What drives seasonal fluctuations of body condition in a semelparous income breeder octopus?

Acta Oecologica 37 (2011) 476e483

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Original article

What drives seasonal fluctuations of body condition in a semelparous income breeder octopus? Antoni Quetglas*, Francesc Ordines, Maria Valls Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent, s/n, Apdo. 291, 07015 Palma, Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 8 November 2010 Accepted 2 June 2011 Available online 25 June 2011

The vast majority of modern cephalopods is single-season breeders, or semelparous in the strict sense, that die soon after the reproduction takes place. Individual body condition in these marine invertebrates is expected to be highly affected by reproduction because: 1) the gonad weight of females, which represents <1% of body weight when immature, increases up to 20e50% during maturation; and 2) octopus females reduce or even cease their food intake during breeding. Based on this expectation, we analysed the interrelationship between condition and reproduction in the temperate octopus Eledone cirrhosa. Results from a previous work using biochemical analyses showed that reproduction in this species is not fuelled by stored reserves (capital breeder), but by food intakes (income breeder). Since income breeders depend strongly on food resources, the effect of several environmental variables related to food availability such as primary production, sea temperature (ST) and river discharges were also analysed. Condition showed a marked intrannual cycle independently of the sex and, noteworthy, the maturity stage. Given that immature individuals are not expected to display seasonal fluctuations in body condition related to maturation, these results preclude reproduction as a driving factor for the observed circannual cycle. Condition was significantly correlated with all the environmental variables analysed, except with ST at the depths where the species lives. Although this last result also precludes concurrent ST as a driving factor of body condition, those correlations suggest that condition might display an intrinsic seasonal cycle, as many other life-history traits in most species such as reproduction, migration or moulting. Finally, there also remains the possibility that condition in this octopus species is determined genetically, as has been reported in recent studies across different taxonomical groups. Ó 2011 Elsevier Masson SAS. All rights reserved.

Keywords: Life-history trade-off Body mass residuals Circannual rhythm Cephalopod

1. Introduction Body condition, as a measure of an individual fitness, plays a key role in the performance of different life-history traits in a wide range of animals, both ectotherms and endotherms (e.g. Green, 2001; Kubicka and Kratochvil, 2009). Most currently available studies focus on the relationships between condition and reproduction or survival related characteristics such as body size, breeding success or storage formation. Given the high interconnection among all these processes, animals have to optimize the limited energy inputs from food for both the maintenance of somatic structures and the reproduction investments (Roff, 2002). Depending on the energy sources used, organisms are classified as those that rely on accumulated energy stores (capital breeders)

* Corresponding author. Fax: þ34 971404945. E-mail address: [email protected] (A. Quetglas). 1146-609X/$ e see front matter Ó 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2011.06.002

or those using current energetic incomes (income breeders). Condition has traditionally been considered to reflect an individual’s nutritional, non-genetic state, and hence to show variations driven by phenotypic related characteristics such as changes in food availability (Chan-McLeod et al., 1999) or reproduction costs (White et al., 1997). However, recent studies reporting evidences for genetic variance in condition have increased steadily (Rowe and Houle, 1996; Kotiaho et al., 2001; Blanckenhorn and Hosken, 2003; Tomkins et al., 2004). Reproduction constitutes a key seasonal period of increased energy demand for the adult individuals of most species, but not for immature animals which are not expected to exhibit seasonal body condition trends associated with reproduction (Ryg et al., 1990; Beck et al., 2003). In general, the reproductive costs show sexspecific patterns given the high differences in energy investments between males and females. Whereas costs to males are generally associated almost exclusively with the mating bounds, females must also face with the additional costs of offspring gestation

