The Conversation: Why are bigger animals more energy-efficient? A new answer to a centuries-old biological puzzle

By Craig White and Dustin Marshall

This article is republished from The Conversation under a Creative Commons licence.

If you think about “unravelling the mysteries of the universe”, you probably think of physics: astronomers peering through telescopes at distant galaxies, or experimenters smashing particles to smithereens at the Large Hadron Collider.

When biologists try to unravel deep mysteries of life, we too tend to reach for physics. But our new research, published in Science, shows physics may not always have the answers to questions of biology.

For centuries scientists have asked why, kilo for kilo, large animals burn less energy and require less food than small ones. Why does a tiny shrew need to consume as much as three times its body weight in food each day, while an enormous baleen whale can get by on a daily diet of just 5-30% of its body weight in krill?

While previous efforts to explain this relationship have relied on physics and geometry, we believe the real answer is evolutionary. This relationship is what maximises an animal’s ability to produce offspring.

How much do physical constraints shape life?

The earliest explanation for the disproportionate relationship between metabolism and size was proposed nearly 200 years ago.

In 1837, French scientists Pierre Sarrus and Jean-François Rameaux argued energy metabolism should scale with surface area, rather than body mass or volume. This is because metabolism produces heat, and the amount of heat an animal can dissipate depends on its surface area.

In the 185 years since Sarrus and Rameaux’s presentation, numerous alternative explanations for the observed scaling of metabolism have been proposed.

Arguably the most famous of these was published by US researchers Geoff West, Jim Brown and Brian Enquist in 1997. They proposed a model describing the physical transport of essential materials through networks of branching tubes, like the circulatory system.

They argued their model offers “a theoretical, mechanistic basis for understanding the central role of body size in all aspects of biology”.

These two models are philosophically similar. Like numerous other approaches put forward over the past century, they try to explain biological patterns by invoking physical and geometric constraints.

Evolution finds a way

Living organisms cannot defy the laws of physics. Yet evolution has proven to be remarkably good at finding ways to overcome physical and geometric constraints.

In our new research, we decided to see what happened to the relationship between metabolic rate and size if we ignored physical and geometric constraints like these.

So we developed a mathematical model of how animals use energy over their lifetimes. In our model, animals devote energy to growth early in their lives and then in adulthood devote increasing amounts of energy to reproduction.

Animals allocate more energy to reproduction after they reach maturity.

We used the model to determine what characteristics of animals result in the greatest amount of reproduction over their lifetimes – after all, from an evolutionary point of view reproduction is the main game.

We found that the animals that are predicted to be most successful at reproducing are those that exhibit precisely the kind of disproportionate scaling of metabolism with size that we see in real life!

This finding suggests disproportionate metabolic scaling is not an inevitable consequence of physical or geometric constraints. Instead, natural selection produces this scaling because it is advantageous for lifetime reproduction.

The unexplored wilderness

In the famous words of Russian-American evolutionary biologist Theodosius Dobzhansky, “nothing makes sense in biology except in the light of evolution”.

Our finding that disproportionate scaling of metabolism can arise even without physical constraints suggests we have been looking in the wrong place for explanations.

Physical constraints may be the principal drivers of biological patterns less often than has been thought. The possibilities available to evolution are broader than we appreciate.

Why have we historically been so willing to invoke physical constraints to explain biology? Perhaps because we are more comfortable in the safe refuge of seemingly universal physical explanations than in the relatively unexplored biological wilderness of evolutionary explanations.
The Conversation

Metabolic scaling is the product of life-history optimization

Authors: Craig R White, Lesley A Alton, Candice L Bywater, Emily J Lombardi and Dustin J Marshall

Published in: Science

Abstract

Organisms use energy to grow and reproduce, so the processes of energy metabolism and biological production should be tightly bound. On the basis of this tenet, we developed and tested a new theory that predicts the relationships among three fundamental aspects of life: metabolic rate, growth, and reproduction.

We show that the optimization of these processes yields the observed allometries of metazoan life, particularly metabolic scaling. We conclude that metabolism, growth, and reproduction are inextricably linked; that together they determine fitness; and, in contrast to longstanding dogma, that no single component drives another.

Our model predicts that anthropogenic change will cause animals to evolve decreased scaling exponents of metabolism, increased growth rates, and reduced lifetime reproductive outputs, with worrying consequences for the replenishment of future populations.

