Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Authors: Martino E Malerba, Dustin J Marshall, Maria M Palacios, John A Raven, and John Beardall

Published in: New Phytologist

Summary

Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume‐specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO2‐concentrating mechanisms (CCMs).

Previous studies have focused on among‐species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3‐fold difference in cell volume. We compared CO2affinity, external carbonic anhydrase (CAext), isotopic signatures (δ13C) and growth among size‐selected lineages.

Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO2 affinity, higher CAext and higher δ13C. Larger cells also achieved faster growth and higher maximum biovolume densities.

We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

Malerba ME, Marshall DJ, Palacios MM, Raven JA, Beardall J (2020) Cell size influences inorganic carbon acquisition in artificially selected phytoplankton. New Phytologist PDF DOI

Projecting marine developmental diversity and connectivity in future oceans

Authors: Dustin J Marshall and Mariana Álvarez-Noriega

Published in: Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

Global change will alter the distribution of organisms around the planet. While many studies have explored how different species, groups and traits might be re-arranged, few have explored how dispersal is likely to change under future conditions.

Dispersal drives ecological and evolutionary dynamics of populations, determining resilience, persistence and spread. In marine systems, dispersal shows clear biogeographical patterns and is extremely dependent on temperature, so simple projections can be made regarding how dispersal potentials are likely to change owing to global warming under future thermal regimes.

We use two proxies for dispersal — developmental mode and developmental duration. Species with a larval phase are more dispersive than those that lack a larval phase, and species that spend longer developing in the plankton are more dispersive than those that spend less time in the plankton.

Here, we explore how the distribution of different development modes is likely to change based on current distributions. Next, we estimate how the temperature-dependence of development itself depends on the temperature in which the species lives, and use this estimate to project how developmental durations are likely to change in the future.

We find that species with feeding larvae are likely to become more prevalent, extending their distribution poleward at the expense of species with aplanktonic development. We predict that developmental durations are likely to decrease, particularly in high latitudes where durations may decline by more than 90%. Overall, we anticipate significant changes to dispersal in marine environments, with species in the polar seas experiencing the greatest change.

This article is part of the theme issue ‘Integrative research perspectives on marine conservation’.

Marshall DJ, Álvarez-Noriega M (2020) Projecting marine developmental diversity and connectivity in future oceans. Philosophical Transactions of the Royal Society B: Biological Sciences PDF DOI

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

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

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

The Conversation: From crocodiles to krill, a warming world raises the ‘costs’ paid by developing embryos

By Dustin Marshall

This article is republished from The Conversation under a Creative Commons licence.

Apart from mammals and birds, most animals develop as eggs exposed to the vagaries of the outside world. This development is energetically “costly”. Going from a tiny egg to a fully functioning organism can deplete up to 60% of the energy reserves provided by a parent.

In cold-blooded animals such as marine invertebrates (including sea stars and corals), fish and reptiles, and even insects, embryonic development is very sensitive to changes in the temperature of the environment.

Thus, in a warming world, many cold-blooded species face a new challenge: developing successfully despite rising temperatures.

For our research, published today in Nature Ecology and Evolution, we mined existing literature for data on how temperature impacts the metabolic and development rates of 71 different species, ranging from tropical crocodiles to Antarctic krill.

We found over time, species tend to fine-tune their physiology so that the temperature of the place they inhabit is the temperature needed to minimise the “costs” of their embryonic development.

Temperature increases associated with global warming could substantially impact many of these species.

The perfect weather to grow an embryo

The energy costs of embryonic development are determined by two key rates. The “metabolic” rate refers to the rate at which energy is used by the embryo, and the “development” rate determines how long it takes the embryo to fully develop, and become an independent organism.

Both of these rates are heavily impacted by environmental temperature. Any change in temperature affecting them is therefore costly to an embryo’s development.

Generally, a 10°C increase in temperature will cause an embryo’s development and metabolic rate to more than triple.

This photo shows a developing sea urchin, from egg (top left) to larva, to a metamorphosed (matured into adult form) individual.

These effects partially cancel each other out. Higher temperatures increase the rate at which energy is used (metabolic), but shorten the developmental time.

But do they balance out effectively?

What are the costs?

For any species, there is one temperature that achieves the perfect energetic balance between relatively rapid development and low metabolism. This optimal temperature, also called the “Goldilocks” temperature, is neither too hot, nor too cold.

When the temperature is too cold for a certain species, development takes a long time. When it’s too hot, development time decreases while the metabolic rate continues to rise. An imbalance on either side can negatively impact a natural population’s resilience and ability to replenish.

As an embryo’s developmental costs increase past the optimum, mothers must invest more resources into each offspring to offset these costs.

