An annual profile of the impacts of simulated oil spills on the Northeast Arctic cod and haddock fisheries.

We simulate the combined natural and pollutant-induced survival of early life stages of NEA cod and haddock, and the impact on the adult populations in response to the time of a major oil spill in a single year. Our simulations reveal how dynamic ocean processes, controlling both oil transport and fate and the frequency of interactions of oil with drifting fish eggs and larvae, mediate the magnitude of population losses due to an oil spill. The largest impacts on fish early life stages occurred for spills initiated in Feb-Mar, concomitant with the initial rise in marine productivity and the earliest phase of the spawning season. The reproductive health of the adult fish populations was maintained in all scenarios. The study demonstrates the application of a simulation system that provides managers with information for the planning of development activities and for the protection of fisheries resources from potential impacts.

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.

The comparative energetics of the carnivorans and pangolins.

Patterns in eco-physiological traits of pangolins and carnivorans are studied, which are functions of underlying Dynamic Energy Budget parameters. The data, parameter values and traits are accessible in the open access Add-my-Pet collection, which currently contains 7 out of 8 species of pangolins and 131 of the extant 276 species of carnivorans and 653 of the extant 6400 species of mammals. Paucity of data and species not included reflect the actual state of knowledge: many species are endangered and/or little measured data is readily available. Although musteloids and pinnipeds form the clade Mustelida, they appear at opposite ends of the classical multidimensional scaling diagram, using 14 traits on all mammals. Yet, in general, the energetic parameters bear a strong taxonomic signal. The weight at birth is proportional to ultimate weight: small for carnivorans and pangolins; extra small for bears; and much larger, but typical for mammals, for the pinnipeds and sea otters. How respiration scales with size is taxon-specific, and we discuss how the body-size scaling of reserve capacity interferes with the waste-to-hurry pattern. Despite their high allocation to soma, the life time cumulated mass of neonates of pangolins and carnivorans equals their own ultimate weight; pinnipeds allocate more to maturation and reproduction. Applying models to support conservation efforts entails needing realistic parameter values. This study contributes to the emerging field of assessing the realism of parameters in biological and evolutionary context.

The comparative energetics of the ray-finned fish in an evolutionary context.

To address challenges in management and conservation of fishes and fisheries it is essential to understand their life histories and energetics. The Add-my-Pet (AmP) collection of data on energetics and Dynamic Energy Budget (DEB) parameters currently contains 1150 of the 40000 extant species of fish. It gives 250-280 traits per species, depending on the model type that was applied, such as maximum reserve capacity, lifespan, specific respiration and precociality index, based on which the ray-finned fish (Actinopterygii) was compared with the four other fish classes (Cyclostomata, Chondrichthyes, Actinistia, Dipnoi) and the Tetrapoda. The Actinopterygii are the only vertebrate class that shows metabolic acceleration, and clearly so in only three sub-clades. Different from chondrichthyans, quite a few species follow the waste-to-hurry strategy, especially small bodied freshwater fish such as tropical annual killifish, but also in small minnows and darters in continental climates. We briefly discuss links between waste-to-hurry, which is associated with a large specific somatic maintenance, and sensitivity for pesticides. We discuss why this interferes with the physical co-variation between maximum reserve capacity and ultimate structural length or weight and explains why maximum reserve capacity increases with body length in chondrichthyans, but not in actinopterygians. Reserve capacity has relevance, e.g. mass-specific maintenance, starvation and the kinetics of lipophyllic compounds (such as pesticides), since reserve is relatively rich in lipids in fish. Also, unlike chondrichthyans, the size at birth is very small and not linked to ultimate size; we discuss the implications. Actinopterygians allocate more to soma, compared with chondrichthyans; the latter allocate more to maturity or reproduction. Actinopterygians, Actinistia and Dipnoi are near the supply-end of the supply-demand spectrum, while chondrichthyans clearly show demand properties.

The role of Dynamic Energy Budgets in conservation physiology.

The contribution of knowledge, concepts and perspectives from physiological ecology to conservation decision-making has become critical for understanding and acting upon threats to the persistence of sensitive species. Here we review applications of dynamic energy budget (DEB) theory to conservation issues and discuss how this theory for metabolic organization of all life on earth (from bacteria to whales) is well equipped to support current and future investigations in conservation research. DEB theory was first invented in 1979 in an applied institution for environmental quality assessment and mitigation. The theory has since undergone extensive development and applications. An increasing number of studies using DEB modelling have provided valuable insights and predictions in areas that pertain to conservation such as species distribution, evolutionary biology, toxicological impacts and ecosystem management. We discuss why DEB theory, through its mechanistic nature, its universality and the wide range of outcomes it can provide represents a valuable tool to tackle some of the current and future challenges linked to maintaining biodiversity, ensuring species survival, ecotoxicology, setting water and soil quality standards and restoring ecosystem structure and functioning in a changing environment under the pressure of anthropogenic driven changes.

