Quantitative aspects of metabolic organization: a discussion of concepts

Metabolic organization of individual organisms follows simple quantitative rules that can be understood from basic physical chemical principles. Dynamic energy budget (DEB) theory identifies these rules, which quantify how individuals acquire and use energy and nutrients. The theory provides constraints on the metabolic organization of subcellular processes. Together with rules for interaction between individuals, it also provides a basis to understand population and ecosystem dynamics. The theory, therefore, links various levels of biological organization. It applies to all species of organisms and offers explanations for body-size scaling relationships of natural history parameters that are otherwise difficult to understand. A considerable number of popular empirical models turn out to be special cases of the DEB model, or very close numerical approximations. Strong and weak homeostasis and the partitionability of reserve kinetics are cornerstones of the theory and essential for understanding the evolution of metabolic organization.     

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.     

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.     

What is the status of metabolic theory one century after Pütter invented the von Bertalanffy growth curve?

Metabolic theory aims to tackle ecological and evolutionary problems by explicitly including physical principles of energy and mass exchange, thereby increasing generality and deductive power. Individual growth models (IGMs) are the fundamental basis of metabolic theory because they represent the organisational level at which energy and mass exchange processes are most tightly integrated and from which scaling patterns emerge. Unfortunately, IGMs remain a topic of great confusion and controversy about the origins of the ideas, their domain and breadth of application, their logical consistency and whether they can sufficiently capture reality. It is now 100 years since the first theoretical model of individual growth was put forward by Pütter. His insights were deep, but his model ended up being attributed to von Bertalanffy and his ideas largely forgotten. Here I review Pütter's ideas and trace their influence on existing theoretical models for growth and other aspects of metabolism, including those of von Bertalanffy, the Dynamic Energy Budget (DEB) theory, the Gill-Oxygen Limitation Theory (GOLT) and the Ontogenetic Growth Model (OGM). I show that the von Bertalanffy and GOLT models are minor modifications of Pütter's original model. I then synthesise, compare and critique the ideas of the two most-developed theories, DEB theory and the OGM, in relation to Pütter's original ideas. I formulate the Pütter, DEB and OGM models in the same structure and with the same notation to illustrate the major similarities and differences among them. I trace the confusion and controversy regarding these theories to the notions of anabolism, catabolism, assimilation and maintenance, the connections to respiration rate, and the number of parameters and state variables their models require. The OGM model has significant inconsistencies that stem from the interpretation of growth as the difference between anabolism and maintenance, and these issues seriously challenge its ability to incorporate development, reproduction and assimilation. The DEB theory is a direct extension of Pütter's ideas but with growth being the difference between assimilation and maintenance rather than anabolism and catabolism. The DEB theory makes the dynamics of Pütter's ‘nutritive material’ explicit as well as extending the scheme to include reproduction and development. I discuss how these three major theories for individual growth have been used to explain ‘macrometabolic’ patterns including the scaling of respiration, the temperature–size rule (first modelled by Pütter), and the connection to life history. Future research on the connections between theory and data in these macrometabolic topics have the greatest potential to advance the status of metabolic theory and its value for pure and applied problems in ecology and evolution.     

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.     

Quantitative steps in the evolution of metabolic organisation as specified by the Dynamic Energy Budget theory

The Dynamic Energy Budget (DEB) theory quantifies the metabolic organisation of organisms on the basis of mechanistically inspired assumptions. We here sketch a scenario for how its various modules, such as maintenance, storage dynamics, development, differentiation and life stages could have evolved since the beginning of life. We argue that the combination of homeostasis and maintenance induced the development of reserves and that subsequent increases in the maintenance costs came with increases of the reserve capacity. Life evolved from a multiple reserves - single structure system (prokaryotes, many protoctists) to systems with multiple reserves and two structures (plants) or single reserve and single structure (animals). This had profound consequences for the possible effects of temperature on rates. We present an alternative explanation for what became known as the down-regulation of maintenance at high growth rates in microorganisms; the density of the limiting reserve increases with the growth rate, and reserves do not require maintenance while structure-specific maintenance costs are independent of the growth rate. This is also the mechanism behind the variation of the respiration rate with body size among species. The DEB theory specifies reserve dynamics on the basis of the requirements of weak homeostasis and partitionability. We here present a new and simple mechanism for this dynamics which accounts for the rejection of mobilised reserve by busy maintenance/growth machinery. This module, like quite a few other modules of DEB theory, uses the theory of Synthesising Units; we review recent progress in this field. The plasticity of membranes that evolved in early eukaryotes is a major step forward in metabolic evolution; we discuss quantitative aspects of the efficiency of phagocytosis relative to the excretion of digestive enzymes to illustrate its importance. Some processes of adaptation and gene expression can be understood in terms of allocation linked to the relative workload of metabolic modules in (unicellular) prokaryotes and organs in (multicellular) eukaryotes. We argue that the evolution of demand systems can only be understood in the light of that of supply systems. We illustrate some important points with data from the literature.     

