The Conversation: From crocodiles to krill, a warming world raises the ‘costs’ paid by developing embryos

By Dustin Marshall

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

Apart from mammals and birds, most animals develop as eggs exposed to the vagaries of the outside world. This development is energetically “costly”. Going from a tiny egg to a fully functioning organism can deplete up to 60% of the energy reserves provided by a parent.

In cold-blooded animals such as marine invertebrates (including sea stars and corals), fish and reptiles, and even insects, embryonic development is very sensitive to changes in the temperature of the environment.

Thus, in a warming world, many cold-blooded species face a new challenge: developing successfully despite rising temperatures.

For our research, published today in Nature Ecology and Evolution, we mined existing literature for data on how temperature impacts the metabolic and development rates of 71 different species, ranging from tropical crocodiles to Antarctic krill.

We found over time, species tend to fine-tune their physiology so that the temperature of the place they inhabit is the temperature needed to minimise the “costs” of their embryonic development.

Temperature increases associated with global warming could substantially impact many of these species.

The perfect weather to grow an embryo

The energy costs of embryonic development are determined by two key rates. The “metabolic” rate refers to the rate at which energy is used by the embryo, and the “development” rate determines how long it takes the embryo to fully develop, and become an independent organism.

Both of these rates are heavily impacted by environmental temperature. Any change in temperature affecting them is therefore costly to an embryo’s development.

Generally, a 10°C increase in temperature will cause an embryo’s development and metabolic rate to more than triple.

This photo shows a developing sea urchin, from egg (top left) to larva, to a metamorphosed (matured into adult form) individual.

These effects partially cancel each other out. Higher temperatures increase the rate at which energy is used (metabolic), but shorten the developmental time.

But do they balance out effectively?

What are the costs?

For any species, there is one temperature that achieves the perfect energetic balance between relatively rapid development and low metabolism. This optimal temperature, also called the “Goldilocks” temperature, is neither too hot, nor too cold.

When the temperature is too cold for a certain species, development takes a long time. When it’s too hot, development time decreases while the metabolic rate continues to rise. An imbalance on either side can negatively impact a natural population’s resilience and ability to replenish.

As an embryo’s developmental costs increase past the optimum, mothers must invest more resources into each offspring to offset these costs.

When offspring become more costly to make, mothers make fewer, larger offspring. These offspring start life with fewer energy reserves, reducing their chances of successfully reproducing as adults themselves.

Thus, when it comes to embryonic development, higher-than ideal temperatures pack a nasty punch for natural populations.

Since the temperature dependencies of metabolic rate and development rate are fairly similar, the slight differences between them had gone unnoticed until recently.

Embryos at risk

For each species in our study, we found a narrow band of temperatures that minimised developmental cost. Temperatures that were too high or too low caused massive blow-outs in the energy budget of developing embryos.

This means temperature increases associated with global warming are likely to have bigger impacts than previously predicted.

Predictions of how future temperature changes will affect organisms are often based on estimates of how temperature affects embryo survival. These measures suggest small temperature increases (1°C-2°C) do not reduce embryo survival by much.

But our study found the developmental costs are about twice as high, and we had underestimated the impacts of subtle temperature changes on embryo development.

In the warming animal kingdom, there are winners and losers

Some good news is our research suggests not all species are facing rising costs with rising temperatures, at least initially.

We’ve created a mathematical framework called the Developmental Cost Theory, which predicts some species will actually experience slightly lower developmental costs with minor increases in temperature.

In particular, aquatic species (fish and invertebrates) in cool temperate waters seem likely to experience lower costs in the near future. In contrast, certain tropical aquatic species (including coral reef organisms) are already experiencing temperatures that exceed their optimum. This is likely to get worse.

It’s important to note that for all species, increasing environmental temperature will eventually come with costs.

Even if a slight temperature increase reduces costs for one species, too much of an increase will still have a negative impact. This is true for all the organisms we studied.

A key question now is: how quickly can species evolve to adapt to our warming climate?The Conversation

The Conversation: Daylight robbery: how human-built structures leave coastal ecosystems in the shadows

Human-built structures are home to a wide variety of creatures.

