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Felipe Briceño, Maite Mascaró, Carlos Rosas, Energy demand during exponential growth of Octopus maya: exploring the effect of age and weight, ICES Journal of Marine Science, Volume 67, Issue 7, October 2010, Pages 1501–1508, https://doi.org/10.1093/icesjms/fsq062
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Abstract
Recent work has reported changes associated with physiological, morphological, and behavioural adaptation during the absorption of yolk reserves. The holobenthic endemic species Octopus maya was used to explore the energy supply needed from the food intake (I; J animal−1 d−1) to supply the rate of production energy needed for body mass (P; J animal−1 d−1) and respiration rate (R; J animal−1 d−1) as a function of weight and age during the exponential early growth phase of the animal. Individually housed juveniles from hatching (1 d) to 105 d after hatching (DAH) were used, with the age and weight known, and the relationship between oxygen consumption (VO2; mg O2 animal−1 d−1) and weight (g) was established. Projections of I, R, and P as a function of age (Z) were made. The food intake destined to supply body mass production (%P/I) and respiration rate energy (%R/I) was analysed for an extended age range of 1–150 DAH. When O. maya juveniles hatched, they had a greater requirement for R than for P from the food intake, 61% (%R/I) and 13% (%P/I), respectively, suggesting high metabolic cost associated with post-hatching (during yolk absorption). Within the period where ZR > ZP (1–105 DAH), there was sufficient metabolic energy to satisfy the demands for sustaining exponential body mass production. The age at which %R/I = %P/I delimits the point where P cannot increase for reasons of metabolic constraint.Briceño, F., Mascaró, M., and Rosas, C. 2010. Energy demand during exponential growth of Octopus maya: exploring the effect of age and weight. – ICES Journal of Marine Science, 67: 1501–1508.
Introduction
The growth of an individual is the result of a series of energy transformations undergone by ingested food, and of the balance between the uses and destinations of the energy contained in that food (Lucas, 1993; Rosas et al., 2007). The manner in which this process is expressed over time (the growth curve) is a product of physiological and energy demands (O'Dor and Wells, 1987; Pauly, 1998) at differing levels of biological organization, i.e. body size, organs, tissue, and cells (Moltschaniwskyj, 2004).
Energy balance is estimated from the equation (Lucas, 1993) I = H + U + R + P, where I is the ingested energy, H and U the energy lost in faeces and products from protein metabolism, respectively, and R and P the energy invested in metabolic processes producing tissues and gametes (body mass), respectively. The difference between the energy from I and the loss in H and U is the assimilated energy (As) which, according to Lucas (1993), can be defined as I–(H + U) or as R + P, and it represents (Rosas et al., 2007) the amount of physiologically useful energy (PUE) available to maintain homeostasis (R) and growth (P).
Bioenergetic models for cephalopods are rare (Rosas et al., 2007; André et al., 2009a, b). Available research can be divided into two forms: (i) studies of ecological adaptation, such as those carried out on Octopus maya (Van Heukelem, 1976; Farías et al., 2009), Octopus vulgaris (O'Dor and Wells, 1987; Wells and Clarke, 1996; Katsanevakis et al., 2005a, b), Pareledone charcoti (Daly and Peck, 2000), Enteroctopus megalocyathus (Farías et al., 2009), Sepia apama (Grist and Jackson, 2004), Octopus pallidus (André et al., 2009a), and Octopus ocellatus (Segawa and Namoto, 2002; André et al., 2009a); and (ii) nutritional evaluation focusing on determining artificial diets for aquaculture (O. vulgaris: Petza et al., 2006; E. megalocyathus: Pérez et al., 2006; O. maya: Aguila et al., 2007; Rosas et al., 2007, 2008). Another aspect of these studies is that most have been limited to subadult and/or adult phases because of their relatively easy maintenance compared with earlier phases, particularly in species whose cycles begin with a planktonic stage (e.g. O. vulgaris). From studies carried out on species with benthic hatchlings such as O. maya, O. pallidus, and O. ocellatus, it has been possible to develop scaling models that describe the ratio between body size and food ingestion rate, metabolism, and ammonia excretion (Van Heukelem, 1976; Segawa and Hanlon, 1988; Segawa and Namoto, 2002; André et al., 2009a; Farías et al., 2009).
