The consequences of sea lamprey parasitism on lake trout energy budgets.

Parasitism is an energetically costly event for host species. Dynamic energy budget (DEB) theory describes the metabolic dynamics of an individual organism through its lifetime. Models derived from DEB theory specify how an organism converts food to reserves (maintenance-free energy available for metabolism) and allocates mobilized reserves to maintenance, growth (increase of structural body mass) and maturation or reproduction. DEB models thus provide a useful approach to describe the consequences of parasitism for host species. We developed a DEB model for siscowet lake trout and modeled the impact of sea lamprey parasitism on growth and reproduction using data collected from studies documenting the long-term effects following a non-lethal sea lamprey attack. The model was parameterized to reflect the changes in allocation of energy towards growth and reproduction observed in lake trout following sea lamprey parasitism and includes an estradiol module that describes the conversion of reproductive reserves to ovarian mass based on estradiol concentration. In our DEB model, parasitism increased somatic and maturity maintenance costs, reduced estradiol and decreased the estradiol-mediated conversion efficiency of reproductive reserves to ovarian mass. Muscle lipid composition of lake trout influenced energy mobilization from the reserve (efficiency of converting reserves allocated to reproduction into eggs) and reproductive efficiency. These model changes accurately reflect observed empirical changes to ovarian mass and growth. This model provides a plausible explanation of the energetic mechanisms that lead to skipped spawning following sea lamprey parasitism and could be used in population models to explore sublethal impacts of sea lamprey parasitism and other stressors on population dynamics.

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.

Metabolic scope, performance and tolerance of juvenile European sea bass Dicentrarchus labrax upon acclimation to high temperatures.

European sea bass is a species of great commercial value for fisheries and aquaculture. Rising temperatures may jeopardize the performance and survival of the species across its distribution and farming range, making the investigation of its thermal responses highly relevant. In this article, the metabolic scope, performance, and tolerance of juvenile E. sea bass reared under three high water temperatures (24, 28, 33°C), for a period of three months was evaluated via analysis of selected growth performance and physiological indicators. Effects on molecular, hormonal, and biochemical variables were analyzed along with effects of acclimation temperature on the metabolic rate and Critical Thermal maximum (CTmax). Despite signs of thermal stress at 28°C indicated by high plasma cortisol and lactate levels as well as the upregulation of genes coding for Heat Shock Proteins (HSP), E. sea bass can maintain high performance at that temperature which is encouraging for the species culture in the context of a warming ocean. Critical survivability thresholds appear sharply close to 33°C, where the aerobic capacity declines and the overall performance diminishes. European sea bass demonstrates appreciable capacity to cope with acute thermal stress exhibiting CTmax as high as 40°C for fish acclimated at high temperatures, which may indicate resilience to future heatwaves events.

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.

Thermal tolerance, metabolic scope and performance of meagre, Argyrosomus regius, reared under high water temperatures.

This article reports on the thermal tolerance, metabolic capacity and performance of juvenile meagre (Argyrosomus regius) reared under three high water temperatures (24, 29 and 34 °C) for three months. The analysis includes the thermal effects on the growth performance, metabolism and physiology of meagre, including a range of molecular, haematological, metabolic, enzymatic and hormonal indicators, as well as the effects on the proximate composition and ingestion speed. Meagre performs best between 24 and 29 °C while the temperature of 34 °C is very close to the upper end of its temperature tolerance range. At 34 °C meagre exhibits a poor growth performance and physiological status, increased blood clotting, high mortality rates and a diminished capacity for aerobic metabolism, as indicated by its low aerobic scope (129 mg kg-1 h-1). Meagre may tolerate short exposures to high temperatures after sufficient acclimation (Critical thermal maximum of 37.5 °C after acclimation to 29 °C) but its overall performance declines under prolonged exposure, suggesting that this emerging aquaculture species may be vulnerable to global warming. Our work corroborates previous findings on the thermal preferences of the species, identifies critical biological thresholds, and provides insights into the effects of prolonged exposure to high temperature regimes.

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.

REGULATION OF REPRODUCTIVE PROCESSES WITH DYNAMIC ENERGY BUDGETS.