White CR, Alton LA, Bywater CL, Lombardi EJ, Marshall DJ (2022) Metabolic scaling is the product of life-history optimization. Science DOI

Long-term experimental evolution decouples size and production costs in Escherichia coli

Authors: Dustin J Marshall, Martino Malerba, Thomas Lines, Aysha L Sezmis, Chowdhury M Hasan, Richard E Lenski, and Michael J McDonald

Published in: Proceedings of the National Academy of Sciences of the United States of America (PNAS)

Significance

Populations of larger organisms should be more efficient in their resource use, but grow more slowly, than populations of smaller organisms.

The relations between size, metabolism, and demography form the bedrock of metabolic theory, but most empirical tests have been correlative and indirect.

Experimental lineages of Escherichia coli that evolved to make larger cells provide a unique opportunity to test how size, metabolism, and demography covary. Despite the larger cells having a relatively slower metabolism, they grow faster than smaller cells. They achieve this growth rate advantage by reducing the relative costs of producing their larger cells.

That evolution can decouple the costs of production from size challenges a fundamental assumption about the connections between physiology and ecology.

Abstract

Body size covaries with population dynamics across life’s domains. Metabolism may impose fundamental constraints on the coevolution of size and demography, but experimental tests of the causal links remain elusive.

We leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters.

Over the course of their evolution, the cells have roughly doubled in size relative to their ancestors. These larger cells have metabolic rates that are absolutely higher, but relative to their size, they are lower.

Metabolic theory successfully predicted the relations between size, metabolism, and maximum population density, including support for Damuth’s law of energy equivalence, such that populations of larger cells achieved lower maximum densities but higher maximum biomasses than populations of smaller cells. The scaling of metabolism with cell size thus predicted the scaling of size with maximum population density. In stark contrast to standard theory, however, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental and intuitive assumption that the costs of building new individuals should scale directly with their size.

The finding that the costs of production can be decoupled from size necessitates a reevaluation of the evolutionary drivers and ecological consequences of biological size more generally.

Marshall DJ, Malerba M, Lines T, Sezmis AL, Hasan CM, Lenski RE, McDonald MJ (2022) Long-term experimental evolution decouples size and production costs in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America PDF DOI

Metabolic phenotype mediates the outcome of competitive interactions in a response-surface field experiment

Authors: Lukas Schuster, Craig R White, and Dustin J Marshall

Published in: Ecology and Evolution

Abstract

Competition and metabolism should be linked. Intraspecific variation in metabolic rates and, hence, resource demands covary with competitive ability. The effects of metabolism on conspecific interactions, however, have mostly been studied under laboratory conditions.

We used a trait-specific response-surface design to test for the effects of metabolism on pairwise interactions of the marine colonial invertebrate, Bugula neritina in the field.

Specifically, we compared the performance (survival, growth, and reproduction) of focal individuals, both in the presence and absence of a neighbor colony, both of which had their metabolic phenotype characterized.

Survival of focal colonies depended on the metabolic phenotype of the neighboring individual, and on the combination of both the focal and neighbor colony metabolic phenotypes that were present.

Surprisingly, we found pervasive effects of neighbor metabolic phenotypes on focal colony growth and reproduction, although the sign and strength of these effects showed strong microenvironmental variability.

Overall, we find that the metabolic phenotype changes the strength of competitive interactions, but these effects are highly contingent on local conditions. We suggest future studies explore how variation in metabolic rate affects organisms beyond the focal organism alone, particularly under field conditions.

Schuster L, White CR, Marshall DJ (2021) Metabolic phenotype mediates the outcome of competitive interactions in a response‐surface field experiment. Ecology and Evolution PDF DOI 

Predicting the response of disease vectors to global change: The importance of allometric scaling

Authors: Louise S Nørgaard, Mariana Álvarez-Noriega, Elizabeth McGraw, Craig R White, and Dustin J Marshall

Published in: Global Change Biology

Abstract

The distribution of disease vectors such as mosquitoes is changing. Climate change, invasions and vector control strategies all alter the distribution and abundance of mosquitoes.

When disease vectors undergo a range shift, so do disease burdens. Predicting such shifts is a priority to adequately prepare for disease control. Accurate predictions of distributional changes depend on how factors such as temperature and competition affect mosquito life-history traits, particularly body size and reproduction.

Direct estimates of both body size and reproduction in mosquitoes are logistically challenging and time-consuming, so the field has long relied upon linear (isometric) conversions between wing length (a convenient proxy of size) and reproductive output. These linear transformations underlie most models projecting species’ distributions and competitive interactions between native and invasive disease vectors.

