Testing the metabolic theory of ecology: allometric scaling exponents in mammals

Many fundamental traits of species measured at different levels of biological organization appear to scale as a power law to body mass (M) with exponents that are multiples of 1/4. Recent work has united these relationships in a "metabolic theory of ecology" (MTE) that explains the pervasiveness of quarter-power scaling by its dependence on basal metabolic rate (B), which scales as M(0.75). Central to the MTE is theory linking the observed -0.25 scaling of maximum population growth rate (rm) and body mass to the 0.75 scaling of metabolic rate and body mass via relationships with age at first reproduction (alpha) derived from a general growth model and demographic theory. We used this theory to derive two further predictions: that age at first reproduction should scale inversely to mass-corrected basal metabolic rate alpha infinity (B/M)(-l) such that rm infinity (B/M)1. We then used phylogenetic generalized least squares and model selection methods to test the predicted scaling relationships using data from 1197 mammalian species. There was a strong phylogenetic signal in these data, highlighting the need to account for phylogeny in allometric studies. The 95% confidence intervals included, or almost included, the scaling exponent predicted by MTE for B infinity M(0.75), rm infinity M(-0.25), and rm infinity alpha(-1), but not for alpha infinity M(0.25) or the two predictions that we generated. Our results highlight a mismatch between theory and observation and imply that the observed -0.25 scaling of maximum population growth rate and body mass does not arise via the mechanism proposed in the MTE.     

One size fits all: stability of metabolic scaling under warming and ocean acidification in echinoderms

Responses by marine species to ocean acidification (OA) have recently been shown to be modulated by external factors including temperature, food supply and salinity. However the role of a fundamental biological parameter relevant to all organisms, that of body size, in governing responses to multiple stressors has been almost entirely overlooked. Recent consensus suggests allometric scaling of metabolism with body size differs between species, the commonly cited ‘universal’ mass scaling exponent (b) of ¾ representing an average of exponents that naturally vary. One model, the Metabolic-Level Boundaries hypothesis, provides a testable prediction: that b will decrease within species under increasing temperature. However, no previous studies have examined how metabolic scaling may be directly affected by OA. We acclimated a wide body-mass range of three common NE Atlantic echinoderms (the sea star Asterias rubens, the brittlestars Ophiothrix fragilis and Amphiura filiformis) to two levels of pCO₂ and three temperatures, and metabolic rates were determined using closed-chamber respirometry. The results show that contrary to some models these echinoderm species possess a notable degree of stability in metabolic scaling under different abiotic conditions; the mass scaling exponent (b) varied in value between species, but not within species under different conditions. Additionally, we found no effect of OA on metabolic rates in any species. These data suggest responses to abiotic stressors are not modulated by body size in these species, as reflected in the stability of the metabolic scaling relationship. Such equivalence in response across ontogenetic size ranges has important implications for the stability of ecological food webs.     

Aluminum neurotoxicity in mammals

Although aluminum comprises a large percentage of the Earth's crust, it is excluded from body tissues, and especially from the central nervous system. When aluminum is experimentally introduced to the central nervous system, several neurotoxic effects are observed:i.e. neurofibrillary changes, behavioral and cognitive deficits and enzymatic and neurotransmitter changes, as well as certain types of epileptic seizures.The localization of relatively high levels of aluminum in Alzheimer disease, Guamanian amyotrophic lateral sclerosis and Parkinsonism-dementia has led to the implication of aluminum as a pathogenic factor in these diseases. Recent studies have shown that microtubule-associated proteins are part of the paired helical filaments which make up the intraneuronal neurofibrillary tangle. Other studies have identified the protein making the vascular and neuritic (senile) plaque amyloid and located the gene responsible for this protein to chromosome 21.Our electron microprobe analysis studies have not found the levels of aluminum or silicon in either the neurofibrillary tangles or amyloid cores reported elsewhere, nor have the levels of aluminum been elevated in approximately one half of the tangles and plaque cores examined to date.     

Phylogeny, niches, and relative abundance in natural communities

Community structure refers to the number of species in a community and the pattern of distribution of individuals among those species. We use a novel way of representing community structure to show that abundance within closely related pairs of co-occurring tree species in a highly diverse Mexican forest is more equitable than is abundance within more distantly related pairs. This observation is at odds with the fundamental assumption of neutral models of community structure, i.e., that species are interchangeable. The observed patterns suggest niche apportionment, in which interaction is focused pairwise between congeners but falls away from the phylogenetic structure above the genus level. Thus niche processes may significantly affect community structure through regulating relative abundance in a substantial proportion of species, which in turn potentially enhances community stability. One such mechanism of stable coexistence has already been shown to be active in this forest.     