1. The simple bioenergetic models in the family of Dynamic Energy Budget (DEB) consist of a small number of state equations quantifying universal processes, such as feeding, maintenance, development, reproduction and growth. Linking these organismal level processes to underlying suborganismal mechanisms at the molecular, cellular and organ level constitutes a major challenge for predictive ecological risk assessments. 2. Motivated by the need for process-based models to evaluate the impact of endocrine disruptors on ecologically relevant endpoints, this paper develops and evaluates two general modeling modules describing demand-driven feedback mechanisms exerted by gonads on the allocation of resources to production of reproductive matter within the DEB modeling framework. 3. These modules describe iteroparous, semelparous and batch-mode reproductive strategies. The modules have a generic form with both positive and negative feedback components; species and sex specific attributes of endocrine regulation can be added without changing the core of the modules. 4. We demonstrate that these modules successfully describe time-resolved measurements of wet weight of body, ovaries and liver, egg diameter and plasma content of vitellogenin and estradiol in rainbow trout (Oncorynchus mykiss) by fitting these models to published and new data, which require the estimation of less than two parameters per data type. 5. We illustrate the general applicability of the concept of demand-driven allocation of resources to reproduction as worked out in this paper by evaluating one of the modules with data on growth and seed production of an annual plant, the common bean (Phaseolis vulgaris).

Water temperature modifies the acute stress response of European sea bass, Dicentrarchus labrax L. (1758).

The effects of water temperature (15, 20 and 25 °C) on the stress response of European sea bass, Dicentrarchus labrax, were studied. Blood and water samples were collected prior and at 0.5, 1, 2, 4 and 8 h post-stress for hormonal and biochemical analysis. Water temperature affected the resting concentrations of all stress indicators examined, as well as their response after stress, apart from lactate which response was unaffected by temperature. Cortisol showed the response with the highest outcome at 15 °C, and the fastest at 25 °C. Cortisol release rate in the water was also faster and of higher magnitude at higher temperatures. Glucose had both the fastest and higher in magnitude response at 25 °C, while lactate responded similarly in all temperatures tested. Finally, osmolality changed only at the highest temperature. These results suggest that temperature should be taken into consideration when evaluating the resting levels of stress indicators of European sea bass in laboratory, rearing and field conditions. Additionally, the present results show that temperature affects the stress response, suggesting that fish can differ in their susceptibility to stress depending on the acclimatization temperature. Moreover, it was shown that cortisol release rate in the water, a non-invasive stress indicator, can depict the effects of temperature on cortisol stress response.

Incorporating Suborganismal Processes into Dynamic Energy Budget Models for Ecological Risk Assessment.

A working group at the National Institute for Mathematical and Biological Synthesis (NIMBioS) explored the feasibility of integrating 2 complementary approaches relevant to ecological risk assessment. Adverse outcome pathway (AOP) models provide "bottom-up" mechanisms to predict specific toxicological effects that could affect an individual's ability to grow, reproduce, and/or survive from a molecular initiating event. Dynamic energy budget (DEB) models offer a "top-down" approach that reverse engineers stressor effects on growth, reproduction, and/or survival into modular characterizations related to the acquisition and processing of energy resources. Thus, AOP models quantify linkages between measurable molecular, cellular, or organ-level events, but they do not offer an explicit route to integratively characterize stressor effects at higher levels of organization. While DEB models provide the inherent basis to link effects on individuals to those at the population and ecosystem levels, their use of abstract variables obscures mechanistic connections to suborganismal biology. To take advantage of both approaches, we developed a conceptual model to link DEB and AOP models by interpreting AOP key events as measures of damage-inducing processes affecting DEB variables and rates. We report on the type and structure of data that are generated for AOP models that may also be useful for DEB models. We also report on case studies under development that merge information collected for AOPs with DEB models and highlight some of the challenges. Finally, we discuss how the linkage of these 2 approaches can improve ecological risk assessment, with possibilities for progress in predicting population responses to toxicant exposures within realistic environments. Integr Environ Assess Manag 2018;14:615-624. © 2018 SETAC.

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.

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.

Resource allocation to reproduction in animals.

