Dietary preferences in filter-feeding animals might explain their crowded co-existence

An enduring concept in ecology is that space is the resource most in demand for communities living on hard substrates such as rocky shores and pier pilings. We have seen before how these communities can be extremely dense and diverse with little or no unoccupied space. But is space the whole story? These communities also need food and oxygen. How do such dense assemblages of animals manage to extract enough food to allow them to co-exist?

Belinda Comerford, Mariana Álvarez-Noriega, and Dustin Marshall have found different species of filter-feeders tend to consume one species of phytoplankton much more than others when offered a selection. They noticed studies looking at the role food plays in structuring filter-feeding communities tend to consider phytoplankton as a uniform resource. This makes no allowance for differences in size, shape or chemical make-up of the different algal species.

Belinda, Mariana and Dustin suspected that different species of filter-feeders will consume different components of the phytoplankton, reducing competition for food and allowing for the dense and diverse communities that we see in nature. So, they set about testing how different species of filter feeder consumed a mix of three different phytoplankton species that varied in size and shape and chemical make-up. 

They used 11 different species of invertebrate filter-feeding animals and offered them a mix of the three phytoplankton species. They measured the concentrations of each phytoplankton species in the animal chambers one minute and one hour after adding equal volumes of each species to the chambers. They also had control chambers that contained no animals which enabled them to estimate how much of the algae settled out to the bottom during the experimental period.

While most of the animals ingested all three phytoplankton species they did so at different rates. The encrusting bryozoan Watersipora subtorquata consumed the largest algal species at a much greater rate than it did the other two species while the sponge Sycon spp. favoured the smallest algal species. Some species such as the sea squirt Ciona intestinalis appear to be generalists, consuming all three algal species at the same rate. 

It seems that Belinda, Mariana and Dustin might be right. Thinking of phytoplankton as a homogenous resource underestimates the potential for reducing competition between filter-feeding species. If, instead of competing for a ‘common pool’ of phytoplankton, filter feeders target specific subsections then the diverse and densely packed communities that we see are more readily explained.

This research is published in the journal Oecologia.

The different invertebrates ingested the different phytoplankton species at different rates.

Food and chemical cues can both drive changes in metabolic rates

Metabolic rate, or energy use, changes with the size of the organism. This general pattern has been observed across different species, as well as among individuals of the same species. But while the broad pattern holds, individuals of the same species and the same size can also vary in the amount of energy they use.

Some studies have shown that individuals have lower metabolic rates as population numbers go up, but no one really knows why. Metabolic rates increase following food intake, so one plausible explanation is that competition for food in crowded conditions reduces food intake and, in turn, metabolic rates.

Melanie Lovass and her supervisors Dustin Marshall and Giulia Ghedini have run a series of experiments to investigate this possibility.

The team used the model species Bugula neritina to test their ideas. They ran a series of experiments where they were able to measure metabolic rates in individual Bugula colonies and they manipulated food, oxygen concentration, water flow and chemical cues to try and tease apart what was causing a reduction in metabolic rates in dense populations.

In the model system, each of these measures are influenced by how sparse or dense the population is. As expected, food availability affected metabolic rates but the team was surprised to find that chemical cues from individuals of the same species are also able to drive changes in metabolic rates.

Metabolic rates were lower in colonies that were starved, but metabolic rates were not affected by changes in water flow and oxygen concentrations.

This graph shows metabolic rates for <em>Bugula<em> colonies that have been exposed to chemical cues from other colonies (red) are lower than metabolic rates for the control colonies (blue).

More interestingly, Melanie and her supervisors found that metabolic rates were suppressed in Bugula colonies that were kept in ‘pre-conditioned’ water. This water had been exposed to other Bugula colonies overnight and so incorporated any chemical cues released from these other colonies. Melanie thought that chemical cues from fellow colonies might signal a reduction in feeding rates. To check if this was the case, she counted the number of feeding structures active in colonies exposed to ‘pre-conditioned’ versus normal seawater.

They found no differences in feeding rates indicating that the chemical cues from Bugula colonies were suppressing physiological processes rather than reducing feeding rates. So, while the chemical cues from other Bugula colonies reduce energy use, this reduction is in processes other than feeding activity.

While searching for food is energetically costly; keeping up feeding activity may be worth the costs and become even more important when access to food is very competitive.

Bugula are colonial organisms made up of ‘modules’. Each module has its own feeding structure – a crown of tentacles – known as a lophophore. There was no difference in the number of active lophophores in the colonies exposed to chemical cues compared to the control colonies. Photo credit: Amy Hall.

This research is published in the Journal of Experimental Biology.

Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake

Authors: Melanie K Lovass, Dustin J Marshall, and Giulia Ghedini

Published in: Journal of Experimental Biology

Abstract

Within species, individuals of the same size can vary substantially in their metabolic rate. One source of variation in metabolism is conspecific density – individuals in denser populations may have lower metabolism than those in sparser populations. However, the mechanisms through which conspecifics drive metabolic suppression remain unclear.

While food competition is a potential driver, other density-mediated factors could act independently or in combination to drive metabolic suppression but these drivers have rarely been investigated.

We used sessile marine invertebrates to test how food availability interacts with oxygen availability, water flow and chemical cues to affect metabolism.

We show that conspecific chemical cues induce metabolic suppression independently of food and this metabolic reduction is associated with the downregulation of physiological processes rather than feeding activity.

Conspecific cues should be considered when predicting metabolic variation and competitive outcomes as they are an important, but underexplored, source of variation in metabolic traits.

Lovass MK, Marshall DJ, Ghedini G (2020) Conspecific chemical cues drive density-dependent metabolic suppression independently of resource intake. The Journal of Experimental Biology PDF DOI

Estimating energy use in communities

As ecologists, we often want to get an idea of how a community functions. For example, how much food does a community of animals consume every day? Or how much oxygen do plants produce every day? We can get an idea of these functions by measuring the energy use (or metabolism) of a community. But such functional measures can be difficult to collect, especially for an entire community. 

Since a community is made up of many species, estimating the total metabolism from the metabolism of each species separately is a way around this problem. But the methods we use, and the data required, vary and may not be validated against actual data because these are rarely available. 

Giulia Ghedini, Martino Malerba and Dustin Marshall have set out to test six different ways of estimating the energy use of a community. The authors measured actual metabolic rates in communities of phytoplankton (tiny marine microalgae) seeded with six different species of various sizes and left to change through time.

Previous work from the CGB meant the team had all the information they needed to estimate community energy use for the six methods. The different methods are summarised below.

There are a number of different ways we can estimate community metabolism that vary in complexity.

It turns out that when we are interested in whole community metabolism, size doesn’t matter. Why? Because larger species tend to be less abundant within communities, so even if each of them consumes more energy, the total energy use remains the same because there are fewer of them. While we knew this was the case for well-established communities, this new work shows that it is also true for communities as they change through time.

What is more, the team found that, in communities, the usual relationship between size and metabolism changed. Metabolism usually increases with size, but to a lesser extent for larger organisms (this is called an allometric relationship). This study showed that when measured across all species in the community, this relationship changed and the average energy use of species increased in direct proportion to their average size (this is an isometric relationship). This is why we can predict the total metabolism from the energy use per unit biomass. 

But towards the end of the experiment, when communities were dominated by larger cells, this ‘perfectly proportional’ relationship broke down. Giulia and her colleagues think that, when large species are very abundant, they suffer more from competition and reduce their metabolism more than smaller species. 

So, the good news is that we may be able to estimate community energy from easy to collect biomass data, but first, we need to see if this result applies to different communities. We also need more studies on how competition affects energy use, as the results from this study suggest they are important drivers of energy flow.

All of the methods are based on underlying theory so testing which methods are best at estimating actual metabolism can help us understand how energy use works in communities. This figure summarises what theory predicts we should have found compared to what we actually found.

This research was published in Proceedings of the Royal Society B: Biological Sciences.

Cell size, genome size and the selfish gene

Classic theories such as the ‘selfish gene hypothesis’ are not always easy to test. If true, then the theory proposes that cells accumulate extra DNA over time even when they provide no benefit to the organism – selfish genes. This means individuals with more DNA relative to their cell size should have reduced fitness. What is more, because the accumulation of DNA creates a burden on the organism, a good evolutionary strategy should be to reduce the amount of redundant DNA over time.

In one of the first tests of the theory using a single species, Martino Malerba, Giulia Ghedini and Dustin Marshall have found direct evidence that reduced amounts of total DNA (genome size) is associated with fitness benefits in a species of marine microalgae.

Scientists face a problem when they compare cell size and genome size between different species. It is hard to separate whether the slower rates of metabolism, development and growth are a result of genome size or the fact that larger organisms tend to have a slower pace of life anyway.

Martino and his colleagues were able to overcome this issue by using their evolved lines of the marine phytoplankton Dunaliella tertiolecta where cells have been artificially selected to be large or small. They were able to use a staining technique to measure the amount of DNA content within cells of different sizes but, importantly, of the same species and the same evolutionary age.

They weren’t surprised to find larger cells had more DNA. But they also found that, in cells of the same size, the cells with smaller genomes grew faster and accumulated more biomass; that is, had greater fitness.

