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).
Similar content being viewed by others
References
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
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
APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC
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, Westport
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
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 149–187
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
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
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
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
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
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
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
Colvin LB, Brand CW (1977) The protein requirement of penaeid shrimp at various life cycle stages in controlled environmental systems. Proc. World. Maricul. Soc 8:821–840
Conover RJ (1966) Assimilation of the organic matter by zooplankton. Limnol Oceanogr 11:345–388
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
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
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
Domingues P (1999) Development of alternative diets for the mass culture of the European cuttlefish Sepia officinalis. University of the Algarve, Portugal, pp 1–95
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
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
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
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
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
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
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
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
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
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
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
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 617–630
Houlihan DF, Kelly K, Boyle PR (1998) Correlates of growth and feeding in laboratory-maintained Eledone cirrhosa (Cephalopoda:Octopoda). J Mar Biol Assoc UK 78:919–932
Ibañez CM, Chong J (2008) Feeding ecology of Enteroctopus megalocyathus (Cephalopoda: Octopodidae) in South Chile. J Mar Biol Assoc UK 88:793–798
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 47:313–322
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
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
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
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 28:245–256
Lucas A (1993) Bioénergétique Des Animaux Aquatiques. Masson, Paris
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 52
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
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
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
O’Dor RK, Wells MJ (1987) Energy and nutrient flow. In: O’Dor RK, Wells MJ (eds) Cephalopod life cycles. Academic Press, London, pp 109–131
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
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
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
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
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
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
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
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 467–476
Schmidt-Nielsen K (1990) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge
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
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 56:217–222
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
Segawa S, Nomoto A (2002) Laboratory growth, feeding, oxygen consumption and ammonia excretion of Octopus ocellatus. Bull Mar Sci 71:801–813
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
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
Solis M (1997) The Octopus maya fishery of the Yucatán Peninsula. Fish Market Potential Octopus Calif CMSC 10:1–10
Stauffer GD (1973) A growth model for salmonids reared in hatchery envionments. Ph.D. Thesis, Univ. Washington, Seattle, p 173
Van Heukelem WF (1977) Laboratory maintenance, breeding, rearing and biomedical research potential of the Yucatan octopus (Octopus maya). Lab Anim Sci 27:852–859
Van Heukelem WF (1983) Octopus maya. Cephalopod life cycles. Academic Press, London, pp 311–323
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
Zar JH (1974) Bioestatistical analysis. Prentice-Hall, Englewood Cliff
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. O. Pörtner.
Rights and permissions
About this article
Cite this article
Farías, A., Uriarte, I., Hernández, J. et al. How size relates to oxygen consumption, ammonia excretion, and ingestion rates in cold (Enteroctopus megalocyathus) and tropical (Octopus maya) octopus species. Mar Biol 156, 1547–1558 (2009). https://doi.org/10.1007/s00227-009-1191-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-009-1191-4