Dynamic energy budget theory restores coherence in biology

We present the state of the art of the development of dynamic energy budget theory, and its expected developments in the near future within the molecular, physiological and ecological domains. The degree of formalization in the set-up of the theory, with its roots in chemistry, physics, thermodynamics, evolution and the consistent application of Occam's razor, is discussed. We place the various contributions in the theme issue within this theoretical setting, and sketch the scope of actual and potential applications.     

Modelling shellfish growth with dynamic energy budget models: an application for cockles and mussels in the Oosterschelde (southwest Netherlands)

Dynamic energy budget models for growth of individual cockles (Cerastoderma edule) and mussels (Mytilus edulis) are adjusted and calibrated to the Oosterschelde by formulating and parametrizing their functional responses using an extensive set of field observations. The resulting model predictions fit the observations satisfactorily. Results indicate that food quality and the importance of detritus as a food source are site-specific as well as species-specific. Despite these differences in their calibrated parameter values, both species show a very similar functional response. Compared with other systems, however, the functional responses of mussels in the present study are clearly higher than those of mussels in other systems. This may be explained by the absence of intra-specific competition in the measurement set-up that was used, and therefore supports the idea that the generally small functional response of M. edulis is caused by intra-specific competition.     

Recovery of methanotrophs from disturbance: population dynamics,evenness and functioning

Biodiversity is claimed to be essential for ecosystem functioning, but is threatened by anthropogenic disturbances. Prokaryotes have been assumed to be functionally redundant and virtually inextinguishable. However, recent work indicates that microbes may well be sensitive to environmental disturbance. Focusing on methane-oxidizing bacteria as model organisms, we simulated disturbance-induced mortality by mixing native with sterilized paddy soil in two ratios, 1:4 and 1:40, representing moderate and severe die-offs. Disturbed microcosms were compared with an untreated control. Recovery of activity and populations was followed over 4 months by methane uptake measurements, pmoA-qPCR, pmoA-based terminal restriction fragment length polymorphism and a pmoA-based diagnostic microarray. Diversity and evenness of methanotrophs decreased in disturbed microcosms, but functioning was not compromised. We consistently observed distinctive temporal shifts between type I and type II methanotrophs, and a rapid population growth leading to even higher cell numbers comparing disturbed microcosms with the control. Overcompensating mortality suggested that population size in the control was limited by competition with other bacteria. Overall, methanotrophs showed a remarkable ability to compensate for die-offs.     

风速和持续时间对树麻雀能量收支的影响

风是自然环境中常见的因子之一,会对动物的行为以及能量收支产生不同程度的影响。为探讨不同风速和持续时间对树麻雀能量收支的影响,以3种风速(0.2-0.4、1.2-1.4、3.2-3.6 m/s)和3种持续时间(1、2、4 h)的9组树麻雀进行为期1周的不同风环境驯化,测定其体重、体温和摄食量、摄水量、排泄粪量、排泄次数、摄入能、排泄粪能、排出水热能散失、消化能、同化能并计算消化率和同化率。去除初体重影响和双因素分析的结果发现,摄水量(排出水量)和排出水热能散失随着风速增大而显著减少(P < 0.001);持续时间与树麻雀的摄入能、粪能和散热调节的次数显著相关(P < 0.01),其能量收支最高和散热调节次数最多为2 h,最低(少)为4 h;双因素交互作用对树麻雀能量收支的影响不显著。3级风速(4 m/s)和持续时间4 h以内的风环境不会对树麻雀的能量收支产生显著影响。     

Bifurcation theory, adaptive dynamics and dynamic energy budget-structured populations of iteroparous species

In this paper, we describe a technique to evaluate the evolutionary dynamics of the timing of spawning for iteroparous species. The life cycle of the species consists of three life stages, embryonic, juvenile and adult whereby the transitions of life stages (gametogenesis, birth and maturation) occur at species-specific sizes. The dynamics of the population is studied in a semi-chemostat environment where the inflowing food concentration is periodic (annual). A dynamic energy budget-based continuous-time model is used to describe the uptake of the food, storage in reserves and allocation of the energy to growth, maintenance, development (embryos, juveniles) and reproduction (adults). A discrete-event process is used for modelling reproduction. At a fixed spawning date of the year, the reproduction buffer is emptied and a new cohort is formed by eggs with a fixed size and energy content. The population consists of cohorts: for each year one consisting of individuals with the same age which die after their last reproduction event. The resulting mathematical model is a finite-dimensional set of ordinary differential equations with fixed 1-year periodic boundary conditions yielding a stroboscopic map. We will study the evolutionary development of the population using the adaptive dynamics approach. The trait is the timing of spawning. Pairwise and mutual invasibility plots are calculated using bifurcation analysis of the stroboscopic map. The evolutionary singular strategy value belonging to the evolutionary endpoint for the trait allows for an interpretation of the reproduction strategy of the population. In a case study, parameter values from the literature for the bivalve Macoma balthica are used.     

