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- The digestive tract of cephalopods: toward non-invasive in vivo monitoring of Its physiologyPublication . Ponte, Giovanna; Sykes, António V.; Cooke, Gavan M.; Almansa, Eduardo; Andrews, Paul L. R.Ensuring the health and welfare of animals in research is paramount, and the normal functioning of the digestive tract is essential for both. Here we critically assess non- or minimally-invasive techniques which may be used to assess a cephalopod's digestive tract functionality to inform health monitoring. We focus on: (i) predatory response as an indication of appetitive drive; (ii) body weight assessment and interpretation of deviations (e.g., digestive gland weight loss is disproportionate to body weight loss in starvation); (iii) oro-anal transit time requiring novel, standardized techniques to facilitate comparative studies of species and diets; (iv) defecation frequency and analysis of fecal color (diet dependent) and composition (parasites, biomarkers, and cytology); (v) digestive tract endoscopy, but passage of the esophagus through the brain is a technical challenge; (vi) high resolution ultrasound that offers the possibility of imaging the morphology of the digestive tract (e.g., food distribution, indigestible residues, obstruction) and recording contractile activity; (vii) needle biopsy (with ultrasound guidance) as a technique for investigating digestive gland biochemistry and pathology without the death of the animal. These techniques will inform the development of physiologically based assessments of health and the impact of experimental procedures. Although intended for use in the laboratory they are equally applicable to cephalopods in public display and aquaculture.
- 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).
- Metabolic rate and rates of protein turnover in food-deprived cuttlefish, Sepia officinalis (Linnaeus 1758)Publication . Lamarre, Simon G.; MacCormack, Tyson J.; Sykes, António; Hall, Jennifer R.; Speers-Roesch, Ben; Callaghan, Neal I.; Driedzic, William R.To determine the metabolic response to food deprivation, cuttlefish (Sepia officinalis) juveniles were either fed, fasted (3 to 5 days food deprivation), or starved (12 days food deprivation). Fasting resulted in a decrease in triglyceride levels in the digestive gland, and after 12 days, these lipid reserves were essentially depleted. Oxygen consumption was decreased to 53% and NH4 excretion to 36% of the fed group following 3-5 days of food deprivation. Oxygen consumption remained low in the starved group, but NH4 excretion returned to the level recorded for fed animals during starvation. The fractional rate of protein synthesis of fasting animals decreased to 25% in both mantle and gill compared with fed animals and remained low in the mantle with the onset of starvation. In gill, however, protein synthesis rate increased to a level that was 45% of the fed group during starvation. In mantle, starvation led to an increase in cathepsin A-, B-, H-, and L-like enzyme activity and a 2.3-fold increase in polyubiquitin mRNA that suggested an increase in ubiquitin-proteasome activity. In gill, there was a transient increase in the polyubiquitin transcript levels in the transition from fed through fasted to the starved state and cathepsin A-, B-, H-, and L-like activity was lower in starved compared with fed animals. The response in gill appears more complex, as they better maintain rates of protein synthesis and show no evidence of enhanced protein breakdown through recognized catabolic processes.
- The effects of feeding with shrimp or fish fry on growth and mantle lipid composition of juvenile and adult cuttlefish (Sepia officinalis)Publication . Almansa, Eduardo; Domingues, Pedro; Sykes, António V.; Tejera, Noemi; Lorenzo, António; Andrade, José PedroIn the present study, cuttlefish (Sepia officinalis) aged 60-day-old (age-group I) and 120-day-old (age-group II) were fed with live shrimp and live fish fry for 60 days, in order to study the diet influence on growth, mantle lipid composition, and astaxanthin content in the skin. The most noteworthy difference was the higher growth observed in shrimp-fed cuttlefish with respect to fishfed cuttlefish in both age groups. Total lipids (TL), lipid classes (LC) and their associated fatty acids (FA) from both diets and mantle of cuttlefish were analysed. The lipid profiles of both diets were clearly different in their LC distribution, with higher levels of Polar Lipids (PL) in shrimp with respect to fish fry. However, both diets did not show outstanding differences in the FA composition of TL except for 20:5n-3 (EPA), which was higher in shrimp than in fish fry. With respect to lipid composition of cuttlefish mantle, the TL content and cholesterol (CHO) percentage increased with age, while phosphatidylinositol (PI) and phosphatidylcholine (PC) percentage decreased. On the other hand, phosphatidylserine (PS), phosphatidylethanolamine (PE) and PC percentages in both cuttlefish age groups were also affected by the different diets, although this difference was higher in agegroup I. The general pattern of fatty acid composition of TL in the mantle of cuttlefish was similar in all groups studied. It is remarkable the low levels of monoene FAs in both age-group cuttlefish mantle, despite of the high level of this FA group in both diets, which suggests that these FAs are not stored in the mantle. An opposite tendency was observed regarding the n-3 HUFA, especially 22:6n-3 (DHA) which remained constant despite the different age or diet. High levels of astaxanthin were found in shrimp with respect to fish, but this was only reflected on skin accumulation in age-group I, showing no differences in age-group II. This suggests differences in the astaxanthin metabolism according to the age. The results suggest that the growth differences observed in shrimp-fed cuttlefish with respect to fish-fed cuttlefish were not reflected in outstanding differences in mantle composition.