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and breeding (Ryg et al., 1990; Beck et al., 2003). In many species, the interdependence between reproduction and condition is so close-knit that the latter can determine both the occurrence and intensity of the reproductive events (e.g. Vleck and Vleck, 2002; Blanchard et al., 2005). Consequently, it is expected that those species investing great amounts of energy in reproductive structures will show a noticeable reduction in body condition, either because of trade-offs between somatic and gonad tissues or the reallocation of energy, that was previously directed to somatic growth, towards gonad enlargement. Cephalopods represent a typical example of organisms making great investments in gonad development, especially the females. With the exception of nautiluses, the vast majority of known modern cephalopods is believed to be single-season breeders, or semelparous in the strict sense, that die soon after the reproduction takes place (Boyle and Rodhouse, 2005). Growth and maturation are very fast and, whereas somatic growth exceeds gonad growth during early life, gamete development dominates tissue production in later stages (Semmens et al., 2004). Although gonad weight in males rarely exceeds 5% of body weight, the reproductive system of females, which represents less than 1% of body weight when immature, increases dramatically to 20e30% (and even as high as 50%) over a short period of time just before spawning (Forsythe and Van Heukelem, 1987). Furthermore, in most octopus species mature females migrate to rocky substrates to lay and take care of the eggs and, once in the rocky shelter, they reduce considerably or even cease their food intake to the point that they die soon after the eggs hatching (Boyle and Rodhouse, 2005). As a consequence of this large energy expenditure in reproduction, mantle tissues suffer important changes in their composition and structure that implies a concomitant loss of somatic condition, such as a general trend of increased water concentration and decreased protein content (Jackson et al., 2004). Therefore, cephalopods are in principle especially suitable case studies for analysing trade-offs between individual condition and reproductive processes. In this study we analysed the interrelationships between individual body condition and both reproductive investments and environmental variables in a wild population of the horned octopus Eledone cirrhosa, a small-sized (<2 kg) cephalopod widely distributed in the northeast Atlantic and the Mediterranean Sea (Boyle and Rodhouse, 2005). Biochemical analyses have already demonstrated that spermatogenesis and oogenesis in this temperate octopus and other sympatric species do not rely on storage reserves, but on energy inputs directly from food intake characteristic of income breeders (Rosa et al., 2004a,b). These results, however, do not preclude energy reallocations of food incomes from somatic towards gonad growth. Assuming a concomitant loss of body condition during reproduction, we expected that condition and gonad weight would exhibit an inverse seasonal pattern, which should be more pronounced in females than in males owing to the strong sex-differences in reproduction investments. If we also assume that condition is mainly driven by the high investments on gonad growth characteristics of mature individuals, especially females, we also predicted that immature octopuses should not display intrannual variations of somatic condition related to maturation. However, in case octopuses exhibited fluctuations not related to reproduction, we expected that such variations should be related to environmental fluctuations given the dependence of individual fitness on food availability, especially in income breeders. As aforementioned, breeding females octopus reduce or even stop eating, which implies that their condition during this spell is obviously very poor. Consequently, we have centred our investigations on the maturation processes prior to this period, the life stage spanning from juveniles to fully mature individuals, when the investment in gonad development is highest and important reallocations of food intakes are expected.