Consistent scaling of persistence time in metapopulations

Recent theory and experimental work in metapopulations and metacommunities demonstrates that long-term persistence is maximized when the rate at which individuals disperse among patches within the system is intermediate; if too low, local extinctions are more frequent than recolonizations, increasing the chance of regional-scale extinctions, and if too high, dynamics exhibit region-wide synchrony, and local extinctions occur in near unison across the region. Although common, little is known about how the size and topology of the metapopulation (metacommunity) affect this bell-shaped relationship between dispersal rate and regional persistence time. Using a suite of mathematical models, we examined the effects of dispersal, patch number, and topology on the regional persistence time when local populations are subject to demographic stochasticity. We found that the form of the relationship between regional persistence time and the number of patches is consistent across all models studied; however, the form of the relationship is distinctly different among low, intermediate, and high dispersal rates. Under low and intermediate dispersal rates, regional persistence times increase logarithmically and exponentially (respectively) with increasing numbers of patches, whereas under high dispersal, the form of the relationship depends on local dynamics. Furthermore, we demonstrate that the forms of these relationships, which give rise to the bell-shaped relationship between dispersal rate and persistence time, are a product of recolonization and the region-wide synchronization (or lack thereof) of population dynamics. Identifying such metapopulation attributes that impact extinction risk is of utmost importance for managing and conserving the earth's evermore fragmented populations.     

Crown ratio influences allometric scaling in trees

Allometric theories suggest that the size and shape of organisms follow universal rules, with a tendency toward quarter-power scaling. In woody plants, however, structure is influenced by branch death and shedding, which leads to decreasing crown ratios, accumulation of heartwood, and stem and branch tapering. This paper examines the impacts on allometric scaling of these aspects, which so far have been largely ignored in the scaling theory. Tree structure is described in terms of active and disused pipes arranged as an infinite branching network in the crown, and as a tapering bundle of pipes below the crown. Importantly, crown ratio is allowed to vary independently of crown size, the size of the trunk relative to the crown deriving from empirical results that relate crown base diameter to breast height diameter through crown ratio. The model implies a scaling relationship in the crown which reduces to quarter-power scaling under restrictive assumptions but would generally yield a scaling exponent somewhat less than three-quarters. For the whole tree, the model predicts that scaling between woody mass and foliage depends on crown ratio. Measurements on three boreal tree species are consistent with the model predictions.     

Scent-rubbing and status signalling by male mammals

Summary There is no consensus about the function of scent-rubbing, a widespread behaviour in which mammals rub their bodies vigorously in substances, many strong-smelling and some artificial, such as rotting meat, intestinal contents and engine oil. Here we suggest that scent-rubbing is involved in status advertisement and that, as in assessment using scent marks, the mechanism used by competitors to assess potential opponents may be scent-matching. In scent-matching a resource holder is assessed (identified) by comparing its odour with odours on or near the defended resource. In scent marking the odour originates from the resource holder (glandular secretion, urine and faeces); in scent-rubbing the odour originates in the environment.A prerequisite of unambiguous scent-matching is that the odour of scent-marks should be uniquely characteristic of one individual. This may be why marking substances are very complex chemically. Scent-rubbing often occurs with scent-marking and, rather than acting independently of scent-marking, the odours acquired may either (i) add to the complexity of the signal, thus reducing signal ambiguity, or (ii) increase the range of the signal by adding a strong smelling component.Subordinates could potentially cheat by rubbing in the same odours as the resource holder. Resource holders could prevent cheating (i) by checking other status cues and by testing competitors whose scent matches, then escalating contests when the competitor's fighting ability (more formally, Resource Holding Power) proves to be lower than that of a resource holder and (ii) by mixing the substances used for scent-rubbing with the unique substances used in scent-marking.     

Social monogamy and the threat of infanticide in larger mammals

The evolution of social monogamy in larger mammals is difficult to explain because males usually do not invest much in direct offspring care and might achieve greater fitness by deserting a pregnant female to reproduce with additional females elsewhere. It has been hypothesized that socially monogamous males remain with the female year-round to protect their offspring from infanticide by new immigrant males. We investigated this idea by analyzing all cases of infant loss in a wild population of white-handed gibbons (Hylobates lar; Primates), in which most groups were socially monogamous and some polyandrous (137.5 group years). We examined the influence of (a) male intruder pressure on male immigration rates and (b) the presence of a new male in the group on infant loss. We found no relation between intruder pressure and male immigration rates. Infant loss was lowest (4.5%) for stable monogamy (probable father stayed from conception through infancy) and intermediate (25.0%; p = 0.166) for stable polyandry. If a new male immigrated after conception, however, the infant was lost in all cases (p < 0.01) independent of the presumed father’s presence. Overall, 83.3% of infant losses were associated with the presence of a presumably unrelated male. Although the sample size is small, our results provide the first true support for the idea that the risk of infanticide is an important factor in the evolution of social monogamy in larger mammals.     

