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- Control of zootechnology leads to improved Cuttlefish (Sepia officinalis, L.) reproduction performance up to pre-industrial levelsPublication . Capaz, Juan Carlos; Hernández-Brooke, Daniel; Balvet, Safia; Couto, Ana T.; Alves, Alexandra; Baptista Gonçalves, Rui; Frias, Paulo A.; Andrade, José Pedro; Sykes, AntónioCephalopods are gaining momentum as an alternate group for aquaculture species diversification, not only because they are a good food source (highly appreciated in some worldwide markets) but they also have the potential to quickly reach a market size. However, there are some bottlenecks impeding the transition of culture technology from the laboratory to industry. One is related to control over reproduction in captivity. The objective of the present experiment was to verify the effects of tanks with different bottom areas/volumes on the reproduction performance of S. officinalis breeding stocks, when sex ratios were controlled a priori; and the food cost associated with such performance when individuals are fed a natural frozen diet. One hundred and ninety two juvenile cuttlefish were used to compare three different round-shaped tanks: one type with 3000L volume and two types with 9000L volume (with differences in bottom areas and water column). Individuals had their sex and maturity stage determined to establish a sexual ratio of 2 female:1 male per tank and assure that cuttlefish were still immature. Biological data was collected during both growth and reproduction stages and until the death of all females in each tank. The experiment lasted nearly 300 days. Temperature differences between tank types were registered during both stages. The optimizing of rearing conditions has allowed for higher growth and a higher amount of cuttlefish available for breeding purposes. A total of 123,751 eggs (in 85 batches) was obtained during this experiment, which is a number that may meet a small scale cuttlefish commercial hatchery facility requirements. The present conditions contributed to a better and predictable reproduction performance in specific 9000L tanks, with values reaching pre-industrial numbers (approximate to 24,000 eggs/tank). Moreover, both the amount of eggs per batch and the overall quality of eggs has increased. Three of these 9000L tanks have an overall consumption of approximate to 38.64 Kg tank(-1), which translates in an investment in feed of approximate to 193 (sic) tank(-1), 8.40 (sic) per cuttlefish and an overall daily tank expense of 1.76 (sic) d(-1).
- Microplastics presence in cultured and wild-caught cuttlefish, Sepia officinalisPublication . Oliveira, Ana R.; Sardinha-Silva, Andreia; Andrews, Paul L. R.; Green, Dannielle; Cooke, Gavan M.; Hall, Sarah; Blackburn, Kirsty; Sykes, Antonio V.Amongst cephalopods microplastics have been reported only in jumbo squid gut. We investigated microplastics in the digestive system of wild cuttlefish (Sepia officinalis) as they are predators and prey and compared the stomach, caecum/intestine and digestive gland (DG) of wild and cultured animals, exposed to seawater from a comparable source. Fibers were the most common type (approximate to 90% of total count) but were approximate to 2x higher in relation to body weight in wild vs. cultured animals. Fibers were transported to the DG where the count was approximate to 2x higher/g in wild (median 1.85 fibers/g) vs. cultured. In wild-caught animals the DG was the predominant location but in cultured animals the fibers were more evenly distributed in the digestive tract. the potential impact of mi-croplastics on health of cuttlefish is discussed. Cuttlefish represent a previously unrecognized source of micro plastic trophic transfer to fish and finding fibers in cultured animals has implications for aquaculture.
- Behavioural aspects of the spotty bobtail squid Euprymna parva (Cephalopoda: Sepiolidae)Publication . Drerup, Christian; Sykes, António; Cooke, Gavan M.Bobtail squids (Sepiolidae, Cephalopoda) have recently been growing in popularity in scientific studies due to their symbiotic relationship with light producing bacteria and their corresponding light emitting organs. However, the overall knowledge on the behaviour of sepiolids is based on observations on just a few of the roughly 70 extant species and must still be considered as sparsely. Understanding their behavioural ecology is not only beneficial to further grasp the complex behavioural patterns of cephalopods, it is also vital for establishing a good welfare practice when holding sepiolids in captivity. Hence, the present study characterised several behavioural aspects of the spotty bobtail squid Euprymna parva. Although the burying, hunting and mating behaviour as well as most escape responses of this less investigated sepiolid species greatly resembled those of other observed bobtail squids, differences to sepiolids from other genera or even from the same genus could be identified in the present study. Additionally, the first observation of an up to now undescribed inking behaviour of sepiolids is reported. E. parva was observed to eject a stretch of ink ('ink rope'), approximately 4-5 times the length of the animal, and hold on to it motionless, potentially as a masquerade to resemble a floating seagrass leave. The present study further provides detailed information on daily time and activity budgets as well as the tentacular strike speed during hunting, two up to now barely investigated behavioural aspects of the sepiolid ecology.