Quantitative steps in symbiogenesis and the evolution of homeostasis

The merging of two independent populations of heterotrophs and autotrophs into a single population of mixotrophs has occurred frequently in evolutionary history. It is an example of a wide class of related phenomena, known as symbiogenesis. The physiological basis is almost always (reciprocal) syntrophy, where each species uses the products of the other species. Symbiogenesis can repeat itself after specialization on particular assimilatory substrates. We discuss quantitative aspects and delineate eight steps from two free-living interacting populations to a single fully integrated endosymbiotic one. The whole process of gradual interlocking of the two populations could be mimicked by incremental changes of particular parameter values. The role of products gradually changes from an ecological to a physiological one. We found conditions where the free-living, epibiotic and endobiotic populations of symbionts can co-exist, as well as conditions where the endobiotic symbionts outcompete other symbionts. Our population dynamical analyses give new insights into the evolution of cellular homeostasis. We show how structural biomass with a constant chemical composition can evolve in a chemically varying environment if the parameters for the formation of products satisfy simple constraints. No additional regulation mechanisms are required for homeostasis within the context of the dynamic energy budget (DEB) theory for the uptake and use of substrates by organisms. The DEB model appears to be dosed under endosymbiosis. This means that when each free-living partner follows DEB rules for substrate uptake and use, and they become engaged in an endosymbiotic relationship, a gradual transition to a single fully integrated system is possible that again follows DEB rules for substrate uptake and use.     

榕小蜂温度耐受性及其对种间共存关系的影响

全球已知有约800种榕属(Ficus)植物, 主要分布在热带, 部分种类延伸至亚热带地区。温度是限制榕‒蜂共生系统分布北界的主要因素, 也显著影响榕树及其榕小蜂的繁殖成功, 其中榕小蜂对温度的响应更加敏感。榕小蜂只有在一定的温度范围内才能保持正常的生理机能, 其对温度耐受能力直接影响榕果内小蜂种群数量和群落内种间关系。然而目前对榕小蜂温度耐受性的研究尚少, 榕小蜂的温度耐受能力如何影响榕果内小蜂的共存关系还未见报道。本文研究了分布于西双版纳的2种雌雄同株和1种雌雄异株榕树果内传粉榕小蜂和非传粉小蜂的温度耐受能力。结果表明: 3种传粉榕小蜂对高温的耐受性极差, 相对于雌雄同株的高榕(F. altissima)和聚果榕(F. racemosa)传粉榕小蜂, 雌雄异株的鸡嗉子榕(F. semicordata)传粉榕小蜂对低温有增强的耐受趋势。聚果榕小蜂群落结构显示: 在适宜其生长的西双版纳地区, 传粉榕小蜂的数量占绝对优势, 在温度较低的季节其数量显著减少; 而非传粉榕小蜂呈相反模式, 较强的温度耐受能力使其在低温的雾凉季维持了较高的种群数量。鸡嗉子榕果内非传粉小蜂Sycoscapter trifemmensis相对于Philotrypesis dunia有更强的温度耐受能力, 在种群数量和种间关系上有更多的竞争优势及数量。榕小蜂的温度耐受性差异在物种分布、种间关系的维持和共存上起了重要作用, 本研究结果为阐明榕小蜂种间共存的维持机制提供了科学依据。     