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2. Materials and methods 2.1. Sampling Monthly random samples of the octopus E. cirrhosa were obtained from the port of Tarragona (41.12 N, 01.25 E), situated on the northern Mediterranean coast of the Iberian Peninsula, between February 2004 and January 2006. In this study area, the E. cirrhosa fishery takes place mainly between 100 and 200 m depth in areas near the Ebro River mouth, one of the most important rivers in the western Mediterranean with a total length of 910 km and a catchment basin of about 85,400 km2 (http://www.chebro.es/ ). A total of 3144 individuals (1659 females, 1485 males) was analysed in the laboratory, where the following measurements were taken: mantle length (ML, to the nearest 0.5 cm), total weight (TW, to the nearest 0.1 g), eviscerated weight (EW, to the nearest 0.1 g), gonad weight (GW, to the nearest 0.01 g), sex and maturity stage (according to the three-stage maturity scale described in Quetglas et al., 2009). In a sample of individuals (N ¼ 483) caught at the four seasons of the year, the stomach weight (SW) and the digestive gland weight (DGW) were also taken (both to the nearest 0.01 g). Octopus size ranges were 3.0e15.5 cm ML in females and 3.0e14.5 cm ML in males. 2.2. Condition vs reproduction To investigate individual body condition and the relationships between somatic and reproductive investment, regression equations were calculated for log-transformed ML-EW and ML-GW using the reduced major axis regression (RMA; Bohonak and van der Linde, 2004). RMA is more appropriate than standard ordinary least squares (OLS) regression when the independent variable is measured with error (Bohonak and van der Linde, 2004), because in such a case the estimates of slopes using OLS regression methods are biased (Sokal and Rohlf, 1995). Subsequently, residuals were obtained and standardized by dividing each by the deviation of the predicted values. Whereas ratio indices of condition (one measure of size divided by a second measure of size) are size-dependent, residual indices (the difference between an observed measure of size and that predicted by a regression equation) are sizeindependent (Hayes and Shonkwiler, 2001). By regressing eviscerated body weight and gonad weight against size, the residual value of each individual provides a size-independent measure for comparing the relative condition of somatic and gonad tissues, considering that individuals with heavier tissues for their length (higher residuals) have tissues in better condition. Hence, ML-EW and ML-GW residuals were used as indicators of somatic condition (SC) and reproductive condition (RC) respectively (see Supplementary material Appendix 1). To analyse if SC was related to reproduction, we first determined the reproductive period of the species following the monthly evolution of the gonadosomatic index (GSI ¼ 100$GW/EW) by means of generalized additive models (GAMs). The response variable GSI was modelled using month and size as explanatory variables for females and males separately given the aforementioned important sex-related differences in gonad investment. Once the monthly evolution of the GSI was determined, we did the same with the SC in order to analyse the relationship between both parameters throughout the year. GAMs were also used for this purpose, modelling the response variable SC with the explanatory variables month, size and RC. In this case, we analysed the immature individuals separately from those that had begun the maturation processes (maturing and mature individuals combined, which are referred to as mature henceforth) to investigate whether both groups displayed different trends in SC related to

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reproduction. The RC was included in the GAM to infer trade-offs between somatic and gonad tissues from the relationship between SC and RC, which would allow us to determine if our results using residuals agree with biochemical analyses (Rosa et al., 2004b). All GAM analyses were carried out with the R package (version 2.5.1; http://www.r-project.org/) using the mgcv library. See Supplementary material Appendix 2 for further details on the GAM analyses. In order to determine whether the octopus food intake displayed any intrannual trend which could be related with the individual body condition, the following three feeding-related indices were calculated by sex and season: 1) fullness weight index (FWI ¼ 100$SW/EW); 2) emptiness index, which is the percentage of empty stomachs; and 3) digestive gland index (DGI ¼ 100$DGW/ EW). Digestive gland in cephalopods is involved in the excretion of dietary lipids, whereby DGI constitutes an indicator of the individual metabolic activity (Semmens, 1998).

production, was taken from the NASA web page (http://reason.gsfc. nasa.gov/Giovanni). Mean monthly sea temperature (ST) at different depths (0, 50, 75 and 100 m) was available from scientific surveys carried out by the Instituto Español de Oceanografía and kindly furnished by Dr M.L. Fernández de Puelles (RAD-BAL project). Lloret et al. (2001) showed that the abundance of E. cirrhosa and other demersal resources from our study area were significantly positively affected by the inflows of the Ebro River. Consequently, the monthly Ebro river flow (RF, in m3 s1), which was obtained from the Ebro’s Hydrological Confederation web page (http://www.chebro.es/), was also analysed. The Pearson correlation coefficient between SC and each one of these environmental variables was calculated with STATISTICA version 6.0 by means of a non-linear estimation using the LevenbergeMarquardt estimation method.

2.3. Condition vs environmental parameters

The GSI showed a clear seasonal trend in both sexes, although their corresponding maximums and minimums were slightly displaced in time (Fig. 1). While values of males were highest between December and March and lowest between July and September, females showed a peak during February and May and a minimum during September and November. The GSI increased steadily with size in females, reflecting the gradual increase in both egg number and size during the maturation phase. The GSI also increased in males, yet at a higher rate than females, up to about 10 cm ML but decreased in larger individuals. Such a decrease might be due to the release of spermatophores during mating in mature males.