- Depth perception: cuttlefish (Sepia officinalis) respond to visual texture density gradientsPublication . Josef, Noam; Mann, Ofri; Sykes, António V.; Fiorito, Graziano; Reis, João; Maccusker, Steven; Shashar, NadavStudies concerning the perceptual processes of animals are not only interesting, but are fundamental to the understanding of other developments in information processing among non-humans. Carefully used visual illusions have been proven to be an informative tool for understanding visual perception. In this behavioral study, we demonstrate that cuttlefish are responsive to visual cues involving texture gradients. Specifically, 12 out of 14 animals avoided swimming over a solid surface with a gradient picture that to humans resembles an illusionary crevasse, while only 5 out of 14 avoided a non-illusionary texture. Since texture gradients are well-known cues for depth perception in vertebrates, we suggest that these cephalopods were responding to the depth illusion created by the texture density gradient. Density gradients and relative densities are key features in distance perception in vertebrates. Our results suggest that they are fundamental features of vision in general, appearing also in cephalopods.
- Common octopus (Octopus vulgaris) performance when including fasting on feeding schemes: preliminary data regarding a formulated feedPublication . Rodríguez-González, Tânia; Valverde, Jesús; Sykes, António V.; García García, BenjamínThe common octopus (Octopus vulgaris) has aroused great interest in recent years as a new species for aquaculture. The current research is focused on developing a formulated feed, although a proper diet management has also promoted rearing success of other commercial cultured species. It is documented that wild animals eat depending on prey availability and most experience fasting in nature. Hence, O. vulgaris subadults were subjected to two different feeding schemes, with a similar semi-moist diet, including either 2 (2FDb, control) or 3 (3FDb) non-consecutive days of fasting per week. Growth, feed efficiency (FE), digestibility and condition were assessed after 56 days of rearing. Both feeding schemes promoted similar growth and digestibility (P>0.05), 100% of survival and higher food-intake after fasting. Interestingly, feed efficiency (FE) was enhanced with the 3 fasting days scheme (58.6% vs. 48.3% for 2FDb scheme; P<0.05). Results might indicate that O. vulgaris has the ability to compensate fasting days through an increase in food intake on the subsequent day or a better use of its reserves. Moreover, a reduction on feeding days might promote a decrease in production costs at commercial scale.
- 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.
- Taurine depresses cardiac contractility and enhances systemic heart glucose utilization in the cuttlefish, Sepia officinalisPublication . MacCormack, Tyson J.; Callaghan, N. I.; Sykes, António V.; Driedzic, W. R.Taurine is the most abundant amino acid in the blood of the cuttlefish, Sepia officinalis, where levels can exceed 200 mmol L-1. In mammals, intracellular taurine modulates cardiac Ca2+ handling and carbohydrate metabolism at much lower concentrations but it is not clear if it exerts similar actions in cephalopods. Blood Ca2+ levels are high in cephalopods and we hypothesized that taurine would depress cardiac Ca2+ flux and modulate contractility in systemic and branchial hearts of cuttlefish. Heart performance was assessed with an in situ perfused systemic heart preparation and contractility was evaluated using isometrically contracting systemic and branchial heart muscle rings. Stroke volume, cardiac output, and Ca2+ sensitivity were significantly lower in systemic hearts perfused with supplemental taurine (100 mmol L-1) than in controls. In muscle ring preparations, taurine impaired relaxation at high contraction frequencies, an effect abolished by supra-physiological Ca2+ levels. Taurine did not affect oxygen consumption in non-contracting systemic heart muscle, but extracellular glucose utilization was twice that of control preparations. Collectively, our results suggest that extracellular taurine depresses cardiac Ca2+ flux and potentiates glucose utilization in cuttlefish. Variations in taurine levels may represent an important mechanism for regulating cardiovascular function and metabolism in cephalopods.