Distribution and ecology of polar cod (Boreogadus saida) in the eastern Barents Sea: A review of historical literature.

The polar cod (Boreogadus saida) has a circumpolar distribution and is the most abundant planktivorous fish in the Arctic. Declining sea-ice coverage impacts polar cod directly and also facilitates expansion of human activities in the region leading to increasing anthropogenic pressures on biota. Here we summarize current data and knowledge on polar cod from the Russian sector of the Barents Sea and discuss knowledge needs for the management of polar cod under changing environmental conditions and anthropogenic impacts. We review 36 Russian historical (1935 - 2020) sources of data and knowledge largely unknown to western researchers, in addition to sources already published in the English language. This effort allowed for digitalization and visualization of 69 separate datasets on polar cod ecology, including maturation, fertility, feeding intensity, diet, lipid content, length-weight relationships and seasonal variation in larval size. Our review suggests that polar cod abundances are particularly large in the eastern Barents Sea and adjacent waters. Here, we identify and discuss key knowledge gaps. The review of polar cod in the eastern Barents Sea revealed 1) major variation in the timing and area of polar cod spawning, 2) uncertainty as to what degree the polar cod is dependent on sea ice, 3) deficient knowledge of juvenile (e.g., 0-group) distributions, particularly in the north-eastern Barents Sea, 4) deficient knowledge of the species' genetic structure and spatio-temporal distributions, and 5) insufficient understanding as to whether ongoing environmental change may induce phenological changes affecting the availability of potential food items for polar cod larvae and their match in space and time. Filling these knowledge gaps would provide an important step towards the reliable knowledge base needed in order to perform well-founded management and impact assessment under environmental changes and increasing anthropogenic impacts.

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.

Exploring inter-species sensitivity to a model hydrocarbon, 2-Methylnaphtalene, using a process-based model.

We compared inter-species sensitivity to a model narcotic compound, 2-Methylnaphthalene, to test if taxonomical relatedness, feeding guilds, and trophic level govern species sensitivities on species distributed in different regions. We fitted a toxicokinetic-toxicodynamic model to survival patterns over time for 26 species using new and raw data from the literature. Species sensitivity distributions provided little insight into understanding patterns in inter-species sensitivity. The range of no-effect concentrations (NEC) obtained for 26 species showed little variation (mean 0.0081 mM; SD 0.009). Results suggest that the NEC alone does not explain the complexity of the species tolerances. The dominant rate constant and the derived time to observe an effect (t0), a function of concentration, might provide the means for depicting patterns in sensitivity and better ecotoxicological testing. When comparing the t0 functions, we observed that Arctic species have shorter time frames to start showing effects. Mollusks and second trophic level species took longer to build up a lethal body burden than the rest. Coupling our results with fate and transport models would allow forecasting narcotic compounds toxicity in time and thus improve risk assessment.

The AmP project: Comparing species on the basis of dynamic energy budget parameters.

We developed new methods for parameter estimation-in-context and, with the help of 125 authors, built the AmP (Add-my-Pet) database of Dynamic Energy Budget (DEB) models, parameters and referenced underlying data for animals, where each species constitutes one database entry. The combination of DEB parameters covers all aspects of energetics throughout the full organism's life cycle, from the start of embryo development to death by aging. The species-specific parameter values capture biodiversity and can now, for the first time, be compared between animals species. An important insight brought by the AmP project is the classification of animal energetics according to a family of related DEB models that is structured on the basis of the mode of metabolic acceleration, which links up with the development of larval stages. We discuss the evolution of metabolism in this context, among animals in general, and ray-finned fish, mollusks and crustaceans in particular. New DEBtool code for estimating DEB parameters from data has been written. AmPtool code for analyzing patterns in parameter values has also been created. A new web-interface supports multiple ways to visualize data, parameters, and implied properties from the entire collection as well as on an entry by entry basis. The DEB models proved to fit data well, the median relative error is only 0.07, for the 1035 animal species at 2018/03/12, including some extinct ones, from all large phyla and all chordate orders, spanning a range of body masses of 16 orders of magnitude. This study is a first step to include evolutionary aspects into parameter estimation, allowing to infer properties of species for which very little is known.

Dynamic energy budget models in ecological risk assessment: From principles to applications.