Some recent studies have used bioenergetic models to shed further light on the factors giving rise to the biphasic growth pattern characteristic of cephalopods (Forsythe and Van Heukelem, 1987; Semmens et al., 2004). Grist and Jackson (2004) formulated a bioenergetic model based on the principle of energy conservation, which theoretically suggests that the shift to a slower growth phase in S. apama may be associated with a body mass and age threshold at which the energy derived from food (I) can no longer satisfy the physiological demands associated with metabolism (R) and production of biomass (P), thereby producing an energy disequilibrium (I < R + P). It is suggested that such disequilibrium could bring a switch from a faster (exponential) to a slower growth phase, described as a power function by some authors (see Grist and Jackson, 2004), and which is more common among marine organisms in which the physiological demands of body mass production remain biologically possible (Grist and Jackson, 2004, 2007; André et al., 2009a). Age and body mass thresholds associated with the transition between the two growth phases under diverse temperature scenarios have also shown how variations in that parameter modulate the use and function of energy, allowing better understanding of the effect that it may have on the life cycle of cephalopods (André et al., 2009b).
Since the end of the 19th century, the use of the term physiological useful energy (PUE) has become more common, because it is known to be related to weight, mainly because the energy demand changes in synchrony with the body mass of an organism (Andrews et al., 1972; Storey and Storey, 1978; Clarke and Johnston, 1999; Gillooly et al., 2001, 2002; Clarke, 2004; Clarke and Fraser, 2004; Pörtner et al., 2005; Farías et al., 2009).
In a recent study, Moguel et al. (2010) characterized the post-hatching development of O. maya. Morphometric changes revealed that juveniles have a “non-growth phase” during the first 10 d after hatching (DAH). Histological analysis revealed that the digestive gland of octopuses changes with age, from a simple tubular gland 2 DAH, to a tubulo-acinar and vacuolar structure with digestive cells characterized by vacuoles 45 DAH. Digestive enzyme activity showed erratic activities until 14 DAH, but thereafter, it started to stabilize. Octopus maya 2 and 3 DAH rarely attacked or showed any response to visual or combined visual and chemical stimuli from a prey organism. In contrast, octopuses 4 DAH responded to visual stimuli from crabs and palaemonids, but they did not display a preference for attacking either prey type. Based on these results, we defined two phases within the early life history of O. maya: a post-hatching phase and a juvenile phase. The period 10–15 DAH was defined as the transition time for O. maya before animals reached the real juvenile stage. Moreover, in the immediate post-hatching period, octopuses showed clear lipid metabolism related to the uptake of yolk. That condition provides a greater opportunity to survive during the first days of life, when food might be limited, mainly when the arms of the animal are insufficiently developed. Evaluation of the rate of energy transferred to carry out basic functions and to growth as an age function could be useful in understanding the physiological adaptations of octopuses to satisfying the energy demands after hatching, during transition to the juvenile stage, and during the juvenile stage itself (Moguel et al., 2010). The exponential growth phase in O. maya has been modelled by a generalized linear mixed model (GLMM), using animals individually housed from hatching to 105 DAH, allowing a more accurate growth rate to be determined alongside greater precision in the predictions of octopus weight from known ages (Briceño et al., 2010). At the same time, other recent studies have increased the knowledge of O. maya physiology, with special attention paid to the relationship between size, ingested food, and oxygen consumption, within a wide range of weights (0.5–1350 g; Farías et al., 2009).
Given the information above, the current work focused on establishing the relationships between the energy supply from food (I) and the energy demands associated with body mass production (P) and respiration (R), using a partial energy model during the exponential growth phase of sibling juvenile O. maya individually housed from hatching date. Applying the model proposed, we estimated how energy demands change as a function of age and body mass during the fastest growth phase of the species, contributing new information on the physiology of early-stage cephalopods.
