Interactive effects of intrinsic and extrinsic factors on metabolic rate.

Metabolism energizes all biological processes, and its tempo may importantly influence the ecological success and evolutionary fitness of organisms. Therefore, understanding the broad variation in metabolic rate that exists across the living world is a fundamental challenge in biology. To further the development of a more reliable and holistic picture of the causes of this variation, we review several examples of how various intrinsic (biological) and extrinsic (environmental) factors (including body size, cell size, activity level, temperature, predation and other diverse genetic, cellular, morphological, physiological, behavioural and ecological influences) can interactively affect metabolic rate in synergistic or antagonistic ways. Most of the interactive effects that have been documented involve body size, temperature or both, but future research may reveal additional 'hub factors'. Our review highlights the complex, intimate inter-relationships between physiology and ecology, knowledge of which can shed light on various problems in both disciplines, including variation in physiological adaptations, life histories, ecological niches and various organism-environment interactions in ecosystems. We also discuss theoretical and practical implications of interactive effects on metabolic rate and provide suggestions for future research, including holistic system analyses at various hierarchical levels of organization that focus on interactive proximate (functional) and ultimate (evolutionary) causal networks. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Maximum likelihood outperforms binning methods for detecting differences in abundance size spectra across environmental gradients.

Individual body size distributions (ISD) within communities are remarkably consistent across habitats and spatiotemporal scales and can be represented by size spectra, which are described by a power law. The focus of size spectra analysis is to estimate the exponent ( λ ) of the power law. A common application of size spectra studies is to detect anthropogenic pressures. Many methods have been proposed for estimating λ most of which involve binning the data, counting the abundance within bins, and then fitting an ordinary least squares regression in log-log space. However, recent work has shown that binning procedures return biased estimates of λ compared to procedures that directly estimate λ using maximum likelihood estimation (MLE). While it is clear that MLE produces less biased estimates of site-specific λ's, it is less clear how this bias affects the ability to test for changes in λ across space and time, a common question in the ecological literature. Here, we used simulation to compare the ability of two normalised binning methods (equal logarithmic and log2 bins) and MLE to (1) recapture known values of λ , and (2) recapture parameters in a linear regression measuring the change in λ across a hypothetical environmental gradient. We also compared the methods using two previously published body size datasets across a natural temperature gradient and an anthropogenic pollution gradient. Maximum likelihood methods always performed better than common binning methods, which demonstrated consistent bias depending on the simulated values of λ . This bias carried over to the regressions, which were more accurate when λ was estimated using MLE compared to the binning procedures. Additionally, the variance in estimates using MLE methods is markedly reduced when compared to binning methods. The error induced by binning methods can be of similar magnitudes as the variation previously published in experimental and observational studies, bringing into question the effect sizes of previously published results. However, while the methods produced different regression slope estimates, they were in qualitative agreement on the sign of those slopes (i.e. all negative or all positive). Our results provide further support for the direct estimation of λ and its relative variation across environmental gradients using MLE over the more common methods of binning.

Environmental drivers of size-based population structure, sexual maturity and fecundity: A study of the invasive blue crab Callinectes sapidus (Rathbun, 1896) in the Mediterranean Sea.

The blue crab Callinectes sapidus (Rathbun, 1896) is one of the most invasive species in the Mediterranean Sea. Understand how the populations are maintained and how the environment is driving the populations in the areas invaded is the key to an effective future management. This current study is presenting a monthly long-term monitoring of the blue crabs' population structure, body size, sexual maturity, reproduction periods and fecundity, and their relationships with environmental factors in a saltmarshes system in Italy. During winter, high densities (15 ± 8 ind m-2) of early juveniles (< 2 cm) were observed, and their numbers decreased due the population growth until summer. The size-spectra showed that across different temperature (18-26°C) and salinity (24-40 psu) gradients, the growth period for males is faster than for females. Based on abdominal analysis, sexual maturity was defined at ∼12 cm for males and females but the population was in favor of males that were more than 66% of the time mature throughout the year. Copulations periods were identified between spring and autumn when more than 50% of females were matures, and ovigerous females' migrations were observed in late summer. Our study expand our understanding of how the environment interacts to effect physiological and biological processes of alien species and improve our ability to make predictions of how environmental change the distribution of the alien species in the future. Based on our results, we also discuss which population control strategy would be most effective based on the data available in the literature.