The standard Dynamic Energy Budget (DEB) model assumes that a fraction κ of mobilised reserve 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). All DEB parameters have been estimated for 276 animal species from most large phyla and all chordate classes. The goodness of fit is generally excellent. We compared the estimated values of κ with those that would maximise reproduction in fully grown adults with abundant food. Only 13% of these species show a reproduction rate close to the maximum possible (assuming that κ can be controlled), another 4% have κ lower than the optimal value, and 83% have κ higher than the optimal value. Strong empirical support hence exists for the conclusion that reproduction is generally not maximised. We also compared the parameters of the wild chicken with those of races selected for meat and egg production and found that the latter indeed maximise reproduction in terms of κ, while surface-specific assimilation was not affected by selection. We suggest that small values of κ relate to the down-regulation of maximum body size, and large values to the down-regulation of reproduction. We briefly discuss the ecological context for these findings.

Modeling the dynamic modulation of light energy in photosynthetic algae.

An integrated cell-based dynamic mathematical model that take into account the role of the photon absorbing process, the partition of excitation energy, and the photoinactivation and repair of photosynthetic units, under variable light and dissolved inorganic carbon (DIC) availability is proposed. The modeling of the photon energy absorption and the energy dissipation is based on the photoadaptive changes of the underlying mechanisms. The partition of the excitation energy is based on the relative availability of light and DIC to the cell. The modeling of the photoinactivation process is based on the common aspect that it occurs under any light intensity and the modeling of the repair process is based on the evidence that it is controlled by chloroplast and nuclear-encoded enzymes. The present model links the absorption of photons and the partitioning of excitation energy to the linear electron flow and other quenchers with chlorophyll fluorescence emission parameters, and the number of the functional photosynthetic units with the photosynthetic oxygen production rate. The energy allocation to the LEF increases as DIC availability increases and/or light intensity decreases. The rate of rejected energy increases with light intensity and with DIC availability. The resulting rate coefficient of photoinactivation increases as light intensity and/or as DIC concentration increases. We test the model against chlorophyll fluorescence induction and photosynthetic oxygen production rate measurements, obtained from cultures of the unicellular green alga Scenedesmus obliquus, and find a very close quantitative and qualitative correspondence between predictions and data.

Temperature tolerance and energetics: a dynamic energy budget-based comparison of North Atlantic marine species.

Temperature tolerance and sensitivity were examined for some North Atlantic marine species and linked to their energetics in terms of species-specific parameters described by dynamic energy budget (DEB) theory. There was a general lack of basic information on temperature tolerance and sensitivity for many species. Available data indicated that the ranges in tolerable temperatures were positively related to optimal growth temperatures. However, no clear relationships with temperature sensitivity were established and no clear differences between pelagic and demersal species were observed. The analysis was complicated by the fact that for pelagic species, experimental data were completely absent and even for well-studied species, information was incomplete and sometimes contradictory. Nevertheless, differences in life-history strategies were clearly reflected in parameter differences between related species. Two approaches were used in the estimation of DEB parameters: one based on the assumption that reserve hardly contributes to physical volume; the other does not make this assumption, but relies on body-size scaling relationships, using parameter values of a generalized animal as pseudo-data. Temperature tolerance and sensitivity seemed to be linked with the energetics of a species. In terms of growth, relatively high temperature optima, sensitivity and/or tolerance were related to lower relative assimilation rates as well as lower maintenance costs. Making the step from limited observations to underlying mechanisms is complicated and extrapolations should be carefully interpreted. Special attention should be devoted to the estimation of parameters using body-size scaling relationships predicted by the DEB theory.

Life history implications of allocation to growth versus reproduction in dynamic energy budgets.

We compare the implications of determinate vs. indeterminate growth of a parthenogenetic iteroparous ectotherm at constant food density in the context of the dynamic energy budget theory, which specifies the tight links between life history traits, such as feeding, aging, growth and reproduction. We do a comparative analysis using, as measure of fitness, the life span reproduction, the population growth rate, and the conversion efficiency of food to biomass. When extrinsic mortality is constant, indeterminate growth cannot maximize fitness if measured by the population growth rate or the conversion efficiency, except when mortality is low, in which case both types of animals are similar. If the fitness measure is life span reproduction, indeterminate growth maximizes fitness even with constant mortality, provided it is not very high. When mortality decreases with size, indeterminate growth maximizes fitness for almost all measures of fitness. Finally, we suggest an evolutionary link between allocation strategies and expected life span. In populations of long living species, each type of animal can establish in the population of the other. In populations of short living species, determinate growers can invade, and displace, a population of indeterminate ones. However, when the mortality risk of organisms with small size is much higher than those of large size, indeterminate growers can be superior.