Decoupling of component and ensemble density feedbacks in birds and mammals

A component density feedback represents the effect of change in population size on single demographic rates, whereas an ensemble density feedback captures that effect on the overall growth rate of a population. Given that a population's growth rate is a synthesis of the interplay of all demographic rates operating in a population, we test the hypothesis that the strength of ensemble density feedback must augment with increasing strength of component density feedback, using long-term censuses of population size, fertility, and survival rates of 109 bird and mammal populations (97 species). We found that compensatory and depensatory component feedbacks were common (each detected in approximately 50% of the demographic rates). However, component feedback strength only explained <10% of the variation in ensemble feedback strength. To explain why, we illustrate the different sources of decoupling between component and ensemble feedbacks. We argue that the management of anthropogenic impacts on populations using component feedbacks alone is ill-advised, just as managing on the basis of ensemble feedbacks without a mechanistic understanding of the contributions made by its components and environmental variability can lead to suboptimal decisions.     

Froude scaling limitations in modeling of turbidity currents

The scaling problem associated with the modeling of turbidity currents has been recognized but is yet to be explored systematically. This paper presents an analysis of the dimensionless governing equations of turbidity currents to investigate the scale effect. Three types of flow conditions are considered: (i) conservative density current; (ii) purely depositional turbidity current; and (iii) mixed erosional/depositional turbidity current. Two controlling dimensionless numbers, the Froude number and the Reynolds number, appear in the non-dimensional governing equations. When densimetric Froude similarity is satisfied, the analysis shows that the results would be scale-invariant for conservative density current under the rough turbulent condition. In the case of purely depositional flows, truly scale-invariant results cannot be obtained, as the Reynolds-mediated scale effects appear in the bottom boundary conditions of the flow velocity and sediment fall velocity. However, the scale effect would be relatively modest. The Reynolds effect becomes more significant for erosional or mixed erosional/depositional turbidity currents as Reynolds-mediated scale effects also appear in the sediment entrainment relation. Numerical simulations have been conducted at three different scales by considering densimetric Froude scaling alone as well as combined densimetric Froude and Reynolds similarity. Simulation results confirm that although the scaling of densimetric Froude number alone can produce scale-invariable results for conservative density currents, variations occur in the case of turbidity currents. The results become scale invariant when densimetric Froude and Reynolds similarities are satisfied simultaneously.     

A dynamic explanation of size-density scaling in carnivores

Population abundance is negatively related to body size for many types of organisms. Despite the ubiquity of size-density scaling relationships, we lack a general understanding of the underlying mechanisms. Although dynamic models suggest that it is possible to predict the intercept and slope of the scaling relationship from prior observations, this has never been empirically attempted. Here we fully parameterize a set of consumer-resource models for mammalian carnivores and successfully predict the size-density scaling relationship for this group without the use of free parameters. All models produced similar predictions, but comparison of nested models indicated that the primary factors generating size-density scaling in mammalian carnivores are prey productivity, predator-prey size ratios, and consumer area of capture.     

Sibling competition and cooperation in mammals: challenges,developments and prospects

Many vertebrates grow up in the company of same or different-age siblings, and relations among them can be expected to significantly influence individual life histories and the development of individual morphological, physiological, and behavioral phenotypes. Although studies in birds still dominate and have stimulated most theoretical considerations, the increasing number of mammalian studies promises to broaden our understanding of this complex field by enabling interesting comparisons with the rather different bird system. It therefore seems timely to bring together recent studies of sibling relations in mammals and to demonstrate what these can offer in the way of fresh insights. In this brief review, intended to accompany a series of papers on a diverse range of mammals, we outline the current state of sibling research in mammals, comparing it to the better studied birds. Most obviously, in mammals, mother and young are in much closer contact during early life than in birds, and siblings can influence each other’s development as well as the mother’s physiology while still in utero. During nursing, mammalian young also encounter a very different feeding situation to bird siblings. These contrasts should help stimulate further debate, as well as provide further opportunities to study the relative importance of maternal versus sibling effects on individual development. Finally, we discuss the need to balance studies of sibling competition and conflict with a consideration of the benefits accruing to individuals from sibling presence and the need for long-term studies of the influence of early sibling relations on individual development and life histories. This contribution represents the introduction to the special issue “Sibling competition and cooperation in mammals”.     