A new approach to assessing the space use behavior of macroinvertebrates by automated video tracking.

Individual space and resource use are central issues in ecology and conservation. Recent technological advances such as automated tracking techniques are boosting ecological research in this field. However, the development of a robust method to track space and resource use is still challenging for at least one important ecosystem component: motile aquatic macroinvertebrates. The challenges are mostly related to the small body size and rapid movement of many macroinvertebrate species and to light scattering and wave signal interference in aquatic habitats.We developed a video tracking method designed to reliably assess space use behavior among individual aquatic macroinvertebrates under laboratory (microcosm) conditions. The approach involves the use of experimental apparatus integrating a near infrared backlight source, a Plexiglas multi-patch maze, multiple infrared cameras, and automated video analysis. It allows detection of the position of fast-moving (~ 3 cm/s) and translucent individuals of small size (~ 5 mm in length, ~1 mg in dry weight) on simulated resource patches distributed over an experimental microcosm (0.08 m2).To illustrate the adequacy of the proposed method, we present a case study regarding the size dependency of space use behavior in the model organism Gammarus insensibilis, focusing on individual patch selection, giving-up times, and cumulative space used.In the case study, primary data were collected on individual body size and individual locomotory behavior, for example, mean speed, acceleration, and step length. Individual entrance and departure times were recorded for each simulated resource patch in the experimental maze. Individual giving-up times were found to be characterized by negative size dependency, with patch departure occurring sooner in larger individuals than smaller ones, and individual cumulative space used (treated as the overall surface area of resource patches that individuals visited) was found to scale positively with body size.This approach to studying space use behavior can deepen our understanding of species coexistence, yielding insights into mechanistic models on larger spatial scales, for example, home range, with implications for ecological and evolutionary processes, as well as for the management and conservation of populations and ecosystems. Despite being specifically developed for aquatic macroinvertebrates, this method can also be applied to other small aquatic organisms such as juvenile fish and amphibians.

Temperature effects on metabolic scaling of a keystone freshwater crustacean depend on fish-predation regime.

According to the metabolic theory of ecology, metabolic rate, an important indicator of the pace of life, varies with body mass and temperature as a result of internal physical constraints. However, various ecological factors may also affect metabolic rate and its scaling with body mass. Although reports of such effects on metabolic scaling usually focus on single factors, the possibility of significant interactive effects between multiple factors requires further study. In this study, we show that the effect of temperature on the ontogenetic scaling of resting metabolic rate of the freshwater amphipod Gammarus minus depends critically on habitat differences in predation regime. Increasing temperature tends to cause decreases in the metabolic scaling exponent (slope) in population samples from springs with fish predators, but increases in population samples from springs without fish. Accordingly, the temperature sensitivity of metabolic rate is not only size-specific, but also its relationship to body size shifts dramatically in response to fish predators. We hypothesize that the dampened effect of temperature on the metabolic rate of large adults in springs with fish, and of small juveniles in springs without fish are adaptive evolutionary responses to differences in the relative mortality risk of adults and juveniles in springs with versus without fish predators. Our results demonstrate a complex interaction among metabolic rate, body mass, temperature and predation regime. The intraspecific scaling of metabolic rate with body mass and temperature is not merely the result of physical constraints related to internal body design and biochemical kinetics, but rather is ecologically sensitive and evolutionarily malleable.

A Perspective on Body Size and Abundance Relationships across Ecological Communities.