So, this first finding was consistent with the prediction that reducing the amount of DNA in a cell can have positive effects for the fitness of a species. But having demonstrated that minimizing DNA can improve fitness, the team then wanted to test the prediction that species should decrease their DNA content as they evolve. Again, they were able to test this by using the Dunaliella and monitoring the evolving lines for a year or approximately100 generations.

Their results confirmed that cells decreased their DNA content by up to 11% across 100 generations of evolution. However, they also found that cells with already low amounts of DNA showed no change over time, which suggests the existence of an absolute lower limit in the DNA content of this species.

Overall, they have direct evidence for fitness benefits associated with reduced relative genome size consistent with the selfish gene hypothesis and as well as a minimum genome size below which an organism can’t maintain functionality.

This figure looks at how genome size or cell DNA content changes with cell size. The continuous black line shows the relationship between the two for the large, small and control algae after 350 generations of evolution. The broken line shows the relationship after 450 generations of evolution – 1 year later. Notice how the cell DNA content has reduced after 1 year of evolution.

This research was published in the journal Current Biology.

Genome size affects fitness in the eukaryotic alga Dunaliella tertiolecta

Authors: Martino E Malerba, Giulia Ghedini, and Dustin J Marshall

Published in: Current Biology

Abstract

Genome size is tightly coupled to morphology, ecology, and evolution among species, with one of the best-known patterns being the relationship between cell size and genome size.

Classic theories, such as the ‘selfish DNA hypothesis,’ posit that accumulating redundant DNA has fitness costs but that larger cells can tolerate larger genomes, leading to a positive relationship between cell size and genome size. Yet the evidence for fitness costs associated with relatively larger genomes remains circumstantial.

Here, we estimated the relationships between genome size, cell size, energy fluxes, and fitness across 72 independent lineages in a eukaryotic phytoplankton. Lineages with relatively smaller genomes had higher fitness, in terms of both maximum growth rate and total biovolume reached at carrying capacity, but paradoxically, they also had lower energy fluxes than lineages with relative larger genomes. We then explored the evolutionary trajectories of absolute genome size over 100 generations and across a 10-fold change in cell size.

Despite consistent directional selection across all lineages, genome size decreased by 11% in lineages with absolutely larger genomes but showed little evolution in lineages with absolutely smaller genomes, implying a lower absolute limit in genome size.

Our results suggest that the positive relationship between cell size and genome size in nature may be the product of conflicting evolutionary pressures, on the one hand, to minimize redundant DNA and maximize performance — as theory predicts — but also to maintain a minimum level of essential function.

Malerba ME, Ghedini G, Marshall DJ (2020) Genome size affects fitness in the eukaryotic alga Dunaliella tertiolecta. Current Biology PDF DOI

‘Oh, the places you’ll go.’ How far can marine larvae travel?

While travel restrictions have become part of the new normal for people all around the world, a recent study has found that the distance travelled by marine larvae is dictated by both biological and physical constraints.

Marine invertebrates face many challenges when it comes to reproduction. Sperm and sometimes eggs are released into the water where they must meet-up to allow fertilisation to take place. These fertilised embryos develop into larvae and remain in the water column until they find a suitable spot to settle. The amount of time they spend in the water column and the distances they travel can be vastly different for different species.

It is not easy to measure how far larvae travel in real-time so, instead, biologists often use genetic information to work out the relatedness of populations as a proxy for dispersal distance. An alternative approach gathers data on larval characteristics to estimate the time spent in the plankton and so the potential for dispersal.

Mariana Noriega and Dustin Marshall from the Centre for Geometric Biology have been working with colleagues from the United States to examine existing data to help them grasp how larval dispersal distance changes on a global scale. Recent exploration of this question has focused on the role of latitude (or temperature) on larval development, developmental mode (feeding or non-feeding larvae), maternal investment into egg size and hydrodynamics. Often these factors are considered separately rather than all together.

Here’s what we know. Higher temperatures speed up larval development so larvae in the tropics may spend less time in the plankton and disperse less far. But to complicate things, larvae in the tropics are more likely to be feeding larvae which means they tend to spend more time in the plankton than their non-feeding counterparts. Plus, mothers in cooler climes tend to invest more energy into their eggs which for non-feeding larvae means more time in the plankton for those that live at higher latitudes.

Mariana and her colleagues were particularly interested in understanding whether these life-history traits that change with latitude will combine with ocean current information to support their prediction that dispersal distances are shorter in the tropics.

The team have looked at data from 766 marine invertebrate species and classified the larvae into feeding or non-feeding. They extracted data on egg size and the time spent in the plankton, plus the latitude and longitude of the recorded observation.