- Effects of culture density on growth and broodstock management of the cuttlefish, Sepia officinalis (Linnaeus, 1758)Publication . Correia, Miguel; Domingues, Pedro M.; Sykes, António V.; Andrade, José PedroThe effects of culture density on growth and broodstock management of the cuttlefish S. officinalis were studied. Cuttlefish used were one month old at the start of the experiment, on average; two densities were used (16 and 76 cuttlefish m 2). During the first experiment (until day 43), dead cuttlefish were replaced by individuals of similar weight. From that day onwards, no cuttlefish were replaced. No significant differences in growth and feeding rates, or food conversions were found between densities, during the first experiment. Results indicate that densities up to 76 cuttlefish m 2 are suitable for cuttlefish weighing approximately 10 g. After day 43 until first female layed eggs (second experiment), no statistical differences were found between densities for all the parameters studied with the exception of growth. In this case, cuttlefish cultured at the lower density grew more than those ones cultured at the higher density, with average weights at the start of egg laying of 137.3F21.6 and 91.8F12.3 g, respectively. This difference in growth could be explained mainly by the different culture densities and biomass associated. Fecundity obtained for cuttlefish cultured at the lower density (834 eggs female 1) was higher than for those ones cultured at the higher density (290 eggs female 1), however fertility was higher for the higher density. These results were expected, since fecundity is directly related to the size of females. Significant differences were found in fertility (hatching percentage) between densities. Mean hatching percentage was of 35.8F9.4% and 62.0F16.9% for low and high density, respectively. This difference was unexpected since we expected eggs from females cultured at lower densities to have higher quality. Mean hatchling weight was of 0.079F0.011 and 0.072F0.012 g for low and high density respectively, and significantly different. Results indicate that lower culture density promoted higher growth, larger eggs and hatchlings, but had no influence on juvenile and adult survival. On the contrary, eggs from females cultured at higher densities resulted in higher hatching rates.
- Enzymatic capacities of metabolic fuel use in cuttlefish (Sepia officinalis) and responses to food deprivation: insight into the metabolic organization and starvation survival strategy of cephalopodsPublication . Speers-Roesch, Ben; Callaghan, Neal I.; MacCormack, Tyson J.; Lamarre, Simon G.; Sykes, António; Driedzic, William R.Food limitation is a common challenge for animals. Cephalopods are sensitive to starvation because of high metabolic rates and growth rates related to their "live fast, die young" life history. We investigated how enzymatic capacities of key metabolic pathways are modulated during starvation in the common cuttlefish (Sepia officinalis) to gain insight into the metabolic organization of cephalopods and their strategies for coping with food limitation. In particular, lipids have traditionally been considered unimportant fuels in cephalopods, yet, puzzlingly, many species (including cuttlefish) mobilize the lipid stores in their digestive gland during starvation. Using a comprehensive multi-tissue assay of enzymatic capacities for energy metabolism, we show that, during long-term starvation (12 days), glycolytic capacity for glucose use is decreased in cuttlefish tissues, while capacities for use of lipid-based fuels (fatty acids and ketone bodies) and amino acid fuels are retained or increased. Specifically, the capacity to use the ketone body acetoacetate as fuel is widespread across tissues and gill has a previously unrecognized capacity for fatty acid catabolism, albeit at low rates. The capacity for de novo glucose synthesis (gluconeogenesis), important for glucose homeostasis, likely is restricted to the digestive gland, contrary to previous reports of widespread gluconeogenesis among cephalopod tissues. Short-term starvation (3-5 days) had few effects on enzymatic capacities. Similar to vertebrates, lipid-based fuels, putatively mobilized from fat stores in the digestive gland, appear to be important energy sources for cephalopods, especially during starvation when glycolytic capacity is decreased perhaps to conserve available glucose.