Using a series of meta-analyses, we show that the relationship between wing length and fecundity are nonlinear (hyperallometric) for most mosquito species. We show that whilst most models ignore reproductive hyperallometry (with respect to wing length), doing so introduces systematic biases into estimates of population growth. In particular, failing to account for reproductive hyperallometry overestimates the effects of temperature and underestimates the effects of competition. Assuming isometry also increases the potential to misestimate the efficacy of vector control strategies by underestimating the contribution of larger females in population replenishment.

Finally, failing to account for reproductive hyperallometry and variation in body size can lead to qualitative errors via the counter-intuitive effects of Jensen’s inequality. For example, if mean sizes decrease, but variance increases, then reproductive outputs may actually increase.

We suggest that future disease vector models incorporate hyperallometric relationships to more accurately predict changes in mosquito distribution in response to global change.

Nørgaard LS, Álvarez‐Noriega M, McGraw E, White CR, Marshall DJ (2021) Predicting the response of disease vectors to global change: The importance of allometric scaling. Global Change Biology PDF DOI 

Phytoplankton diversity affects biomass and energy production differently during community development

Authors: Giulia Ghedini, Dustin J Marshall, and Michel Loreau

Published in: Functional Ecology

Abstract

Biodiversity determines the productivity and stability of ecosystems but some aspects of biodiversity–ecosystem functioning relationships remain poorly resolved. One key uncertainty is the inter-relationship between biodiversity, energy and biomass production as communities develop over time. Energy production drives biomass accumulation but the ratio of the two processes can change during community development. How biodiversity affects these temporal patterns remains unknown.

We empirically assessed how species diversity mediates the rates of increase and maximum values of biomass and net energy production in experimental phytoplankton communities over 10 days in the laboratory. We used five phytoplankton species to assemble three levels of diversity (monocultures, bicultures and communities) and we quantify their changes in biomass production and energy fluxes (energy produced by photosynthesis, consumed by metabolism, and net energy production as their difference) as the cultures move from a low density, low competition system to a high density, high competition system.

We find that species diversity affects both biomass and energy fluxes but in different ways. Diverse communities produce net energy and biomass at faster rates, reaching greater maximum biomass but with no difference in maximum net energy production. Bounds on net energy production seem stronger than those on biomass because competition limits energy fluxes as biomass accumulates over time.

In summary, diversity initially enhances productivity by diffusing competitive interactions but metabolic density dependence reduces these positive effects as biomass accumulates in older communities. By showing how biodiversity affects both biomass and energy fluxes during community development, our results demonstrate a mechanism that underlies positive biodiversity effects and offer a framework for comparing biodiversity effects across systems at different stages of development and disturbance regimes.

Ghedini G, Marshall DJ, Loreau M (2021) Phytoplankton diversity affects biomass and energy production differently during community development. Functional Ecology PDF DOI 

How does spawning frequency scale with body size in marine fishes?

Authors: Dustin J Marshall, Diego R Barneche, and Craig R White

Published in: Fish and Fisheries

Abstract

How does fecundity scale with female size? Female size not only affects the number and size of offspring released in any one reproductive bout (i.e. batch fecundity) but also affects frequency of bouts that occur within a given spawning season (i.e. spawning frequency).

Previous studies have noted contrasting effects of female size on spawning frequency such that the effect of female size on reproductive output and total egg production of a population remains unclear. If smaller females spawn more frequently, this could effectively nullify hyperallometry—the disproportionate contribution of larger females to batch fecundity.

Here, we explore the relationship between female size and spawning frequency in marine fishes and test this relationship while controlling for phylogeny.

Within all of the species considered, spawning frequency scaled positively with body size. Comparing across species, the smallest species showed steeper scaling than the largest.

Considering only batch fecundity scaling probably underestimates the relationship between body size and absolute fecundity for many species; reproduction is likely to be more hyperallometric than is currently appreciated based on batch fecundity estimates. Second, an understanding of fecundity scaling depends on estimates of batch fecundity, spawning frequency and spawning duration—we have far more estimates of the first parameter than we do the others, and more studies are required.

Marshall DJ, Barneche DR, White CR (2021) How does spawning frequency scale with body size in marine fishes? Fish and Fisheries PDF DOI 

Metabolism drives demography in an experimental field test

Authors: Lukas Schuster, Hayley Cameron, Craig R White, and Dustin J Marshall

Published in: Proceedings of the National Academy of Sciences of the United States of America

Significance

Biology has long-standing rules about how metabolism and demography should covary. These rules connect physiology to ecology but remarkably, these rules have only ever been tested indirectly.