Material and methods
Food intake energy rate (I)
Body mass production to growth (P)
The energy invested in producing body mass (P) was estimated from the weight differences over the age ranges listed above (e.g. ΔW1–15 = W15 DAH−W1 DAH). The value 10.01 kJ g−1 dry weight was used to convert each ΔW into its energy equivalent (Rosas et al., 2007). It was determined for groups of 10 animals in a Parr© calorimeter pump.
Oxygen consumption and respiratory rate energy (R)
Oxygen consumption (VO2) was measured using a continuous flow respirometer comprising respirometric chambers connected to a recirculating system (Rosas et al., 2007). Juveniles were placed in 125 and 110 ml chambers, depending on size, with an approximate flow rate of 0.1 l min−1. All animals were acclimatized into the chambers for 6 h before measurements were made. Empty shells (Melongena corona bispinosa) and pieces of PVC tube were used as shelter. A chamber without an octopus (with a shelter) was used as a control. Measurements of dissolved oxygen (DO) were made for each chamber (inlet and outlet) every 15 s with oxygen sensors attached to flowcells that were connected by optical fibre to an Oxy 10 mini-amplifier (PreSens©, Germany). The sensors were calibrated at 27°C with saturated seawater (100% DO) and with a 5% sodium sulphate solution (0% DO). All measurements were taken at night from 18:00 to 09:00 local time, a period of quiet and little movement in the laboratory, to reduce stress of the experimental animals. Values of oxygen consumption obtained from 42 juvenile O. maya were used in estimating the body mass function.
We integrated our VO2 dataset within the Farías et al. (2009) oxygen consumption model for O. maya by weight to attain a more reliable metabolic coefficient during the exponential growth phase. The factor 14.3 J mg−1 was used to transform VO2 values into metabolic rate energy (R), expressed in J animal−1 d−1 (Lucas, 1993).
Partial energy balance
Energy values as a function of age
Results
DGR varied between 3.39 and 2.89%BW d−1 from 1 to 105 DAH, with an average of 2.23 ± 1.62%BW d−1. Maximum and minimum values were observed from 15 to 45 DAH and from 1 to 15 DAH, respectively (Table 1). A rate of survival close to 100% was observed until 45 DAH, decreasing subsequently to 28% at 105 d (Table 1).
Juvenile age range (d) and parameter . | Mean . | s.d. . | n . |
---|---|---|---|
1–15 DAH | |||
Weight (g) at 1 DAH | 0.11 | 0.02 | 53 |
Weight (g) at 15 DAH | 0.18 | 0.05 | 53 |
DGR (%BW d−1) (ΔW1–15) | 2.89 | 1.29 | 53 |
Survival (%) | 100 | ||