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3. Results

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The SC followed a common intrannual trend independently of the sex and, noteworthy, the maturity stage (Fig. 2). In all cases, SC values were lowest during February and May but increased thereafter up to a marked peak between August and September. Although this intrannual trend was inverse to the GSI trend, RC increased with increasing SC in both sexes and both maturity stages. Contrary to all other variables, which showed a common trend in both sexes, the SC displayed an inverse pattern between sexes and maturity stages. Mean FWI did not show important intrannual variations (Fig. 3), especially in males which values ranged between 0.80 and 0.85. Females had higher FWI than males throughout the year, being the highest value in spring (1.12%) and the lowest value in winter (0.85%). The percentage of empty stomachs was always lower in females than in males, especially during spring and summer when EMI was near 40% in females but up to 70% in males. Mean DGI of females were slightly higher in spring and summer (w5.7%) than in autumn and winter (w5.0%). Although the DGI of males was markedly lower than that of females during spring and summer (3.5e4.0%), the values were similar to those of females during autumn and winter. The existence of a common general intrannual pattern of SC in both immature and mature octopuses suggests that condition might be driven by parameters other than reproduction such as environmental variables. In fact, condition of the whole octopus population (both sexes combined) showed highly significant correlations with all the local environmental variables analysed (Fig. 4). Both Chla and RF were negatively correlated with condition, being the peaks of these two parameters and the peak in condition separated by lag times of 4e6 months. In contrast, ST at 0, 50 and 75 m depth displayed a marked positive correlation with condition; however, the relationship was not significant at 100 m depth. 4. Discussion Body condition plays a pivotal role in the performance of different life-history traits, especially the maturation and reproduction processes (e.g. Green, 2001; Kubicka and Kratochvil, 2009). As a matter of fact, the success of reproduction can even depend on the individual fitness in some species (e.g. Vleck and Vleck, 2002; Blanchard et al., 2005). In those organisms relying on current energetic incomes (income breeders), body condition greatly depends on the availability of contemporary food resources, which are invariably related to environmental factors. In order to determine the interdependence between condition and reproduction, we analysed in this paper the relationships between individual condition and both reproductive investments and environmental variables in the semelparous, income breeder octopus E. cirrhosa. Although the existence (absence) of trade-offs between two lifehistory traits is often tested by searching for the negative (positive) correlation between measures of these traits, this is not always conclusive (Roff, 2002; Kubicka and Kratochvil, 2009). Indeed, we found that SC and GSI exhibited an inverse intrannual trend, together with a highly positive correlation between SC and RC both in immature and mature individuals of males and females. These apparently contradictory results could be explained if we think on the reallocation of resources from food intake rather than on energy trade-offs between tissues (See Supplementary Material Appendix 3). In such a case, the decrease of SC during the reproduction period could be explained if the inputs from food intake in mature octopuses were progressively rechanneled from somatic to gonad growth. In immature individuals, the energy from food intake invested to somatic growth would exceed gonad growth. However, during sexual maturation the investment on gonad tissues would be greater than in somatic tissues. This would explain

