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.

The outsized trophic footprint of marine urbanization

Authors: Martino E Malerba, Craig R White, and Dustin J Marshall

Published in: Frontiers in Ecology and the Environment

Abstract

Artificial structures are proliferating along coastlines worldwide, creating new habitat for heterotrophic filter feeders. The energy demand of this heterotrophic biomass is likely to be substantial, but is largely unquantified.

Combining in situ surveys, laboratory assays, and information obtained from geographic information systems, we estimated the energy demands of sessile invertebrates found on marine artificial structures worldwide.

At least 950,000 metric tons of heterotrophic biomass are associated with commercial ports around the world, emitting over 600 metric tons of carbon dioxide into the atmosphere and consuming 5 million megajoules of energy per day.

We propose the concept of a trophic “footprint” of marine urbanization, in which every square meter of artificial structure can negate the primary production of up to 130 square meters of surrounding coastal waters; collectively, these structures not only act as energy sinks and carbon sources, but also potentially reduce the productivity of coastal food webs.

Malerba ME, White CR, Marshall DJ (2019) The outsized trophic footprint of marine urbanization. Frontiers in Ecology and the Environment PDF DOI

Underestimating the benefits of marine protected areas for the replenishment of fished populations

Authors: Dustin J Marshall, Steven Gaines, Robert Warner, Diego R Barneche, and Michael Bode

Published in: Frontiers in Ecology and the Environment

Abstract

Marine protected areas (MPAs) are important tools for managing marine ecosystems. MPAs are expected to replenish nearby exploited populations through the natural dispersal of young, but the models that make these predictions rely on assumptions that have recently been demonstrated to be incorrect for most species of fish.

A meta‐analysis showed that fish reproductive output scales “hyperallometrically” with fish mass, such that larger fish produce more offspring per unit body mass than smaller fish. Because fish are often larger inside MPAs, they should exhibit disproportionately higher reproductive output as compared to fish outside of MPAs.

We explore the consequences of hyperallometric reproduction for a range of species for population replenishment and the productivity of exploited species.

We show that the reproductive contribution of fish inside MPAs has been systematically underestimated and that fisheries yields can be enhanced by the establishment of reservoirs of larger, highly fecund fish.

Marshall DJ, Gaines S, Warner R, Barneche DR, Bode M (2019) Underestimating the benefits of marine protected areas for the replenishment of fished populations. Frontiers in Ecology and the Environment PDF DOI

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

Abstract

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.

Size‐abundance rules? Evolution changes scaling relationships between size, metabolism and demography

Authors: Martino E Malerba and Dustin J Marshall

Published in: Ecology Letters

Abstract

Body size often strongly covaries with demography across species. Metabolism has long been invoked as the driver of these patterns, but tests of causal links between size, metabolism and demography within a species are exceedingly rare.

We used 400 generations of artificial selection to evolve a 2,427% size difference in the microalga Dunaliella tertiolecta. We repeatedly measured size, energy fluxes and demography across the evolved lineages. Then, we used standard metabolic theory to generate predictions of how size and demography should covary based on the scaling of energy fluxes that we measured.

The size dependency of energy remained relatively consistent in time, but metabolic theory failed to predict demographic rates, which varied unpredictably in strength and even sign across generations.

Classic theory holds that size affects demography via metabolism – our results suggest that both metabolism and size act separately to drive demography and that among‐species patterns may not predict within‐species processes.

Malerba ME, Marshall DJ (2019) Size-abundance rules? Evolution changes scaling relationships between size, metabolism and demography. Ecology Letters PDF DOI