1–45 DAH/15–45 DAH | |||
Weight (g) at 45 DAH | 0.58 | 0.26 | 52 |
DGR (%BW d−1) (ΔW15–45) | 3.63 | 1.41 | 51 |
DGR (%BW d−1) (ΔW1–45) | 3.39 | 0.98 | 51 |
Survival 1–45 DAH (%) | 98.1 | ||
Survival 15–45 DAH (%) | 98.1 | ||
1–75 DAH/45–75 DAH | |||
Weight (g) at 75 DAH | 1.22 | 0.59 | 32 |
DGR (%BW d−1) (ΔW1–75) | 2.59 | 0.74 | 31 |
DGR (%BW d−1) (ΔW45–75) | 3.04 | 0.66 | 31 |
Survival 1–75 (%) | 60.4 | ||
Survival 45–75 (%) | 61.5 | ||
1–105 DAH/75–45 DAH | |||
Weight (g) at 105 DAH | 2.65 | 1.34 | 15 |
DGR (%BW d−1) (ΔW1–105) | 2.23 | 1.62 | 14 |
DGR (%BW d−1) (ΔW75–105) | 2.90 | 0.56 | 14 |
Survival 1–105 (%) | 28.3 | ||
Survival 75–105 (%) | 46.8 |
Juvenile age range (d) and parameter . | Mean . | s.d. . | n . |
---|---|---|---|
1–15 DAH | |||
Weight (g) at 1 DAH | 0.11 | 0.02 | 53 |
Weight (g) at 15 DAH | 0.18 | 0.05 | 53 |
DGR (%BW d−1) (ΔW1–15) | 2.89 | 1.29 | 53 |
Survival (%) | 100 | ||
1–45 DAH/15–45 DAH | |||
Weight (g) at 45 DAH | 0.58 | 0.26 | 52 |
DGR (%BW d−1) (ΔW15–45) | 3.63 | 1.41 | 51 |
DGR (%BW d−1) (ΔW1–45) | 3.39 | 0.98 | 51 |
Survival 1–45 DAH (%) | 98.1 | ||
Survival 15–45 DAH (%) | 98.1 | ||
1–75 DAH/45–75 DAH | |||
Weight (g) at 75 DAH | 1.22 | 0.59 | 32 |
DGR (%BW d−1) (ΔW1–75) | 2.59 | 0.74 | 31 |
DGR (%BW d−1) (ΔW45–75) | 3.04 | 0.66 | 31 |
Survival 1–75 (%) | 60.4 | ||
Survival 45–75 (%) | 61.5 | ||
1–105 DAH/75–45 DAH | |||
Weight (g) at 105 DAH | 2.65 | 1.34 | 15 |
DGR (%BW d−1) (ΔW1–105) | 2.23 | 1.62 | 14 |
DGR (%BW d−1) (ΔW75–105) | 2.90 | 0.56 | 14 |
Survival 1–105 (%) | 28.3 | ||
Survival 75–105 (%) | 46.8 |
Juvenile age range (d) and parameter . | Mean . | s.d. . | n . |
---|---|---|---|
1–15 DAH | |||
Weight (g) at 1 DAH | 0.11 | 0.02 | 53 |
Weight (g) at 15 DAH | 0.18 | 0.05 | 53 |
DGR (%BW d−1) (ΔW1–15) | 2.89 | 1.29 | 53 |
Survival (%) | 100 | ||
1–45 DAH/15–45 DAH | |||
Weight (g) at 45 DAH | 0.58 | 0.26 | 52 |
DGR (%BW d−1) (ΔW15–45) | 3.63 | 1.41 | 51 |
DGR (%BW d−1) (ΔW1–45) | 3.39 | 0.98 | 51 |
Survival 1–45 DAH (%) | 98.1 | ||
Survival 15–45 DAH (%) | 98.1 | ||
1–75 DAH/45–75 DAH | |||
Weight (g) at 75 DAH | 1.22 | 0.59 | 32 |
DGR (%BW d−1) (ΔW1–75) | 2.59 | 0.74 | 31 |
DGR (%BW d−1) (ΔW45–75) | 3.04 | 0.66 | 31 |
Survival 1–75 (%) | 60.4 | ||
Survival 45–75 (%) | 61.5 | ||
1–105 DAH/75–45 DAH | |||
Weight (g) at 105 DAH | 2.65 | 1.34 | 15 |
DGR (%BW d−1) (ΔW1–105) | 2.23 | 1.62 | 14 |
DGR (%BW d−1) (ΔW75–105) | 2.90 | 0.56 | 14 |
Survival 1–105 (%) | 28.3 | ||
Survival 75–105 (%) | 46.8 |
Juvenile age range (d) and parameter . | Mean . | s.d. . | n . |
---|---|---|---|
1–15 DAH | |||
