The benefits of big neighbours

Larger offspring typically have higher survival, growth and reproduction than smaller offspring. So why then, do we see such a range in offspring size? PhD student Hayley Cameron tackles this conundrum and the results of her latest experimental study contradict accepted theoretical models by showing that bigger is not always better.

Classic life-history models assume a trade-off in the investment mothers make in the next generation; large offspring perform better but smaller offspring are ‘cheaper’ to make and so mothers make them in large numbers. These models predict that a single offspring size will maximise reproductive success in a particular environment. But, we don’t see single offspring sizes, we see a range of sizes.

Game-theory takes the models further and explains the variation in offspring size by generating a ‘competition-colonisation’ trade-off.  In these scenarios, larger offspring will win contests over smaller offspring, but smaller offspring are better able to colonise unoccupied areas because they are more abundant. This means, no single offspring size will maximise reproductive success for any given population and so variation in offspring size is maintained.

Hayley and her supervisor Dustin Marshall test the idea that larger offspring will out-compete smaller offspring in a well-studied model organism, the invertebrate Bugula neritina. This idea has received surprisingly little testing.

To do this Hayley collected larvae and measured each one before settling them on to acetate squares. She glued these acetate squares, with their newly settled offspring, onto PVC plates in pairs of different sizes. These plates were deployed at a field site and every week Hayley measured survival, growth and number of developing larvae for 336 individuals of known offspring size.

To their surprise Hayley and Dustin found, instead of being out-competed as predicted, small offspring received benefits from having larger offspring as neighbours. Large offspring did compete with large neighbours though, and these bigger offspring did best on their own.

The graph and table both show how reproduction (measured by the number of ovicells) in big and small Bugula changed depending on the size of its neighbour. Hayley found that when small Bugula were paired with big neighbours then the overall reproductive output of the small Bugula increased. In contrast, big Bugula did best with no neighbours at all.

Why did this happen? In this study, larger offspring grew into larger colonies and Hayley and Dustin think these larger colonies disrupt the flow which affects the supply of resources (food and oxygen) available to their neighbours.  A slower flow is likely to benefit smaller colonies which tend to be less efficient at capturing resources in high flows. Conversely, larger, more efficient, colonies may deplete the resources available for their large neighbours.

So, while life history theory has traditionally viewed offspring interactions through the lens of competition, Hayley’s PhD work suggests facilitation might also be important in maintaining variation in offspring size.

More of Hayley’s PhD work on variation in offspring size: Should mothers provision their offspring equally? A manipulative field test

This research is published in the journal Evolution.

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 license.

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 license. 

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

Estimating the effects of marine urbanization on coastal food webs

Marine urbanization is a term that describes the increasing proliferation of structures such as piers, jetties, marinas, sea walls and other coastal defences in the marine environment. Martino Malerba, Craig White and Dustin Marshall from the Centre for Geometric Biology are proposing that this type of urban spread into the ocean could rob local systems of some of their productivity, changing local food web structure as well as function.

Many artificial structures, including floating platforms, barges, piers, pontoons seawalls and port quays, decrease the access of direct sunlight into the water. This means that instead of ecological communities dominated by ‘energy-producing’ seaweeds that require light to photosynthesise, there tends to be a shift toward dense assemblages of ‘energy-consuming’ filter-feeding invertebrates. The research team are particularly interested in finding out how this additional filter-feeding biomass affects energy flow and the productivity of coastal food webs.

The sheltered and shaded nature of marine urbanization disproportionately favours the development of dense fouling invertebrate communities. Examples of marine artificial structures in Australia: (left panel) mussels in the port of Hobart, (right top) mixed fouling communities in Port Phillip Bay, and (right bottom) colonies of mussels and polychaetes in Brighton (Melbourne).

Martino and his colleagues have combined data from field surveys, laboratory studies and satellite data to analyse total energy usage of invertebrate communities on artificial structures in Port Phillip and Moreton Bays. The team then used estimates from other studies to estimate the amount of primary production required to support the metabolic demands of the entire filter-feeding biomass living on artificial structures of all main commercial ports worldwide: the ‘trophic footprint’.

In order to do this, Martino and colleagues first used satellite photos to estimate how much area available for colonisation is created by artificial structures in Port Phillip and Moreton Bays. They then used field surveys to estimate the total invertebrate biomass occurring on all artificial structures in the two bays. In Port Phillip Bay, the estimated biomass on artificial structures is the equivalent of 3,151 female African bush elephants.

