Energy acquisition strategy for reproduction in a semelparous squid

Abstract

Background Energy demand for reproduction leads to a wide diversity of foraging and life-history strategy among wild animals, linking to a common objective to maximize reproductive success. Semelparous squid species in particular can use up to 50% of the total energy intake for reproduction. However, the energy acquisition strategy for reproduction is still a controversial issue regarding whether the squid shift in diet ontogenetically. Here we used Argentinean shortfin squid (Illex argentinus) as a case study to investigate the strategy of energy acquisition for reproduction, by analyzing energy density of the squid’s reproductive tissues including ovary, nidamental glands and oviduct eggs, and stable isotopes and fatty acids of the squid’s ovary. Results The reproductive energy (the sum of the energy accumulated in ovary, nidamental glands and oviduct eggs) increased significantly with maturation. The ovary nitrogen stable isotopes (δ15N) showed a significant increase with maturation, but the increase by maturity stage was not equal to the typical enrichment of about 3‰ per trophic level. Isotopic niche width showed an increasing trend with maturation, and isotopic niche space exhibited greater overlap at advanced maturity stages. The relative amounts of 16:0, 20:5n3 and 20:4n6 in the ovary, tracing for carnivores and top predators, increased after the onset of maturation. The overall fatty acid profiles of the ovary showed significant differences among maturity stages, but obvious overlaps were found for mature squids. Mixed-effects model results revealed that reproductive energy was positively correlated with δ15N values. The reproductive energy was also positively related to the relative amounts of 18:0 and 20:4n6, respectively tracing for herbivores and top predators. Conclusions Our results validate that the squid shifts to feed on higher trophic prey for reproduction as energy demand increases once maturation commences. However, the squid does not shift feeding habits at a trophic level but instead broadens prey spectrum, coupled with increasing intake of higher trophic prey items, to meet the energy demand for reproduction. Such energy acquisition strategy may be selected by the squid to maximize reproductive success by balancing energy intake and expenditure from foraging, warranting future studies that aim to clarify such strategy for reproduction among semelparous species.

Variation in energy density of northwest Atlantic forage species: Ontogenetic, seasonal, annual, and spatial patterns

“…Other studies have reported that energy was only weakly related to mantle length in the Argentine shortfin squid Illex argentinus (Lin et al. 2022; Song et al. 2023).…”

“…These species showed high variability in ED at a given size, and only weak effects of size were evident for Silver Hake and longfin inshore squid. Other studies have reported that energy was only weakly related to mantle length in the Argentine shortfin squid Illex argentinus (Lin et al 2022;Song et al 2023). All three moderate-quality species have broad distributions: the Silver Hake is more temperate, the northern shortfin squid is boreal and temperate to subtropical, and the longfin inshore squid is temperate to subtropical.…”

“…2015), the semelparous squid species spawn only once in their lifetime and they devote a large portion (~50%) of stored body energy to reproduction (Lin et al. 2022). Squid energetics are geared to consume high‐protein diets (crustaceans, mollusks, and fish), which are digested rapidly to convert into growth rather than storage (O'Dor and Webber 1986).…”

“…Both the northern shortfin squid and the longfin inshore squid have typical cephalopod life histories: a short life span (usually 1 year), fast growth, and semelparous reproduction. Unlike iteroparous species that balance reproductive expenditures against the probability of survival to the next year (McBride et al 2015), the semelparous squid species spawn only once in their lifetime and they devote a large portion (~50%) of stored body energy to reproduction (Lin et al 2022). Squid energetics are geared to consume high-protein diets (crustaceans, mollusks, and fish), which are digested rapidly to convert into growth rather than storage (O'Dor and Webber 1986).…”