- Natural geochemical markers reveal environmental history and population connectivity of common cuttlefish in the Atlantic Ocean and Mediterranean SeaPublication . Rooker, Jay R.; Wells, R. J. David; Addis, Piero; Arrizabalaga, Haritz; Baptista, Miguel; Bearzi, Giovanni; Dance, Michael A.; Fraile, Igaratza; Lacoue-Labarthe, Thomas; Lee, Jessica M.; Megalofonou, Persefoni; Rosa, Rui; Sobrino, Ignacio; Sykes, António; Villanueva, RogerNatural markers (delta C-13 and delta O-18 stable isotopes) in the cuttlebones of the European common cuttlefish (Sepia officinalis) were determined for individuals collected across a substantial portion of their range in the Northeast Atlantic Ocean (NEAO) and Mediterranean Sea. Cuttlebone delta C-13 and delta O-18 were quantified for core and edge material to characterize geochemical signatures associated with early (juvenile) and recent (sub-adult/adult) life-history periods, respectively. Regional shifts in cuttlebone delta C-13 and delta O-18 values were detected across the 12 sites investigated. Individuals collected from sites in the NEAO displayed more enriched delta C-13 and delta O-18 values relative to sites in the Mediterranean Sea, with the latter also showing salient differences in both markers among western, central and eastern collection areas. Classification success based on cuttlebone delta C-13 and delta O-18 values to four geographical regions (NEAO, western, central and eastern Mediterranean Sea) was relatively high, suggesting that environmental conditions in each region were distinct and produced area-specific geochemical signatures on the cuttlebones ofS. officinalis. A modified delta C-13 and delta O-18 baseline was developed from sites proximal to the Strait of Gibraltar in both the NEAO and Mediterranean Sea to assess potential mixing through this corridor. Nearly, all (95%) of delta C-13 and delta O-18 signatures ofS. officinaliscollected in the area of the NEAO closest to the Strait of Gibraltar (Gulf of Cadiz) matched the signatures of specimens collected in the western Mediterranean, signifying potential movement and mixing of individuals through this passageway. This study extends the current application of these geochemical markers for assessing the natal origin and population connectivity of this species and potentially other taxa that inhabit this geographical area.
- Effects of feeding with different live preys on the lipid composition, growth and survival ofOctopus vulgarisparalarvaePublication . Reis, Diana B.; Shcherbakova, Anastasia; Riera, Rodrigo; Martín, M. Virginia; Domingues, Pedro; Andrade, Jose; Jimenez-Prada, Pablo; Rodriguez, Covandonga; V. Sykes, Antonio; Almansa, EduardoTo move forward in the farming ofOctopus vulgarisparalarvae, it is necessary to search for a live prey easy to obtain and maintain in the laboratory that meets the nutritional requirements of the octopus paralarvae and adapts to its predatory behaviour.Grapsus adscensioniszoeae (Crustacea, Decapoda) seems to fulfil most of these targets, and it was herein used to deepen knowledge of paralarvae lipid requirements and composition, growth and survival. To this purpose, the effects of feeding withGrapsuszoeae as sole prey were compared withArtemiaat two different stages (nauplii and juveniles), which also differed in their lipid profiles. After 15 days of feeding, the best growth and survival of paralarvae was obtained in theGrapsusgroup, and no differences were observed between bothArtemiagroups. Triacylglycerides storage in paralarvae seemed to be co-related with a lower growth and survival, but not with its prey levels. Contrarily, sterol ester levels were higher in paralarvae fedGrapsus, reflecting its content in the prey. The best paralarval viability was related to higher levels of 22:6n-3 (DHA) and 20:4n-6 (ARA), also reflecting its higher content in the prey. On the other hand, neither the 20:5n-3 (EPA) levels in the prey nor in paralarvae were related to growth or survival. The implications of these results are discussed considering the lipid requirements ofO. vulgarisparalarvae.
