Fish reproductive-energy output increases disproportionately with body size

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

Published in: Science, volume 360, issue 6389 (11 May 2018)


Body size determines total reproductive-energy output.

Most theories assume reproductive output is a fixed proportion of size, with respect to mass, but formal macroecological tests are lacking. Management based on that assumption risks underestimating the contribution of larger mothers to replenishment, hindering sustainable harvesting.

We test this assumption in marine fishes with a phylogenetically controlled meta-analysis of the intraspecific mass scaling of reproductive-energy output.

We show that larger mothers reproduce disproportionately more than smaller mothers in not only fecundity but also total reproductive energy.

Our results reset much of the theory on how reproduction scales with size and suggest that larger mothers contribute disproportionately to population replenishment.

Global change and overharvesting cause fish sizes to decline; our results provide quantitative estimates of how these declines affect fisheries and ecosystem-level productivity.

Barneche DR, Robertson DR, White CR, Marshall DJ (2018) Fish reproductive-energy output increases disproportionately with body size. ScienceDOI

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Bigger is better when it comes to female fish and feeding the planet

An international study led by the Centre for Geometric Biology has found that larger fish are much more important to feeding the planet than previously thought.

The research confirmed what field biologists have long suggested: that larger mothers reproduced disproportionately much more than smaller ones. Furthermore, larger mothers may produce offspring that perform better and are more likely to survive to adulthood.

The findings clash with current theories. And the results have major implications for fisheries, the value placed on marine protected areas, the impacts of climate change and the 20% of people globally who rely on fish for protein.

The Centre’s Diego Barneche, Craig White, and Dustin Marshall, with Ross Robertson from The Smithsonian Tropical Research Institute, collated and analysed data from 342 species of fish across 14 orders gathered from studies undertaken over a 100-year time span. The team were particularly interested in understanding the relationships between female size and the number of eggs produced, egg volume and egg energy content.

Most life-history theories assume that reproductive output increases proportionately with female size; for every unit increase in female size, there is a proportional increase in reproductive output.  That is, the combined reproductive output of two one-kilogram fish is assumed to be the same as a single two-kilogram fish. But for the overwhelming majority of species, the research team found that overall reproductive output increased disproportionately with female body size. Bigger is much, much better.

The consequences for fisheries cannot be understated. Reproductive output drives population replenishment, and larger fish are much more important for the replenishment of marine fish populations than previously assumed. Outdated models for sustainable harvesting of fish populations are fundamentally flawed.

Our models of how organisms grow and reproduce are based on the wrong assumptions, and as a consequence we are overharvesting wild populations with calamitous consequences.Dustin Marshall

The costs of global change make the study findings even more stark. Climate change is predicted to cause fish body sizes to decrease. Warmer oceans will likely have fewer (and smaller) fish, and drastically reproductive output.

But the research also points to some good news, suggesting that current conservation strategies are more potent than previously thought.  Marine protected areas have been shown to increase fish size by 28% on average. That means that the per-capita reproductive output of fish inside these areas will be much higher than is generally appreciated.

Our discovery means that the benefits of marine protected areas have been massively underestimated, they produce far more new fish than unprotected areas of the same size.Dustin Marshall

This research is published in the Journal Science.

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Do good things come in small packages?

Good things don’t always come in small packages: large-evolved phytoplankton cells had greater oxygen production and growth performance than small-evolved cells.

Biologists have been striving to understand the basic rules regulating the physiology and ecology of phytoplankton species for decades.  Now, more than ever, this is important because temperature increases may be changing the geometry (shape and size) of phytoplankton throughout the world’s oceans.

Post-doc Martino Malerba and his colleagues have used the artificially evolved large and small plankton cells to assess how efficiently cells of different sizes can utilise light, and if differences are predicted by current theories.

Previous studies have focused on looking at different species that range in size and have often showed physical constraints in the way cells use light. The long-standing theory of the ‘package effect’ says that as cells get bigger their ability to absorb light decreases, due to increasing self-shading of pigments within a cell.