Weight (g) at 1 DAH | 0.11 | 0.02 | 53 |
Weight (g) at 15 DAH | 0.18 | 0.05 | 53 |
DGR (%BW d−1) (ΔW1–15) | 2.89 | 1.29 | 53 |
Survival (%) | 100 | ||
1–45 DAH/15–45 DAH | |||
Weight (g) at 45 DAH | 0.58 | 0.26 | 52 |
DGR (%BW d−1) (ΔW15–45) | 3.63 | 1.41 | 51 |
DGR (%BW d−1) (ΔW1–45) | 3.39 | 0.98 | 51 |
Survival 1–45 DAH (%) | 98.1 | ||
Survival 15–45 DAH (%) | 98.1 | ||
1–75 DAH/45–75 DAH | |||
Weight (g) at 75 DAH | 1.22 | 0.59 | 32 |
DGR (%BW d−1) (ΔW1–75) | 2.59 | 0.74 | 31 |
DGR (%BW d−1) (ΔW45–75) | 3.04 | 0.66 | 31 |
Survival 1–75 (%) | 60.4 | ||
Survival 45–75 (%) | 61.5 | ||
1–105 DAH/75–45 DAH | |||
Weight (g) at 105 DAH | 2.65 | 1.34 | 15 |
DGR (%BW d−1) (ΔW1–105) | 2.23 | 1.62 | 14 |
DGR (%BW d−1) (ΔW75–105) | 2.90 | 0.56 | 14 |
Survival 1–105 (%) | 28.3 | ||
Survival 75–105 (%) | 46.8 |
Food intake rate energy (I)
Body mass production rate energy (P) and respiratory rate energy (R)
Equation . | Parameter . | Values ± s.e. . | p-value . |
---|---|---|---|
log P vs. log W | α | 2.29 ± 0.02 | t = 147.5*** |
β | 0.98 ± 0.03 | t = 31.7*** | |
σ | 0.153 | ||
AIC | −128.8 | ||
log R vs. log W | α | 2.63 ± 1.05 | t = 250* |
β | 0.64 ± 0.02 | t = 28.4*** | |
σ | 0.1995 | ||
AIC | −7.16 |
Equation . | Parameter . | Values ± s.e. . | p-value . |
---|---|---|---|
log P vs. log W | α | 2.29 ± 0.02 | t = 147.5*** |
β | 0.98 ± 0.03 | t = 31.7*** | |
σ | 0.153 | ||
AIC | −128.8 | ||
log R vs. log W | α | 2.63 ± 1.05 | t = 250* |
β | 0.64 ± 0.02 | t = 28.4*** | |
σ | 0.1995 | ||
AIC | −7.16 |
Corresponding values of Akaike information criterion (AIC) and σ are also shown.
*p < 0.05.
***p < 0.001.
Equation . | Parameter . | Values ± s.e. . | p-value . |
---|---|---|---|
log P vs. log W | α | 2.29 ± 0.02 | t = 147.5*** |
β | 0.98 ± 0.03 | t = 31.7*** | |
σ | 0.153 | ||
AIC | −128.8 | ||
log R vs. log W | α | 2.63 ± 1.05 | t = 250* |
β | 0.64 ± 0.02 | t = 28.4*** | |
σ | 0.1995 | ||
AIC | −7.16 |
Equation . | Parameter . | Values ± s.e. . | p-value . |
---|---|---|---|
log P vs. log W | α | 2.29 ± 0.02 | t = 147.5*** |
β | 0.98 ± 0.03 | t = 31.7*** | |
σ | 0.153 | ||
AIC | −128.8 | ||
log R vs. log W | α | 2.63 ± 1.05 | t = 250* |
β | 0.64 ± 0.02 | t = 28.4*** | |
σ | 0.1995 | ||
AIC | −7.16 |
Corresponding values of Akaike information criterion (AIC) and σ are also shown.
*p < 0.05.
***p < 0.001.
Partial energy balance
According to the model, the energy needed to produce an octopus of 2.66 g is 135 kJ, equivalent to 7.9 g of crab meat. An animal can reach such a weight 120 DAH. The conversion factor is therefore 3 (3 g of food for 1 g of octopus; Table 3).
