Authors: Giulia Ghedini, Martino E Malerba, and Dustin J Marshall
Published in:Proceedings of the Royal Society B: Biological Sciences
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 SciencesPDFDOI
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
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 PDFDOI
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.
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.
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.
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?
Authors: Dustin J Marshall, Amanda K Pettersen, Michael Bode, and Craig R White
Published in:Nature Ecology & Evolution
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 & EvolutionPDFDOI
Authors: Giulia Ghedini, Michel Loreau, and Dustin J Marshall
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 PDFDOI
Body size often declines with increasing temperature. Although there is ample evidence for this effect to be adaptive, it remains unclear whether size shrinking at warmer temperatures is driven by specific properties of being smaller (e.g., surface to volume ratio) or by traits that are correlated with size (e.g., metabolism, growth).
We used 290 generations (22 months) of artificial selection on a unicellular phytoplankton species to evolve a 13‐fold difference in volume between small‐selected and large‐selected cells and tested their performance at 22 °C (usual temperature), 18 °C (−4), and 26 °C (+4).
Warmer temperatures increased fitness in small‐selected individuals and reduced fitness in large‐selected ones, indicating changes in size alone are sufficient to mediate temperature‐dependent performance.
Our results are incompatible with the often‐cited geometric argument of warmer temperature intensifying resource limitation. Instead, we find evidence that is consistent with larger cells being more vulnerable to reactive oxygen species. By engineering cells of different sizes, our results suggest that smaller‐celled species are pre‐adapted for higher temperatures.
We discuss the potential repercussions for global carbon cycles and the biological pump under climate warming.
Malerba ME, Marshall DJ (2019) Testing the drivers of the temperature-size covariance using artificial selection. EvolutionPDFDOI
Authors: Evatt Chirgwin, Dustin J Marshall, and Keyne Monro
Published in:Functional Ecology
Global warming may threaten fertility, which is a key component of individual fitness and vital for population persistence. For males, fertility relies on the ability of sperm to collide and fuse with eggs; consequently, sperm morphology is predicted to be a prime target of selection owing to its effects on male function.
In aquatic environments, warming will expose gametes of external fertilizers to the physiological effects of higher temperature and the physical effects of lower viscosity. However, the consequences of either effect for fertility, and for selection acting on sperm traits to maintain fertility, are poorly understood.
Here, we test how independent changes in water temperature and viscosity alter male fertility and selection on sperm morphology in an externally fertilizing marine tubeworm. To create five fertilization environments, we manipulate temperature to reflect current-day conditions (16.5 °C), projected near-term warming (21 °C) and projected long-term warming (25 °C), then adjust two more environments at 21 °C and 25 °C to the viscosity of environments at 16.5 °C and 21 °C, respectively. We then use a split-ejaculate design to measure the fertility of focal males, and selection on their sperm, in each environment.
Projected changes in temperature and viscosity act independently to reduce male fertility, but act jointly to alter selection on sperm morphology. Specifically, environments resulting from projected warming alter selection on the sperm midpiece in ways that suggest shifts in the energetic challenges of functioning under stressful conditions. Selection also targets sperm head dimensions and tail length, irrespective of environment.
We provide the first evidence that projected changes in ocean temperature and viscosity will not only impact the fertility of marine external fertilizers, but expose their gametes to novel selection pressures that may drive them to adapt in response if gamete phenotypes are sufficiently heritable.
Chirgwin E, Marshall DJ, Monro K (2019) Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology. Functional EcologyPDFDOI
Authors: Hayley Cameron, Tim Coulson, and Dustin J Marshall
Published in:Ecology Letters
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 LettersPDFDOI
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.
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.
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 PDFDOI