Martino and his colleagues were interested in disentangling the underlying reasons for differences in size – are species a certain size because of specific features of their photosynthetic apparatus, or, are there ways to get around the physical limitation of increasing in size? The team wanted to find out what would happen when they only manipulated the size of a cell; would other things co-evolve in a way that is predicted by current theory? Or would the evolution of size take an unexpected path?

The research team monitored a number of photosynthetic traits in evolved cells that differed in size by up to 1,500%.  Small evolved cells were more efficient at producing oxygen (per unit of chlorophyll) which is what the physics behind the package effect predicts.  But the researchers also found that large-evolved cells not only showed a massive increase in chlorophyll content but also greater photosynthetic and growth performance (both per-cell and per-volume). This was possible because of a decrease in ‘sunscreen’ pigments (such as β-carotene) and a reorganization of the photosynthetic apparatus (more light receptors but of smaller sizes), which optimised light penetration within larger cells by reducing physical constraints.

The research team found that the evolution of size results in changes to many of the organelles within the cell, with many changing in direct proportion to the size of the cell. Some traits such as chlorophyll increased disproportionally in relation to the size of the cell while others such as β-carotene decreased disproportionally to the size of the cell. The photos show cells of large-evolved and small-evolved cells taken with a scanning electron microscope and coloured to emphasise some of the cells structures.

So while the ‘package effect’ successfully predicts the chlorophyll-standardised performance in cells of different sizes, this research shows that it doesn’t translate to whole cell performance.  This is because the loss of efficiency per chlorophyll pigment is more than made up for by the increased chlorophyll content and other changes that allow greater light penetration in larger cells.

Overall, Martino and his colleagues showed that altering the size of a cell profoundly alters many fundamental traits of algal physiology and ecology, with potentially serious impacts on global carbon cycles.

Cell size, photosynthesis and the package effect: an artificial selection approach

Authors: Martino E Malerba, Maria M Palacios, Yussi M, Palacios Delgado, John Beardall, and Dustin J Marshall

Published in: New Phytologist


Cell size correlates with most traits among phytoplankton species. Theory predicts that larger cells should show poorer photosynthetic performance, perhaps due to reduced intracellular self‐shading (i.e. package effect). Yet current theory relies heavily on interspecific correlational approaches and causal relationships between size and photosynthetic machinery have remained untested.

As a more direct test, we applied 250 generations of artificial selection (c. 20 months) to evolve the green microalga Dunaliella teriolecta (Chlorophyta) toward different mean cell sizes, while monitoring all major photosynthetic parameters.

Evolving larger sizes (>1500% difference in volume) resulted in reduced oxygen production per chlorophyll molecule – as predicted by the package effect. However, large‐evolved cells showed substantially higher rates of oxygen production – a finding unanticipated by current theory. In addition, volume‐specific photosynthetic pigments increased with size (Chla+b), while photo‐protectant pigments decreased (β‐carotene). Finally, larger cells displayed higher growth performances and Fv/Fm, steeper slopes of rapid light curves (α) and smaller light‐harvesting antennae (σPSII) with higher connectivity (ρ).

Overall, evolving a common ancestor into different sizes showed that the photosynthetic characteristics of a species coevolves with cell volume. Moreover, our experiment revealed a trade‐off between chlorophyll‐specific (decreasing with size) and volume‐specific (increasing with size) oxygen production in a cell.

Malerba ME, Palacios MM, Palacios Delgado YM, Beardall J, Marshall DJ (2018) Cell size, photosynthesis and the package effect: an artificial selection approach, New Phytologist, PDF DOI 

The energetics of fish growth

Ecologists have long been interested in the causes of differences in trophic structures in marine systems.  A new study by Diego Barneche of the Centre for Geometric Biology and Andrew Allen of Macquarie University, that has been looking at the theoretical underpinning of the growth patterns in fish, has found that the ‘cost of growth’ is paramount to determining how energy moves between levels in the food chain.

Diego and Andrew were particularly interested in using a model framework that allowed for the inclusion of this previously neglected parameter – the cost of growth – which is the amount of energy that must be expended in respiration to produce a fixed quantity of biomass.  The researchers used existing datasets to investigate the relationship between the energy allocated to growth at different developmental stages, temperatures, levels of activity and position in the food chain.