. | Required food . | Body mass production . | . | ||
---|---|---|---|---|---|
Age (DAH) . | kJ . | Food (g) . | kJ . | Body mass (g) . | Food conversiona . |
0–15 | 3.17 | 0.19 | 0.45 | 0.04 | 4.18 |
16–30 | 4.62 | 0.27 | 0.70 | 0.07 | 3.92 |
31–60 | 16.59 | 0.98 | 2.78 | 0.28 | 3.55 |
61–90 | 35.34 | 2.08 | 6.72 | 0.66 | 3.13 |
91–120 | 75.27 | 4.43 | 16.22 | 1.61 | 2.76 |
Total | 134.99 | 7.94 | 26.87 | 2.66 | 2.99 |
. | Required food . | Body mass production . | . | ||
---|---|---|---|---|---|
Age (DAH) . | kJ . | Food (g) . | kJ . | Body mass (g) . | Food conversiona . |
0–15 | 3.17 | 0.19 | 0.45 | 0.04 | 4.18 |
16–30 | 4.62 | 0.27 | 0.70 | 0.07 | 3.92 |
31–60 | 16.59 | 0.98 | 2.78 | 0.28 | 3.55 |
61–90 | 35.34 | 2.08 | 6.72 | 0.66 | 3.13 |
91–120 | 75.27 | 4.43 | 16.22 | 1.61 | 2.76 |
Total | 134.99 | 7.94 | 26.87 | 2.66 | 2.99 |
aFood (g) required to produce 1 g of body mass.
. | Required food . | Body mass production . | . | ||
---|---|---|---|---|---|
Age (DAH) . | kJ . | Food (g) . | kJ . | Body mass (g) . | Food conversiona . |
0–15 | 3.17 | 0.19 | 0.45 | 0.04 | 4.18 |
16–30 | 4.62 | 0.27 | 0.70 | 0.07 | 3.92 |
31–60 | 16.59 | 0.98 | 2.78 | 0.28 | 3.55 |
61–90 | 35.34 | 2.08 | 6.72 | 0.66 | 3.13 |
91–120 | 75.27 | 4.43 | 16.22 | 1.61 | 2.76 |
Total | 134.99 | 7.94 | 26.87 | 2.66 | 2.99 |
. | Required food . | Body mass production . | . | ||
---|---|---|---|---|---|
Age (DAH) . | kJ . | Food (g) . | kJ . | Body mass (g) . | Food conversiona . |
0–15 | 3.17 | 0.19 | 0.45 | 0.04 | 4.18 |
16–30 | 4.62 | 0.27 | 0.70 | 0.07 | 3.92 |
31–60 | 16.59 | 0.98 | 2.78 | 0.28 | 3.55 |
61–90 | 35.34 | 2.08 | 6.72 | 0.66 | 3.13 |
91–120 | 75.27 | 4.43 | 16.22 | 1.61 | 2.76 |
Total | 134.99 | 7.94 | 26.87 | 2.66 | 2.99 |
aFood (g) required to produce 1 g of body mass.
Discussion
The food intake rate (I) and respiratory rate (R) energy modelled here for O. maya during its exponential growth phase revealed a means of diverting ingested energy to body mass production (P). The results showed that, besides the transition between embryonic and juvenile stages reported for O. maya by Moguel et al. (2010), juveniles pass through metabolic changes that constrain the way they can grow. Between 1 and 100 DAH, juveniles invest more energy in respiration (%R/I) than in body mass production (%P/I), showing that the costs associated with nutrient movement and tissue synthesis during morphological, physiological, and behavioural changes at such stages are greater than body mass production (Wells and Clarke, 1996). Taking this into account, the extension of the initial growth phase observed in species with benthic hatchlings, such as O. pallidus and O. maya, may be explained by the high metabolic requirements at the beginning of the life cycle (Leporati et al., 2007; Briceño et al., 2010; Moguel et al., 2010). Several explanations are possible for these metabolic constraints: (i) culture conditions can stunt growth through the increment on metabolic rate for instance as a stress response by animals housed individually, resulting in a slower growth rate than expected for cephalopods during fastest growth phase; (ii) the nutritional property of the food provided under culture conditions is not sufficient to satisfy the requirements for high rates of body mass production; (iii) the efficiency of octopuses in transforming energy into biomass after hatching is poor; (iv) artificially maintaining octopuses in isolation included some animals that, in open tanks or in nature, are not part of the population, except through their role as food via cannibalism (Ibañez and Keyl, 2010). In the last case, cannibalism provides an extra bonus of energy to a population that can be transformed into body mass and reflected in a faster growth rate than observed when animals are isolated.