When offspring become more costly to make, mothers make fewer, larger offspring. These offspring start life with fewer energy reserves, reducing their chances of successfully reproducing as adults themselves.

Thus, when it comes to embryonic development, higher-than ideal temperatures pack a nasty punch for natural populations.

Since the temperature dependencies of metabolic rate and development rate are fairly similar, the slight differences between them had gone unnoticed until recently.

Embryos at risk

For each species in our study, we found a narrow band of temperatures that minimised developmental cost. Temperatures that were too high or too low caused massive blow-outs in the energy budget of developing embryos.

This means temperature increases associated with global warming are likely to have bigger impacts than previously predicted.

Predictions of how future temperature changes will affect organisms are often based on estimates of how temperature affects embryo survival. These measures suggest small temperature increases (1°C-2°C) do not reduce embryo survival by much.

But our study found the developmental costs are about twice as high, and we had underestimated the impacts of subtle temperature changes on embryo development.

In the warming animal kingdom, there are winners and losers

Some good news is our research suggests not all species are facing rising costs with rising temperatures, at least initially.

We’ve created a mathematical framework called the Developmental Cost Theory, which predicts some species will actually experience slightly lower developmental costs with minor increases in temperature.

In particular, aquatic species (fish and invertebrates) in cool temperate waters seem likely to experience lower costs in the near future. In contrast, certain tropical aquatic species (including coral reef organisms) are already experiencing temperatures that exceed their optimum. This is likely to get worse.

It’s important to note that for all species, increasing environmental temperature will eventually come with costs.

Even if a slight temperature increase reduces costs for one species, too much of an increase will still have a negative impact. This is true for all the organisms we studied.

A key question now is: how quickly can species evolve to adapt to our warming climate?The Conversation

Developmental cost theory predicts thermal environment and vulnerability to global warming

Authors: Dustin J Marshall, Amanda K Pettersen, Michael Bode, and Craig R White

Published in: Nature Ecology & Evolution

Abstract

Metazoans must develop from zygotes to feeding organisms. In doing so, developing offspring consume up to 60% of the energy provided by their parent.

The cost of development depends on two rates: metabolic rate, which determines the rate that energy is used; and developmental rate, which determines the length of the developmental period. Both development and metabolism are highly temperature-dependent such that developmental costs should be sensitive to the local thermal environment.

Here, we develop, parameterize and test developmental cost theory, a physiologically explicit theory that reveals that ectotherms have narrow thermal windows in which developmental costs are minimized (Topt).

Our developmental cost theory-derived estimates of Topt predict the natural thermal environment of 71 species across seven phyla remarkably well (R2⁓0.83).

Developmental cost theory predicts that costs of development are much more sensitive to small changes in temperature than classic measures such as survival. Warming-driven changes to developmental costs are predicted to strongly affect population replenishment and developmental cost theory provides a mechanistic foundation for determining which species are most at risk. Developmental cost theory predicts that tropical aquatic species and most non-nesting terrestrial species are likely to incur the greatest increase in developmental costs from future warming.

Marshall DJ, Pettersen AK, Bode M, White CR (2020) Developmental cost theory predicts thermal environment and vulnerability to global warming. Nature Ecology & Evolution PDF DOI

Community efficiency during succession: a test of MacArthur’s minimization principle in phytoplankton communities

Authors: Giulia Ghedini, Michel Loreau, and Dustin J Marshall

Published in: Ecology

Abstract

Robert MacArthur’s niche theory makes explicit predictions on how community function should change over time in a competitive community. A key prediction is that succession progressively minimizes

the energy wasted by a community, but this minimization is a trade‐off between energy losses from unutilised resources and costs of maintenance. By predicting how competition determines community efficiency over time MacArthur’s theory may inform on the impacts of disturbance on community function and invasion risk.

We provide a rare test of this theory using phytoplankton communities, and find that older communities wasted less energy than younger ones but that the reduction in energy wastage was not monotonic over time. While community structure followed consistent and clear trajectories, community function was more idiosyncratic among adjoining successional stages and driven by total community biomass rather than species composition.

Our results suggest that subtle shifts in successional sequence can alter community efficiency and these effects determine community function independently of individual species membership.

We conclude that, at least in phytoplankton communities, general trends in community function are predictable over time accordingly to MacArthur’s theory. Tests of MacArthur’s minimization principle across very different systems should be a priority given the potential of this theory to inform on the functional properties of communities.

Ghedini G, Loreau M, Marshall DJ (2020) Community efficiency during succession: a test of MacArthur’s minimization principle in phytoplankton communities. Ecology PDF DOI