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.

Investigating the Ability of Growth Models to Predict In Situ Vibrio spp. Abundances.

Vibrio spp. have an important role in biogeochemical cycles; some species are disease agents for aquatic animals and/or humans. Predicting population dynamics of Vibrio spp. in natural environments is crucial to predicting how the future conditions will affect the dynamics of these bacteria. The majority of existing Vibrio spp. population growth models were developed in controlled environments, and their applicability to natural environments is unknown. We collected all available functional models from the literature, and distilled them into 28 variants using unified nomenclature. Next, we assessed their ability to predict Vibrio spp. abundance using two new and five already published longitudinal datasets on Vibrio abundance in four different habitat types. Results demonstrate that, while the models were able to predict Vibrio spp. abundance to an extent, the predictions were not reliable. Models often underperformed, especially in environments under significant anthropogenic influence such as aquaculture and urban coastal habitats. We discuss implications and limitations of our analysis, and suggest research priorities; in particular, we advocate for measuring and modeling organic matter.

The comparative energetics of the turtles and crocodiles.

The Add-my-Pet collection of data on energetics and Dynamic Energy Budget parameters currently contains 92 species of turtles and 23 species of crocodiles. We discuss patterns of eco-physiological traits of turtles and crocodiles, as functions of parameter values, and compare them with other taxa. Turtles and crocodiles accurately match the general rule that the life-time cumulated neonate mass production equals ultimate weight. The weight at birth for reptiles scales with ultimate weight to the power 0.6. The scaling exponent is between that of amphibians and birds, while that for mammals is close to 1. We explain why this points to limitations imposed by embryonic respiration, the role of water stress and the accumulation of nitrogen waste during the embryo stage. Weight at puberty is proportional to ultimate weight, and is the largest for crocodiles, followed by that of turtles. These facts explain why the precociality coefficient, s H bp -approximated by the ratio of weight at birth and weight at puberty at abundant food-decreases with ultimate weight. It is the smallest for crocodiles because of their large size and is smaller for turtles than for lizards and snakes. The sea turtles have a smaller s H bp than the rest of the turtles, linked to their large size and small offspring size. We link their small weight and age at birth to reducing risks on the beach. The maximum reserve capacity in both turtles and crocodiles clearly decreases with the precociality coefficient. This relationship has not been found that clearly in other taxa, not even in other reptiles, with the exception of the chondrichthyans. Among reptiles, crocodiles and sea turtles have a relatively large assimilation rate and a large reserve capacity.

Physiological performance of native and invasive crayfish species in a changing environment: insights from Dynamic Energy Budget models.

Crayfish are keystone species important for maintaining healthy freshwater ecosystems. Crayfish species native to Europe, such as Astacus astacus and Austropotamobius torrentium, are facing decline and are increasingly endangered by changing climate and invasions of non-native crayfish, such as Pacifastacus leniusculus and Procambarus virginalis. The success of these invasions largely depends on differences in ontogeny between the native species and the invaders and how changes in the environment will affect the ontogeny. Dynamic Energy Budget (DEB) models can be used to investigate such differences because the models capture dependence of metabolism, and therefore ontogeny, on environmental conditions. We develop DEB models for all four species and investigate key elements of ontogeny and metabolism affecting interspecific competition. We then use the DEB models to predict individual growth and reproduction in current and new conditions that are expected to arise from climate change. Although observations suggest that P. leniusculus poses the major threat to native species, our analysis identifies P. virginalis, in spite of its smaller size, as the superior competitor by a large margin-at least when considering metabolism and ontogeny. Our simulations show that climate change is set to increase the competitive edge of P. virginalis even further. Given the prospects of P. virginalis dominance, especially when considering that it is able to withstand and spread at least some crayfish plague strains that severely affect native species, additional research into P. virginalis is necessary.

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.

Quantifying impacts of plastic debris on marine wildlife identifies ecological breakpoints.

Quantifying sublethal effects of plastics ingestion on marine wildlife is difficult, but key to understanding the ontogeny and population dynamics of affected species. We developed a method that overcomes the difficulties by modelling individual ontogeny under reduced energy intake and expenditure caused by debris ingestion. The predicted ontogeny is combined with a population dynamics model to identify ecological breakpoints: cessation of reproduction or negative population growth. Exemplifying this approach on loggerhead turtles, we find that between 3% and 25% of plastics in digestive contents causes a 2.5-20% reduction in perceived food abundance and total available energy, resulting in a 10-15% lower condition index and 10% to 88% lower total seasonal reproductive output compared to unaffected turtles. The reported plastics ingestion is insufficient to impede sexual maturation, but population declines are possible. The method is readily applicable to other species impacted by debris ingestion.

Predicting perceived level of disturbance of visitors due to crowding in protected areas.

Managing the disturbance of visitors due to crowding is an important management task in protected areas with high use levels. To achieve this, managers need to know how the use level affects the perceived disturbance due to crowding. Here we present a method to predict the level of disturbance as a function of use level measured by number of visitors. In contrast to the visual approach where subjects are asked to evaluate acceptability of use levels from manipulated images of scenery, our approach uses data gathered from actual experiences: actual (measured) use levels and concurrent on-site data on levels of disturbance experienced by visitors. Using the example of Nature Park Telascica, we show how these data can be acquired with limited resources (a smart-phone and short, time-stamped questionnaires), and demonstrate the subsequent analysis and model fitting. The resulting model estimates the probability that a visitor experiencing a given use level will report certain level of disturbance. We suggest a way of using the probability density functions to define an inherent limit of acceptable disturbance (LAD) due to crowding; the LAD can also be set to a desired value by management. Regardless of the definition, LAD can be used to determine the maximum acceptable use level as dictated by crowding considerations. The method gives predictions consistent with previous literature and can be used even when data are collected at low use levels.