The integration of our VO2 dataset within the VO2 model of Farías et al. (2009) at 27°C presented here allows us to obtain more accurate oxygen consumption estimates for O. maya over an extended weight range (82 animals measured under the same experimental conditions). A new constant and new power exponent (metabolic exponent) have been calculated as α = 1.25 and β = 0.64, rather than αf = 0.93 and βf = 0.69, respectively (see Farías et al., 2009). The metabolic exponent obtained (β = 0.64) was lower than reported by Segawa and Hanlon (1988) for O. maya (β = 0.9), but similar to the values reported for other species of octopus: O. vulgaris (0.70–0.95; Cerezo-Valverde and García-García, 2004; Katsanevakis et al., 2005a, b); O. ocellatus (0.78–0.84; Segawa and Namoto, 2002); and E. megalocyathus (0.69; Farías et al., 2009). These results suggest that the relationship between size and metabolic rate in octopuses, such as in some fish species and aquatic invertebrates (Clarke and Johnston, 1999), is close to an exponent ∼0.75 proposed as a generalized value under the power law (3/4; Gillooly et al., 2001). On the other hand, Wells and Clarke (1996) stated that cephalopods use between 60 and 80% of assimilated energy for body mass production, and that the balance (20–40%) is lost in thermodynamic costs associated with the movement of nutrients and tissue synthesis. Unfortunately, those values were obtained from late juveniles or subadults of several octopus species without taking into account possible changes in the metabolic rate associated with age (Cerezo-Valverde and García-García, 2004; Katsanevakis et al., 2005a, b). The results obtained here reveal that the proportion of ingested energy available for body mass production and metabolism changes with age. When O. maya hatched (1 DAH), R consumed 61% of the ingested energy and P 13%, suggesting that, at that point, the efficiency with which an octopus transforms energy to body mass is poor. That condition is inverted with age, according to the models, and during maturation, there are metabolic changes.
Recent studies carried out on O. maya and other species (Vidal et al., 2002) demonstrated that octopuses and cephalopods in general pass through a transitional post-embryonic stage in which the digestive processes and the use of nutrients are rather inefficient. Those authors reported zero growth in Loligo opalescens during the first few days of life, a period when the animals change from endogenous to exogenous food, once the yolk has been absorbed. That period has been identified as critical in squid, because survival can be severely compromised by an energy disequilibrium arising from the high metabolic demand attributable to hatching and the exponential absorption of yolk. Depending on the temperature, this period may last from 10 to 15 d in L. opalescens, and it has been recognized as a time at which most of the energy content of the yolk is lost through respiration (Vidal et al., 2002). In our study, O. maya hatched with a yolk reserve that was absorbed rapidly over the first 10 DAH (Moguel et al., 2010), when the digestive gland of the octopus passes through a maturation stage similar to that reported for Sepia officinalis (Yim and Boucaud-Camou, 1980; Nixon and Mangold, 1998). This stage is accompanied by changes in the activity of digestive enzymes during the multiplication phases (0–8 DAH) and cellular maturation (10–20 DAH). Changes in the proportion of arm length relative to total length were also observed, suggesting that, besides digestive maturation, octopuses also complete their development and acquire the morphology characteristic of their juvenile phase (20 DAH; Moguel et al., 2010). Taking into account the period of yolk absorption reported for cephalopods and digestive and morphological changes, we suggest that the high metabolic rate observed during the first days of life is a reflection of the low efficiency of these organisms during the early transitional period between post-embryonic life and the juvenile phase. Segawa and Hanlon (1988) demonstrated great variability in VO2 values at 18 DAH (0.17–0.19 g), an age at which they suggested that individuals undergo certain changes associated with lipid metabolism during yolk absorption. Such low efficiency seems to be common among cephalopods. The no-net-growth period after hatching to 15 DAH is followed by an exponential growth phase, in which a rapid transformation of ingested energy into biomass takes place. In L. opalescens, this process begins when squid feed for the first time and compensate for the low efficiency associated with yolk absorption. For O. maya, Moguel et al. (2010) stated that exponential growth begins between 10 and 15 DAH, when prey selection has started. Moreover, recent histological studies carried out by López-Ripoll (2009) on O. maya during the first days of life showed that juveniles 15 DAH had completely developed digestive gland cells in which the nutrients and food are transported to the blood.
