Limited use of stored energy reserves for reproduction by the tropical loliginid squid Photololigo sp.

Abstract

This study sought to determine if the tropical loliginid squid Photololigo sp. stores energy in the form of lipid, carbohydrate or protein for reproductive investment. Individuals were examined for changes in morphometry, mantle muscle structure and concentrations of water, lipid, carbohydrate and protein in muscle tissue and the digestive gland, associated with the stage of reproductive maturation. Muscle mass was affected by reproductive maturation in females. Mature individuals were lighter for their length compared with females in the early stages of maturation. Concentrations of lipid and carbohydrate in the muscle tissue were very low, and female Photololigo sp. showed equivocal evidence of declining lipid and carbohydrate levels with egg production. There was no evidence of dramatic changes in protein concentration in the mantle muscle with reproductive maturation. Male Photololigo sp. showed a change in the digestive gland with maturation, with water content increasing and protein concentrations decreasing.The digestive gland of both male and female Photololigo sp. increased in size and contained less water with growth. There was little evidence that the storage and transfer of energy for reproduction occurred in Photololigo sp. Instead, it is probable that energy for reproduction is predominantly sourced directly from consumed food.

'Superbull' males: what role do they play and what drives their appearance within the Doryteuthis gahi Patagonian Shelf population?

“…Energy for production of reproductive organs appears to be derived from diet rather than a stored energy source, given the gradual decline of the DGI with size. An obvious drop would suggest that lipid deposits within the digestive gland are being used as an energy source at the onset of reproductive maturation (Guerra and Castro 1994;Moltschaniwskyj and Semmens 2000).…”

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

“…Overall, this study produced a model of protein turnover that indicates that when Euprymna tasmanica allocates energy to reproductive growth, there was no difference in retention of protein for somatic growth between mature and immature individuals. Significantly slower mean fractional rates of mantle protein degradation in mature females (this study) and no evidence that lipid is used as a storage product (Moltschaniwskyj and Johnston 2006) support an income energy model for reproduction in some cephalopod species (Hatfield et al 1992;Moltschaniwskyj 1995;Moltschaniwskyj and Semmens 2000;Semmens and Moltschaniwskyj 2000). This study has revealed that both fractional rates of mantle protein synthesis and degradation were slower in mature individuals, suggesting that less energy is available for protein synthesis but slower rates of protein degradation allowed somatic growth to continue (Moltschaniwskyj and Carter 2010); this supports an adaptive response in mantle protein turnover (Hawkins 1991).…”

“…There is little doubt that for E. tasmanica there was a somatic cost associated with reproduction; a reduction in mantle muscle protein synthesis with the onset of reproduction suggests lower availability of amino acid and/or energy-restricted protein synthesis in the muscle tissue (Carter and Houlihan 2001). Given that E. tasmanica shares a number of life-history and ecological characteristics with the reef loliginid squid and cuttlefish, it is highly likely that for most cephalopod species for whom the cost of reproduction is not apparent at the whole-animal level (Rodhouse et al 1988;Hatfield et al 1992;Moltschaniwskyj and Semmens 2000;Semmens and Moltschaniwskyj 2000), the cost may be evident at the suborganismal level. Highly variable retention of synthesized protein for somatic growth would also explain why, for many cephalopod species, proximal analysis fails to detect changes in mantle muscle protein concentrations associated with reproduction (Moltschaniwskyj and Semmens 2000;McGrath and Jackson 2002;Rosa et al 2005).…”

“…Given that E. tasmanica shares a number of life-history and ecological characteristics with the reef loliginid squid and cuttlefish, it is highly likely that for most cephalopod species for whom the cost of reproduction is not apparent at the whole-animal level (Rodhouse et al 1988;Hatfield et al 1992;Moltschaniwskyj and Semmens 2000;Semmens and Moltschaniwskyj 2000), the cost may be evident at the suborganismal level. Highly variable retention of synthesized protein for somatic growth would also explain why, for many cephalopod species, proximal analysis fails to detect changes in mantle muscle protein concentrations associated with reproduction (Moltschaniwskyj and Semmens 2000;McGrath and Jackson 2002;Rosa et al 2005). For Octopus species and some ommastrephid squid, rates of protein degradation are correlated with reproduction (O'Dor and Wells 1978;Jackson and Mladenov 1994;Arkhipkin and Bjorke 1999); the loss of muscle protein is dramatic in these species and results in almost complete loss of structural protein.…”

“…Many of these species show no evidence of significant changes in morphometric or proximal composition of the digestive gland and mantle muscle tissue associated with reproduction, appearing to fuel reproduction directly through ingested food (i.e., income energy). Use of income energy sources in cephalopods is proposed across a wide range of species-ommastrephid squids (McGrath and Jackson 2002;Rosa et al 2005), loliginid squid (Hatfield et al 1992;Moltschaniwskyj and Semmens 2000;Semmens and Moltschaniwskyj 2000), and octopus (Rosa et al 2004)-and may explain the variability in the age and size at reproductive maturation typical of many cephalopods (Arkhipkin and Laptikhovsky 1994;Pecl et al 2004;Tafur et al 2010). However, identifying the best metrics to use to determine the use of capital versus income reproduction is challenging (Houston et al 2007).…”