Size and density mediate transitions between competition and facilitation

Authors: Hayley Cameron, Tim Coulson, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Species simultaneously compete with and facilitate one another. Size can mediate transitions along this competition–facilitation continuum, but the consequences for demography are unclear.

We orthogonally manipulated the size of a focal species, and the size and density of a heterospecific neighbour, in the field using a model marine system. We then parameterised a size‐structured population model with our experimental data.

We found that heterospecific size and density interactively altered the population dynamics of the focal species. Size determined whether heterospecifics facilitated (when small) or competed with (when large) the focal species, while density strengthened these interactions.

Such size‐mediated interactions also altered the pace of the focal’s life history. We provide the first demonstration that size and density mediate competition and facilitation from a population dynamical perspective. We suspect such effects are ubiquitous, but currently underappreciated.

We reiterate classic cautions against inferences about competitive hierarchies made in the absence of size‐specific data.

Cameron H, Coulson T, Marshall DJ (2019) Size and density mediate transitions between competition and facilitation. Ecology Letters PDF DOI

How can pathogens optimise both transmission and dispersal?

Certain pathogens (disease-producing organisms) are stuck in a Catch-22; to survive they need to continue to find, and infect, new hosts. But infection makes their hosts sick and less likely to move to where there are new hosts to infect.

PhD student Louise Nørgaard and her supervisors Ben Phillips and Matt Hall have found evidence of a pathogen that resolves this issue by exploiting the differences in size and behaviour of male and female hosts to optimize its own chance of successful infection.

The team uses the freshwater crustacean Daphnia magna and its common pathogen Pasteuria ramosa as a model system to test the idea that a pathogen can exploit differences between the sexes of a host to its advantage. The pathogen P. ramosa is ingested by Daphnia after which it sterilises and kills the host, releasing transmission spores that are ready to infect a new host. Female Daphnia are bigger, live longer and are more susceptible to infection than males.

Louise set up two separate experiments, allowing her to monitor the probability that Daphnia would disperse from a crowded area to a less crowded area and to measure the rate and distance travelled by infected and uninfected male and female individuals.

In the first experiment Louise was able to capitalise on previous work that has shown that Daphnia will disperse when conditions are crowded. Exposure to water taken from high densities of Daphniais enough to encourage dispersal. Louise used ‘crowded-conditioned’ water and found infected male Daphnia were more likely to disperse than uninfected males. Infected females, on the other hand, were a lot less likely to disperse than uninfected females.

A second experiment found that infected females had four times the number of transmission spores than infected males and moved less far and more slowly than males or uninfected females. Infected males though, moved at the same rate and travelled the same distance as uninfected males.

The figure A shows how far male (blue) and females (green) disperse when infected with the pathogen compared to uninfected individuals. Louise tested two types of pathogen C1 and C19. She also measured the distance travelled (B) and the spore load in infected individuals (C).

So how do these differences between the sexes help the pathogen? Females are bigger and can host large numbers of transmission spores. Staying put when densities are high means they are releasing this large number of spores into a crowd – potentially maximising the chance of further infections.  Smaller males have fewer spores to release and the chance of secondary infections may be maximised when they move to new areas where few individuals are already infected.

Importantly the differences in dispersal behaviour between infected males and females seem to relate directly to the way the pathogen interacts with each sex. Uninfected males and females had similar rates and distance of dispersal while uninfected females were more likely to move away from crowded habitats than males. These patterns disappear when both sexes are infected.

Do these different infection strategies in different sexes provide a form of bet-hedging for the pathogen? Louise and her supervisors think they do and, if widespread, will have important implications for disease dynamics.

This research is published in the journal Biology Letters.

Mirth recognised with Crozier medal

The Centre for Geometric Biology’s Christen Mirth has been recognised for her research on how nutrition shapes development, having been awarded the Ross Crozier medal by the Genetics Society of Australasia.

When Christen first began working on this problem in 2003, using the fruit fly Drosophila melangoster as a model, researchers knew that nutrition had a role in the secretion of insulin-like peptides. These peptides, in turn, influenced the rates of body growth.  What they didn’t know, was what made insects stop growing.

During her postdoc, Christen and her colleagues discovered there was another hormone involved in regulating when growth should stop: ecdysone, the steroid that controls moulting in insects. It turned out that nutritional changes can control the timing of a critical pulse of ecdysone, which commits an insect to metamorphosis. In other words, ecdysone was the key they had been looking for, determining the developmental rate and the final size of the insect.