In this study, either P or R was modelled as a power function of age (ZR or ZP), with differences in the way that energy usage is scaled (β2 > β3). This suggests that during exponential growth, the energy demand for body mass production is greater than for respiration, at least from 1 to 149 DAH. These differences in values of β suggest a disequilibrium between the supply (β1) and uptake of energy (β2), which should not extend beyond the limits imposed by thermodynamic laws (Wells and Clarke, 1996). The results obtained show that within the period when ZR > ZP (between 1 and 149 DAH), there would be sufficient metabolic energy to satisfy the demands to sustain body mass growing exponentially, which would reach a limit once %R/I = %P/I. The age at which %R/I = %P/I is when the body mass production demand cannot increase faster than that of metabolic energy, and it could be associated with a transition between exponential and slower growth phases, as suggested by Grist and Jackson (2004) and André et al. (2009a) for other cephalopod species. Briceño et al. (2010) provided an exponential growth model based on a GLMM using animals from 1 to 105 DAH, from known-age juveniles taken on hatching. No weight data have been published under the same experimental design proposed by those authors (initial size categories) for O. maya between 105 and 165 DAH, showing that a decreased growth rate could be a consequence of growth deceleration associated with a second growth phase (Semmens et al., 2004). That supports the notion that as a consequence of the disequilibrium resulting from maintaining exponential growth, octopuses >150 DAH reduce their growth rate simply because they cannot obtain an adequate energy supply.
Using data from partial energy models, we have calculated the energy required for body mass production in different age ranges of O. maya. From these models, body mass (g) and food quantity can be estimated to support culture (Rosas et al., 2009; Table 3). For example, the quantity of food necessary to attain a body mass of 2.66 g is 7.94 g (for crab meat). Therefore, a conversion factor close to 3 and a ratio of one-third of ingested energy would be needed to attain this body mass. These values were similar to those reported by Mangold (1983) for Eledone moschata (18–70%), Eledone cirrhosa (37%), Octopus cyanea and O. maya (40%), Octopus joubini (40%), and Octopus tetricus (47%).
Our results represent a contribution to better understanding the way in which octopuses exchange and transform energy during their fast growth phase. As age is the factor that constrains the differences in efficiency of food assimilation, perhaps management techniques accounting for these differences will facilitate optimal weight gain and growth of O. maya under culture conditions. Allowing cannibalism as a strategy to improve the growth rate of culture populations could be valuable in future, but more work is needed first. The asymmetry in size between cannibalizing animals and their victims needs to be explored by searching for the “cannibalistic window” through an intra- and inter-cohort approach, and evaluating its consequences in cultured and wild populations (Ibañez and Keyl, 2010). Such studies could alter the growth models developed with animals in isolation that could not take into account the energy value of a victim to the growth of the cannibal. The incorporation of temperature in future studies would also allow exploration of how the metabolic processes associated with respiration can be altered by varying the environmental conditions. Further analyses integrating other factors, such as sex, the metabolic cost associated with transportation, and prey selection, will be needed to contribute to an even better understanding of the physiological demands of O. maya, to continue gathering information required to determine the source of the great variability in growth of cephalopods.
Acknowledgements
The study was partially funded by grants SEP-CONACYT-24743 and PAPIIT-UNAM IN202909-3 provided to CR. FB thanks the Organization of American States for a scholarship to carry out MSc studies at the Postgraduate Programme of Marine Sciences and Limnology, National Autonomous University of México. We thank Jessica André for her suggestions and comments during the drafting process, and Gretta Pecl for valued comments on the submitted draft. Both these last are from the Tasmanian Aquaculture Fisheries Institute, Australia.