By Martino Malerba, Craig White, Dustin Marshall, and Liz Morris, Monash University.

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

About half of the coastline of Europe, the United States and Australasia is modified by artificial structures. In newly published research, we identified a new effect of marine urbanisation that has so far gone unrecognised.

When we build marinas, ports, jetties and coastal defences, we introduce hard structures that weren’t there before and which reduce the amount of sunlight hitting the water. This means energy producers such as seaweed and algae, which use light energy to transform carbon dioxide into sugars, are replaced by energy consumers such as filter-feeding invertebrates. These latter species are often not native to the area, and can profoundly alter marine habitats by displacing local species, reducing biodiversity, and decreasing the overall productivity of ecosystems.

Incorporating simple designs in our marine infrastructure to allow more light penetration, improve water flow, and maintain water quality, will go a long way towards curbing these negative consequences.

Pier life

We are used to thinking about the effects of urbanisation in our cities – but it is time to pay more attention to urban sprawl in the sea. We need to better understand the effects on the food web in a local context.

Most animals that establish themselves on these shaded hard structures are “sessile” invertebrates, which can’t move around. They come in a variety of forms, from encrusting species such as barnacles, to tree-shaped or vase-like forms such as bryozoans or sponges. But what they all have in common is that they can filter out algae from the water.

In Australian waters, we commonly see animals from a range of different groups including sea squirts, sponges, bryozoans, mussels and worms. They can grow in dense communities and often reproduce and grow quickly in new environments.

The sheltered and shaded nature of marine urbanisation disproportionately favours the development of dense invertebrate communities, as shown here in Port Phillip Bay.

How much energy do they use?

In our new research, published in the journal Frontiers in Ecology and the Environment, we analysed the total energy usage of invertebrate communities on artificial structures in two Australian bays: Moreton Bay, Queensland, and Port Phillip Bay, Victoria. We did so by combining data from field surveys, laboratory studies, and satellite data.

We also compiled data from other studies and assessed how much algae is required to support the energy demands of the filter-feeding species in commercial ports worldwide.

In Port Phillip Bay, 0.003% of the total area is taken up by artificial structures. While this doesn’t sound like much, it is equivalent to almost 50 soccer fields of human-built structures.

We found that the invertebrate community living on a single square metre of artificial structure consumes the algal biomass produced by 16 square metres of ocean. Hence, the total invertebrate community living on these structures in the bay consumes the algal biomass produced by 800 football pitches of ocean!

Similarly, Moreton Bay has 0.005% of its total area occupied by artificial structures, but each square metre of artificial structure requires around 5 square metres of algal production – a total of 115 football pitches. Our models account for various biological and physical variables such as temperature, light, and species composition, all of which contribute to generate differences among regions.

Overall, the invertebrates growing on artificial structures in these two Australian bays weigh as much as 3,200 three-tonne African elephants. This biomass would not exist were it not for marine urbanisation.

Colonies of mussels and polychaetes near Melbourne.

How does Australia compare to the rest of the world?

We found stark differences among ports in different parts of the world. For example, one square metre of artificial structure in cold, highly productive regions (such as St Petersburg, Russia) can require as little as 0.9 square metres of sea surface area to provide enough algal food to sustain the invertebrate populations. Cold regions can require less area because they are often richer in nutrients and better mixed than warmer waters.

In contrast, a square metre of structure in the nutrient-poor tropical waters of Hawaii can deplete all the algae produced in the surrounding 120 square metres.

All major commercial ports worldwide with associated area of the underwater artificial structures (size of grey dots) and trophic footprint (size of red borders). Trophic footprints indicate how much ocean surface is required to supply the energy demand of the sessile invertebrate community growing on all artificial structures of the port, averaged over the year. This depends on local conditions of ocean primary productivity and temperature. Ports located in cold, nutrient-rich waters (dark blue) have a lower footprint than ports in warmer waters (light blue).

Does it matter?

Should we be worried about all of this? To some extent, it depends on context.

These dense filter-feeding communities are removing algae that normally enters food webs and supports coastal fisheries. As human populations in coastal areas continue to increase, so will demand on these fisheries, which are already under pressure from climate change. These effects will be greatest in warmer, nutrient-poor waters.