Size-structured risk assessments govern Daphnia migration

One of the more fascinating phenomena in nature is animal mass migrations and in oceans and freshwaters, diel variations in depth distribution of zooplankton are a phenomenon that has intrigued scientists for more than a century. In our study, we show that zooplankton are able to assess the threat level of ultraviolet radiation and adjust their depth distribution to this level at a very fine tuned scale. Moreover, predation risk induces a size-structured depth separation, such that small individuals, which we show are less vulnerable to predation than larger, make a risk assessment and continue feeding in surface waters during day, offering a competitive release from down-migrating larger animals. Hence, we mechanistically show that such simple organisms as invertebrate zooplankton are able to make individual, size-specific decisions regarding how to compromise between threats from both predators and UV radiation, and adjust their diel migratory patterns accordingly.     

Population dynamics and production of Daphnia hyalina Leydig and Daphnia cucullata Sars in Tjeukemeer

As part of a research programme on the food chains in Tjeukemeer, the Daphnia hyalina and Daphnia cucullata populations were studied for three successive years. To analyse the factors regulating the production of these two species, their population parameters (density, size distribution, fecundity) and population dynamics (birth rate, mortality rate) were studied and related to environmental factors. Since Daphnia in Tjeukemeer shows continuous recruitment, the population dynamics model INSTAR was developed and used to integrate field data with laboratory data on development rates and length-weight relationships. The dynamics of the Daphnia species are mainly regulated by temperature and fish predation, the latter affects both birth rate and mortality. Total annual Daphnia production was 3.1–6.9 g org. dry wt M^–2, and annual P/B ratio ranged from 25 to 40 for D. cucullata and from 45 to 49 for D. hyalina.     

Daphnia magna shows reduced infection upon secondary exposure to a pathogen

Previous pathogen exposure is an important predictor of the probability of becoming infected. This is deeply understood for vertebrate hosts, and increasingly so for invertebrate hosts. Here, we test if an initial pathogen exposure changes the infection outcome to a secondary pathogen exposure in the natural host–pathogen system Daphnia magna and Pasteuria ramosa. Hosts were initially exposed to an infective pathogen strain, a non-infective pathogen strain or a control. The same hosts underwent a second exposure, this time to an infective pathogen strain, either immediately after the initial encounter or 48 h later. We observed that an initial encounter with a pathogen always conferred protection against infection compared with controls.     

The productivity and carbon budget of a natural population of Daphnia lumholtzi Sars

D. lumholtzi in Lake Samsonvale, Queensland, Australia, is a small species (max. size approx. 7 µgC) that occurs in low abundance (max. abundance 6400 m^–3), with an average daily biomass of 3.32 mgC m^–3. Its annual rates of carbon assimilation, production and respiration, are 166, 110, and 56 mgC m^–3 y^–1 respectively. Annual biomass turnover (annual production/average daily biomass) is 33 and production efficiency is 50–66%. The population may consume 1.65–2.20 mgC m^–3 daily, equivalent to about 1% of the average daily standing crop of phytoplankton. Clutch size is small, 2 eggs, but represents 30–80% of a female's weight. A female may only produce 8–10 offspring in a full lifespan, nevertheless egg production may account for 56% of total production. The population shows autumn and spring peaks in abundance, and is believed to oversummer (4 months) as ephippia.     