In ecological risk assessment of chemicals, hazard identification and hazard characterisation are most often based on ecotoxicological tests and expressed as summary statistics such as No Observed Effect Concentrations or Lethal Concentration values and No Effect Concentrations. Considerable research is currently ongoing to further improve methodologies to take into account toxico kinetic aspects in toxicological assessments, extrapolations of toxic effects observed on individuals to population effects and combined effects of multiple chemicals effects. In this context, the principles of the Dynamic Energy Budget (DEB), namely the conserved allocation of energy to different life-supporting processes in a wide variety of different species, have been applied successfully to the development of a number of DEB models. DEB models allow the incorporation of effects on growth, reproduction and survival within one consistent framework. This review aims to discuss the principles of the DEB theory together with available DEB models, databases available and applications in ecological risk assessment of chemicals for a wide range of species and taxa. Future perspectives are also discussed with particular emphasis on ongoing research efforts to develop DEB models as open source tools to further support the research and regulatory community to integrate quantitative biology in ecotoxicological risk assessment.

Assessing impacts of simulated oil spills on the Northeast Arctic cod fishery.

We simulate oil spills of 1500 and 4500m3/day lasting 14, 45, and 90days in the spawning grounds of the commercial fish species, Northeast Arctic cod. Modeling the life history of individual fish eggs and larvae, we predict deviations from the historical pattern of recruitment to the adult population due to toxic oil exposures. Reductions in survival for pelagic stages of cod were 0-10%, up to a maximum of 43%. These reductions resulted in a decrease in adult cod biomass of <3% for most scenarios, up to a maximum of 12%. In all simulations, the adult population remained at full reproductive potential with a sufficient number of juveniles surviving to replenish the population. The diverse age distribution helps protect the adult cod population from reductions in a single year's recruitment after a major oil spill. These results provide insights to assist in managing oil spill impacts on fisheries.

Modelling survival: exposure pattern, species sensitivity and uncertainty.

The General Unified Threshold model for Survival (GUTS) integrates previously published toxicokinetic-toxicodynamic models and estimates survival with explicitly defined assumptions. Importantly, GUTS accounts for time-variable exposure to the stressor. We performed three studies to test the ability of GUTS to predict survival of aquatic organisms across different pesticide exposure patterns, time scales and species. Firstly, using synthetic data, we identified experimental data requirements which allow for the estimation of all parameters of the GUTS proper model. Secondly, we assessed how well GUTS, calibrated with short-term survival data of Gammarus pulex exposed to four pesticides, can forecast effects of longer-term pulsed exposures. Thirdly, we tested the ability of GUTS to estimate 14-day median effect concentrations of malathion for a range of species and use these estimates to build species sensitivity distributions for different exposure patterns. We find that GUTS adequately predicts survival across exposure patterns that vary over time. When toxicity is assessed for time-variable concentrations species may differ in their responses depending on the exposure profile. This can result in different species sensitivity rankings and safe levels. The interplay of exposure pattern and species sensitivity deserves systematic investigation in order to better understand how organisms respond to stress, including humans.

An individual-based model of zebrafish population dynamics accounting for energy dynamics.

Developing population dynamics models for zebrafish is crucial in order to extrapolate from toxicity data measured at the organism level to biological levels relevant to support and enhance ecological risk assessment. To achieve this, a dynamic energy budget for individual zebrafish (DEB model) was coupled to an individual based model of zebrafish population dynamics (IBM model). Next, we fitted the DEB model to new experimental data on zebrafish growth and reproduction thus improving existing models. We further analysed the DEB-model and DEB-IBM using a sensitivity analysis. Finally, the predictions of the DEB-IBM were compared to existing observations on natural zebrafish populations and the predicted population dynamics are realistic. While our zebrafish DEB-IBM model can still be improved by acquiring new experimental data on the most uncertain processes (e.g. survival or feeding), it can already serve to predict the impact of compounds at the population level.

Effects of chronic exposure to environmentally relevant concentrations of waterborne depleted uranium on the digestive tract of zebrafish, Danio rerio.

Uranium is a naturally occurring element, but activities linked to the nuclear fuel cycle can increase background levels in the surrounding waters. For this reason it is important to understand how this affects organisms residing in the water column. The objective of this study was to assess histopathological effects of uranium on the gut wall of a widely used model organism: zebrafish, Danio rerio. To this end we exposed zebrafish to 84 and 420 nM depleted uranium for over a month and then examined the histology of intestines of exposed individuals compared to controls. The gut wall of individuals exposed to 84 and 420 nM of uranium had large regions of degraded mucosa. Using transmission electron microscopy (TEM) coupled to energy-dispersive X-ray spectroscopy microanalysis (EDX) we found that uranium induced a decrease in the amount of calcium containing mitochondrial matrix granules per mitochondria. This is suggestive of perturbations to cellular metabolism and more specifically to cellular calcium homeostasis. TEM-EDX of the gut wall tissue further showed that some uranium was internalized in the nucleus of epithelial cells in the 420 nM treatment. Fluorescent in situ hybridization using specific probes to detect all eubacteria was performed on frozen sections of 6 individual fish in the 84 nM and 420 nM treatments. Bacterial colonization of the gut of individuals in the 420 nM seemed to differ from that of the controls and 84 nM individuals. We suggest that host-microbiota interactions are potentially disturbed in response to uranium induced stress. The damage induced by waterborne uranium to the gut wall did not seem to depend on the concentration of uranium in the media. We measure whole body residues of uranium at the end of the experiment and compute the mean dose rate absorbed for each condition. We discuss why effects might be uncoupled from external concentration and highlight that it is not so much the external concentration but the dynamics of internalization which are important players in the game.

