How does size, fragmentation and food affect metabolic rates in a bryozoan?

We know that metabolic rate (a measure of energy use) tends to vary among individuals of different sizes and also with food availability. Lukas Schuster has been working with his PhD supervisors Craig White and Dustin Marshall to find out how metabolic rate changes with size in the colonial marine invertebrate Bugula neritina. They are also interested in how (or if) manipulating an organism’s size affects metabolic rate in individuals that were either starved or fed.

Lukas and his supervisors chose to work with Bugula because it is a colonial organism. These types of animals can be used for testing metabolic theories because the size of the colonies can be changed by removing fragments.

Lukas measured metabolic rate by measuring oxygen consumption of intact and size-manipulated colonies of Bugula that had been fed or starved as well as colonies that he had grown up in the field so he knew how old they were.

When Lukas measured metabolic rates for individuals of known age he found that rates increased proportionally with size across the different ages, that is, metabolic rate scaled isometrically with size when looking at individuals that ranged in age / developmental stage.  In contrast, when he looked at metabolic rates for a specific age or developmental stage he found that rates didn’t scale proportionally with size but, instead, had allometric scaling as has been found in previous studies.

Lukas and his supervisors point out that it is important to be aware of these differences. Measuring metabolic rates of field-collected specimens of unknown age may result in isometric scaling of metabolic rate with size. Conversely, measurements of specimens at the same developmental stage is likely to result in allometric scaling where larger individuals have proportionally lower metabolic rates compared to smaller individuals.

To the team’s surprise, they also found that when they measured metabolic rate in size-manipulated Bugula that has been collected from the field, metabolic rate reverted to allometric scaling. Manipulating size in Bugula may lead to a leaking of nutrients through the pores between the zooids that make up the colony and this may be driving the change in the relationship of metabolic rates with size.

Bugula responded to food deprivation by reducing its metabolic rate, and conversely responded to feeding by increasing its metabolic rate, which was consistent with what other researchers have found in other species. But, in comparison to other species, the rate at which Bugula increased its metabolic rate following feeding, was rather low. This may also relate to the fact that Bugula is a colonial species but as there are very few studies investigating the way metabolic rate responds to feeding in colonial organisms, it is hard to know for sure.

Clearly, the relationship between size and metabolic rates in Bugula is complicated and may relate, in part, to the fact that Bugula is a colonial organism. But to fully understand the effects of size manipulation on metabolic rates and biological processes within Bugula colonies, further studies will be needed.

This research is published in the journal Invertebrate Biology.

The origin and maintenance of metabolic allometry in animals

Authors:Craig R White, Dustin J Marshall, Lesley A Alton, Pieter A Arnold, Julian E Beaman, Candice L Bywater, Catriona Condon, Taryn S Crispin, Aidan Janetzki, Elia Pirtle, Hugh S Winwood-Smith, Michael J Angilletta Jr, Stephen F Chenoweth, Craig E Franklin, Lewis G Halsey, Michael R Kearney, Steven J Portugal, and Daniel Ortiz-Barrientos

Published in: Nature Ecology & Evolution


Organisms vary widely in size, from microbes weighing 0.1 pg to trees weighing thousands of megagrams — a 1021-fold range similar to the difference in mass between an elephant and the Earth.

Mass has a pervasive influence on biological processes, but the effect is usually non-proportional; for example, a tenfold increase in mass is typically accompanied by just a four- to sevenfold increase in metabolic rate.

Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns.

We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds and mammals.

We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.

White CR, Marshall DJ, Alton LA, Arnold PA, Beaman JE, Bywater CL, Condon C, Crispin TS, Janetzki A, Pirtle E, Winwood-Smith HS, Angilletta MJ, Chenoweth SF, Franklin CE, Halsey LG, Kearney MR, Portugal SJ, Ortiz-Barrientos D (2019) The origin and maintenance of metabolic allometry in animals. Nature Ecology & Evolution PDF DOI 

Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate

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

Published in: Invertebrate Biology


Metabolic rates vary among individuals according to food availability and phenotype, most notably body size. Disentangling size from other factors (e.g., age, reproductive status) can be difficult in some groups, but modular organisms may provide an opportunity for manipulating size experimentally. While modular organisms are increasingly used to understand metabolic scaling, the potential of feeding to alter metabolic scaling has not been explored in this group.

Here, we perform a series of experiments to examine the drivers of metabolic rate in a modular marine invertebrate, the bryozoan Bugula neritina. We manipulated size and examined metabolic rate in either fed or starved individuals to test for interactions between size manipulation and food availability.

Field collected colonies of unknown age showed isometric metabolic scaling, but those colonies in which size was manipulated showed allometric scaling.

To further disentangle age effects from size effects, we measured metabolic rate of individuals of known age and again found allometric scaling. Metabolic rate strongly depended on access to food: starvation decreased metabolic rate by 20% and feeding increased metabolic rate by 43%.