But there is a flip side. Ports and urban coastlines are often polluted with increased nutrient inputs, such as sewage effluents or agricultural fertilisers. The dense populations of filter-feeders on the structures near these areas may help prevent this nutrient runoff from triggering problematic algal blooms, which can cause fish kills and impact human health. But we still need to know what types of algae these filter-feeding communities are predominantly consuming.

Our analysis provides an important first step in understanding how these communities might affect coastal production and food webs.

In places like Southeast Asia, marine managers should consider how artificial structures might affect essential coastal fisheries. Meanwhile, in places like Port Phillip Bay, we need to know whether and how these communities might affect the chances of harmful algal blooms.The Conversation

Mussels in the port of Hobart.

The Conversation

The Conversation: No-take marine areas help fishers (and fish) far more than we thought

A juvenile Plectropomus leopardus from the Whitsundays. Image credit: David Williamson, James Cook University.

By Dustin Marshall and Liz Morris, Monash University

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

One hectare of ocean in which fishing is not allowed (a marine protected area) produces at least five times the amount of fish as an equivalent unprotected hectare, according to new research published today.

This outsized effect means marine protected areas, or MPAs, are more valuable than we previously thought for conservation and increasing fishing catches in nearby areas.

Previous research has found the number of offspring from a fish increases exponentially as they grow larger, a disparity that had not been taken into account in earlier modelling of fish populations. By revising this basic assumption, the true value of MPAs is clearer.

Marine Protected Areas

Marine protected areas are ocean areas where human activity is restricted and at their best are “no take” zones, where removing animals and plants is banned. Fish populations within these areas can grow with limited human interference and potentially “spill-over” to replenish fished populations outside.

Obviously MPAs are designed to protect ecological communities, but scientists have long hoped they can play another role: contributing to the replenishment and maintenance of species that are targeted by fisheries.

Wild fisheries globally are under intense pressure and the size fish catches have levelled off or declined despite an ever-increasing fishing effort.

Yet fishers remain sceptical that any spillover will offset the loss of fishing grounds, and the role of MPAs in fisheries remains contentious. A key issue is the number of offspring that fish inside MPAs produce. If their fecundity is similar to that of fish outside the MPA, then obviously there will be no benefit and only costs to fishers.

Big fish have far more babies

Traditional models assume that fish reproductive output is proportional to mass, that is, doubling the mass of a fish doubles its reproductive output. Thus, the size of fish within a population is assumed to be less important than the total biomass when calculating population growth.

But a paper recently published in Science demonstrated this assumption is incorrect for 95% of fish species: larger fish actually have disproportionately higher reproductive outputs. That means doubling a fish’s mass more than doubles its reproductive output.

When we feed this newly revised assumption into models of fish reproduction, predictions about the value of MPAs change dramatically.

Fish are, on average, 25% longer inside protected areas than outside. This doesn’t sound like much, but it translates into a big difference in reproductive output – an MPA fish produces almost 3 times more offspring on average. This, coupled with higher fish populations because of the no-take rule means MPAs produce between 5 and 200 times (depending on the species) more offspring per unit area than unprotected areas.

Put another way, one hectare of MPA is worth at least 5 hectares of unprotected area in terms of the number of offspring produced.

We have to remember though, just because MPAs produce disproportionately more offspring it doesn’t necessarily mean they enhance fisheries yields.

For protected areas to increase catch sizes, offspring need to move to fished areas. To calculate fisheries yields, we need to model – among other things – larval dispersal between protected and unprotected areas. This information is only available for a few species.

We explored the consequences of disproportionate reproduction for fisheries yields with and without MPAs for one iconic fish, the coral trout on the Great Barrier Reef. This is one of the few species for which we had data for most of the key parameters, including decent estimates of larval dispersal and how connected different populations are.

No-take protected areas increased the amount of common coral trout caught in nearby areas by 12%. Image credit: Paul Asman and Jill Lenoble via Flickr.

We found MPAs do in fact enhance yields to fisheries when disproportionate reproduction is included in relatively realistic models of fish populations. For the coral trout, we saw a roughly 12% increase in tonnes of caught fish.