They were then able to use statistical models to estimate planktonic duration at different latitudes by incorporating their data on development mode and egg size. Having the location of the record also enabled Mariana and the team to estimate local current speeds using the publicly available Mercator-Ocean modelling system. Finally, the expected planktonic duration for the ‘average larvae’ was then multiplied by current speed at each location to estimate dispersal potential.

To the team’s surprise, they didn’t find that dispersal distances were shorter in the tropics.

Instead, they found that the faster surface current speeds in the tropics overcame the effects of temperature on larval development time. So, even though larvae spend less time in the plankton they still have the potential to disperse further than the team predicted due to the faster current speeds.

In fact, the team found that larvae travel further at high and low latitudes, that is, the tropics and the poles. Dispersal distances were shortest in temperate regions where the time spent in the plankton is intermediate and current speeds are slower.

Planktonic duration (PD, days) across latitudes. Planktonic duration was estimated for both feeding and non-feeding larvae and then the potential time spent in the plankton was calculated using data for larval development times and egg size (a proxy measure for reserves available for the larvae). Grey circles show the distribution of studies from which data were obtained. The size of circle corresponds to the number of studies (n) at each location; n ranges from 1 to 33.

Predicted dispersal distance. These predictions incorporate both the biological data of the previous figure with current speeds and demonstrate that dispersal distance is actually shorter in temperate regions, (the dark blue areas), in contrast to the research team’s expectations.

Species richness is greater in the tropics but it seems as if this pattern is not driven by larval dispersal as has been previously suggested. If species richness were driven purely by dispersal distance, this study suggests we would find similar species richness at high latitudes and in the tropics, yet this is not the case.

Understanding patterns in larval dispersal is essential for understanding patterns in marine biodiversity and managing our marine systems. Without this, we will struggle to adequately design marine protected areas, effectively manage biological invasions and predict the consequences of climate change.

This research was published in the journal Nature Ecology & Evolution.

What role does oxygen supply play in determining a species’ thermal tolerance?

It is generally recognised that animals perform best at certain temperatures, so-called optimal temperatures. To understand how measures of performance, such as growth or running ability, will change with changing temperatures we need to understand the physiological processes limiting performance.

One compelling theory, known as the oxygen and capacity-limited thermal tolerance (OCLTT), suggests that a reduction in oxygen availability limits performance.

As temperature shifts away from optimal, the demand for oxygen in tissues is thought to outpace the rate of supply. This means a shift to anaerobic metabolism, a process far less efficient than aerobic metabolism, causing a reduction in performance.

Emily Lombardi, Candice Bywater and Craig White wanted to test the theory and used the speckled cockroach as their experimental animal because they are easy to breed and keep in the lab. Unlike other studies testing the OCLTT hypothesis, their interest was in the less extreme ends of the temperature range, which the OCLTT hypothesis specifically addresses.

Emily, Candice and Craig predicted that performance would be reduced (↓) in hypoxic environments and sub-optimal temperatures but increased (↑) in hyperoxic environments at optimal temperatures and stay the same (−) as atmospheric oxygen conditions at optimal temperatures when in a hyperoxic environment but at sub-optimal temperatures.

First, Emily and her colleagues calculated the temperature that optimised growth by allowing juvenile cockroaches to develop for 35 days at 8 temperatures ranging between 10 and 36 °C. They also determined the temperatures (both above and below the optimal temperature) where growth was reduced by 32%. These 3 temperatures (optimal, lower and upper developmental temperatures) were then used in oxygen manipulation experiments.

Next, they ran an experiment including the three temperatures plus three oxygen concentrations; atmospheric (21%), hypoxic (10%) and hyperoxic (40%). Cockroaches were assigned to one of the 9 treatments and growth rate was measured repeatedly over 5 weeks. Running performance – time on a treadmill – was measured at the end of the 5 weeks at the three temperatures. Tracheal morphology was also quantified because, in some species, changes to the oxygen delivery system can alleviate the demand for increased oxygen supply.

If the OCLTT theory held, then the team expected to see a difference in performance at the different oxygen concentrations at each temperature. But, instead, they found increasing oxygen concentrations did not mitigate the effects of sub-optimal temperatures. There was also no evidence that tracheal morphology changed as a result of the developmental temperature or oxygen environment. The team concluded that oxygen supply was not the main determinant of temperature-related performance limitations for the speckled cockroach.

It seems, the OCLTT may not provide the unifying theory its proponents hoped, but instead, a species’ thermal tolerance is likely shaped by a range of factors.