Using a model marine invertebrate, we created experimental field populations that varied in metabolic rate but not body size.

We show that metabolism qualitatively affects population growth and carrying capacity in ways predicted by theory but that scaling relationships for these parameters, as well as estimates of energy use at carrying capacity, depart from classic predictions.

That metabolism affects demography in ways that depart from canonical theory has important implications for predicting how populations may respond to global change and size-selective harvesting.

Abstract

Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing “rules” for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries.
Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare.

In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment.

We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory—in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence.

Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.

Schuster L, Cameron H, White CR, Marshall DJ (2021) Metabolism drives demography in an experimental field test. Proceedings of the National Academy of Sciences of the United States of America PDF DOI

Reproductive hyperallometry and managing the world’s fisheries

Authors: Dustin J Marshall, Michael Bode, Marc Mangel, Robert Arlinghaus, and EJ Dick

Published in: Proceedings of the National Academy of Sciences of the United States of America

Significance

We find that a ubiquitous assumption in fisheries models for predicting population replenishment introduces systematic overestimates of replenishment in fished populations.

For 32 of the world’s major fisheries, these biases result in harvest thresholds being set too high: in most cases, reference points based on spawning potential ratios are more than 2.5 times higher than those necessary to achieve the desired level of replenishment.

When we use the more biologically appropriate assumption of reproductive hyperallometry, we find that management tools such as spatiotemporal closures and harvest slots can outperform traditional approaches in terms of yield.

Failing to consider reproductive hyperallometry overestimates the efficacy of traditional fisheries management and underestimates the benefits of approaches that create reservoirs of larger individuals.

Abstract

Marine fisheries are an essential component of global food security, but many are close to their limits and some are overfished. The models that guide the management of these fisheries almost always assume reproduction is proportional to mass (isometry), when fecundity generally increases disproportionately to mass (hyperallometry).

Judged against several management reference points, we show that assuming isometry overestimates the replenishment potential of exploited fish stocks by 22% (range: 2% to 78%) for 32 of the world’s largest fisheries, risking systematic overharvesting.

We calculate that target catches based on assumptions of isometry are more than double those based on assumptions of hyperallometry for most species, such that common reference points are set twice as high as they should be to maintain the target level of replenishment.

We also show that hyperallometric reproduction provides opportunities for increasing the efficacy of tools that are underused in standard fisheries management, such as protected areas or harvest slot limits. Adopting management strategies that conserve large, hyperfecund fish may, in some instances, result in higher yields relative to traditional approaches.

We recommend that future assessment of reference points and quotas include reproductive hyperallometry unless there is clear evidence that it does not occur in that species.

Marshall DJ, Bode M, Mangel M, Arlinghaus R, Dick EJ (2021) Reproductive hyperallometry and managing the world’s fisheries. Proceedings of the National Academy of Sciences of the United States of America PDF DOI

Effects of light variation in algal cultures: a systematic map of temporal scales

Authors: Belinda Comerford, Nicholas Paul, and Dustin J Marshall

Published in: Journal of Applied Phycology

Abstract

Algal aquaculture is a rapidly growing field, with a proliferation of studies exploring algal growth. The expansion of the field not only presents opportunities for synthesis, but also creates challenges in identifying where the strengths and knowledge gaps exist.

One tool for formally quantifying the state of knowledge is a systematic map, already useful in many fields, but underutilised in algal research. We used a systematic map to describe variable light regimes in algal cultures.

Light variation is ubiquitous in algal cultures and spans a range of temporal scales (microseconds to months), but it is unclear which scales have been explored.

We characterised 1393 experiments according to the temporal scale of light variation that was manipulated. Intensely studied light variation frequencies were either very short (< seconds) or long (diel cycles); the prominent gap was frequencies between these extremes (seconds to hours), especially for experiments that lasted for long durations (> months). Experiments that lasted for days were most common, while few studies lasted for months or more. Most studies were conducted in small culture vessels, used instantaneous changes in light regimes, and few studies reported initial stocking density metrics consistently.

Our map highlights that the field has accumulated a rich knowledge base that is ripe for synthesis in some areas, particularly very short or relatively long frequency light variation. The map indicates that the key priorities are explorations of intermediate frequencies and our understanding of their effects is limited. Similarly, our understanding of evolutionary responses to variable light regimes of all scales is lagging.

Comerford B, Paul N, Marshall D (2021) Effects of light variation in algal cultures: a systematic map of temporal scales. Journal of Applied Phycology PDF DOI