What’s more, the team found certain organs, such as the wings and the ovaries, require this ecdysone pulse for cells to acquire organ-specific identities and to grow. Organs also change the way they respond to nutritional cues with time by changing the combination of hormones required for growth, providing a further buffer against nutritional environments determining organ size. Such differences in the way organs respond to nutrition (and the associated hormone releases) are important as they allow for variation in animal shape and ensure that correct organ function is maintained in different nutritional conditions.

Christen has gone on to investigate other hormones and, in collaboration with colleague Associate Professor Alexander Shingleton of the University of Illinois, has found another developmental hormone that regulates body size but not developmental timing. This ‘juvenile hormone’ reduces insulin signalling and increases the concentration of ecdysone without altering the timing of ecdysone pulses.

Now as leader of the Mirth Lab, Christen emphasises how the group’s work provides a theory for the way nutrition might influence the growth of other animals. Nutrition may act as a stimulus, modifying insulin signalling and the synthesis of key developmental hormones like sex steroids in mammals.

The Ross Crozier medal was established by the Genetics Society of Australasia to recognise outstanding contributions to the field of genetics research by mid-career Australasian scientists. It has been awarded annually since 2011. The medal commemorates celebrated Australian evolutionary geneticist Ross Crozier (1943–2009).

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.

Can competitive asymmetries maintain offspring size variation? A manipulative field test

Authors: Hayley Cameron and Dustin J Marshall

Published in: Evolution

Abstract

Offspring sizes vary within populations but the reasons are unclear. Game‐theoretic models predict that selection will maintain offspring‐size variation when large offspring are superior competitors (i.e., competition is asymmetric), but small offspring are superior colonizers. Empirical tests are equivocal, however, and typically rely on interspecific comparisons, whereas explicit intraspecific tests are rare.

In a field study, we test whether offspring size affects competitive asymmetries using the sessile marine invertebrate, Bugula neritina. Surprisingly, we show that offspring size determines whether interactions are competitive or facilitative — large neighbours strongly facilitated small offspring, but also strongly competed with large offspring. These findings contradict the assumptions of classic theory — that is, large offspring were not superior competitors. Instead, smaller offspring actually benefit from interactions with large offspring— suggesting that asymmetric facilitation, rather than asymmetric competition, operates in our system.

We argue that facilitation of small offspring may be more widespread than currently appreciated, and may maintain variation in offspring size via negative frequency‐dependent selection.

Offspring size theory has classically viewed offspring interactions through the lens of competition alone, yet our results and those of others suggest that theory should accommodate positive interactions in explorations of offspring‐size variation.

Cameron H, Marshall DJ (2019) Can competitive asymmetries maintain offspring size variation? A manipulative field test. Evolution PDF DOI

Celebrating 500 generations of experimental evolution

It’s party time in the Centre for Geometric Biology: We’ve reached 500 generations of experimental evolution in our large and small algal cells!

Three and a half years ago Martino Malerba set up the first culture of the single-celled marine phytoplankton Dunaliella tertiolecta and begun to artificially select for large and small cells.  The selection process of separating the largest and the smallest cells has continued twice a week ever since.  Martino is now the proud ‘father’ of algal cells where the big cells are more than 10 times the size of the smaller cells.

The evolved algae lines have enabled Martino and his colleagues to look at the consequences of being a particular size without having to compare different species, which vary in many other ways than just size. This research directly supports the fundamental question the Centre for Geometric Biology seeks to understand “why do organisms grow to the size they do?”

The team has looked at the effects of size at both the level of the cell and the population. They have found that altering the size of a cell profoundly alters many fundamental traits of algal physiology and ecology. This affects how cells of different sizes will cope with fluctuating resources and, in turn, how those populations of cells use energy and grow.

Exciting research underway looks at community-level effects. What happens when grazers are only offered either large or small algal cells: does changing algal size have repercussions up the food chain?

Understanding how individuals grow and regulate their energy is critical in helping scientists predict how large-scale impacts, such as climate change, affect organisms.

Phytoplankton have critical roles in the ocean; they form the base of most food webs and fix large amounts of carbon.  So, while the research stemming from these artificially evolved algal cells is theoretically interesting, it also has a very direct and immediate application to how we understand and manage climate change.

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.