The next step was to transport communities back to the laboratory to measure mean daily energy consumption per unit area and then scale this up to artificial structures within the whole bay.  Based on their estimates they found that biomass on artificial structures can consume between 0.005% and 0.05% of the total yearly energy production in Port Phillip Bay and Morton Bay respectively.  This means that each square metre of artificial structure will consume 6 to 20 m² of marine primary productivity in these bays.

When they went through essentially the same process using data available from the scientific literature, the team found, on average, each metre of port consumes 26 m²of ocean primary productivity.  But there are stark differences between ports in different parts of the world. For example, one square metre of artificial structure in cold, highly productive regions can require as little as 0.9 m² of ocean (e.g. St. Petersburg, Russia), whereas a square metre of artificial structure in the nutrient-poor tropical waters of Hawaii can deplete all of the productivity in the surrounding ~120 m².

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

Martino, Craig and Dustin point out that a large percentage of ocean shoreline is now modified by engineering, with associated impacts on primary production. Burgeoning coastal human populations are expected to increase demands on fisheries in the future and food web productivity is already forecasted to decrease, due to the effects of climate change. Understanding the impacts of marine urbanisation on food webs is becoming increasingly important so that design of artificial structures minimises impacts on food webs and remediation efforts can be undertaken if necessary.

This research is published in Frontiers in Ecology and the Environment.

Are we undervaluing the contribution of marine protected areas to fisheries?

Our recent research has found that we are systematically underestimating the true value of marine protected areas (MPAs) to fisheries.

An important function of MPAs is to protect both representative and unique ecological communities, but scientists have long hoped they can play another role: contributing to the replenishment and maintenance of exploited fish stocks.

Wild fisheries are under intense pressure and landings of fish catches have flattened out despite an ever-increasing fishing effort. The most effective kind of MPAs are areas we set aside as ‘no take’ zones, where removal of animals and plants is banned. Fish populations within these areas can grow with limited human interference and potentially ‘spill-over’ to replenish fished stocks outside of MPAs. Despite the potential benefit, anglers remain sceptical that any spill-over will offset the loss of fishing grounds and the role of MPAs in fisheries remains contentious.

When we calculate how much a protected area contributes to a fishery, we work out the average length of both fished and unfished populations. Fish inside MPAs are bigger, on average, than those outside and so will produce more offspring than their smaller relatives outside MPAs. Generally, fisheries scientists relate the size of the fish to the reproductive output, whereby one unit increase in size equates to one unit increase in egg production.  They estimate how many juveniles will ‘spill-over’ and enter the fishing grounds.

It turns out there are a number of problems with the way the spill-over effect is currently calculated. Length is generally the measure of fish size recorded in a survey, but focusing on length risks underestimating the differences in reproduction inside and outside of MPAs.  Length and mass do not change at the same rate, so a 28% increase in fish length results in a 109% increase in mass. It can seem counter-intuitive that increasing fish length by around one quarter more than doubles the mass because the human brain tends to struggle when thinking about non-linear relationships.

This is compounded when we consider another non-linear relationship; fish mass and reproductive output. Our research team from the Centre for Geometric Biology and collaborator Ross Robertson from the Smithsonian Tropical Research Institute, recently found that bigger fish produce disproportionately more eggs than smaller fish in all fish species they looked at. This research made us realise that we need to be focused on protecting the biggest fish in a fishery.

And that is not all. In 1906, Danish mathematician Johan Jensen described the ‘fallacy of the average’, now known as Jensen’s inequality. Jensen pointed out that when relationships are non-linear we can’t assume that the average performance is equal to the performance under average conditions.

In our example, Jensen’s inequality means we further under-estimate reproductive output from inside the MPA. This is because fish size relates to reproductive output in a non-linear way so the reproductive output at average size is not the same as the average reproductive output. The inequality is greater inside the MPA where fish sizes are bigger and so this makes a further contribution to our under-estimate of reproductive output.

Overall benefits of MPAs when we re-calculate total reproduction accounting for non-linear relationships between length and mass and mass and reproduction. Pink bars show length, mass, and reproductive output of fish of average size outside the protected area; blue bars show length, mass, and reproductive output of fish inside protected areas.

When we take Jensen’s inequality into account, and add it to the underestimates relating to the non-linear relationships already discussed, we find that there is a 175% increase in reproductive output for fish inside MPAs compared to those outside.

