Aquaculture 211 (2002) 171 182 www.elsevier.

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Influence of diet on ongrowing and nutrient utilization in the common octopus (Octopus vulgaris)
n Garc a Garc a *, Felipe Aguado Gime nez Benjam
a de Agricultura, Agua y Medio Ambiente de la Regio n de Murcia, C.I.D.A.-Acuicultura, Consejer Puerto de San Pedro del Pinatar, Apdo 65, 30740 San Pedro del Pinatar, Murcia, Spain Received 11 April 2001; received in revised form 22 August 2001; accepted 22 August 2001

Abstract Octopus vulgaris ongrowing has recently begun to develop in Spanish coastal waters. The need to diversify aquaculture products in terms of its biological and market potential makes octopus a serious candidate for rearing. Ongrowing success depends on several factors, such as environmental rearing conditions, diet and nutritive utilization. Two fresh diets of low market value (Boops boops and Sardina pilchardus) were used to assess growth rate, feeding rate and efficiency by means of multiple regression analysis. Factors considered were sex and diet as qualitative variables, and body weight and temperature as quantitative ones. No significant differences were observed regarding growth and sex although it was slightly higher in males. Nevertheless, food intake was higher in females as well as in the sardine-fed females. Growth with bogue-fed octopus was significantly higher. Smaller specimens grew more than the larger ones in proportion to initial body weight. The rise in temperature increased growth and food intake over our experimental range. Differences in growth may have been due to the different lipid content of the diets since digestibility of lipid in cephalopods is poor and their main energy source is protein. The higher food intake in females may be caused by metabolic changes related to the reproduction period although this remains to be confirmed. D 2002 Elsevier Science B.V. All rights reserved.
Keywords: Octopus vulgaris; Ongrowing; Feeding and nutrition; Growth; Temperature; Body weight; Mediterranean Sea

* Corresponding author. Centro de Recursos Marinos, Puerto de San Pedro del Pinatar, Apdo 65, 30740 San Pedro del Pinatar, Murcia, Spain. Tel.: +34-968-184518; fax: +34-968-184518. a Garc a). E-mail address: benjamin.garcia@carm.es (B. Garc 0044-8486/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 ( 0 1 ) 0 0 7 8 8 - 8

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1. Introduction The common octopus (Octopus vulgaris) has many suitable characteristics for rearing such as high fecundity rate (producing 100,000 500,000 eggs per female) (Wells, 1978), fast growth (Mangold, 1983; Iglesias et al., 1997), high food conversion rate (assimilating 40 60% of ingested food) (Mangold and von Boletzky, 1973), and good market prices and increasing demand. In Spanish Atlantic coastal waters, some trials have been carried out, providing excellent results (Iglesias et al., 1997; Luaces-Canosa ndez, 1999; Rodr guez and Carrasco, 1999). Octopuses were fed mainly and Rey-Me crabs, and to a lesser extent, fish and other cephalopods, similar to their natural diet (Nigmatullin and Ostapenko, 1976; Guerra, 1978). Under experimental conditions, Cagnetta and Sublimi (1999) observed better growth in octopus when fed crabs than fish. In the Mediterranean, crab supply is poor and expensive due to low catches. Therefore, Mediterranean industrial octopus ongrowing must be carried out by mainly feeding low market value fish, such as the small pelagic fishes Boops boops, Sardina pilchardus, Sardinella aurita, Trachurus mediterraneus, etc. Among these species, two groups can be distinguished according to their lipid content: the bluefish group formed by S. pilchardus and S. aurita have a higher lipid content than the whitefish group formed by B. boops and T. mediterraneus. This distinction is important since cephalopod lipid digestibility is very poor (ODor et al., 1984) and their capacity to catabolize lipid is limited (Ballantyne et al., 1981; Mommsen and Hochachka, 1981; Navarro and Villanueva, 2000). Protein is the principal energy source for cephalopods. However, lipid and protein content of food must have some influence in on-growing and nutrient utilization. This work investigates growth and nutrient utilization of O. vulgaris fed with two diets based on low market value fish with different lipid content as B. boops and S. pilchardus in Southeastern Mediterranean. In addition, the influence of culture variables is considered, such as body weight, sex and water temperature.

