A bioenergetics approach to modelling tolerance limits under acute thermal stress in farmed finfish

Pinpointing thermal tolerance thresholds for commercially important species, such as aquaculture finfish, under acute and chronic thermal stress is becoming increasingly relevant in the context of climate change. While experimental research, traditionally quantified by the determination of the Critical Thermal Maximum (CTmax), offers valuable insights, it is necessary to further develop appropriate tools to provide predictions and shed light on the underlying mechanisms of thermal tolerance. Bioenergetic models have long been used to study the effects of temperature on fish metabolism under chronic, but rarely under acute, scales. In this study, we present a modelling approach based on the Dynamic Energy Budget (DEB) theory that describes the tolerance limits of fish under acute thermal stress in bioenergetics terms. It adopts the notion of an energy-dependent tolerance to stress and defines acute tolerance limits at the intersection of fundamental energy fluxes, namely those relating to the mobilization of energy and to maintenance costs. To showcase this approach, DEB models for two finfish, the European sea bass (Dicentrarchus labrax) and the meagre (Argyrosomus regius) were used to run acute thermal challenge simulations and study shifts in the critical temperature achieved by the fish. The results suggest that the model can adequately capture the general tolerance patterns observed experimentally for the two species as well as pinpoint the parameters that may influence them. In particular, the simulations showed a positive relation between acclimation temperature and tolerance while the opposite stands for the body size of the fish, with smaller fish achieving higher critical temperatures than their larger counterparts. Also, tolerance limits were affected by the state of internal reserves, with well-fed fish exhibiting higher values. Finally, the potential application of this modelling approach on higher taxonomic scales was evaluated, by running simulations on species belonging to major fish orders. The preliminary results suggest that the method can capture differences among groups that are consistent with literature, suggesting it may be a realistic mechanistic approach for studying thermal tolerance in ectotherms

Multidimensional scaling for animal traits in the context of dynamic energy budget theory

The method of multidimensional scaling (MDS) has long existed, but could only recently be applied to animal traits in the context of dynamic energy budget (DEB) theory. The application became possible because of the following: (i) the Add-my-Pet (AmP) collection of DEB parameters and traits (approximately 280) recently reached 3000 animal species with 45000 data sets of measurements; (ii) we found a natural distance measure for species based on their traits as a side result of our research on parameter estimation in DEB context; and (iii) we developed plotting code for visualization that allows labelling of taxonomic relationships. Traits, here defined as DEB parameters or any function of these parameters, have different dimensions, which hamper application of many popular distance measures since they (implicitly) assume that all traits have the same dimensions. The AmP collection follows the workflow that measured data determine parameters and parameters determine trait values. In this way we could fill up the species traits table completely, which we could not do by using measured values only, as data availability varies considerably between species and is typically poor. The goodness of fit of predictions for all data sets is generally excellent. This paper discusses links between the MDS method and parameter estimation and illustrates the application of MDS for the AmP collection to five taxa, three ectothermic and two endothermic, which we consider to be ‘complete’, in the sense that we expect that it will be difficult to find more species with data in the open literature. This application of MDS shows links between traits and taxonomy that supplements our efforts to find patterns in the co-variation of parameter values. Knowledge about metabolic performance is key to conservation biology, sustainable management and environmental risk assessment, which are seen as interlinked fields

Energetic basis for bird ontogeny and egg-laying applied to the bobwhite quail

Birds build up their reproductive system and undergo major tissue remodeling for each reproductive season. Energetic specifics of this process are still not completely clear, despite the increasing interest. We focused on the bobwhite quail — one of the most intensely studied species due to commercial and conservation interest — to elucidate the energy fluxes associated with reproduction, including the fate of the extra assimilates ingested prior to and during reproduction. We used the standard Dynamic Energy Budget model, which is a mechanistic process-based model capable of fully specifying and predicting the life cycle of the bobwhite quail: its growth, maturation and reproduction. We expanded the standard model with an explicit egg-laying module and formulated and tested two hypotheses for energy allocation of extra assimilates associated with reproduction: Hypothesis 1, that the energy and nutrients are used directly for egg production ; and Hypothesis 2, that the energy is mostly spent fueling the increased metabolic costs incurred by building up and maintaining the reproductive system and, subsequently, by egg-laying itself. Our results suggest that Hypothesis 2 is the more likely energy pathway. Model predictions capture well the whole ontogeny of a generalized northern bobwhite quail and are able to reproduce most of the data variability via variability in (i) egg size, (ii) egg-laying rate and (iii) inter-individual physiological variability modeled via the zoom factor, i.e. assimilation potential. Reliable models with a capacity to predict physiological responses of individuals are relevant not only for experimental setups studying effects of various natural and anthropogenic pressures on the quail as a bird model organism, but also for wild quail management and conservation. The model is, with minor modifications, applicable to other species of interest, making it a most valuable tool in the emerging field of conservation physiology

Is reproduction limiting growth? Comment on "Physics of metabolic organization" by Marko Jusup et al.