- Regional patterns of δ13C and δ15N for European common cuttlefish (Sepia officinalis) throughout the Northeast Atlantic Ocean and Mediterranean SeaPublication . David Wells, R. J.; Rooker, Jay R.; Addis, Piero; Arrizabalaga, Haritz; Baptista, Miguel; Bearzi, Giovanni; Fraile, Igaratza; Lacoue-Labarthe, Thomas; Meese, Emily N.; Megalofonou, Persefoni; Rosa, Rui; Sobrino, Ignacio; Sykes, Antonio V.; Villanueva, RogerThe European common cuttlefish, Sepia officinalis Linnaeus, 1758 is a coastal nektobenthic species ranging from the Shetland Islands through the Northeast Atlantic Ocean and Northwest Africa into the Mediterranean Sea [1]. This species constitutes one of the most economically valuable cephalopod resources in the Northeast Atlantic Ocean, supporting an important fishery resource [2,3]. Sepia officinalis has a relatively short lifespan of 1–2 years, early sexual maturity and an extended spawning season laying eggs on the seafloor with direct benthic, large hatchlings [4,5]. Given this species geographical distribution combined with limited dispersal, it has been a targeted model species to examine connectivity throughout the Northeast Atlantic Ocean and Mediterranean Sea (hereafter NEAO-MS) [6]. Natural biomarkers such as stable isotopes are commonly used to examine food web structure and ecosystem connectivity in marine environments [7,8]. Stable isotopes of carbon (δ13C) and nitrogen (δ15N) are particularly useful tracers due to their natural abundance being influenced by the environment and ease of measurement in body tissues without having to track individuals in a population. δ13C is traditionally used to trace carbon pathways because little fractionation occurs between predator and prey, and different primary producers (energy sources) often have unique δ13C values [9]. δ13C values of consumers are a product of the primary producers’ composition and influenced by the dissolved inorganic carbon (DIC) pool, as well as local abiotic factors including sea surface temperature, and can differ across ocean basins [10] and region-specific freshwater to marine gradients [9]. δ15N becomes enriched with increasing trophic level and is used to infer trophic position [7], but can also differ at the base of the food web. Depending upon the types of nutrients available to stimulate growth, δ15N values can be used to track energy flow in high-nutrient (nitrate) and low-nutrient (N2 fixation) ecosystems as well as new nitrogen (upwelled nitrate) versus regenerated nitrogen (ammonia, urea). Combining both δ13C and δ15N offers the potential to study the connectivity and population structure of species because longitudinal and latitudinal gradients exist throughout marine ecosystems [11,12], including the NEAO-MS [8,13].
- Felasa working group report: capture and transport of live cephalopods – recommendations for scientific purposesPublication . Sykes, António; Galligioni, Viola; Estefanell, Juan; Hetherington, Stuart; Brocca, Marco; Correia, Joao; Ferreira, André; Pieroni, Eleonora M.; Fiorito, GrazianoOn 1 January 2013, research using cephalopod molluscs, from hatchlings to adults, became regulated within Directive 2010/63/EU. There are significant difficulties in captive breeding in the great majority of currently utilised species. Thus, scientific research relies upon the use of wild-caught animals. Furthermore, live cephalopods are shared and transported between different stakeholders and laboratories across Europe and other continents. Despite existing European and national legislation, codes, guidelines and reports from independent organisations, a set of recommendations specifically addressing the requirements for the capture and transport of animals belonging to this taxon are missing. In addition, although training and development of competence for all people involved in the supply chain are essential and aim to ensure that animals do not suffer from pain, distress or lasting harm, the requirements for those capturing and transporting wild cephalopods have not been considered. This Working Group reviewed the current literature to recognise scientific evidence and the best practice, and compiled a set of recommendations to provide guidance on the ‘techniques’ to be used for the capture and transport of live cephalopods for their use in scientific procedures. In addition, we propose to (a) develop standardised approaches able to assess recommended methods and objectively quantify the impact of these processes on animals’ health, welfare and stress response, and (b) design a training programme for people attaining the necessary competence for capture and transportation of live cephalopods, as required by Directive 2010/63/EU.
- Can Cephalopods vomit? Hypothesis based on a review of circumstantial evidence and preliminary experimental observationsPublication . Sykes, António; Almansa, Eduardo; Ponte, Giovanna; Cooke, Gavan M.; Andrews, Paul L. R.In representative species of all vertebrate classes, the oral ejection of upper digestive tract contents by vomiting or regurgitation is used to void food contaminated with toxins or containing indigestible material not voidable in the feces. Vomiting or regurgitation has been reported in a number of invertebrate marine species (Exaiptasia diaphana, Cancer productus, and Pleurobranchaea californica), prompting consideration of whether cephalopods have this capability. This "hypothesis and theory" paper reviews four lines of supporting evidence: (1) the mollusk P. californica sharing some digestive tract morphological and innervation similarities with Octopus vulgaris is able to vomit or regurgitate with the mechanisms well characterized, providing an example of motor program switching; (2) a rationale for vomiting or regurgitation in cephalopods based upon the potential requirement to void indigestible material, which may cause damage and ejection of toxin contaminated food; (3) anecdotal reports (including from the literature) of vomiting- or regurgitation-like behavior in several species of cephalopod (Sepia officinalis, Sepioteuthis sepioidea, O. vulgaris, and Enteroctopus dofleini); and (4) anatomical and physiological studies indicating that ejection of gastric/crop contents via the buccal cavity is a theoretical possibility by retroperistalsis in the upper digestive tract (esophagus, crop, and stomach). We have not identified any publications refuting our hypothesis, so a balanced review is not possible. Overall, the evidence presented is circumstantial, so experiments adapting current methodology (e.g., research community survey, in vitro studies of motility, and analysis of indigestible gut contents and feces) are described to obtain additional evidence to either support or refute our hypothesis. We recognize the possibility that further research may not support the hypothesis; therefore, we consider how cephalopods may protect themselves against ingestion of toxic food by external chemodetection prior to ingestion and digestive gland detoxification post-ingestion. Reviewing the evidence for the hypothesis has identified a number of gaps in knowledge of the anatomy (e.g., the presence of sphincters) and physiology (e.g., the fate of indigestible food residues, pH of digestive secretions, sensory innervation, and digestive gland detoxification mechanisms) of the digestive tract as well as a paucity of recent studies on the role of epithelial chemoreceptors in prey identification and food intake.
