Integrating lipid storage into general representations of fish energetics

Abstract

Fish, even of the same species, can exhibit substantial variation in energy density (energy per unit wet weight). Most of this variation is due to differences in the amount of storage lipids. In addition to their importance as energy reserves for reproduction and for survival during unfavourable conditions, the accumulation of lipids represents a large energetic flux for many species, so figuring out how this energy flux is integrated with other major energy fluxes (growth, reproduction) is critical for any general theory of organismal energetics. Here, we synthesize data from a wide range of fish species and identify patterns of intraspecific variation in energy storage, and use these patterns to formulate a general model of energy allocation between growth, lipid storage and reproduction in fishes. From the compiled data we identified two patterns: (1) energy density increases with body size during the juvenile period, but is invariant with body size within the adult size range for most species, and (2) energy density changes across seasons, with depletion over winter, but increases fastest in periods of transition between favourable and unfavourable conditions for growth (i.e. fall). Based on these patterns we propose DEBlipid, a simple, general model of energy allocation that is closely related to a simplified version of Dynamic Energy Budget theory, DEBkiss. The crux of the model is that assimilated energy is partitioned, with κ fraction of energy allocated to pay maintenance costs first, and the surplus allocated to growth, and 1 - κ fraction of assimilated energy is allocated to accumulating storage lipids during the juvenile phase, and later to reproduction as adults. This mechanism, in addition to capturing the two patterns that motivated the model, was able to predict lipid dynamics in a novel context, the migration of anadromous fish from low-food freshwater to high-food marine environments. Furthermore, the model was used to explain intra and interspecific variation in reproductive output based on patterns of lipid accumulation as juveniles. Our results suggest that many seemingly complex, adaptive energy allocation strategies in response to ontogeny, seasonality and habitat quality can emerge from a simple physiological heuristic.

Influence of larval and juvenile life history on age at first maturity in two tropical amphidromous fish species

“…The energetic storage accumulated by fish before maturation is usually allocated to growth and/or maturation (Martin, Heintz, Danner, & Nisbet, 2017). The dynamic of maturation for both species spans a continuous gradient from spending a long period at sea and maturing quickly after returning to freshwater, to spending less time at sea and waiting for a longer period of time in the river before maturing.…”

“…The dynamic of maturation for both species spans a continuous gradient from spending a long period at sea and maturing quickly after returning to freshwater, to spending less time at sea and waiting for a longer period of time in the river before maturing. The energetic storage accumulated by fish before maturation is usually allocated to growth and/or maturation (Martin, Heintz, Danner, & Nisbet, 2017). Sicyopterus lagocephalus and C. acutipinnis display a large range of PLD; the individuals with a longer PLD generally return to freshwater at larger size .…”

Environmental change effects on life history traits and population dynamics of anadromous fishes

“…The model follows the bioenergetics approach introduced by Kooijman and colleagues (Kooijman & Metz, 1983;Nisbet et al, 2000) in which the energy allocation to somatic and reproductive metabolism are proportional to a fraction and a 1− of the total energy assimilation rate, respectively. More specifically, we adopt the model developed and described in detail by (Martin, Heintz, Danner, & Nisbet, 2017). Below we provide only a concise synopsis of the model.…”

Low marine food levels mitigate high migration costs in anadromous populations

“…Martin et al (Martin, Heintz, Danner, & Nisbet, 2017) offered a mechanistic explanation for the increase in somatic growth at the expense of energy density after a transition from low to high food levels based on a well-established theory of individual energetics (S. a. L. M. Kooijman, 2010) (see supporting information, Energy allocation effects of the habitat switch explained by dynamic energy budget theory). Yet, it is not known how these energetic changes experienced by individuals during the habitat switch interact with the negative effects that low marine food levels and infrastructure building in freshwater streams independently have on individual energetics.…”

“…Effect of step-up change in food on energy reserves and fecundity A: Observed energy density as a function of individual body length in Sacramento RiverChinook salmon before (blue circles) and after the habitat switch (red crosses) (Kruskal-Wallis test p<0.001)(Martin et al, 2017). The right panel summarizes the observations for individuals before and after the habitat switch independent of their length.…”