The Adaptive Response of Protein Turnover to the Energetic Demands of Reproduction in a Cephalopod

Moltschaniwskyj, Natalie A.; Carter, Chris

doi:10.1086/667799

Cited by 15 publications

(11 citation statements)

References 53 publications

(80 reference statements)

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“…Prior to our study, the fractional rate of protein synthesis had only been measured in two species of cephalopods; the common octopus (Octopus vulgaris) (14) and the Southern dumpling squid (Euprymna tasmanica) (5,25,26), but never in a cuttlefish. Our work is the first to measure the fractional rate of protein synthesis in S. officinalis.…”

Section: Discussionmentioning

confidence: 99%

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Lamarre

MacCormack

Sykes

et al. 2016

American Journal of Physiology-Regulatory, Integrative and Comp

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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.

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Section: Discussionmentioning

confidence: 99%

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Lamarre

MacCormack

Sykes

et al. 2016

American Journal of Physiology-Regulatory, Integrative and Comp

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“…then as the animal is likely to experience some suffering it arguably comes within the scope of Directive 2010/63/EU (see Smith et al, 2013, for discussion). As the reduction in food intake progresses the animals will rapidly pass through metabolic phases I, II described above in animals deprived of food and will probably spend the longest time in phase III until death ensues (Moltschaniwskyj and Carter, 2013). Studying senescence is further complicated because animals not only stop eating but may develop other symptoms such as cataracts, skin lesions and increased, but uncoordinated, locomotor activity (Anderson et al, 2002; Sykes et al, 2012; Sykes and Gestal, 2014) none of which can be alleviated.…”

Section: Reduced Food Intake As a Humane End-point In Procedures: Whamentioning

confidence: 99%

The Digestive Tract of Cephalopods: a Neglected Topic of Relevance to Animal Welfare in the Laboratory and Aquaculture

et al. 2017

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Maintenance of health and welfare of a cephalopod is essential whether it is in a research, aquaculture or public display. The inclusion of cephalopods in the European Union legislation (Directive 2010/63/EU) regulating the use of animals for scientific purposes has prompted detailed consideration and review of all aspects of the care and welfare of cephalopods in the laboratory but the information generated will be of utility in other settings. We overview a wide range of topics of relevance to cephalopod digestive tract physiology and their relationship to the health and welfare of these animals. Major topics reviewed include: (i) Feeding cephalopods in captivity which deals with live food and prepared diets, feeding frequency (ad libitum vs. intermittent) and the amount of food provided; (ii) The particular challenges in feeding hatchlings and paralarvae, as feeding and survival of paralarvae remain major bottlenecks for aquaculture e.g., Octopus vulgaris; (iii) Digestive tract parasites and ingested toxins are discussed not only from the perspective of the impact on digestive function and welfare but also as potential confounding factors in research studies; (iv) Food deprivation is sometimes necessary (e.g., prior to anesthesia and surgery, to investigate metabolic control) but what is the impact on a cephalopod, how can it be assessed and how does the duration relate to regulatory threshold and severity assessment? Reduced food intake is also reviewed in the context of setting humane end-points in experimental procedures; (v) A range of experimental procedures are reviewed for their potential impact on digestive tract function and welfare including anesthesia and surgery, pain and stress, drug administration and induced developmental abnormalities. The review concludes by making some specific recommendations regarding reporting of feeding data and identifies a number of areas for further investigation. The answer to many of the questions raised here will rely on studies of the physiology of the digestive tract.

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“…Additional key words: energy reserve, somatic condition Sourcing energy for reproduction is a major driver of the life-history characteristics of animals (Moltschaniwskyj & Carter 2013). Investment in reproduction or the optimal trade-off between investment in reproduction and investment in somatic growth may be impacted by low internal energy reserves at the beginning of the breeding season (Elkin & Reid 2005).…”

mentioning

confidence: 99%

“…Moreover, coleoid cephalopods are characterized by short-life spans, monocyclic reproductive patterns and single-season breeding, with body mass and reproductive system shrinking once spawning commences (Laptikhovsky & Nigmatullin 1993;Boyle & Rodhouse 2005). These monocyclic animals have evolved an adaptive response to the concurrent energy demands of reproduction and continued somatic growth and muscle function (Moltschaniwskyj & Carter 2013). Both protein in the mantle muscle tissue and lipid in the digestive gland have been suggested as possible substrates and sites for energy storage in cephalopods (O'Dor & Wells 1978;Castro et al 1992;Clarke et al 1994;Moltschaniwskyj & Semmens 2000).…”

mentioning

confidence: 99%

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Sex‐specific reproductive investment of summer spawners of Illex argentinus in the southwest Atlantic

Lin

Chen

et al. 2015

Invertebrate Biology

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Energy investment in reproduction and somatic growth was investigated for summer spawners of the Argentinean shortfin squid Illex argentinus in the southwest Atlantic Ocean. Sampled squids were examined for morphometry and intensity of feeding behavior associated with reproductive maturation. Residuals generated from length‐weight relationships were analyzed to determine patterns of energy allocation between somatic and reproductive growth. Both females and males showed similar rates of increase for eviscerated body mass and digestive gland mass relative to mantle length, but the rate of increase for total reproductive organ weight relative to mantle length in females was three times that of males. For females, condition of somatic tissues deteriorated until the mature stage, but somatic condition improved after the onset of maturity. In males, there was no correlation between somatic condition and phases of reproductive maturity. Reproductive investment decreased as sexual maturation progressed for both females and males, with the lowest investment occurring at the functionally mature stage. Residual analysis indicated that female reproductive development was at the expense of body muscle growth during the immature and maturing stages, but energy invested in reproduction after onset of maturity was probably met by food intake. However, in males both reproductive maturation and somatic growth proceeded concurrently so that energy allocated to reproduction was related to food intake throughout the process of maturation. For both males and females, there was little evidence of trade‐offs between the digestive gland and reproductive growth, as no significant correlation was found between dorsal mantle length‐digestive gland weight residuals. The role of the digestive gland as an energy reserve for gonadal growth should be reconsidered. Additionally, feeding intensity by both males and females decreased after the onset of sexual maturity, but feeding never stopped completely, even during spawning.

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The Adaptive Response of Protein Turnover to the Energetic Demands of Reproduction in a Cephalopod

Cited by 15 publications

References 53 publications

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

The Digestive Tract of Cephalopods: a Neglected Topic of Relevance to Animal Welfare in the Laboratory and Aquaculture

Sex‐specific reproductive investment of summer spawners of Illex argentinus in the southwest Atlantic

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