RJ (1966) Assimilation of the organic matter by zooplankton. Limnol Oceanogr 11:345–388Google Scholar
  16. Crocos PJ, Coman GJ (1997) Seasonal and age variability in the reproductive performance of Penaeus semisulcatus broodstock: optimising broodstock selection. Aquaculture 155:57–69. doi: https://doi.org/10.1016/S0044-8486(97)00109-9 CrossRefGoogle Scholar
  17. Dall W, Smith DM (1986) Oxygen consumption and ammonia-N excretion in fed and starved tiger prawns Penaeus esculentus Haswell. Aquaculture 55:23–33. doi: https://doi.org/10.1016/0044-8486(86)90052-9 CrossRefGoogle Scholar
  18. Daly HI, Peck LS (2000) Energy balance and cold adaptation in the octopus Paraledone charcoti. J Exp Mar Biol Ecol 245:197–214. doi: https://doi.org/10.1016/S0022-0981(99)00161-6 CrossRefGoogle Scholar
  19. Domingues P (1999) Development of alternative diets for the mass culture of the European cuttlefish Sepia officinalis. University of the Algarve, Portugal, pp 1–95Google Scholar
  20. Domingues P, Sykes A, Andrade P (2001) The use of Artemia sp. or mysids as food source for hatchlings of the cuttlefish (Sepia officinalis L.); effects on growth and survival throughout the life cycle. Aquac Int 319–331. doi: https://doi.org/10.1023/A:1020416811568 CrossRefGoogle Scholar
  21. Domingues P, Sykes A, Sommerfield A, Almansa E, Lorenzo A, Andrade P (2004) Growth and survival of cuttlefish, Sepia officinalis (Linnaeus, 1758) of different ages fed crustaceans and fish. Effects of frozen and live prey. Aquaculture 229:239–254. doi: https://doi.org/10.1016/S0044-8486(03)00351-X CrossRefGoogle Scholar
  22. Domingues P, DiMarco FP, Andrade JP, Lee PG (2005) Effect of artificial diets on growth, survival and condition of adult cuttlefish, Sepia officinalis Linnaeus, 1758. Aquac Int 13:423–440. doi: https://doi.org/10.1007/s10499-005-6978-9 CrossRefGoogle Scholar
  23. Domingues P, López N, Muñoz JA, Maldonado T, Gaxiola G, Rosas C (2007) Effects of an artificial diet on growth and survival of the Yucatan octopus, Octopus maya. Aquac Nutr 13:1–9. doi: https://doi.org/10.1111/j.1365-2095.2007.00474.x CrossRefGoogle Scholar
  24. Farias A, García-Esquivel Z, Viana MT (2003) Physiological energetics of the green abalone, Haliotis fulgens, fed on balanced diet. J Exp Mar Biol Ecol 289:263–276. doi: https://doi.org/10.1016/S0022-0981(03)00049-2 CrossRefGoogle Scholar
  25. Gallardo PP, Alfonso E, Gaxiola G, Soto LA, Rosas C (1995) Feeding schedule of Penaeus setiferus larvae based in diatoms (Chaetoceros ceratosporum), Flagellates (Tetraselmis chuii) and Artemia nauplii. Aquaculture 131:239–253. doi: https://doi.org/10.1016/0044-8486(94)00321-E CrossRefGoogle Scholar
  26. García-García B, Aguado-Giménez F (2002) Influence of diet on growing and nutrient utilization in the common octopus (Octopus vulgaris). Aquaculture 211:173–184. doi: https://doi.org/10.1016/S0044-8486(01)00788-8 CrossRefGoogle Scholar
  27. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251. doi: https://doi.org/10.1126/science.1061967 CrossRefGoogle Scholar
  28. Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH (2002) Effect of size and temperature on developmental time. Nature 417:70–73. doi: https://doi.org/10.1038/417070a CrossRefGoogle Scholar
  29. Giménez FA, Garcia E (2002) Growth and food intake models in Octopus vulgaris Couvier (1797): Influence of body weight, temperature, sex and diet. Aquac Int 10:361–367. doi: https://doi.org/10.1023/A:1023335024053 CrossRefGoogle Scholar
  30. Hagerman L, Szaniawska A (1994) Hemolymph nitrogen compounds and ammonia efflux rates under anoxia in the brackish water isopod Saduria entomodon. Mar Ecol Prog Ser 103:285–289. doi: https://doi.org/10.3354/meps103285 CrossRefGoogle Scholar
  31. Hérnandez-Flores A, Solis-Ramirez M, Espinoza Méndez JC, Agilar RM, Gil TR (2001) Pulpo: Octopus maya. Sustentabilidad y pesca responsable en México: Evaluación y Manejo. INP/SAGARPA, Mexico, pp 617–630Google Scholar