The bijection from data to parameter space with the standard DEB model quantifies the supply-demand spectrum.

The standard Dynamic Energy Budget (DEB) model assumes that food is converted to reserve and a fraction κ of mobilised reserve of an individual is allocated to somatic maintenance plus growth, while the rest is allocated to maturity maintenance plus maturation (in embryos and juveniles) or reproduction (in adults). The add_my_pet collection of over 300 animal species from most larger phyla, and all chordate classes, shows that this model fits energy data very well. Nine parameters determine nine data points at abundant food: dry/wet weight ratio, age at birth, puberty, death, weight at birth, metamorphosis, puberty, ultimate weight and ultimate reproduction rate. We demonstrate that, given a few other parameters, these nine data points also determine the nine parameters uniquely that are independent of food availability: maturity at birth, metamorphosis and puberty, specific assimilation, somatic maintenance and costs for structure, allocation fraction of mobilised reserve to soma, energy conductance, and ageing acceleration. We provide an efficient algorithm for mapping between data and parameter space in both directions and found expressions for the boundaries of the parameter and data spaces. One of them quantifies the position of species in the supply-demand spectrum, which reflects the internalisation of energetic control. We link eco-physiological properties of species to their position in this spectrum and discuss it in the context of homeostasis. Invertebrates and ray-finned fish turn out to be close to the supply end of the spectrum, while other vertebrates, including cartilaginous fish, have stronger demand tendencies. We explain why birds and mammals up-regulate metabolism during reproduction. We study some properties of the bijection using elasticity coefficients. The properties have applications in parameter estimation and in the analysis of evolutionary constraints on parameter values; the relationship between DEB parameters and data has similarities to that between genotype and phenotype.

The trade-off between maturation and growth during accelerated development in frogs.

Developmental energetics are crucial to a species' life history and ecology but are poorly understood from a mechanistic perspective. Traditional energy and mass budgeting does not distinguish between costs of growth and maturation, making it difficult to account for accelerated development. We apply a metabolic theory that uniquely considers maturation costs (Dynamic Energy Budget theory, DEB) to interpret empirical data on the energetics of accelerated development in amphibians. We measured energy use until metamorphosis in two related frogs, Crinia georgiana and Pseudophryne bibronii. Mass and energy content of fresh ova were comparable between the species. However, development to metamorphosis was 1.7 times faster in C. georgiana while P. bibronii produced nine times the dry biomass at metamorphosis and had lower mass-specific oxygen requirements. DEB theory explained these patterns through differences in ontogenetic energy allocation to maturation. P. bibronii partitioned energy in the same (constant) way throughout development whereas C. georgiana increased the fraction of energy allocated to maturation over growth between hatching and the onset of feeding. DEB parameter estimation for additional, direct-developing taxa suggests that a change in energy allocation during development may result from a selective pressure to increase development rate, and not as a result of development mode.

Effects of uranium on the metabolism of zebrafish, Danio rerio.

The increasing demand for nuclear energy results in heightened levels of uranium (U) in aquatic systems which present a potential health hazard to resident organisms. The aim of this study was to mechanistically assess how chronic exposure to environmentally relevant concentrations of U perturbs the complex interplay between feeding, growth, maintenance, maturation and reproduction throughout the life-cycle of an individual. To this end we analysed literature-based and original zebrafish toxicity data within a same mass and energy balancing conceptual framework. U was found to increase somatic maintenance leading to inhibition of spawning as well as increase hazard rate and costs for growth during the early life stages. The fish's initial conditions and elimination through reproduction greatly affected toxico-kinetics and effects. We demonstrate that growth and reproduction should be measured on specific individuals since mean values were hardly interpretable. The mean food level differed between experiments, conditions and individuals. This last 'detail' contributed substantially to the observed variability by its combined effect on metabolism, toxic effects and toxico-kinetics. The significance of this work is that we address exactly how these issues are related and derive conclusions which are independent of experimental protocol and coherent with a very large body of literature on zebrafish eco-physiology.