They have demonstrated the ‘cost of growth’ limits the possible structure of food webs because it has an effect on the efficiency of energy transfer between the different levels of the food chain. For example the model suggested that fish higher up the food chain had to expend more energy to produce a fixed quantity of biomass.

This figure shows the modelling outputs relating the energy needed to gain a unit of biomass to the developmental stage (ontogenetic stage) of prey at the time of predation.

Energy transfer is more efficient if the prey are young and sedentary and recognizing that the efficiency of energy transfer changes not only with the developmental stage of the prey but also with temperature, position in the food chain and activity levels is an important step forward.

The model demonstrated that top heavy food web structures were ecologically and energetically unlikely (red area in accompanying figure) because the energy needed to gain a unit of biomass would have to be very low meaning that energy transfer between levels would have to be extremely efficient. While this could be achieved by exclusive predation on offspring which would provide a high-efficiency prey resource (young, sedentary prey requiring little movement of predators), it is a short term solution.

Understanding the energetics of growth is of immense importance, particularly in the field of fisheries science.  Knowing how long wild fish stocks take to achieve maturity and how much food they need to do so, is crucial for establishing sustainable yields.

This research is published in Ecology Letters.

Biochemical evolution in response to intensive harvesting in algae: evolution of quality and quantity

Authors: Dustin J Marshall, Rebecca J Lawton, Keyne Monro, and Nicholas A Paul

Published in: Evolutionary Applications


Evolutionary responses to indirect selection pressures imposed by intensive harvesting are increasingly common. While artificial selection has shown that biochemical components can show rapid and dramatic evolution, it remains unclear as to whether intensive harvesting can inadvertently induce changes in the biochemistry of harvested populations. For applications such as algal culture, many of the desirable bioproducts could evolve in response to harvesting, reducing cost‐effectiveness, but experimental tests are lacking.

We used an experimental evolution approach where we imposed heavy and light harvesting regimes on multiple lines of an alga of commercial interest for twelve cycles of harvesting and then placed all lines in a common garden regime for four cycles. We have previously shown that lines in a heavy harvesting regime evolve a “live fast” phenotype with higher growth rates relative to light harvesting regimes. Here, we show that algal biochemistry also shows evolutionary responses, although they were temporarily masked by differences in density under the different harvesting regimes. Heavy harvesting regimes, relative to light harvesting regimes, had reduced productivity of desirable bioproducts, particularly fatty acids.

We suggest that commercial operators wishing to maximize productivity of desirable bioproducts should maintain mother cultures, kept at higher densities (which tend to select for desirable phenotypes), and periodically restart their intensively harvested cultures to minimize the negative consequences of biochemical evolution.

Our study shows that the burgeoning algal culture industry should pay careful attention to the role of evolution in intensively harvested crops as these effects are nontrivial if subtle.

Marshall DJ, Lawton RJ, Monro K, Paul NA (2018) Biochemical evolution in response to intensive harvesting in algae: evolution of quality and quantity. Evolutionary Applications, PDF DOI 

Director’s message

The Centre for Geometric Biology entered its third year in 2017.  It has been an extremely busy year with many research highlights.  The different research groups are working with a variety of organisms and approaches to explore a wide range of specific questions about organismal growth.  There has been a palpable feeling of excitement as the different research streams and collaborations are starting to come together under the unifying theme of energy acquisition and use.

Success in the realms of external funding and publications in high ranking journals has been excellent in 2017 and this applies to all career levels from PhD students to early career researchers and above.

A meeting with board members and the Monash University internal review process has provided ample opportunity to reflect on our progress and identify where we want to be headed.  A priority target is to improve the theoretical underpinning of our work.  Successful visits followed on from theoretical ecologist Professor Andre de Roos in 2016 (University of Amsterdam), with visits from mathematical modeler Professor Tim Coulson (University of Oxford) and theoretician Professor Troy Day (Queens University, Ontario) in 2017.  These visits have all resulted in ongoing collaborations and I think we have all found them highly motivating.

Finally, we would like to thank the board members and the internal review team for their ongoing interest and support of our research and of course congratulate all the members of the Centre for Geometric Biology for their many successes in 2017.

Prof Dustin Marshall, Director
Prof Craig White, Deputy Director