2. Materials and methods The octopuses (O. vulgaris) were caught in November by professional fishing boats using drag nets. Until arrival at the port, the octopuses were kept in 100-l tanks with the water being renewed every 15 30 min. From the port (Cartagena) to the laboratory in San Pedro del Pinatar 35 km away, the octopuses were transported in 1000-l tanks in seawater supplied with oxygen. The temperature did not exceed 16 jC and oxygen never fell below 70%. Survival, which in such conditions is inversely and lineally related with temperature (Aguado et al., 2001), was 90%. Before the experiment started, the octopuses were kept together in a raceway tank of 4 m3 for 15 days. During this period of acclimation, the water temperature was 16 jC, the dissolved oxygen was of 80% saturation, and no mortality was observed. Twenty-four specimens were used, distributed individually in 400-l cylindrical tanks with open seawater flow. Each tank had a 20-cm diameter PVC tube as refugee. Initial experimental conditions are showed in Table 1.

a Garc a, F. Aguado Gime nez / Aquaculture 211 (2002) 171182 B. Garc Table 1 Initial experimental conditions Experimental group (sex and diet) FS FB MB MS Specimen number 6 6 6 6

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Average weight F S.D. (g) 316 F 57 378 F 77 418 F 69 346 F 47

FS = female with diet of sardine; FB = female with diet of bogue; MB = male with diet of bogue; and MS = male with diet of sardine. S.D. = standard deviation.

The trial was carried out from December 1998 to May 1999. The flow-through of seawater in tanks was adjusted so that oxygen saturation was never below 80% at the outlet, for which measurements were taken twice a day. The photoperiod (37j50VN, 0j46VW) and water temperature (ranging from 13 jC in February to 19 jC in May) were natural (see Table 3). The octopuses were fed to satiation, the food being provided once a day during the morning. Fish were provided without tails or heads since octopuses do not usually consume these parts. Every day, more fish were introduced into the tanks than the octopus could consume. The following day, uneaten fish were removed from the tanks and dried with absorbent paper before weighing. The amount of food consumed was calculated as the difference between food supplied and that removed. The amount of food provided daily was adjusted so that the octopuses were always fed to satiation. Table 2 shows the nutritional composition of both food fishes. Protein content was determined by the Kjeldhal method using the factor conversion of 6.25. Lipid was obtained with ether extraction (SOXTEC System-HTC). Moisture was obtained by drying (105 F 1 jC, 24 h) until constant weight, and ash by incineration (loss in weight: 450 F 1 jC, 24 h). Net energy was estimated using Miglavs and Jobling (1989) energy coefficients: protein 23.6 kJ/g and lipid 38.9 kJ/g. Assays lasted for 176 days and octopuses were sampled every 30 days. During the experiment, the octopuses that died were replaced by others of similar body weight. In

Table 2 Macronutrient composition of each diet (percent wet substance F S.D.) Sardine Crude lipid Crude protein Ash Moisture Gross energy (GE) (kJ / 100 g food) Protein / energy ratio (P / E ) (g protein/MJ) 19.64 F 3.02 17.77 F 0.66 2.73 F 0.35 60.51 F 2.01 1183.37 15.02 Bogue 5.94 F 2.56 18.48 F 1.11 3.29 F 0.05 70.52 F 3.60 667.19 27.70

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total, seven octopuses died, six of which were replaced; the last specimen died at the end of the experiment and so was not replaced. After each sampling, the following indices were calculated: Absolute growth rate (AGR): Wf Wi /t Specific growth rate (SGR): (lnWf lnWi)100 /t Absolute feeding rate (AFR): IF/t Specific feeding rate (SFR): AFR 100/Wa Feed efficiency (FE): (Wf Wi)100/IF