Recently, several studies have reported relationships between the abundance of organisms in an ecological community and their mean body size (called cross-community scaling relationships: CCSRs) that can be described by simple power functions. A primary focus of these studies has been on the scaling exponent (slope) and whether it approximates -3/4, as predicted by Damuth's rule and the metabolic theory in ecology. However, some CCSR studies have reported scaling exponents significantly different from the theoretical value of -3/4. Why this variation occurs is still largely unknown. The purpose of our commentary is to show the value of examining both the slopes and elevations of CCSRs and how various ecological factors may affect them. As a heuristic exercise, we reanalyzed three published data sets based on phytoplankton, rodent, and macroinvertebrate assemblages that we subdivided according to three distinctly different ecological factors (i.e., climate zone, season, and trophic level). Our analyses reveal significant variation in either or both the CCSR slopes and elevations for marine phytoplankton communities across climate zones, a desert rodent community across seasons, and saltwater lagoon macroinvertebrate communities across trophic levels. We conclude that achieving a comprehensive understanding of abundance-size relationships at the community level will require consideration of both slopes and elevations of these relationships and their possible variation in different ecological contexts.

Size dependency of patch departure behavior: evidence from granivorous rodents.

Individual size is a major determinant of mobile organisms' ecology and behavior. This study aims to explore whether allometric scaling principles can provide an underlying framework for general patterns of resource patch use. To this end, we used giving-up densities (GUDs), that is, the amount of resources remaining in a patch after a forager has quit feeding, as a comparative measure of the amount of resources exploited by a forager of any given size. We specifically tested the hypothesis that size-dependent responses to both internal (energy requirement) and external (risk management) forces may have an effect on GUDs. We addressed this topic by conducting an extensive meta-analysis of published data on granivorous rodents, including 292 GUD measurements reported in 25 papers. The data set includes data on 22 granivorous rodent species belonging to three taxonomic suborders (Castorimorpha, Myomorpha, and Sciuromorpha) and spans three habitat types (desert, grassland, and forest). The observations refer to both patches subject to predation risk and safe patches. Pooling all data, we observed positive allometric scaling of GUDs with average forager size (scaling exponent = 0.45), which explained 15% of overall variance in individual GUDs. Perceived predation risk during foraging led to an increase in GUDs independently of forager size and taxonomy and of habitat type, which explained an additional 12% of overall GUD variance. The size scaling exponent of GUDs is positive across habitat types and taxonomic suborders of rodents. Some variation was observed, however. The scaling coefficients in grassland and forest habitat types were significantly higher than in the desert habitat type. In addition, Sciuromorpha and Myomorpha exhibited a more pronounced size scaling of GUDs than Castorimorpha. This suggests that different adaptive behaviors may be used in different contexts and/or from different foragers. With body size being a fundamental ecological descriptor, research into size scaling of GUDs may help to place patch-use observations in a broader allometric framework.

A process based model of cohesive sediment resuspension under bioturbators' influence.

Macrozoobenthos may affect sediment stability and erodibility via their bioturbating activities, thereby impacting both the short- and long-term development of coastal morphology. Process-based models accounting for the effect of bioturbation are needed for the modelling of erosion dynamics. With this work, we explore whether the fundamental allometric principles of metabolic activity scaling with individual and population size may provide a framework to derive general patterns of bioturbation effect on cohesive sediment resuspension. Experimental flumes were used to test this scaling approach across different species of marine, soft-sediment bioturbators. The collected dataset encompasses a range of bioturbator functional diversity, individual densities, body sizes and overall population metabolic rates. Measurements were collected across a range of hydrodynamic stress from 0.02 to 0.25 Pa. Overall, we observed that bioturbators are able to slightly reduce the sediment resuspension at low hydrodynamic stress, whereas they noticeably enhance it at higher levels of stress. Along the whole hydrodynamic stress gradient, the quantitative effect of bioturbators on sediment resuspension can be efficiently described by the overall metabolic rate of the bioturbating benthic communities, with significant variations across the bioturbators' taxonomic and functional diversity. One of the tested species (the gallery-builder Polychaeta Hediste diversicolor) had an effect that was partially deviating from the general trend, being able to markedly reduce sediment resuspension at low hydrodynamic stress compared to other species. By combining bioturbators' influence with hydrodynamic force, we were able to produce a process-based model of biota-mediated sediment resuspension.