WOS:000396960400014International audienceJusup et al. [1] aimed at covering the theoretical foundations of DEB theory and presenting the broadness of its applications for both physicists and biologists and they successfully do so. One of the most striking assumptions of DEB theory for biologists that is, as mentioned by the authors, at odds with an existing body of literature in fisheries sciences [2,3], is the so-called κ-rule. A constant allocation to growth and somatic maintenance throughout ontogeny is indeed at odds with the widely accepted limitation of growth at the onset of sexual maturity by the reproduction process

Body size as emergent property of metabolism

Body size is not an independent variable, but an emergent property: the result of a number of inter-linked eco-physiological processes, like most other quantities that we can measure on organisms. Organisms do not have a particular body size. They are born small and grow to larger sizes during their life trajectory, while changing properties during the growth process in interaction with the environment. The use of maximum body mass of a species as an independent variable when analyzing some other trait, bypasses the important question: What factors control maximum body mass and how do these factors affect the trait of interest? We argue that the old, famous question of why weight-specific respiration decreases for increasing maximum body mass of species was difficult to explain because ecological literature typically treats body size as an independent variable. We demonstrate that Dynamic Energy Budget (DEB) theory could explain this phenomenon by treating body size as an emergent property. The question of why specific respiration decreases with increasing body size then translates to the question of why specific assimilation and/or specific maintenance would vary among species. We discuss the four parameters that control maximum body weight in the DEB theory and study how they co-vary. One of these parameters, the allocation fraction to soma, turned out to follow a beta distribution in the Add-my-Pet collection, with perplexing accuracy. We found the explanation after discovering that the supply stress, i.e. maturity maintenance times squared somatic maintenance divided by cubed assimilation, also followed a (scaled) beta distribution. The allocation fraction can be written as the ratio of somatic maintenance and assimilation for fully-grown individuals and we found that these rates turn out to follow Weibull distributions. Beta-distributions are known to result from appropriate ratios of gamma-distributed variables and we demonstrate that this also applies, to a very good approximation, for ratios of Weibull-distributed variables. We noticed similarities between Weibull distributions and allometric functions and suggest that they fit data well because many factors contribute to the underlying processes. This explains why the allocation fraction, the supply stress and some other ratios of fluxes follow beta distributions. We support our findings with empirical data

Altricial-precocial spectra in animal kingdom

Traditionally, the terms altricial and precocial are used to described the state at birth of birds and mammals. We suggest an explanation for why birds evolved from precocial to altricial and mammals from altricial to precocial. However, the concept is not confined to these groups alone and is an important pattern underlying all animal metabolism. Being able to quantify it, helps position species in multi-dimensional diversity trait space. We here argue that a quantification of the state of development of an individual at birth, in the context of its life cycle, can best be done by comparison with the state at puberty. Two natural quantifiers for the altricial-precocial spectrum exist in the context of the Dynamic Energy Budget (DEB) theory that are applicable to the whole animal kingdom: maturity and maturity density at birth divided by that at puberty. These quantities have been estimated, in combination with other parameters, for some 875 species belonging to all large phyla. We study how taxa are ranked according to both the maturity and maturity density ratios. We conclude that only the maturity ratio qualifies as quantifier for the altricial-precocial spectrum. We were able to retrieve known patterns in altriciality for birds and mammals, while the concept is now applicable to all animal taxa. This new quantifier for animal altriciality can be linked quantitatively to other properties. These linkages are studied by examining how maturity parameters interact with other DEB parameters and implied properties. With the exception of mammals, cartilaginous fish and insects, bigger-bodied species show a clear tendency for to be more frequently altricial. We discuss possible explanations. Age at birth as fraction of age at puberty was found to be proportional to the maturity ratio to the power 1/3; this is consistent with DEB's co-variation rules, but does not follow from them. Maturity at puberty follows a Weibull distribution with great accuracy while that at birth does not, which is consistent with the idea that Weibull distributions can be expected when many factors contribute. We found that species from all taxa with a very high allocation fraction to soma, tend to have low maturities at birth and puberty. We discuss the possible implications of these patterns

Why big-bodied animal species cannot evolve a waste-to-hurry strategy

Reserve capacity quantifies the ability of an animal to smooth out fluctuations in food availability. It is defined as the maximum reserve density, and can be quantified through the application of the Dynamic Energy Budget (DEB) theory. In this study, we analyze inter-specific patterns in DEB parameters of 1041 animal species, focusing on those that control reserve capacity (maximum specific assimilation and energy conductance) and maintenance. The co-variation rules of DEB theory expect that specific somatic maintenance and energy conductance are independent of maximum structural length, with the implication that reserve capacity is proportional to maximum structural length among species and independent of somatic maintenance. We found however that the reserve density increases with somatic maintenance among all large animal taxa in the collection: invertebrates, fish and amphibians, sauropsids and mammals. The waste-to-hurry phenomenon implies that small-bodied species frequently have both a higher specific maintenance and higher specific assimilation (with respect to larger species) allowing them to boost growth and reproduction. If waste-to-hurry strategists would increase both parameters in proportion, maximum structural length would not be affected, reserve capacity would become proportional to somatic maintenance and its relationship with maximum structural length would depend on quantitative details. We did find a positive relationship between reserve capacity and specific somatic maintenance, but the increase (as an average over all taxa) is less than proportional. The reason is that specific assimilation is less than proportional to specific somatic maintenance, the scaling parameter roughly being 0.8, while energy conductance hardly depends on somatic maintenance. The implication is that maximum assimilation is proportional to structural length to the power − 0.7, which explains why the waste-to-hurry strategy is not a viable route for big-bodied species: they would need more assimilates than small-bodied ones, not less. We discuss applications of these findings in the context of parameter estimation. As a side-result we also found that birds have a higher specific somatic maintenance and also a higher (mean) energy conductance, compared to other sauropsids at the same body temperature. The first is to be expected because they are demand species, the latter might be an adaptation to flight: reserve density increases for decreasing energy conductance, while it contributes to weight