Table 3 Average values F S.D. for each index of each experimental period and overall results Period December, T = 15 jC (13 16 jC) Group FS FB MB MS FS FB MB MS FS FB MB MS FS FB MB MS FS FB MB MS FS FB MB MS FS FB MB MS AGR 3.43 F 0.77 3.97 F 0.96 7.36 F 2.02 3.29 F 1.72 0.99 F 0.41 2.59 F 1.28 2.24 F 0.43 1.38 F 0.52 1.97 F 0.85 2.37 F 1.31 3.59 F 2.01 2.58 F 0.47 3.48 F 1.51 6.50 F 2.04 7.29 F 2.15 5.38 F 1.07 9.40 F 2.22 9.25 F 3.53 10.65 F 4.05 7.80 F 3.85 6.53 F 3.84 12.62 F 3.16 13.19 F 2.98 4.15 F 2.75 4.25 F 0.62 6.10 F 1.63 7.12 F 1.30 4.36 F 1.39 SGR 0.95 F 0.14 0.96 F 0.19 1.50 F 0.33 0.76 F 0.35 0.24 F 0.10 0.50 F 0.18 0.37 F 0.05 0.30 F 0.13 0.45 F 0.20 0.39 F 0.15 0.50 F 0.22 0.48 F 0.10 0.66 F 0.26 0.91 F 0.24 0.86 F 0.33 0.82 F 0.19 1.33 F 0.35 0.95 F 0.33 0.91 F 0.32 0.86 F 0.30 0.68 F 0.40 1.00 F 0.21 0.90 F 0.15 0.38 F 0.22 0.72 F 0.08 0.76 F 0.14 0.79 F 0.09 0.65 F 0.08 AFR 6.96 F 1.50 9.85 F 2.72 9.55 F 2.31 8.60 F 2.23 8.50 F 1.15 8.23 F 1.88 9.93 F 1.66 8.49 F 1.56 10.47 F 2.10 9.65 F 1.21 9.60 F 0.92 9.37 F 0.87 14.81 F 1.67 13.32 F 1.66 12.74 F 0.62 14.41 F 1.46 18.42 F 21.2 21.24 F 3.11 21.37 F 2.60 17.21 F 22 28.83 F 4.56 35.92 F 10.5 36.70 F 4.30 26.70 F 4.54 14.58 F 1.90 16.06 F 2.66 16.40 F 1.32 13.73 F 1.90 SFR 1.94 F 0.36 2.32 F 0.28 1.91 F 0.34 2.02 F 0.29 2.11 F 0.50 1.63 F 0.20 1.63 F 0.11 1.81 F 0.39 2.38 F 0.35 1.71 F 0.40 1.41 F 0.37 1.80 F 0.41 2.84 F 0.33 1.88 F 0.36 1.50 F 0.22 2.17 F 0.24 2.56 F 0.32 2.23 F 0.29 1.86 F 0.19 1.97 F 0.22 3.04 F 0.49 2.81 F 0.66 2.48 F 0.26 2.64 F 0.75 2.17 F 0.13 1.77 F 0.20 1.58 F 0.14 1.94 F 0.40 FE 49.27 F 2.63 41.68 F 9.48 80.55 F 26.08 38.65 F 19.55 11.60 F 4.59 30.58 F 11.48 22.65 F 2.61 17.47 F 8.13 19.91 F 10.37 25.75 F 16.61 39.03 F 26.07 27.99 F 6.83 24.26 F 12.45 49.26 F 15.86 57.20 F 16.07 37.60 F 7.85 53.14 F 20.86 42.56 F 14.67 49.71 F 18.20 44.37 F 19.53 22.09 F 11.04 36.30 F 9.19 35.90 F 6.22 14.83 F 7.46 29.18 F 1.94 37.84 F 8.03 43.27 F 5.32 31.65 F 9.48

January, T = 14 jC (12 15 jC)

February, T = 13 jC (12 14 jC)

March, T = 15 jC (14 16 jC)

April, T = 17 jC (16 19 jC)

May, T = 19 jC (17 21 jC)

Overall

Mean temperature and range of each experimental period.

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Fig. 1. Weight gained of experimental groups (bars = standard deviation).

where Wf = final weight (g); Wi = initial weight (g); Wa = average weight (g); t = time in days; and IF = ingested food (difference between food supplied and food consumed). 2.1. Statistical analyses Considered variables that may have some influence on growth and food average body weight between sampling (Wa) and temperature (T a) as factors, and sex (S) and diet (D) as qualitative factors. Partial correlation were used in order to assess the influence of these variables. Changes in intake were quantitative tests (PCT) growth and

Table 4 Results of partial correlation test (PCT) AGR Temperature (jC) Weight Sex Diet 0.32 P < 0.001 0.45 P < 0.001 0.03 n.s. 0.21 P < 0.05 SGR 0.41 P < 0.001 0.23 P < 0.05 0.06 n.s. 0.27 P < 0.05 AFR 0.56 P < 0.001 0.70 P < 0.001 0.31 P < 0.001 0.21 P < 0.05 SFR 0.56 P < 0.001 0.24 P < 0.05 0.35 P < 0.001 0.28 P < 0.05 FE 0.17 n.s. 0.12 n.s. 0.18 P < 0.05 0.32 P < 0.001

Sex: 0 = male and 1 = female; diet: 0 = bogue and 1 = sardine; and n.s. = not significant.