  32. Houlihan DF, Kelly K, Boyle PR (1998) Correlates of growth and feeding in laboratory-maintained Eledone cirrhosa (Cephalopoda:Octopoda). J Mar Biol Assoc UK 78:919–932CrossRefGoogle Scholar
  33. Ibañez CM, Chong J (2008) Feeding ecology of Enteroctopus megalocyathus (Cephalopoda: Octopodidae) in South Chile. J Mar Biol Assoc UK 88:793–798Google Scholar
  34. Iglesias J, Sánchez FJ, Otero JJ, Moxica C (2000) Culture of octopus (Octopus vulgaris, Cuvier): present knowledge, problems and perspectives. Recent advances in Mediterranean Marine Aquaculture Finifish Species Diversification. Cah Options Mediterr 47:313–322Google Scholar
  35. Katsanevakis S, Protopapas N, Miliou H, Verriopoulos G (2005a) Effect of temperature on specific dynamic action in the common octopus Octopus vulgaris (Cephalopoda). Mar Biol (Berl) 146:733–738. doi: https://doi.org/10.1007/s00227-004-1476-6 CrossRefGoogle Scholar
  36. Katsanevakis S, Stephanopoulou S, Miliou H, Moraitou-Apostolopoulou M, Verriopoulos G (2005b) Oxygen consumption and ammonia excretion of Octopus vulgaris (Cephalopoda) in relation to body mass and temperature. Mar Biol (Berl) 146:725–732. doi: https://doi.org/10.1007/s00227-004-1473-9 CrossRefGoogle Scholar
  37. Koueta N, Boucaud-Camou E (1999) Food intake and growth in reared early juvenile cuttlefish Sepia officinalis L. Mollusca Cephalopoda. J Exp Mar Biol Ecol 240:93–109. doi: https://doi.org/10.1016/S0022-0981(99)00054-4 CrossRefGoogle Scholar
  38. Lei CH, Hsieh LH, Chen CK (1989) Effects of salinity on the oxygen consumption and ammonia-N excretion of young juvenile of the grass shrimp, Penaeus monodon. Bull Inst Zool Acad Sin 28:245–256Google Scholar
  39. Lucas A (1993) Bioénergétique Des Animaux Aquatiques. Masson, ParisGoogle Scholar
  40. Mancilla E (2004) Bases sobre el manejo y mantención de Enteroctopus megalocyathus: crecimiento y reproducción. Undergraduate Degree Thesis in Marine Biology, Instituto de Biología Marina. Universidad Austral de Chile, p 52Google Scholar
  41. Mayzaud P, Conover RJ (1988) O:N atomic ratio as a tool to describe zooplankton metabolism. Mar Ecol Prog Ser 45:289–302. doi: https://doi.org/10.3354/meps045289 CrossRefGoogle Scholar
  42. Miliou H, Fintikaki M, Kountouris T, Verriopoulos G (2005) Combined effects of temperature and body weight on growth and protein utilization of the common octopus Octopus vulgaris. Aquaculture 249:245–256. doi: https://doi.org/10.1016/j.aquaculture.2005.03.038 CrossRefGoogle Scholar
  43. Navarro JC, Villanueva R (2003) The fatty acid composition of Octopus vulgaris paralarvae reared with live and inert food: deviation from their natural fatty acid profile. Aquaculture 219:613–631. doi: https://doi.org/10.1016/S0044-8486(02)00311-3 CrossRefGoogle Scholar
  44. O’Dor RK, Wells MJ (1987) Energy and nutrient flow. In: O’Dor RK, Wells MJ (eds) Cephalopod life cycles. Academic Press, London, pp 109–131Google Scholar
  45. Obaldo LG, Divakaran S, Tacon AG (2002) Method for determining the physical stability of shrimp feeds in water. Aquac Res 33(5):369–377. doi: https://doi.org/10.1046/j.1365-2109.2002.00681.x CrossRefGoogle Scholar
  46. Peixoto S, Cavalli RO, Wasielesky W, D’Incao F, Krummenauer D, Milach AM (2004) Effects on age and size on reproductive performance of captive Farfantepenaeus paulensis broodstock. Aquaculture 238:173–182. doi: https://doi.org/10.1016/j.aquaculture.2004.04.024 CrossRefGoogle Scholar
  47. Pérez MC, López DA, Aguila K, González ML (2006) Feeding and growth in captivity of the octopus Enteroctopus megalocyathus. Aquac Res 37:550–555. doi: https://doi.org/10.1111/j.1365-2109.2006.01454.x CrossRefGoogle Scholar
  48. Petza D, Katsanevakis S, Verriopoulos G (2006) Experimental evaluation of the energy balance in Octopus vulgaris, fed ad libitum on a high-lipid diet. Mar Biol (Berl) 148:827–832. doi: https://doi.org/10.1007/s00227-005-0129-8 CrossRefGoogle Scholar