恒温和变温下中国对虾生长和能量收支的比较

对比研究了模拟自然昼夜温度变化节律的4个变温(22±2)、(25±2)、(28±2)和(31±2)℃与相应的恒温22、25、28和31℃下中国对虾(F ennerop enaeus ch inensis O sbeck)生长和能量收支的差异。结果表明,对虾在(22±2)℃、(25±2)℃和(28±2)℃变温条件下的生长率显著高于相应的恒温,但(31±2)℃与恒温31℃相比没有显著差异。与相应的恒温相比,(25±2)℃、(28±2)℃和(31±2)℃变温下对虾的摄食量显著增大,(22±2)℃、(25±2)℃和(28±2)℃变温下对虾的饵料转化率则显著提高。但变温下对虾对食物的消化率与相应的恒温相比没有显著差异。能量收支研究结果则发现,(22±2)℃、(25±2)℃和(28±2)℃变温下对虾摄食能中,用于生长的能量比例显著增加,而(31±2)℃与31℃相比则未见显著差异。从而表明,变温促长的主要机制可归因于变温下摄食量的增大、饵料转化率的提高及其摄食能中用于生长能比例的增加。     

Body size mediated coexistence of consumers competing for resources in space

Body size is a major phenotypic trait of individuals that commonly differentiates co-occurring species. We analyzed inter-specific competitive interactions between a large consumer and smaller competitors, whose energetics, selection and giving-up behaviour on identical resource patches scaled with individual body size. The aim was to investigate whether pure metabolic constraints on patch behaviour of vagile species can determine coexistence conditions consistent with existing theoretical and experimental evidence. We used an individual-based spatially explicit simulation model at a spatial scale defined by the home range of the large consumer, which was assumed to be parthenogenic and semelparous. Under exploitative conditions, competitive coexistence occurred in a range of body size ratios between 2 and 10. Asymmetrical competition and the mechanism underlying asymmetry, determined by the scaling of energetics and patch behaviour with consumer body size, were the proximate determinant of inter-specific coexistence. The small consumer exploited patches more efficiently, but searched for profitable patches less effectively than the larger competitor. Therefore, body-size related constraints induced niche partitioning, allowing competitive coexistence within a set of conditions where the large consumer maintained control over the small consumer and resource dynamics. The model summarises and extends the existing evidence of species coexistence on a limiting resource, and provides a mechanistic explanation for decoding the size-abundance distribution patterns commonly observed at guild and community levels.     

The need of hypothesis-driven designs and conceptual models in impact assessment studies: An example from the free-living marine nematodes

The literature on the use of marine nematodes as bioindicators of anthropogenic impact is extensive. Nevertheless, review studies have reported a high degree of variability among results and no consistent overall pattern has so far emerged. This lack of congruence might be partially because hypotheses formulation in environmental assessment studies has been largely inductive or abductive and not deductive or hypothesis-driven. In the present study, we emphasize the need of using hypothesis-driven designs and conceptual models in impact assessment studies. Hypotheses for individual and population level studies can be derived from the dynamic energy budget model (DEB). By means of differential equations, DEB model can infer whether a stressor promotes a shift in energy allocation along the life history of the individuals. For community/assemblage level studies, the predictions of the dynamic equilibrium model (DEM) for species richness is presented and extended for abundance, evenness, taxonomic distinctness, and changes in assemblage structure and sample dispersion. While it is predicted that species richness peaks at intermediate levels of disturbances and enrichment, evenness decreases with increasing disturbances and reducing enrichment/pollutant concentrations. Based on DEM,enrichment and pollutants may promote change in community structure by favoring the tolerant species, while physical disturbances may promote sample dispersion as a result of unselective mortality. Finally, we discuss the benefits of using niche-based models to select the indicator species, instead of using classical ordination methods, twinspan and similarity percentage analysis. The selection of indicator species have to be independent from the other species and must consider the set of environmental conditions. The use of conceptual models to select the best ecological indicators is highly recommended. It allows a logical way of testing for causalities and of scaling the different studies for comparisons.     

Differential time budgets of two forms of juvenile brook charr in the open-water zone

No significant differences were found in the time budget (time spent in feeding, moving and stationary), attack rate (number of feeding bouts min⁻¹), and microhabitat use of juvenile (1+ years) littoral and pelagic brook charr Salvelinus fontinalis at 2 and 4 m depth, when restricted to feeding in pelagic enclosures. In contrast, fish of the littoral form allocated significantly more time than pelagic ones to feeding, moving and in total activity at 3 m depth. No significant differences were found in attack rate between the two forms at any given depth. Based on the mean for the water column (all depths pooled), however, fish of the littoral form executed a significantly higher attack rate than fish of the pelagic one. In multiple regressions analyses, the best predictors of time allocated to feeding and attack rate were the dummy variable 'form' (littoral individuals spend significantly more time in feeding than pelagic ones), light intensity at the surface (negative) and water temperature (positive), and explained 48 and 55% of these variations, respectively. Time allocated to moving was only explained by water temperature (negative) and explained 43% of the variation. Time in a stationary position was best explained by water temperature (negative) and light intensity at the surface (positive), explaining 52% of the variation. The results of this study support the hypothesis that littoral brook charr spend more energy in foraging than pelagic ones when restricted to feeding in the pelagic habitat, and thus that trophic diversification is adaptive in this species.     

