Differential resource use in filter-feeding marine invertebrates

Authors: Belinda Comerford, Mariana Álvarez-Noriega, and Dustin J Marshall

Published in: Oecologia

Abstract

Coexistence theory predicts that, in general, increases in the number of limiting resources shared among competitors should facilitate coexistence.

Heterotrophic sessile marine invertebrate communities are extremely diverse but traditionally, space was viewed as the sole limiting resource. Recently planktonic food was recognized as an additional limiting resource, but the degree to which planktonic food acts as a single resource or is utilized differentially remains unclear. In other words, whether planktonic food represents a single resource niche or multiple resource niches has not been established.

We estimated the rate at which 11 species of marine invertebrates consumed three phytoplankton species, each different in shape and size.

Rates of consumption varied by a 240-fold difference among the species considered and, while there was overlap in the consumer diets, we found evidence for differential resource usage (i.e. consumption rates of phytoplankton differed among consumers). No consumer ingested all phytoplankton species at equivalent rates, instead most species tended to consume one of the species much more than others.

Our results suggest that utilization of the phytoplankton niche by filter feeders is more subdivided than previously thought, and resource specialization may facilitate coexistence in this system. Our results provide a putative mechanism for why diversity affects community function and invasion in a classic system for studying competition.

Comerford B, Álvarez-Noriega M, Marshall D (2020) Differential resource use in filter-feeding marine invertebrates. Oecologia. PDF DOI

Facultative feeding in a marine copepod: effects of larval food and temperature on performance

Authors: Alexander N Gangur, and Dustin J Marshall

Published in: Marine Ecology Progress Series

Abstract

Most marine invertebrate larvae either feed or rely on reserves provisioned by parents to fuel development, but facultative feeders can do both.

Food availability and temperature are key environmental drivers of larval performance, but the effects of larval experience on performance later in life are poorly understood in facultative feeders. In particular, the functional relevance of facultative feeding is unclear. One feature to be tested is whether starved larvae can survive to adulthood and reproduce.

We evaluated effects of larval temperature and food abundance on performance in a marine harpacticoid copepod, Tisbe sp. In doing so, we report the first example of facultative feeding across the entire larval stage for a copepod.

In a series of experiments, larvae were reared with ad libitum food or with no food, and at 2 different temperatures (20 vs 24 °C). We found that higher temperatures shortened development time, and larvae reared at higher temperature tended to be smaller. Larval food consistently improved early performance (survival, development rate and size) in larvae, while starvation consistently decreased survival, increased development time and decreased size at metamorphosis. Nonetheless, a small proportion (3–9.5%, or 30–42.7% with antibiotics) of larvae survived to metamorphosis, could recover from a foodless larval environment, reach maturity and successfully reproduce.

We recommend that future studies of facultative feeding consider the impact of larval environments on adult performance and ability to reproduce.

Gangur A, Marshall D (2020) Facultative feeding in a marine copepod: effects of larval food and temperature on performance. Marine Ecology Progress Series PDF DOI

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. Although 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

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.

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.

How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux

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

Published in: Proceedings of the Royal Society B: Biological Sciences

Abstract

Size and metabolism are highly correlated, so that community energy flux might be predicted from size distributions alone. However, the accuracy of predictions based on interspecific energy–size relationships relative to approaches not based on size distributions is unknown.

We compare six approaches to predict energy flux in phytoplankton communities across succession: assuming a constant energy use among species (per cell or unit biomass), using energy–size interspecific scaling relationships and species-specific rates (both with or without accounting for density effects).

Except for the per cell approach, all others explained some variation in energy flux but their accuracy varied considerably. Surprisingly, the best approach overall was based on mean biomass-specific rates, followed by the most complex (species-specific rates with density).

We show that biomass-specific rates alone predict community energy flux because the allometric scaling of energy use with size measured for species in isolation does not reflect the isometric scaling of these species in communities. We also find energy equivalence throughout succession, even when communities are not at carrying capacity.

Finally, we discuss that species assembly can alter energy–size relationships, and that metabolic suppression in response to density might drive the allometry of community energy flux as biomass accumulates.

Ghedini G, Malerba ME, Marshall DJ (2020) How to estimate community energy flux? A comparison of approaches reveals that size-abundance trade-offs alter the scaling of community energy flux. Proceedings of the Royal Society B: Biological Sciences PDF DOI

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.

Global biogeography of marine dispersal potential

Authors: Mariana Álvarez-Noriega, Scott C Burgess, James E Byers, James M Pringle, John P Wares, and Dustin J Marshall

Published in: Nature Ecology & Evolution

Abstract

The distance travelled by marine larvae varies by seven orders of magnitude. Dispersal shapes marine biodiversity, and must be understood if marine systems are to be well managed.

Because warmer temperatures quicken larval development, larval durations might be systematically shorter in the tropics relative to those at high latitudes. Nevertheless, life history and hydro-dynamics also covary with latitude—these also affect dispersal, precluding any clear expectation of how dispersal changes at a global scale.

Here we combine data from the literature encompassing >750 marine organisms from seven phyla with oceanographic data on current speeds, to quantify the overall latitudinal gradient in larval dispersal distance.

We find that planktonic duration increased with latitude, confirming predictions that temperature effects outweigh all others across global scales. However, while tropical species have the shortest planktonic durations, realized dispersal distances were predicted to be greatest in the tropics and at high latitudes, and lowest at mid-latitudes. At high latitudes, greater dispersal distances were driven by moderate current speed and longer planktonic durations. In the tropics, fast currents overwhelmed the effect of short planktonic durations.

Our results contradict previous hypotheses based on biology or physics alone; rather, biology and physics together shape marine dispersal patterns.

Álvarez-Noriega M, Burgess SC, Byers JE, Pringle JM, Wares JP, Marshall DJ (2020) Global biogeography of marine dispersal potential. Nature Ecology & Evolution PDF DOI