The top-down mechanism for body-mass-abundance scaling

Scaling relationships between mean body masses and abundances of species in multitrophic communities continue to be a subject of intense research and debate. The top-down mechanism explored in this paper explains the frequently observed inverse linear relationship between body mass and abundance (i.e., constant biomass) in terms of a balancing of resource biomasses by behaviorally and evolutionarily adapting foragers, and the evolutionary response of resources to this foraging pressure. The mechanism is tested using an allometric, multitrophic community model with a complex food web structure. It is a statistical model describing the evolutionary and population dynamics of tens to hundreds of species in a uniform way. Particularities of the model are the detailed representation of the evolution and interaction of trophic traits to reproduce topological food web patterns, prey switching behavior modeled after experimental observations, and the evolutionary adaptation of attack rates. Model structure and design are discussed. For model states comparable to natural communities, we find that (1) the body-mass abundance scaling does not depend on the allometric scaling exponent of physiological rates in the form expected from the energetic equivalence rule or other bottom-up theories; (2) the scaling exponent of abundance as a function of body mass is approximately -1, independent of the allometric exponent for physiological rates assumed; (3) removal of top-down control destroys this pattern, and energetic equivalence is recovered. We conclude that the top-down mechanism is active in the model, and that it is a viable alternative to bottom-up mechanisms for controlling body-mass-abundance relations in natural communities.     

Allocation within a generic scaling framework

Barnes and Roderick [Barnes, B., Roderick, M.L., 2004. An ecological framework linking scales across space and time based on self-thinning. Theoret. Popul. Biol. 66, 113–128] developed a generic ecological framework for scaling from individuals to ecosystems. Their approach is general and can be applied to predict above-ground, or total (above- and below-ground), dry mass. In practice, the most common situation is to measure above-ground dry mass, and apply an allometric relationship to estimate the below-ground component. In this paper we develop a general theory for incorporating the dynamics of plant partitioning into the generic framework. We consider the inclusion of allometric relationships between components (such as between roots and shoots), as well as process driven relationships, and illustrate the application of each case. Through this approach, local scale measurements and individual-based dynamic relationships pertaining to plant partitioning can be applied to an understanding of partitioning at the patch (or ecosystem) scale. Moreover, we also demonstrate that the empirically based allometric relationships have, in some circumstances, a physical explanation, providing biological meaning to empirically established allometric constants.     

Allometric scaling of resource acquisition by ruminants in dynamic and heterogeneous environments

We present a mechanistic formulation of the intake response of ruminants to vegetation biomass based solely on physiological and morphological parameters that scale allometrically with the animal's body mass. The model is applied to describe herbivore-vegetation interactions in dynamic and heterogeneous landscapes with low quality but abundant “tall grass” and high quality but sparsely available “short grass”, under two conditions: “uncoupled” (such that the effect of food intake on vegetation biomass can be neglected), or “coupled” (such that the vegetation biomass is determined by herbivore feeding). The results show that under uncoupled conditions, the minimum acceptance (proportion of vegetation consumed by the herbivore) at which the herbivore can leave its current patch without reducing its intake rate is when it has depleted the current patch by the energetic cost required to travel to another patch. The maximum acceptance at which the herbivore should leave its patch is when it has depleted the current patch by the cumulative energetic cost of traveling, handling, cropping, and digesting. Under coupled conditions, the optimal acceptance equals half the relative growth rate of the vegetation. Analytical solutions are obtained for equilibrium values for utilization of the vegetation, and for the densities of vegetation and ruminants, expressed in physiological and morphological herbivore parameters.     

Safety in numbers and the spatial scaling of density-dependent mortality in a coral reef fish

In coral reef fishes, density-dependent population regulation is commonly mediated via predation on juveniles that have recently settled from the plankton. All else being equal, strong density-dependent mortality should select against the formation of high-density aggregations, yet the juveniles of many reef fishes aggregate. In light of this apparent contradiction, we hypothesized that the form and intensity of density dependence vary with the spatial scale of measurement. Individual groups might enjoy safety in numbers, but predators could still produce density-dependent mortality at larger spatial scales. We investigated this possibility using recently settled juvenile bluehead wrasse, Thalassoma bifasciatum, a small, aggregating reef fish. An initial caging experiment demonstrated that juvenile bluehead wrasse settlers suffer high predation, and spatial settlement patterns indicated that bluehead wrasse juveniles preferentially settle in groups, although they are also found singly. We then monitored the mortality of recently settled juveniles at two spatial scales: microsites, occupied by individual fish or groups of fish and separated by centimeters, and sites, consisting of approximately 2400-m2 areas of reef and separated by kilometers. At the microsite scale, we measured group size and effective population density independently and found that per capita mortality decreased with group size but was not related to density. At the larger spatial scale, however, per capita mortality increased with settler density. This shift in the form of density dependence with spatial scale could reconcile the existence of small-scale aggregative behavior typical of many reef fishes with the population-scale density dependence that is essential to population stability and persistence.     