Scaling in stream communities

Scaling relationships between population density (N) and body size (W), and of their underlying size distributions, can contribute to an understanding of how species use resources as a function of size. In an attempt to resolve the controversy over the form of scaling relationships, an extensive dataset, comprising 602 invertebrate species, was obtained from two geographically separate stream communities (Seebach in Austria and Mynach in Wales). We analysed the temporal consistency of the N-W relationship, which was subjected to ordinary least squares (OLS), bisector (OLS(BIS)) and quantile regressions, and species-size spectra with seasonally collated data. Slopes of seasonal OLS(BIS) regressions did not depart from -1 in either community, indicating a seasonally convergent scaling relationship, which is not energetically constrained. Species-size spectra may scale with habitat complexity, providing an alternative explanation for the observed body-size scaling. In contrast to the right-skewed species-size frequency distributions of single-species assemblages, the size spectra of these benthic communities exhibited 'central tendencies', reflecting their phyletic constitution. The shape of species body-mass spectra differed between the two communities, with a bimodal and seasonally convergent pattern in the Seebach community and a seasonally shifting unimodality in the Mynach community. The body-size spectra of large, mostly insect, species (greater than or equal to 1 mm) scaled to seasonal variations in habitat complexity (i.e. fractal D), suggesting that habitat structure constrains the community organization of stream benthos.     

Is the scaling of swim speed in sharks driven by metabolism?

The movement rates of sharks are intrinsically linked to foraging ecology, predator–prey dynamics and wider ecosystem functioning in marine systems. During ram ventilation, however, shark movement rates are linked not only to ecological parameters, but also to physiology, as minimum speeds are required to provide sufficient water flow across the gills to maintain metabolism. We develop a geometric model predicting a positive scaling relationship between swim speeds in relation to body size and ultimately shark metabolism, taking into account estimates for the scaling of gill dimensions. Empirical data from 64 studies (26 species) were compiled to test our model while controlling for the influence of phylogenetic similarity between related species. Our model predictions were found to closely resemble the observed relationships from tracked sharks, providing a means to infer mobility in particularly intractable species.     

Dynamic energy budget theory and population ecology: lessons from Daphnia

Dynamic energy budget (DEB) theory offers a perspective on population ecology whose starting point is energy utilization by, and homeostasis within, individual organisms. It is natural to ask what it adds to the existing large body of individual-based ecological theory. We approach this question pragmatically--through detailed study of the individual physiology and population dynamics of the zooplankter Daphnia and its algal food. Standard DEB theory uses several state variables to characterize the state of an individual organism, thereby making the transition to population dynamics technically challenging, while ecologists demand maximally simple models that can be used in multi-scale modelling. We demonstrate that simpler representations of individual bioenergetics with a single state variable (size), and two life stages (juveniles and adults), contain sufficient detail on mass and energy budgets to yield good fits to data on growth, maturation and reproduction of individual Daphnia in response to food availability. The same simple representations of bioenergetics describe some features of Daphnia mortality, including enhanced mortality at low food that is not explicitly incorporated in the standard DEB model. Size-structured, population models incorporating this additional mortality component resolve some long-standing questions on stability and population cycles in Daphnia. We conclude that a bioenergetic model serving solely as a 'regression' connecting organismal performance to the history of its environment can rest on simpler representations than those of standard DEB. But there are associated costs with such pragmatism, notably loss of connection to theory describing interspecific variation in physiological rates. The latter is an important issue, as the type of detailed study reported here can only be performed for a handful of species.     

The temperature of two welsh lakes and its effect on the distribution of two freshwater insects

Temperature data are presented from the littoral zones of two lakes in North Wales, Llyn Coron and Llyn Dinas. Recording, mainly on a continuous basis, was over a two year period. Despite their different situations, the lakes had similar temperature regimes. Regional weather factors were of greater importance than local variations. However, some differences were present, especially during the summer months. Laboratory experiments were conducted to determine the temperature relationships of Nemoura avicularis Morton (Plecoptera) and Leptophlebia vespertina (L.) (Ephemeroptera), common species in Llyn Dinas but absent from Llyn Coron. Aspects considered included nymphal temperature tolerance and the effect of temperature on egg development and emergence. From the background of the results, it was concluded that the differences in temperature regime between the two lakes were insufficient to explain the absence of the two species from Llyn Coron.     

Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments

Scaling relationships such as the variation of population abundance with body size provide links between individual organisms and ecosystem functioning. Previous work, in marine pelagic ecosystems, has focused on the relationship between total phytoplankton abundance and the assemblage mean cell size. However, the relationship between specific population abundance and cell size in marine phytoplankton has received little attention. Here, we show that cell size accounts for a significant amount of variability in the population abundance of phytoplankton species across a cell volume range spanning seven orders of magnitude. The interspecific scaling of population abundance and cell size takes a power exponent near −3/4. Unexpectedly, despite the constraints imposed on large phytoplankton by limited resource acquisition, the size scaling exponent does not differ between contrasting marine environments such as coastal and subtropical regions. These findings highlight the adaptive abilities of individual species to cope with different environmental conditions and suggest that a general rule such as the 'energetic equivalence' constrains the abundance of phytoplankton populations in marine pelagic ecosystems.     

Tree height–diameter allometry across the United States

The relationship between tree height and diameter is fundamental in determining community and ecosystem structure as well as estimates of biomass and carbon storage. Yet our understanding of how tree allometry relates to climate and whole organismal function is limited. We used the Forest Inventory and Analysis National Program database to determine height–diameter allometries of 2,976,937 individuals of 293 tree species across the United States. The shape of the allometric relationship was determined by comparing linear and nonlinear functional forms. Mixed‐effects models were used to test for allometric differences due to climate and floristic (between angiosperms and gymnosperms) and functional groups (leaf habit and shade tolerance). Tree allometry significantly differed across the United States largely because of climate. Temperature, and to some extent precipitation, in part explained tree allometric variation. The magnitude of allometric variation due to climate, however, had a phylogenetic signal. Specifically, angiosperm allometry was more sensitive to differences in temperature compared to gymnosperms. Most notably, angiosperm height was more negatively influenced by increasing temperature variability, whereas gymnosperm height was negatively influenced by decreasing precipitation and increasing altitude. There was little evidence to suggest that shade tolerance influenced tree allometry except for very shade‐intolerant trees which were taller for any given diameter. Tree allometry is plastic rather than fixed and scaling parameters vary around predicted central tendencies. This allometric variation provides insight into life‐history strategies, phylogenetic history, and environmental limitations at biogeographical scales.     

Distribution and abundance of larval fish in the northern Aegean Sea--eastern Mediterranean--in relation to early summer oceanographic conditions

Two ichthyoplanktonic surveys were conducted during June 1995and 1996 along the northern Aegean Sea coast with the aim ofdescribing species composition, abundance and distribution patternsof the assemblages of fish larvae and their relationships tooceanographic regimes. The upper water column was generallycooler, fresher and richer in zooplankton during June 1996.The mean abundance of larvae of the small-sized pelagic fish(anchovy and most mesopelagics) was higher in 1996. In contrast,larvae of the middle-sized pelagics (Sardinella aurita, Trachurusmediterraneus, Scomber jaconicus and Auxis rochei) were moreabundant in 1995. The eastern part of the surveyed area (NEAegean Sea) was colder and less saline during both years becauseof the influence of Black Sea and riverine waters. In the colderJune 1996, larvae of many ‘summer spawners', e.g., themiddle-sized pelagics, were present infrequently and at verylow numbers in the NE Aegean Sea. Cluster analysis using theBray–Curtis similarity index revealed well-defined groupsof stations and assemblages of larvae. Ordination scores derivedfrom non-metric multidimensional scaling were compared by multipleregression with various parameters and the analysis showed thattaxonomic composition and abundance was primarily explainedby bathymetry. In the cooler June 1996, a significant amountof variation in ordination scores was related to longitudinaldifferences in temperature, salinity and the width of the continentalshelf. The membership of station and species groups definedby the cluster analysis differed between 1995 and 1996 and reflectedinterannual differences in the distribution and abundance ofcomponent species. Spatial and temporal spawning patterns ofadults played the key role in the formation of assemblages ofearly larvae.