In comparison to other marine invertebrates, however, the increase in metabolic rate, as well as the duration of the increase (known as specific dynamic action, SDA), were both low. Importantly, neither starvation nor feeding altered the metabolic scaling of our colonies.

Overall, we found that field‐collected individuals showed isometric metabolic scaling, whereas metabolic rate of size‐manipulated colonies scaled allometrically with body size. Thus, metabolic scaling is affected by size manipulation but not feeding in this colonial marine invertebrate.

Schuster L, White CR, Marshall DJ (2019) Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate. Invertebrate Biology PDF DOI 

Debating growth and reproduction

In a recent post we described a paper written by Dustin Marshall and Craig White and published in Trends in Ecology and Evolution (TREE). The published article was called “Have we outgrown the existing models of growth?” In it, Dustin and Craig suggest that the growth dynamics that biologists have long sought to understand probably emerge simply from hyperallometric scaling of reproduction.

Daniel Pauly is a fisheries scientist from the University of British Columbia and is a proponent of the Gill-Oxygen Limitation Theory (GOLT) of growth. This theory applies to water-breathing animals and is structured around the proposition that growth is necessarily constrained by the size of the gills and the oxygen they are able to extract from the water.

Professor Pauly argues in a letter to TREE that there is a good reason why growth is not considered to be influenced by reproduction in the context of GOLT. While he agrees that reproductive output tends to scale hyperallometrically in fish, he does not agree that fish slow their growth because they allocate increasingly more to reproduction. Instead, he thinks that as growth slows (due to oxygen limitation caused by physical constraints on gill size) increased allocation of resources is directed to reproduction.

In their rebuttal, Dustin and Craig summarise their difference in opinion as one of causality; while Professor Pauly argues that body size in fish is limited by gill area, they believe that organs evolve to provide capacity to meet an organisms requirements. Or, in other words, the trait of body size is the product of selection whereby the size of an organisms is the best it can be to maximise fitness in a particular environment. Most importantly, taken to its logical extension, Dustin and Craig argue that Pauly’s own arguments imply fish reproduction should decrease with size.

In a separate letter, Michael Kearney from the University of Melbourne suggests that a radical revision of growth models is premature. In this case, Associate Professor Kearney suggests that a mechanistic modelling approach (such as Dynamic Energy Budget theory) based on a thermodynamically explicit theory of metabolism is better suited to understanding growth than the phenomenological modelling approach proposed by Dustin and Craig.

While Assoc. Prof. Kearney argues that the Dynamic Energy Budget model can incorporate hyperallometric scaling by adjusting the ‘rules’ governing how much energy is allocated to reproduction, Craig and Dustin say that to do this requires a phenomenological approach and is an unjustified post hoc model fitting solution. According to Craig and Dustin, this means that Assoc. Prof. Kearney’s model is not strictly mechanistic, with some parameters estimated by fitting mechanistic functions and some parameters requiring empirical data (a phenomenological approach).

But there is some agreement. Dustin, Craig and Michael Kearney are all interested in seeing studies of growth and metabolism that are conducted in the context of a full accounting of energy and mass balances (food in, changes in length and weight, respiration, faeces and eggs out) to continue improving our understanding of why organisms are the size they are.

You can read the original article and the follow-up letters.

Aquatic life history trajectories are shaped by selection, not oxygen limitation

Authors: Dustin J Marshall and Craig R White

Published in: Trends in Ecology & Evolution

Pauly1 argues that, as espoused in the gill-oxygen limitation theory (GOLT), growth slows as size increases because oxygen supply via the gills is unable to keep up with the oxygen demands of an increasingly large body. Thus, according to GOLT, growth determines the timing of reproduction, and fish reproduce when they become oxygen limited and growth starts to decline. GOLT has been critiqued on physiological grounds2,3 and we agree with those critiques. Large fish are no more oxygen limited than small fish, primarily because their respiratory surface area matches their metabolic demand for oxygen over a large size range…

Marshall DJ, White CR (2019) Aquatic life history trajectories are shaped by selection, not oxygen limitation, Trends in Ecology & Evolution. PDF DOI

Linking life-history theory and metabolic theory explains the offspring size-temperature relationship

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson‐Richardson, and Dustin J Marshall

Published in: Ecology Letters


Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved.

We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla.

We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecology Letters PDF DOI

Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

Authors: Colin Olito and Dustin J Marshall

Published in: Journal of Evolutionary Biology


The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory – broadcast spawning males often release sperm slowly, with weak resource‐dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter‐intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal.

Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae).

We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per‐gamete fertilization rate decreases precipitously with ejaculate size.

Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.

Olito C, Marshall DJ (2018) Releasing small ejaculates slowly increases per‐gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae), Journal of Evolutionary Biology PDF DOI