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feeding rates could be explained with mathematical equations like lnY = lna + blnWa + a Garc a, 1994; Petridis and Rogdakis, 1996). Therefore, data were adjusted clnT a (Garc by means of multiple regression analyses to a model like lnY = lna + blnWa + clnT a + dS + eD (S = 0 for males, S = 1 for females, D = 0 for B. boops and D = 1 for S. pilchardus). ANOVA was used to test the significance of models and the Students t-test for the coefficient significance. Statistical analyses were done with STATISTICA version 5.0 program.

3. Results Average values of growth, feeding rates and feed efficiency of each experimental group for each period between sampling are shown in Table 3, as well as the overall values. Fig. 1 shows body weight evolution of each group throughout the experiment, and Table 4 shows the results of PCT between different variables considered. Bogue-fed individuals achieved significantly higher growth rates and final weight than those fed sardine. For the same kind of food, males obtained higher final weight than females. Nevertheless, PCT displayed no significant correlation between sex and AGR or SGR although there was significance between sex and AFR and SFR: females had higher feeding rates than males. The type of diet correlated significantly with growth and feeding rate, resulting in higher growth for bogue-fed and higher food intake for sardine-fed individuals. Body weight and

Table 5 Results of multiple regression analyses Coefficients lna Intercept b Weight c Temperature d Sex e Diet R 2 Raj S.E.E. ANOVA df F P< AGR 10.082 F 1.078 P < 0.0001 0.677 F 0.186 P < 0.001 2.668 F 0.587 P < 0.0001 0.041 F 0.102 P = 0.688, n.s. 0.306 F 0.108 P < 0.01 0.755 55.63 0.538 SGR 5.504 F 1.084 P < 0.0001 0.323 F 0.187 P = 0.087, n.s. 2.679 F 0.590 P < 0.0001 0.041 F 0.102 P = 0.693, n.s. 0.307 F 0.108 P < 0.01 0.467 19.19 0.541 AFR 7.073 F 0.369 P < 0.0001 0.806 F 0.064 P < 0.0001 1.579 F 0.201 P < 0.0001 0.135 F 0.035 P < 0.001 0.121 F 0.037 P < 0.01 0.935 87.05 0.184 SFR 2.468 F 0.369 P < 0.0001 0.194 F 0.064 P < 0.01 1.579 F 0.201 P < 0.0001 0.135 F 0.035 P < 0.001 0.121 F 0.037 P < 0.01 0.721 50.34 0.184

120 39.86 0.0001

120 8.36 0.0001

120 209.4 0.0001

120 32.42 0.0001

Values F S.D.; S.E.E.: standard error of estimate; df = degree of freedom; n.s. = not significant. lnY = lna + blnWa + clnT a + dS + eD.

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temperature were significantly correlated with growth and feeding rate. As body weight increased, AGR increased and SGR decreased, that is, like most cultured marine animals, younger specimens grew proportionally more than the older ones. Over our temperature range, as temperature increased, growth and feeding rates increased. Feeding rate correlated significantly and positively with sex and diet: females and sardine-fed showed higher AFR and SFR. FE only correlated significantly with diet and sex, indicating better food utilization in bogue-fed animals and males. Usually, FE correlates significantly with body weight and temperature, but this effect was not observed in this study. Table 5 shows results of multiple regression analyses. ANOVA shows that all models are highly significant ( P < 0.0001). Nevertheless, fitting was better when we used absolute terms (AGR and AFR, Eqs. (1) and (3)). lnAGR 10:82 0:67lnW 2:668lnT a 0:041S 0:306D lnSGR 5:504 0:323lnW 2:679lnT a 0:041S 0:307D lnAFR 7:703 0:806lnW 1:579lnT a 0:135S 0:121D lnSFR 2:468 0:194lnW 1:579lnT a 0:135S 0:121D 1 2 3 4

In AGR equations, sex coefficient was negative and very low in absolute terms, and not significantly different from zero, so it may be disregarded. Males had higher growth

Fig. 2. Effect of temperature on AGR, AFR and FE in males and females of 1000-g body weight.

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Fig. 3. Effect of temperature on AGR, AFR and FE in males bogue- and sardine-fed of 1000-g body weight.

Fig. 4. Effect of body weight on AGR, AFR and FE in specimens fed with bogue and sardine at a constant sea temperature of 18 jC.

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rates but not more significant than females. On the other hand, in the AFR equation, sex coefficient was significantly different from zero: females fed more than males. From Eqs. (1) and (3), we estimated AGR and AFR, and FE from AGR and AFR for three different situations (Figs. 2 4).