While this translates to a much smaller ‘spill-over’ effect, (more like a 12% increase in tonnes of caught fish per year for the coral trout fishery when MPAs are included in the management of the fishery), it is still a substantial increase in yield.

Jensen’s inequality for fish reproduction. Left: the benefit of MPAs for average fish reproduction driven by differences in mean size. Right: the benefits of MPAs are enhanced because of the greater ‘inequality’ in the MPAs where fish sizes are larger and more variable..

MPAs represent an essential tool for protecting larger fish, and the research team hope that a more accurate accounting of the value of MPAs will increase support for their use by a wide variety of stakeholders, including anglers themselves.

This research is published in the journal Frontiers in Ecology and the Environment.

Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts?

Authors: Louise Solveig Nørgaard, Ben L Phillips, and Matthew D Hall

Published in: Biology Letters


Pathogens often rely on their host for dispersal. Yet, maximizing fitness via replication can cause damage to the host and an associated reduction in host movement, incurring a trade-off between transmission and dispersal.

Here, we test the idea that pathogens might mitigate this trade-off between reproductive fitness and dispersal by taking advantage of sexual dimorphism in their host, tailoring responses separately to males and females.

Using experimental populations of Daphnia magna and its bacterial pathogen Pasteuria ramosa as a test-case, we find evidence that this pathogen can use male hosts as a dispersal vector, and the larger females as high-quality resource patches for optimized production of transmission spores.

As sexual dimorphism in dispersal and body size is widespread across the animal kingdom, this differential exploitation of the sexes by a pathogen might be an unappreciated phenomenon, possibly evolved in various systems.

Nørgaard LS, Phillips BL, Hall MD (2019) Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts? Biology Letters PDF DOI

How well do we understand the way body size affects populations?

We have all heard the saying “live fast, die young” but it doesn’t only apply to film stars; smaller life forms also abide by this rule. Microscopic phytoplankton cells can double in numbers every few days, while the much larger elephant lives almost 100 years and reproduces slowly. This relationship between body mass and the ‘pace of life’ is well known. But the underlying mechanisms are far from resolved.

A number of years ago, scientists proposed a theory to link the ‘pace of life’ of individuals to the ecology of populations, communities, and ecosystems. The Metabolic Theory of Ecology predicts how energy use (metabolism) is affected by body size and how growth rate, development time and death rates change with energy use. These changes in individual rates will, in turn, affect rates of change in populations.

Metabolic Theory is very appealing because it explains many patterns we see in nature and is based on a fundamental rate which applies to all levels of organisation. But it is difficult to test. Detecting differences in energy use accurately requires having consistent differences in body sizes among organisms, while controlling for other variables (e.g. age, nutrition, health). This usually means comparing across species, which differ in more ways than just size.

The artificially evolved phytoplankton were almost 400 generations old when this work was done. The graph shows the considerable differences in size between small and large algae which allowed Martino and Dustin to ask their questions about body size, metabolism and populations within a species.

Few tests of these predictions have been able to control for these variables but recently Martino Malerba and Dustin Marshall were able to do this and they found that the body size-metabolism relationship did not predict population change as expected.

Martino and Dustin were in the enviable position of having access to artificially-evolved large and small phytoplankton cells of the same species that differed in size enough for them to ask “what happens to the population of a species if the average body size of individuals change?” They could see how body size affected energy use, growth rates, density and biomass.

It turns out that the story was far more complex than expected. The effect of body size on how organisms use energy and grow was very strong but also varied during the course of evolution.

So why didn’t body size explain trends in growth and energy use among size-evolved organisms? The answer may lie with previous work from the Centre for Geometric Biology. Martino and his colleagues found that large-evolved plankton cells optimized their photosynthetic pigments and produced more energy overall than smaller cells. This suggests larger cells have greater access to resources than smaller cells and so the way in which body size and metabolic rate influence the demography of a species is not as predictable as we once thought.

Instead of the classical view, where body size determines the rate at which organisms use energy, which then determines demographics, Martino and Dustin suggest that body size can affect metabolism and populations at the same time.

IIf these laboratory cultures are representative of natural populations, we would predict that current trends of reduced body size (from global warming) could lead to lower rates of population increase, biomass productivity and maximum biomass. This is the opposite of what current theory would predict. This is particularly important when we consider the role of phytoplankton in fixing carbon and supporting food chains.

This research was published in Ecology Letters.