  49. Pörtner HO, Storch D, Heilmayer O (2005) Constraints and trade offs in climate-dependent adaptation: energy budget and growth in a latitudinal cline. Sci Mar 69:271–285. doi: https://doi.org/10.3989/scimar.2005.69s2271 CrossRefGoogle Scholar
  50. Rosas C, Cuzon G, Pascual C, Gaxiola G, López N, Maldonado T, Domingues P (2007) Energy balance of Octopus maya fed crab and artificial diet. Mar Biol (Berl) 152:371–378. doi: https://doi.org/10.1007/s00227-007-0692-2 CrossRefGoogle Scholar
  51. Rosas C, Tut J, Baesa J, Sánchez A, Sosa V, Pascual C, Arena L, Domingues P, Cuzon G (2008) Effect of type of binder on growth, digestibility, and energetic balance of Octopus maya. Aquaculture 275:291–297. doi: https://doi.org/10.1016/j.aquaculture.2008.01.015 CrossRefGoogle Scholar
  52. Sakurai Y, Ikeda Y, Shimizu M, Shimeno S, Shimazaki K (1993) Feeding and growth of captive adult Japanese common squid, Todarodes pacificus, mesauring initial body size by cold anesthesia. In: Okutani T, O’Dor RK, Kubodera T (eds) Advances in fisheries biology. Tokai University Press, Tokyo, pp 467–476Google Scholar
  53. Schmidt-Nielsen K (1990) Animal physiology: adaptation and environment. Cambridge University Press, CambridgeGoogle Scholar
  54. Schmitt ASC, Uglow RF (1997) Effects of ambient ammonia levels on blood ammonia, ammonia excretion and heart scaphognathite of Nephrops norvegicus. Mar Biol (Berl) 127:411–418. doi: https://doi.org/10.1007/s002270050028 CrossRefGoogle Scholar
  55. Segawa S (1990) Food consumption, food conversion and growth rates of the oval squid Sepioteuthis lessoniana by laboratory experiments. Nippon Suisam Gakkaishi. Bull Jpn Soc Sci Fish 56:217–222CrossRefGoogle Scholar
  56. Segawa S, Hanlon RT (1988) Oxygen consumption and ammonia excretion rates in Octopus maya, Loligo forbesi and Lolliguncula brevis (Molluscs: Cephalopoda). Mar Behav Physiol 13:389–400. doi: https://doi.org/10.1080/10236248809378687 CrossRefGoogle Scholar
  57. Segawa S, Nomoto A (2002) Laboratory growth, feeding, oxygen consumption and ammonia excretion of Octopus ocellatus. Bull Mar Sci 71:801–813Google Scholar
  58. Seibel BA, Childress JJ (2000) Metabolism of benthic octopods (Cephalopoda) as a function of habitat depth and oxygen concentration. Deep Sea Res 47:1247–1260. doi: https://doi.org/10.1016/S0967-0637(99)00103-X CrossRefGoogle Scholar
  59. Smith CD (2003) Diet of Octopus vulgaris in False Bay, South Africa. Mar Biol (Berl) 143:1127–1133. doi: https://doi.org/10.1007/s00227-003-1144-2 CrossRefGoogle Scholar
  60. Solis M (1997) The Octopus maya fishery of the Yucatán Peninsula. Fish Market Potential Octopus Calif CMSC 10:1–10Google Scholar
  61. Stauffer GD (1973) A growth model for salmonids reared in hatchery envionments. Ph.D. Thesis, Univ. Washington, Seattle, p 173Google Scholar
  62. Van Heukelem WF (1977) Laboratory maintenance, breeding, rearing and biomedical research potential of the Yucatan octopus (Octopus maya). Lab Anim Sci 27:852–859PubMedGoogle Scholar
  63. Van Heukelem WF (1983) Octopus maya. Cephalopod life cycles. Academic Press, London, pp 311–323Google Scholar
  64. Wells MJ, O’Dor RK, Mangold K, Wells R (1983) Diurnal changes in activity and metabolic rate in Octopus vulgaris. Mar Behav Physiol 9:275–287. doi: https://doi.org/10.1080/10236248309378598 CrossRefGoogle Scholar
  65. Zar JH (1974) Bioestatistical analysis. Prentice-Hall, Englewood CliffGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Ana Farías
    • 1
    • 2
  • Iker Uriarte
    • 1
    • 2
  • Jorge Hernández
    • 1
    • 2
    • 5
  • Soledad Pino
    • 2
  • Cristina Pascual
    • 3
  • Claudia Caamal
    • 3
  • Pedro Domíngues
    • 4
  • Carlos Rosas
    • 3
  1. 1.Instituto de AcuiculturaUniversidad de AustralPuerto MonttChile
  2. 2.CIEN AustralPuerto MonttChile
  3. 3.Unidad Multidisciplinaria de Docencia e Investigación, Facultad de CienciasUNAMYucatánMexico
  4. 4.Centro IFAPACartayaSpain
  5. 5.Departamento de Ecología y Biología Animal Edificio de Ciencias ExperimentalesUniversidad de VigoVigoSpain

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