There are two lessons here. First, a fivefold increase in the production of eggs inside MPAs results in only modest increases in yield. This is because limited dispersal and higher death rates in the protected areas dampen the benefits.

However the exciting second lesson is these results suggest MPAs are not in conflict with the interests of fishers, as is often argued.

While MPAs restrict access to an entire population of fish, fishers still benefit from from their disproportionate affect on fish numbers. MPAs are a rare win-win strategy.

It’s unclear whether our results will hold for all species. What’s more, these effects rely on strict no-take rules being well-enforced, otherwise the essential differences in the sizes of fish will never be established.

We think that the value of MPAs as a fisheries management tool has been systematically underestimated. Including disproportionate reproduction in our assessments of MPAs should correct this view and partly resolve the debate about their value. Well-designed networks of MPAs could increase much-needed yields from wild-caught fish.
The Conversation

Causes and consequences of variation in offspring size

Offspring size affects all aspects of an organism’s life, from birth through to reproduction, and  studies show that larger offspring do better overall. 

Despite the long standing interest in the drivers of differences in offspring size, most studies focus only on one particular taxon or system.

Dustin Marshall, Amanda Pettersen and Hayley Cameron were interested in looking at offspring size across all taxa and at different levels of organisation – within a brood, between individuals and across different species and environments – to see if this wider scope could help them better understand the causes and consequences of variation in offspring size.

They started by looking at a pattern that will be familiar to many ecologists and bio-geographers; offspring size tends to get bigger as you move from the tropics to the poles. They found that this was true for practically all species they compiled data for, with the notable exception of turtles and plants. 

Dustin, Amanda and Hayley suspect that the difference in the patterns they recorded relates to the way offspring size and temperature affects development.  Small increases in temperature are known to yield large increases in development rate. The lower number of warmer days in higher latitudes might just mean that there just isn’t time for larger seeds or turtle eggs to complete development. Importantly, turtles don’t incubate their eggs and so will be more susceptible to environmental temperature than taxa that do (birds for example). Collecting data on egg size variation in other reptiles would help to test this theory.  

For taxa such as fish, amphibians and invertebrates the overall smaller egg size in comparison to seeds and other vertebrates might preclude development time as a limitation on size.

Offspring size also varies across populations and within broods from the same females.  Dustin and colleagues highlight that sources of variation might be external whereby mothers buffer their offspring from harsher environments by making them bigger, or choose to maximise numbers in more benign environments, meaning that offspring are smaller. Mothers might also provision offspring unequally within a brood to ensure that whatever environment the offspring find themselves in, some at least, will do well.  

Hayley’s PhD work however, suggests that variation in size within a brood reduces competition between siblings and all offspring, regardless of their size, do better.

Finally the team considered the question as to why larger offspring generally tend to perform better than smaller offspring. They were interested in understanding the costs and benefits of a larger size to the energy available for fitness-enhancing functions such as growth and reproduction.  

It seems that larger offspring often access more energy resources than smaller offspring. In plants, seed size likely affects photosynthetic capacity, in certain fish and snakes, a larger gape size at birth allows for more efficient energy acquisition and, in filter feeding invertebrates, larger offspring initially produce more or larger feeding structures. In addition, larger offspring should expend relatively less energy than smaller offspring and complete energetically costly developmental stages with more energy reserves intact.

This research was published in the journal Functional Ecology.

Time to go back to school? Geometry helps predict change in ecosystem function

Humans are continually modifying the marine environment either directly, with activities such as fishing, or indirectly as with climate change or the introduction of invasive species. A common consequence of these activities is a change in the body size of individuals that make up an ecological community. 

Understanding the impacts of such changes on the way in which communities gain and use energy is of particular interest to Giulia Ghedini, a post-doc in the Centre for Geometric Biology.

“We know that human impacts can change the size of organisms and we also know that the size of an organism determines the speed at which it uses resources and contributes to the flow of energy within a system” explains Dr Ghedini.

“Understanding how changes in the ‘geometry’ of a whole community might affect ecosystem functioning through changes in metabolic rates is not only theoretically interesting but of practical significance as well” she said. 