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the positive relationship between SC and RC, since both parameters always increase jointly, but also the decrease of SC during the reproduction period, because the amount inverted to SC decreases as maturation progresses. In this sense, our results using residuals would agree with the biochemical analyses performed by Rosa et al. (2004b), who analysed the effect of spermatogenesis and oogenesis on protein, lipid, glycogen, cholesterol and energy contents, total amino acid and fatty acid profiles on different tissues (gonad, digestive gland and muscle) of E. cirrhosa and Eledone moschata. Rosa et al. (2004b) concluded that there was no evidence of reserve transfers among the organs analysed, and hence their composition was not influenced by sexual maturation, but instead by other biotic factors such as feeding activity. The inverse behaviour between sexes in the evolution of SC with size suggests the aforementioned sex-specific patterns of reproductive costs in many species (see Introduction), from which cephalopods are a clear example. The sharp decrease of SC with size in mature females agrees with the reallocation of food intakes from somatic to gonad growth during reproduction to cope with the large investments on ovary development. The positive relationship found in mature males, by contrast, indicates that their energy inputs from diet allow concomitant increases of somatic and testis tissues given the lower energy requirements for gonad production compared with females. Fittingly, our results from feeding indices tally with this need of higher metabolic rates in females than males, especially during the reproduction period (spring). During spring, females had the highest FWI and DGI values together with the lowest EMI; by contrast, during spring and summer males displayed lower DGI and higher EMI compared with the rest of the year. This pattern of higher metabolic rates in females than males, especially during reproduction, seems to be general among Mediterranean octopuses (e.g. Quetglas et al., 2009, and references therein), and adds support to similar results from other taxonomic groups indicating that these sex-differences may be rather common among taxa (Chicharo et al., 2007; Wilder et al., 2010). Contrary to our predictions, immature octopuses exhibited the same intrannual pattern in body condition as mature individuals, which indicate that the seasonal variations of condition were not governed by reproduction. This leads on to consider alternative hypotheses such as the environment or genetics as factors determining body condition. We first investigated the effects of seasonal environmental factors, since it is frequently assumed that condition is determined primarily by an individual’s nutritional state, and hence it should track circannual fluctuations in food resources availability (Tomkins et al., 2004; Ketola and Kotiaho, 2009). Furthermore, individual fitness in income breeders is expected to be largely dependent on the habitat quality and therefore to respond promptly to changes in food availability (Elkin and Reid, 2005). Fittingly, octopus condition was highly correlated with the three environmental variables analysed (Chla, RF and ST), with the only exception of ST at depths greater than 75 m. Although with our results we have no means to determine if such correlations are functional or spurious, relationships between body condition and environmental parameters have been reported in other works (Bradshaw et al., 2000; Lourdais et al., 2002). It is well known that productivity (Chla) and temperature are directly or indirectly related with food availability or food consumption rates in most animals, including octopuses (Dahlhoff et al., 2002; André et al., 2008; Otero et al., 2009). As we have already mentioned (see Material and methods), the positive effect of river discharges on the abundance of E. cirrhosa and other marine resources in our study area is also known (Lloret et al., 2001); the effect, however, was displaced by time lags of 2e6 and 6e10 months in juveniles and adult octopuses respectively. According to Lloret et al. (2001), such lags might indicate the time required for

Fig. 2. Evolution of somatic condition with respect to month, size (ML, mantle length) and reproductive condition (RC) in immature and mature females (above) and males (below) of the octopus Eledone cirrhosa modelled using generalized additive models.

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Fig. 3. Evolution of different feeding indices (mean  S.E.) by season and sex (males: solid line; females: dotted line) in the octopus Eledone cirrhosa: fullness weight index (FWI), emptiness index (EMI) and digestive gland index (DGI).

incorporation of nutrients into the food chain and for growth of the larvae to fishery recruitment sizes. This would also apply to the time lags we found between condition and both Chla and RF (4e6 months), and our results would indicate that these environmental variables, aside from enhancing the abundance of octopus populations reported by Lloret et al. (2001), would also enhance the individual fitness as it is expected to occur in income breeders. Further evidence of delayed responses in cephalopods comes from the Patagonian squid, which seasonal variations in average size usually lag 6 months behind similar seasonal variations of ST (Grist and des Clers, 1999). The effect of ST deserves to be treated separately from Chla and RF because seasonality of ST depends on the depth considered. The statistical significance of correlations between octopus condition and ST decreased with increasing depth and became uncorrelated at 100 m depth, where ST remains approximately constant at 13  C. Consequently, in spite of the marked effect of temperature on condition related traits in living organisms in general (e.g. Gillooly et al., 2001) and particularly cephalopods (e.g. Andre et al., 2009), it should be rejected as a factor determining condition in our study area because E. cirrhosa inhabits preferentially on the 100e200 m depth stratum and its abundance out of this stratum is negligible. Nevertheless, the effect of ST might be relevant in shallow water

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Fig. 4. Relationships between somatic condition (SC, in grey) and several environmental parameters in the octopus Eledone cirrhosa: chlorophyll-a concentration (Chla), river flow (RF) and sea temperature (ST). The RF corresponds to the Ebro River, one of the most important rivers from the western Mediterranean (http://www.chebro.es/); ST was taken at different depths (0, 50, 75 and 100 m).