- Histological and scanning electron microscope observations on the developing retina of the cuttlefish (Sepia officinalis Linnaeus, 1758)Publication . Arias-Montecino, Alejandro; Álvarez-Hernán, Guadalupe; Mera-Rodríguez, José Antonio de; Calle-Guisado, Violeta; Martín-Partido, Gervasio; Rodríguez-León, Joaquín; Francisco-Morcillo, Javier; Sykes, AntónioIn this work we present a detailed study of the major events during retinal histogenesis of the cuttlefish Sepia officinalis from early embryos to newly hatched animals and juveniles. For this purpose, we carried out morphometric and histological analyses using light and scanning electron microscopy. From St19, the first embryonic stage analysed, to St23/24 the embryonic retina is composed of a pseudostratified epithelium showing abundant mitotic figures in the more internal surface. At St24 the first photoreceptor nuclei appear in the presumptive inner segment layer, while an incipient layer of apical processes of the future rhabdomeric layer become visible at St25. From this stage onwards, both the rhabdomeric layer and the inner segment layer increase in size until postnatal ages. In contrast, the width of the supporting cell layer progressively decreases from St25/26 until postnatal ages. S. officinalis embryos hatched in a morphologically advanced state, showing a differentiated retina even in the last stages of the embryonic period. However, features of immaturity are still observable in the retinal tissue during the first postnatal weeks of life, such as the existence of mitotic figures in the apical region of the supporting cell layer and migrating nuclei of differentiating photoreceptors crossing the basal membrane to reach their final location in the inner segment layer. Therefore, postnatal retinal neurogenesis is present in juvenile specimens of S. officinalis.
- Excitation–contraction coupling reflects the metabolic profile of mantle muscle in young cuttlefishPublication . Callaghan, Neal I.; Ducros, Loïck; Bennett, J. Craig; Capaz, Juan Carlos; Andrade, José Pedro Andrade; Sykes, António; Driedzic, William R.; Lamarre, Simon G.; MacCormack, Tyson J.The mantle muscle of common cuttlefish, Sepia officinalis, is responsible both for high-magnitude and rapid movements for locomotion, as well as sustained ventilation, which require specific metabolic, electrophysiological, and structural organization. Young cuttlefish have a highly oxidative phenotype and a rapid growth rate. Here, we show high rates of oxygen consumption and protein synthesis in juveniles, and these rates decay exponentially over the first few weeks of growth. This is associated with considerable citrate synthase activity (relative to larger cuttlefish) but a lack of glucose metabolism based on zero uptake of glucose by isolated muscle sheets and minimal activity of hexokinase (similar to larger animals). In contrast to glucose metabolism in the heart, glucose metabolism in these muscle sheets was not stimulated by extracellular taurine. Previous research revealed an unusual ion channel complement in mantle myocytes, the most notable feature of which is the lack of a Na+ current during depolarization. Because this adaptation is not consistent across the coleoid clade, we investigated excitation-contraction coupling. Here, mantle energetics and contractility, including the individual components of the total Ca2+ flux driving contraction, were studied. Results indicate that the majority of Ca2+ current underlying contractile stress development capacity in cuttlefish juveniles is not mediated by dihydropyridine-sensitive L-type channels, in contrast to their adult counterparts, and the sarcoplasmic reticulum contributes little to routine contractility. We had previously noted an influence of physiological levels of taurine in limiting cardiac contractility but found no analogous sensitivity in mantle muscle. Finally, transmission electron microscopy of subcellular architecture revealed the presence of sarcoplasmic tubular aggregates, suggesting that oxidative inhibition of sarcoplasmic reticulum function limits its role in this life stage.