Vertical distributions of zooplankton and population dynamics of Daphnia in a meromictic lake

Vertical distributions of zooplankton were studied in relation to profiles of temperature, oxygen and chlorophyll a in Roi Lake, a small meromictic lake in central Alberta. Zooplankton were distributed fairly evenly through the oxygenated part of the water column in early summer, but a gradual descent of several species became evident in June. The vertical distribution of chlorophyll was dominated by a huge peak at the 8- to 9-m-deep chemocline. the location of a plate of photosynthetic sulfur bacteria. Ambient concentration of chlorophyll was a poor predictor of the numbers of zooplankton and the fecundity of Daphnia pulicaria at different depths, and per capita birth rates of Daphnia were usually highest in the surface waters. The reproductively disadvantageous restriction of daphnids to deep water by late summer and their catastrophic decline in the face of high ambient concentrations of chlorophyll suggest that factors other than temperature and food supply are important in influencing the dynamics and distribution of zooplankton in this lake.     

Size-selective dispersal of Daphnia resting eggs by backswimmers (Notonecta maculata)

Freshwater zooplankton is increasingly used to study effects of dispersal on community and metacommunity structure. Yet, it remains unclear how zooplankton disperses. Clearly, birds and wind play a significant role as zooplankton dispersal agents, but they may not always be the main vectors. This experimental study shows that a cosmopolitan aquatic insect, Notonecta, can be an important vector of cladoceran resting eggs (ephippia). Dispersing Notonecta frequently transported ephippia during flight, with a bias towards smaller ephippia in two species. A similar trend was present at the species level: Daphnia species with smaller ephippia were more often dispersed, suggesting that Notonecta could generate specific colonist communities. In addition, buoyancy appeared a critical trait, as non-floating ephippia of Daphnia magna were never dispersed. Our data suggest that Notonecta could be important dispersers of Daphnia, and that knowledge of dispersal dynamics of Notonecta may be used to predict Daphnia dispersal, colonization and resilience to disturbance.     

Stylized facts in microalgal growth: interpretation in a dynamic energy budget context

A dynamic energy budget (DEB) model for microalgae is proposed. This model deviates from the standard DEB model as it needs more reserves to cope with the variation of assimilation pathways, requiring a different approach to growth based on the synthesizing unit (SU) theory for multiple substrates. It is shown that the model is able to accurately predict experimental data in constant and light-varying conditions with most of the parameter values taken directly from the literature. Also, model simulations are shown to be consistent with stylized facts (SFs) concerning NC ratio. These SFs are reinterpreted and the general conclusion is that all forcing variables (dilution rate, temperature and irradiance) impose changes in the nitrogen or carbon limitation status of the population, and consequently on reserve densities. Model predictions are also evaluated in comparison with SFs on chlorophyll concentration. It is proposed that an extra structure, more dependent on the nitrogen reserve, is required to accurately model chlorophyll dynamics. Finally, SFs concerning extracellular polymeric substances (EPSs) production by benthic diatoms are collected and interpreted and a formulation based on product synthesis and rejection flux is proposed for the EPSs production rate.     

Extrapolating toxic effects on individuals to the population level: the role of dynamic energy budgets

The interest of environmental management is in the long-term health of populations and ecosystems. However, toxicity is usually assessed in short-term experiments with individuals. Modelling based on dynamic energy budget (DEB) theory aids the extraction of mechanistic information from the data, which in turn supports educated extrapolation to the population level. To illustrate the use of DEB models in this extrapolation, we analyse a dataset for life cycle toxicity of copper in the earthworm Dendrobaena octaedra. We compare four approaches for the analysis of the toxicity data: no model, a simple DEB model without reserves and maturation (the Kooijman-Metz formulation), a more complex one with static reserves and simplified maturation (as used in the DEBtox software) and a full-scale DEB model (DEB3) with explicit calculation of reserves and maturation. For the population prediction, we compare two simple demographic approaches (discrete time matrix model and continuous time Euler-Lotka equation). In our case, the difference between DEB approaches and population models turned out to be small. However, differences between DEB models increased when extrapolating to more field-relevant conditions. The DEB3 model allows for a completely consistent assessment of toxic effects and therefore greater confidence in extrapolating, but poses greater demands on the available data.     