Inferring physiological energetics of loggerhead turtle (Caretta caretta) from existing data using a general metabolic theory.

Loggerhead turtle is an endangered sea turtle species with a migratory lifestyle and worldwide distribution, experiencing markedly different habitats throughout its lifetime. Environmental conditions, especially food availability and temperature, constrain the acquisition and the use of available energy, thus affecting physiological processes such as growth, maturation, and reproduction. These physiological processes at the population level determine survival, fecundity, and ultimately the population growth rate-a key indicator of the success of conservation efforts. As a first step towards the comprehensive understanding of how environment shapes the physiology and the life cycle of a loggerhead turtle, we constructed a full life cycle model based on the principles of energy acquisition and utilization embedded in the Dynamic Energy Budget (DEB) theory. We adapted the standard DEB model using data from published and unpublished sources to obtain parameter estimates and model predictions that could be compared with data. The outcome was a successful mathematical description of ontogeny and life history traits of the loggerhead turtle. Some deviations between the model and the data existed (such as an earlier age at sexual maturity and faster growth of the post-hatchlings), yet probable causes for these deviations were found informative and discussed in great detail. Physiological traits such as the capacity to withstand starvation, trade-offs between reproduction and growth, and changes in the energy budget throughout the ontogeny were inferred from the model. The results offer new insights into physiology and ecology of loggerhead turtle with the potential to lead to novel approaches in conservation of this endangered species.

The universality and the future prospects of physiological energetics: Reply to comments on "Physics of metabolic organization".

In response to the comments on review "Physics of metabolic organization", we discuss the universality and the future prospects of physiological energetics. The topics range from the role of entropy in modeling living organisms to the apparent ubiquity of the von Bertalanffy curve, and the potential applications of the theory in yet unexplored domains. Tradeoffs in outreach to non-specialists are also briefly considered.

Physics of metabolic organization.

We review the most comprehensive metabolic theory of life existing to date. A special focus is given to the thermodynamic roots of this theory and to implications that the laws of physics-such as the conservation of mass and energy-have on all life. Both the theoretical foundations and biological applications are covered. Hitherto, the foundations were more accessible to physicists or mathematicians, and the applications to biologists, causing a dichotomy in what always should have been a single body of work. To bridge the gap between the two aspects of the same theory, we (i) adhere to the theoretical formalism, (ii) try to minimize the amount of information that a reader needs to process, but also (iii) invoke examples from biology to motivate the introduction of new concepts and to justify the assumptions made, and (iv) show how the careful formalism of the general theory enables modular, self-consistent extensions that capture important features of the species and the problem in question. Perhaps the most difficult among the introduced concepts, the utilization (or mobilization) energy flow, is given particular attention in the form of an original and considerably simplified derivation. Specific examples illustrate a range of possible applications-from energy budgets of individual organisms, to population dynamics, to ecotoxicology.

Size Scaling in Western North Atlantic Loggerhead Turtles Permits Extrapolation between Regions, but Not Life Stages.

INTRODUCTION: Sea turtles face threats globally and are protected by national and international laws. Allometry and scaling models greatly aid sea turtle conservation and research, and help to better understand the biology of sea turtles. Scaling, however, may differ between regions and/or life stages. We analyze differences between (i) two different regional subsets and (ii) three different life stage subsets of the western North Atlantic loggerhead turtles by comparing the relative growth of body width and depth in relation to body length, and discuss the implications. RESULTS AND DISCUSSION: Results suggest that the differences between scaling relationships of different regional subsets are negligible, and models fitted on data from one region of the western North Atlantic can safely be used on data for the same life stage from another North Atlantic region. On the other hand, using models fitted on data for one life stage to describe other life stages is not recommended if accuracy is of paramount importance. In particular, young loggerhead turtles that have not recruited to neritic habitats should be studied and modeled separately whenever practical, while neritic juveniles and adults can be modeled together as one group. Even though morphometric scaling varies among life stages, a common model for all life stages can be used as a general description of scaling, and assuming isometric growth as a simplification is justified. In addition to linear models traditionally used for scaling on log-log axes, we test the performance of a saturating (curvilinear) model. The saturating model is statistically preferred in some cases, but the accuracy gained by the saturating model is marginal.

Epigenetic drug 5-azacytidine impairs proliferation of rat limb buds in an organotypic model-system in vitro.

AIM: To establish an organotypic in vitro model of limb bud development to verify whether epigenetic drug and teratogen 5-azacytidine (5azaC) has an effect on limb buds independent of its effects on the placenta. METHODS: Fischer strain rat fore- and hindlimb buds were microsurgically isolated from 13 days old embryos and cultivated in vitro for two weeks at the air-liquid interface in Eagle's minimum essential medium (MEM) with 50% rat serum. 30 µmol of 5azaC was added to the fresh medium. Overall growth was measured by an ocular micrometer. Routine histology, immunohistochemical detection of the proliferating cell nuclear antigen (PCNA), and stereological quantification of PCNA expression were performed. RESULTS: At four time points, significantly lower overall growth was detected for fore- and hindlimb bud explants cultivated with 5azaC in comparison to controls. After the culture period, numerical density of the PCNA signal for both types of limb buds was lower than for controls (P<0.001). Limb buds were initially covered by immature epithelium and contained mesenchyme, myotubes, single hemangioblasts, hemangioblast aggregates, blood islands, and capillaries. Regardless of the treatment, cartilage and epidermis differentiated, but cells and structures typical for vasculogenesis disappeared. CONCLUSION: Our findings, obtained outside of the maternal organism, stress the importance of compromised cell proliferation for 5azaC impact on limb buds. This investigation points to the necessity to establish alternatives to in vivo research on animals using teratogenic agents.