Metabolic scaling,buoyancy, and growth in larval Atlantic menhaden,Brevoortia tyrannus

We measured growth of larval Atlantic menhaden, Brevoortia tyrannus in terms of mass, volume, and weight in water as well as the mass-specific activities of the metabolic enzymes citrate synthase, lactate dehydrogenase, and malate dehydrogenase. Weight in water, the force the fish must exert to maintain vertical position, increases by a factor of 18 in larvae growing from 10 to 15 mm. The weight increase coincides with the development of the larval swim bladder. The activities of all three enzymes per unit mass of fish tissue decline greatly over this time period, indicating that the fish does not further develop its aerobic and anaerobic metabolic capacity for swimming during this growth interval.     

Active density-dependent habitat selection in a controlled population of small mammals

Density-dependent habitat selection has numerous and far-reaching implications to population dynamics and evolutionary processes. Although several studies suggest that organisms choose and occupy high-quality habitats over poorer ones, definitive experiments demonstrating active selection, by the same individuals at the appropriate population scale, are lacking. We conducted a reciprocal food supplementation experiment to assess whether voles would first occupy a habitat receiving extra food, then change their preference to track food supplements moved to another habitat. Meadow voles, as predicted, were more abundant in food-supplemented habitat than in others. Density declined when food supplements ceased because the voles moved to the new habitat receiving extra food. Although males and females appeared to follow different strategies, meadow-vole densities reflected habitat quality because voles actively selected the best habitat available. It is thus clear that behavioral decisions on habitat use can motivate patterns of abundance, frequency, and gene flow that have widespread effects on subsequent evolution.     

Identifying conservation priorities for threatened Eastern Himalayan mammals

To augment mammal conservation in the Eastern Himalayan region, we assessed the resident 255 terrestrial mammal species and identified the 50 most threatened species based on conservation status, endemism, range size, and evolutionary distinctiveness. By using the spatial analysis package letsR and the complementarity core‐area method in the conservation planning software Zonation, we assessed the current efficacy of their protection and identified priority conservation areas by comparing protected areas (PAs), land cover, and global ecoregion 2017 maps at a 100 × 100 m spatial scale. The 50 species that were most threatened, geographically restricted, and evolutionarily distinct faced a greater extinction risk than globally nonthreatened and wide‐ranging species and species with several close relatives. Small, medium‐sized, and data‐deficient species faced extinction from inadequate protection in PAs relative to wide‐ranging charismatic species. There was a mismatch between current PA distribution and priority areas for conservation of the 50 most endangered species. To protect these species, the skewed regional PA distribution would require expansion. Where possible, new PAs and transboundary reserves in the 35 priority areas we identified should be established. There are adequate remaining natural areas in which to expand current Eastern Himalayan PAs. Consolidation and expansion of PAs in the EH requires strengthening national and regional transboundary collaboration, formulating comprehensive regional land‐use plans, diversifying conservation funding, and enhancing information sharing through a consolidated regional database.     

Critical factors for the recovery of marine mammals

{en} Over the past decades, much research has focused on understanding the critical factors for marine extinctions with the aim of preventing further species losses in the oceans. Although conservation and management strategies are enabling several species and populations to recover, others remain at low abundance levels or continue to decline. To understand these discrepancies, we used a published database on abundance trends of 137 populations of marine mammals worldwide and compiled data on 28 potentially critical factors for recovery. We then applied random forests and additive mixed models to determine which intrinsic and extrinsic factors are critical for the recovery of marine mammals. A mix of life‐history characteristics, ecological traits, phylogenetic relatedness, population size, geographic range, human impacts, and management efforts explained why populations recovered or not. Consistently, species with lower age at maturity and intermediate habitat area were more likely to recover, which is consistent with life‐history and ecological theory. Body size, trophic level, social interactions, dominant habitat, ocean basin, and habitat disturbance also explained some differences in recovery patterns. Overall, a variety of intrinsic and extrinsic factors were important for species’ recovery, pointing to cumulative effects. Our results provide insight for improving conservation and management strategies to enhance recoveries in the future.