In fact, they found that growth did not differ between oxygen concentrations at the lower temperature, but growth was lower in hypoxic environments at optimal temperatures when compared to atmospheric oxygen concentrations and lastly growth was lower in hyperoxic environments at high temperatures compared to atmospheric oxygen concentrations. All points that share a letter are not significantly different from one another.

This research was published in the Journal of Experimental Biology.

Competition plays a part in maintaining variation in metabolic rates

We know that the rate at which organisms use energy (metabolic rate) varies substantially between individuals of the same species, even after accounting for size and temperature. What we are less sure about, is, why we see this variation.

When Amanda Pettersen and her colleagues thought about this question they considered it plausible that the competitive environments that individuals find themselves in might be important in determining whether a faster or slower metabolic rate is selected for. They wanted to find out whether variation in competition affects selection on metabolic rates and whether that could account for the variation in metabolic rate that persists more generally.

To test this idea Amanda used the model species Bugula neritina because it allowed the team to collect larvae in the lab, measure size and metabolic rate of larvae before assigning the larvae to one of three ‘competition’ treatments. Once the larval measurements were made, larvae were randomly assigned to either a no-competition environment, a competitive environment where they were put with other Bugula neritina (intraspecific competition) or, a competitive environment with an established mixed-species community (interspecific competition).

Individuals were then returned to the field and monitored weekly for survival, growth, age when first become reproductive and fecundity (total reproductive output).

Following measurements of size and metabolic rate, larvae were settled on small plates that were either kept bare (no competition), had other Bugula on the plate (intraspecific competition) or had an established community already there (interspecific competition). Plates were submerged in the field and monitored weekly.

The team already knew that higher metabolic rates are linked to faster growth, earlier onset of reproduction, and a shorter lifespan, while low metabolic rates are associated with a slow pace-of-life (slow growth, late onset of reproduction and long lifespan).

This experiment showed that individuals with higher metabolic rates were more likely to survive, more likely to reproduce and had greater numbers of ovicells at the start of reproduction, in the more intense, interspecific competition treatment. The team speculates that the individuals with higher metabolic rates grow more quickly enabling them to reach resources such as food and oxygen that are less available to smaller, slower growing organisms. There is a downside: these higher metabolic rate individuals also had a shorter lifespan.

The expectation amongst evolutionary biologists is that where there is strong selection pressure for a particular trait then the variation within that trait is reduced. So even accounting for the shorter lifespan, the overall increase in reproduction should mean that a higher metabolic rate is strongly selected for in competitive environments.

But the team also found that individuals with lower metabolic rates had a higher probability of living for longer in the absence of competition and would have continued to reproduce long after the individuals with a higher metabolic rate had died.

Bugula live on hard substrates and these areas commonly vary in their composition. Complex three-dimensional, highly diverse communities are interspersed with sparse populations of a few species and patches of bare areas. Individuals with lower metabolic rates that happen to arrive at a bare patch will have a long reproductive period and high overall fecundity. In contrast, individuals with a high metabolic rate that settle in amongst other species will be reproductive quickly and so successfully produce large numbers of offspring.

Because Bugula larvae are likely to find themselves in a variety of different competitive environments – even when they settle relatively close to each other – there is a strong evolutionary argument to explain the persistence of variation in metabolic rate, for Bugula at least.

This research is published in the journal Evolution Letters.

Metabolic rate, context-dependent selection, and the competition-colonization trade-off

Authors: Amanda K Pettersen, Matthew D Hall, Craig R White, and Dustin J Marshall

Published in: Evolution Letters

Abstract

Metabolism is linked with the pace-of-life, co-varying with survival, growth, and reproduction. Metabolic rates should therefore be under strong selection and, if heritable, become less variable over time. Yet intraspecific variation in metabolic rates is ubiquitous, even after accounting for body mass and temperature.

Theory predicts variable selection maintains trait variation, but field estimates of how selection on metabolism varies are rare.

We use a model marine invertebrate to estimate selection on metabolic rates in the wild under different competitive environments.

Fitness landscapes varied among environments separated by a few centimetres: interspecific competition selected for higher metabolism, and a faster pace‐of‐life, relative to competition‐free environments.

Populations experience a mosaic of competitive regimes; we find metabolism mediates a competition-colonization trade-off across these regimes. Although high metabolic phenotypes possess greater competitive ability, in the absence of competitors, low metabolic phenotypes are better colonizers.

Spatial heterogeneity and the variable selection on metabolic rates that it generates is likely to maintain variation in metabolic rate, despite strong selection in any single environment.

Pettersen AK, Hall MD, White CR, Marshall DJ (2020) Metabolic rate, context-dependent selection, and the competition-colonization trade-off. Evolution Letters PDF DOI