cephalopods, since it was demonstrated that temperature acts to synchronize other life-history traits in seasonal habitats, such as reproduction in the Pacific pygmy octopus (Voight, 1992) or growth rates in the Patagonian squid (Grist and des Clers, 1999). Even though temperature is rejected as a zeitgeber for the observed strong intrannual variation in octopus condition, such seasonality, which is coincident with different major seasonal ecological parameters, leads us to consider the possibility that it constitutes a circannual endogenous cycle. Circannual rhythms, in phase with the seasons, are commonplace in nature and are manifest in various aspects of animal behaviour and physiology (Oster et al., 2002; Zucker, 2010). Circadian and circannual clocks are even present in many organisms living in constant environments (e.g. Trajano and MennaBarreto, 1996, in cave-dwelling fishes; Koilraj et al., 2000, in millipedes), which suggests that these clocks may have some intrinsic adaptive value such as the coordination of metabolic processes (Sharma, 2003). In case ST has an effect on the seasonal fluctuations of body condition in E. cirrhosa, this might be a reminiscence of its earliest life stage, since most octopus species have a brief planktonic phase on superficial waters during which they show positive phototaxis, before settlement on the bottom where

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they display negative phototaxis and reclusive behaviour (Villanueva and Norman, 2008). There is also the possibility of synchronization for the time of hatching occurring when environmental conditions, such as food availability, are optimal for offspring growth as has been reported in many cases (Durant et al., 2007; van Asch et al., 2010). Considering that the spawning peak occurs in AprileMay (a month after the peak of GSI) and that the embryonic life lasts about 4 months (Mangold et al., 1971), hatching would take place during AugusteSeptember. These are precisely the months when condition of both immature and mature octopuses is highest, which indicate that this is the best period of the year for the individual fitness. Biological clocks have a genetic basis and several genes involved in clock mechanisms have now been identified (Oster, 2006; Nolan and Parsons, 2009). This leads on to consider finally the hypothesis that seasonal fluctuations in octopus condition might be determined genetically. In fact, a significant additive genetic component of variance in body condition has been reported during the last years in different organisms, both invertebrates (Kotiaho et al., 2001; Blanckenhorn and Hosken, 2003) and vertebrates (Svensson et al., 2002; Gienapp and Merila, 2010). Such results agree with the genic capture hypothesis (Rowe and Houle, 1996), which attempts to explain the maintenance of genetic variation in sexually selected traits by assuming that these are condition-dependent and that many loci contribute to condition, sustaining high genetic variation for condition (Tomkins et al., 2004). The analyses performed in our work were based on the nondestructive method of residuals, calculated by means of the reduced major axis (RMA) regression. The use of residuals to estimate condition constitutes an endless controversial issue in the ecological literature even nowadays. In many cases, the conclusions are contradictory because whereas ones state that residuals are often likely to be more reliable when calculated with alternative methods to ordinary least squares (OLS) such as RMA (Green, 2001; Peig and Green, 2009), others found that OLS is better than RMA (Schulte-Hostedde et al., 2005; Ardia, 2005). Anyway, this reminds us that no method is ideal (Peig and Green, 2009) and the necessity of validating condition indices with mass-independent physiological measures of condition such as liver glycogen or blood glucose (Schulte-Hostedde et al., 2005). As aforementioned, we counted in our case with the results of a previous study (Rosa et al., 2004b) analysing these mass-independent measures for comparison and validation with ours. Both biochemical (Rosa et al., 2004b) and residual (this study) analyses agreed in the final conclusion that the intrannual variations of body condition in the temperate octopus E. cirrhosa do not rely on energy transfers among organs, but on other biotic factors such as feeding incomes. Furthermore, the seasonal trend observed in the somatic condition index used in this work is consistent with the life-history of the species studied, which would reinforce the usefulness of this index (Peig and Green, 2009). 5. Conclusion Our results showed that the individual body condition of the semelparous, income breeder octopus E. cirrhosa showed a marked intrannual cycle independently of the sex and, noteworthy, the maturity stage. This precludes the large investment in gonad tissues, especially in octopus females, as a driving factor explaining the observed intrannual fluctuations in octopus condition. The significant correlations found between condition and several environmental variables such as productivity or sea temperature, suggest that condition might display an intrinsic seasonal cycle, as many other life-history traits in most species such as reproduction, migration or moulting. There also remains the possibility that condition is determined genetically, as has been reported in recent

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