Bacterial epibionts of Daphnia: a potential route for the transfer of dissolved organic carbon in freshwater food webs

The identification of interacting species and elucidation of their mode of interaction may be crucial to understand ecosystem-level processes. We analysed the activity and identity of bacterial epibionts in cultures of Daphnia galeata and of natural daphnid populations. Epibiotic bacteria incorporated considerable amounts of dissolved organic carbon (DOC), as estimated via uptake of tritiated leucine: three times more tracer was consumed by microbes on a single Daphnia than in 1 ml of lake water. However, there was virtually no incorporation if daphnids were anaesthetised, suggesting that their filtration activity was essential for this process. Microbial DOC uptake could predominantly be assigned to microbes that were located on the filter combs of daphnids, where the passage of water would ensure a continuously high DOC supply. Most of these bacteria were Betaproteobacteria from the genus Limnohabitans. Specifically, we identified a monophyletic cluster harbouring Limnohabitans planktonicus that encompassed sequence types from D. galeata cultures, from the gut of Daphnia magna and from daphnids of Lake Zurich. Our results suggest that the epibiotic growth of bacteria related to Limnohabitans on Daphnia spp. may be a widespread and rather common phenomenon. Moreover, most of the observed DOC flux to Daphnia in fact does not seem to be associated with the crustacean biomass itself but with its epibiotic microflora. The unexplored physical association of daphnids with heterotrophic bacteria may have considerable implications for our understanding of carbon transfer in freshwater food webs, that is, a trophic ‘shortcut'' between microbial DOC uptake and predation by fish.     

The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella

In food-web studies, parasites are often ignored owing to their insignificant biomass. We provide evidence that parasites may affect trophic transfer in aquatic food webs. Many phytoplankton species are susceptible to parasitic fungi (chytrids). Chytrid infections of diatoms in lakes may reach epidemic proportions during diatom spring blooms, so that numerous free-swimming fungal zoospores (2-3 microm in diameter) are produced. Analysis shows that these zoospores are rich in polyunsaturated fatty acids and sterols (particularly cholesterol), which indicates that they provide excellent food for zooplankters such as Daphnia. In life-table experiments using the large diatom Asterionella formosa as food, Daphnia growth increased significantly in treatments where a parasite was present. By grazing on the zoospores, Daphnia acquired important supplementary nutrients and were able to grow. When large inedible algae are infected by parasites, nutrients within the algal cells are consumed by these chytrids, some of which, in turn, are grazed by Daphnia. Thus, chytrids transfer energy and nutrients from their hosts to zooplankton. This study suggests that parasitic fungi alter trophic relationships in freshwater ecosystems and may be the important components in shaping the community and the food-web dynamics of lakes.     

Oscillations in continuous culture populations of Streptococcus pneumoniae: population dynamics and the evolution of clonal suicide

Agents that kill or induce suicide in the organisms that produce them or other individuals of the same genotype are intriguing puzzles for ecologists and evolutionary biologists. When those organisms are pathogenic bacteria, these suicidal toxins have the added appeal as candidates for the development of narrow spectrum antibiotics to kill the pathogens that produce them. We show that when clinical as well as laboratory strains of Streptococcus pneumoniae are maintained in continuous culture (chemostats), their densities oscillate by as much as five orders of magnitude with an apparently constant period. This dynamic, which is unanticipated for single clones of bacteria in chemostats, can be attributed to population-wide die-offs and recoveries. Using a combination of mathematical models and experiments with S. pneumoniae, we present evidence that these die-offs can be attributed to the autocatalytic production of a toxin that lyses or induces autolysis in members of the clone that produces it. This toxin, which our evidence indicates is a protein, appears to be novel; S. pneumoniae genetic constructs knocked out for lytA and other genes coding for known candidates for this agent oscillate in chemostat culture. Since this toxin lyses different strains of S. pneumoniae as well as other closely related species of Streptococcus, we propose that its ecological role is as an allelopathic agent. Using a mathematical model, we explore the conditions under which toxins that kill members of the same clone that produces them can prevent established populations from invasion by different strains of the same or other species. We postulate that the production of the toxin observed here as well as other bacteria-produced toxins that kill members of the same genotype, ‘clonal suicide’, evolved and are maintained to prevent colonization of established populations by different strains of the same and closely related species.     

