Our results reflected that the population structure of common cuttlefish Sepia officinalis in the Balearic Sea showed depth related differences in size linked to their reproductive cycle. The largest individuals were distributed inshore (< 50 m) while smaller individuals occurred mainly offshore (> 50 m). Additionally, the structure of maturity stages by fishing gear observed also support this migration. While spawning individuals were predominant in both inshore and offshore, immature and developing showed a significant higher abundance in offshore waters (20%). The observed pattern coincides with previous studies conducted in the Mediterranean (Belcari et al. 2002; Bettoso et al. 2016).
Regarding sex-ratio, males predominate over females in inshore waters while the opposite trend was observed deeper. This trend was also observed by Bettoso et al. (2016) in the Adriatic Sea, where the common cuttlefish analysed were caught by different fisheries, including static and trawling gears. Bloor et al. (2013) pointed out that male movements were higher along different spawning areas than females, which were more territorial, staying on the same spawning area. The observed differences in the size structure, maturity stages distribution and sex-ratio of individuals caught by trammel net and bottom trawl gears could be explained by the migratory movements and the differences in mesh size of the two fishing gears used in this study.
It is well known that body size and reproductive traits of cephalopods vary with temperature and resources availability over gradients of latitude (Guerra 2006). In this study, the size at maturity was calculated for the first time in the Balearic Sea, being 87 mm ML and 78 mm ML, for females and males respectively. These values match with those observed in the Catalan (Mangold-Wirz 1963) and Aegean (Duysak et al. 2014; Önsoy & Salman 2005) Seas. Our specimens attained sexual maturity earlier than those found in the North Atlantic (146 and 164 mm ML, for males and females respectively), which populations have larger sizes due to lower water temperature and higher food availability (Dunn et al. 1999).
In accordance with previous works, our results showed that both offshore and inshore S. officinalis have a mean size (119 and 134 mm respectively) smaller than those observed in the Atlantic waters (146 and 170 mm for trawling and trammel net respectively; Dunn 1999). The same match was found when comparing our results of length distribution of offshore individuals with those found in the Oran Bay (100–120 mm; Saddikioui et al. 2017). By contrast, smaller mean sizes were reported in the Adriatic Sea (90–99 mm; Bettoso et al. 2016; Duysak et al. 2014). This variability in sizes might be potentially relate to the higher exploitation of this species in the Adriatic (Bettoso et al. 2016; Lazzari et al. 2012).
The temporal distribution of maturity stages indicated that S. officinalis has a semi-continuous reproductive cycle in Balearic Sea. Spawning individuals occur from January to July with an intensification of spawning activity during March-June. The peak of the gonadosomatic index from March to June also highlighted the increase of spawning, when light hours and temperature increase (Richard 1968; Bloor et al 2013). These results differed from those observed in the Oran Bay (Saddikioui et al. 2017), where the spawning peak was found to be notably shorter (in March); however, differences might be due to the fact that this study only analysed individuals taken by commercial trawlers. In Turkish waters, the spawning extends from February to June (Duysak et al. 2014), and in the Adriatic Sea spawning takes place all over the year with an intensification from April to August (Bettoso et al. 2016). In the Aegean Sea a semi-continuous reproductive cycle from January to July was observed, with two main peaks, a first peak in March followed by a second and more intense peak in June (Onsoy & Salman 2005). These geographical differences in spawning periods may be related to temperature variations between the regions (Bloor 2013; Richard 1971; Wang et al. 2003).
The size distribution of ovarian eggs was similar to the observed in previous studies (Boletzky 1987; Laptikhovsky et al. 2003; Lin et al. 2019; Mangold- Wirz 1983). Our results showed that S. officinalis has an asynchronous ovarian development organisation, with the presence of a continuous oocyte size frequency distribution in the ovary according to the strategy of this species defined by Rocha et al (2001) as intermittent terminal spawner.
In this study, Batch fecundity of S. officinalis, defined as the standing stock of yolk oocytes larger than 3.15 mm, was calculated for the first time in the Balearic Sea. Our results showed values ranging from 53 to 480 eggs and a significant positive relationship between batch fecundity and eviscerated weight of females. However, these results were lower than those observed by Laptikhovsky et al. (2003) in the Aegean Sea, where the number of large eggs varied from 130 to 839 eggs, probably because their study was performed at the beginning of the spawning season when the largest spawning individuals of the population occurs (Mangold-Wirz 1963).
Food intake analysis reflect a close relationship with the reproductive development showing a similar trend but reflecting different intensities between females and males. The feeding intake was highest in immature and developing individuals. As maturation proceeded, the stomach fullness progressively decreased while the vacuity index followed the opposite trend indicating that cuttlefish lessened its feeding activity during the spawning period. Different results have been published for common cuttlefish indicating there is not a common pattern. In Atlantic waters, some authors observed higher feeding intensity in mature females (Castro & Guerra 1990; Neves et al. 2009a), whereas others found minimum repletion ratio for reproductive individuals (Piczon du Sel et al. 2000). In the Mediterranean, feeding activity was also found to be lower in mature individuals caught in shallower waters compared to smaller individuals from offshore probably conditioned by the fishing method used (Bettoso et al. 2016). Owing to the physiological plasticity of S. officinalis (Oellermann et al. 2012) the trade-off between energy intake and stored resources to fuel reproduction might differ among geographical locations depending on environmental conditions and food availability. Besides this general feeding pattern, it was also observed that females feeding activity was higher than males suggesting that females need greater energy intakes to fulfil oocyte maturation (Castro & Guerra 1990; Neves et al. 2009a; Quintela & Andrade 2002). Despite the reduction of feeding intensity with sexual maturation, no variation was observed in mature and spawning female’s digestive gland index probably caused by the lower lipid requirements in female’s diet for gonadal maturation. On the contrary, males showed a decreasing trend in digestive gland index as they use more lipids as energy source during spawning (Castro et al. 1992; Castro & Guerra 1990). Other authors observed non-significant differences in the digestive gland in relation to maturity stages in other cuttlefish (Castro et al. 1991; Gabr et al. 1999) and squid species (Lin et al. 2017). In cephalopods, the body muscle is thought to be one of the most important sites for energy reserves instead of the digestive gland (Castro et al. 1992; Guerra & Castro, 1994). However, males at full maturity stage showed lowest values for the digestive gland index and the highest number of empty stomach (50%) reflecting differences in their allocation strategy compared to females, at least at the end of sexual maturation. Contrary to Keller et al. (2014), those results suggested that common cuttlefish fulfil the cost of reproduction through both current food intake and accumulated somatic reserves.
In conclusion and regarding the large variability of its biological traits along its geographical distribution, S. officinalis of the Balearic Sea showed similar patterns as in other warm areas, such as long spawning period, short life span, bathymetric migrations and decreasing feeding activity with sexual maturation. Additionally, the fecundity features also supports the flexibility of this species as its reproduction may be driven by the season or the area where it lives.