Metabolism measurements indicate how much oxygen and food an individual, or an entire community, consumes. Understanding how changes in individual body size affect the energy use of whole communities provides direct information on the amount of resources required for these communities to live. 

Researchers from the Centre for Geometric Biology at Monash University were able to test predictions that older communities, made up of larger organisms, would have lower metabolic rates per unit mass than younger communities of smaller individuals. 

“We know that increases in metabolic rates slow down as organisms get larger – and we wanted to know if this same pattern occurs at the level of whole communities” said Dr Ghedini.

To their surprise, the research team found that the community metabolic rates remained directly proportional to total community mass as communities got older and larger, which contrasted with the way metabolic rate scaled with changes in size of the dominant species. 

“But,” said Dr Ghedini “when we deconstructed the community into individuals and calculated their individual metabolic rates based on their size and species-specific metabolism, we found that community rates were largely the sum of their parts with respect to metabolism.” 

Measuring metabolism of a whole community can be hard, and so studies frequently estimate community metabolism from the dominant species in that community; we now know that for these estimates to be accurate we need to know the sizes of the individuals that make up the community.

“We also found that as communities got older, the same area was able to support much higher biomasses and energy use – three times as much as the younger communities. We attributed this to changes in the shape of the community; that is, a more 3D structure allowed certain individuals greater access to food in the water column and increased oxygen delivery via increased water flow.”

Changes in rates of energy use have long been used as an indicator of change in ecosystem function. 

By unravelling the relationship between the size of individuals and the energy use of whole communities, this study will help us predict how changes in the geometry of communities will impact on the use of resources; a measure of ecosystem function.

This research was published in a special issue of the journal Functional Ecology.

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. Science PDF DOI

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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Understanding how age and sex can influence host-pathogen interactions

Pathogens, or disease producing organisms, will inevitably encounter hosts that differ in their resistance to infection and theory suggests that this will affect pathogen evolution.  If a pathogen routinely only encounters one type of host resistance, it will develop a specialist strategy that dictates the severity of infection.  It is likely that the age and sex of a host will be a source of variation governing the evolution of infectious disease.

As part of his PhD, Stephen Gipson has used a series of experimental infection trials to test these ideas by investigating how males and females of different ages would respond to infection by two strains of a pathogen. Stephen and his PhD supervisor, Matt Hall, predicted that mortality rates and virulence (severity of infection) would increase with the age at exposure as a consequence of the aging process and, in addition, that these increasing costs would be felt most strongly by the less resistant sex.

Stephen used the freshwater crustacean Daphnia magna and its common pathogen Pasteuria ramosa as a model system to test these ideas. Daphnia can produce genetically identical male and female clones where the females live longer and are less resistant to infection. The pathogen P. ramosa invades the host via attachment to the oesophagus and reproduces within the haemolymph (fluid analogous to blood in the in the arthropod circulatory system) of the infected Daphnia, filling the body with transmission spores, which are released when the host dies.

The two strains of the pathogen (C24 and C20) differed in the proportion of Daphnia infected, spore loadings and the transmission potential in females (left panel in each pair of graphs) but not in males (right panel in each pair).

What Stephen and Matt found was actually a bit more complicated than their predictions. Mortality rates were higher in females (the less resistant sex in Daphnia) as predicted but mortality rates only increased with age in females.  They proposed that the patterns observed might have more to do with the exploitation potential of males and females to a pathogen rather than an ageing immune system; the larger size and longer life span of females may provide more resources and more time for exploitation by the pathogen.

Stephen also found that when infecting females, the two pathogen genotypes displayed a range of relationships between spore loads (transmission potential) and virulence (relative reduction in lifespan), in contrast with males, where patterns of virulence and transmission were the same for both strains of pathogen (see graphs).

In general, evolution favours pathogens which strike a balance between transmission and virulence. Stephen and Matt have shown how complex interactions between host-sex and the age at which a host encounters a pathogen can facilitate greater variation in the evolution of infectious disease.  Understanding a population’s sex ratio and age structure may be crucial in predicting the severity and spread of disease.

This research was published in the Journal of Evolutionary Biology.