[树]麻雀羽再生的能量预算和水代谢散热调节

为探讨[树]麻雀的羽再生能力、能量预算对策和有效的散热调节方式,对3组(对照CF、去飞羽FF和去尾羽组TF)[树]麻雀(Passer montanus)进行4周驯养(Acclimation)。结果发现:[树]麻雀具有较强的羽再生能力和飞羽参与个体保温。羽再生[树]麻雀能量收支水平降低极显著(P﹤0.001),FF组和TF组比CF组减少依次为:摄入能19.77%和7.17%、消化能18.79%和6.47%、同化能18.73%和6.46%、粪能28.66%和13.35%、水代谢散热热能26.95%和7.43%、排泄次数33.71%和14.40%,增加依次为:消化率1.23%和0.78%、同化率1.35%和0.84%。个体能值水平,体重CF、TF和FF组(P﹤0.05)依次降低,体温组间变化不显著(P﹥0.05)。体内能量储备,血糖、肌糖原、体脂和水分含量组间差异不显著(P﹥0.05),肝糖原含量、体脂重组间差异显著(P﹤0.05)。器官水平包括心脏、肾脏、腺胃、小肠、盲肠和总消化道长度及质量出现积极的响应。日代谢水量组间差异极显著(P﹤0.001)。组间日排泄次数最少平均为56.11次和最多可达96.34次/只。结果表明:羽再生[树]麻雀分别选择了不同程度的降低能量收支水平,提高摄入食物的消化、吸收效率,动用体内能量储备来获取摄入能量不足部分,降低器官总能耗的能量预算对策和不同的新羽(再生羽枚数:飞羽部分和尾羽全部)再生的能量投资对策。泄殖腔排出(粪尿混合物)水是鸟类特有的、迅速的和有效的散热调节方式。     

A dynamic energy budget model: parameterisation and application to the Pacific oyster Crassostrea gigas in New Zealand waters

A dynamic energy budget (DEB) model was developed and applied to the Pacific oyster Crassostrea gigas in central New Zealand. The model was based on DEB theory and developed prior to empirical information according to a common mechanistic rule in organisms' physiology. Subsequently, both laboratory and field experiments were specifically designed to collect datasets for parameter estimation and testing of the model. This approach to the modelling aimed to reduce uncertainties in parameter estimates and hence improve the applicability of the model. A lab-based starvation experiment was done over 170 days. Changes in body flesh weight were monitored and the respiration rate was measured. Dry flesh weight and the oxygen consumption rate decreased by 63.4% and 44.0% respectively over the experiment. Ash free dry flesh weight was proportional to the dry flesh weight, with coefficients of 83.5% and 58.7% respectively at the beginning and late stages of the experiment. Field-based growth experiments were done on a marine farm at two depths over 150 days to obtain biological and environmental information. The growth rate of oysters at 8 m depth was significantly greater than at 32 m depth. Chlorophyll-a concentration was highly variable, both spatially and temporally. Variation between depths provided ideal information for validation of the DEB model. Estimates of model parameters were augmented from studies in a local population. In comparison with previous studies on the same species from other ecosystems in the world, intraspecies variation was apparent in some parameters including maximum surface area-specific assimilation rate, which governs the ability of an individual for energy acquisition, and the fraction of energy utilisation rate used for maintenance plus growth, which determines energy fluxes to different components. The maximum storage density and volume-specific cost for growth also showed considerable intraspecies variability. Application of the model developed here showed that it is capable of simulating energetics and growth of the oyster in the growing area of central New Zealand.     

A population of sexual Daphnia pulex resists invasion by asexual clones

Asexual reproduction avoids the costs associated with sex, predicting that invading asexual clones can quickly replace sexual populations. Daphnia pulex populations in the Great Lakes area are predominately asexual, but the elimination of sexual populations by invading clones is poorly understood. Asexual clones were detected at low frequency in one rare sexual population in 1995, with some increase in frequency during 2003 and 2004. However, these clones remained at low frequency during further yearly sampling (2005–2013) with no evidence that the resident sexual population was in danger of elimination. There was evidence for hybridization between rare males produced by asexual clones and sexual females with the potential to produce new asexual genotypes and spread the genetic factors for asexuality. In a short-term laboratory competition experiment, the two most common asexual clones did not increase in frequency relative to a genetically diverse sexual population due in part to a greater investment in diapausing eggs that trades-off current population growth for increased contribution to the egg bank. Our results suggest that a successful invasion can be prolonged, requiring a combination of clonal genotypes with high fitness, persistence of clones in the egg bank and negative factors affecting the sexual population such as inbreeding depression resulting from population bottlenecks.