4. Discussion The trend in growth and food ingestion change according to body weight and temperature in this experiment is similar to that observed in other cultured species. The body weight coefficient in the AGR model was 0.677, similar but slightly higher than that in salmonids (0.60, Brett and Groves, 1979) or gilthead sea bream (0.55, a Garc a, 1994; 0.62, Lupatsch and Kissil, 1998), and Muller-Feuga, 1990; 0.60, Garc in the AFR model, the coefficient was 0.806, which was within the observed range for fish (0.47 1, Brett and Groves, 1979). These coefficient values confirm that absolute growth increases with body weight and food intake and specific growth decreases exponentially. Temperature coefficients in the AGR (2.66) and AFR (1.57) models were also similar a Garc a, 1994). For to cultured fish as Sparus aurata (2.43 and 1.47, respectively, Garc our wide temperature range, this parameter induced higher food intake and if it was not limited, it also increased growth (Figs. 2 and 3). However, growth rate in O. vulgaris was higher than in cultured fish such as sea bass or gilthead sea bream. According to Lee (1994), cephalopod growth rates are comparable with those of terrestrial mammals and are higher than in fish. FE did not correlate significantly with either body weight or temperature. Nevertheless, when estimated from the AGR and AFR models, it changed like in fish (Figs. 2 4), i.e., when body weight is constant and temperature range is optimal, increases in temperature result in better nutritive utilization. When temperature is constant, FE decreases when body weight increases. Mangold and von Boletzky (1973) suggested that the conversion index (CI = 1/FE) in O. vulgaris does not depend on temperature and does not seem to be reduced with body weight but is influenced by diet. It is also suggested that CI shows great individual variability. Precisely because of this variability, it was not possible to establish a clear relationship between CI or FE with body weight and temperature, as has been done with other ectotherm organisms like fish (Goolish and a Garc a, 1994). It Adelman, 1984; Hidalgo et al., 1987; Xie and Sun, 1992; Garc seems, therefore, more appropriate to establish growth and food intake models and estimate FE. Sex did not seem to have any influence on growth rate for our experimental conditions but showed influence on feeding rate, being higher in females. Some authors have observed that males reach higher body weight than females (Mangold, 1983; Forsythe and Van Heukelem, 1987) because females experience stronger metabolic changes during sexual maturing, stopping somatic growth (ODor and Wells, 1978) and decreasing their trophic activity (Mangold and von Boletzky, 1973). Before sexual maturation, females grew as much as males. The reasons for higher feeding rates in females with both diets are unclear. It may be due to higher energy requirements,

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hormonal changes, lower digestibility, etc. In any case, this observation must be ascertained and corroborated. Diet was demonstrated to have a clear influence on growth, food intake and FE. Better results were obtained in bogue-fed specimens than in sardine-fed ones. These differences may be related to lipid content more than protein content (Table 2). Differences in protein/energy ratio ( P/E) between both diets may also be important. Sardine-fed octopuses produced floating oily feces. ODor et al. (1984) suggested that lipid digestion in octopus was low and inefficient, probably due to the scarcity of emulsifier in its digestive tract. However, some cephalopods store significant quantities of lipid in the digestive gland, which are reduced during starvation. These same authors observed a drop in digestive gland lipid content after 6 days of starvation, from 0.3% body weight to 0.06% in O. vulgaris. In homeotherms, optimum P/E is between 10 and 15 (NRC, 1983; Halver, 1989). In fish and crustaceans, this ratio is higher, around 20 30 (Cowey et al., 1985). In cephalopods, P/E optimum value must be higher. In Sepia officinalis, optimum growth was achieved when P/E reached 50 (Lee, 1994). Our best results were obtained with feeding with bogue, of which P/E was 27.7, whereas with sardines, it was 15.02. The natural diet of O. vulgaris is composed mainly of crabs. The P/E value for crabs obtained from macronutrient composition data from ODor et al. (1984) is 35, so it is possible that P/E optimum for O. vulgaris was around it and thus higher than in fish. These high values might be explained by the predominance of amino acid metabolism for energy production (Lee, 1994). High quantities of protein obtained from a natural diet with low carbohydrates together with low lipid digestibility suggest that protein is the main energy source in O. vulgaris (ODor et al., 1984). Lee (1994) suggested that P/E might not be accurate in cephalopods to establish energetic requirements, and rather that a balance of amino acid levels provide those amino acids that were better in obtaining energy for routine metabolism (proline, aspartate and arginine) and essential amino acids for protein synthesis.

Acknowledgements This work has been financed by JACUMAR Spanish National Plans for Aquaculture nez for their help (1999). Authors wishes to thank Julia Pastor Bajo and Pilar Aguado Gime in the English translation.

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