Does energy flux predict density-dependence? An empirical field test

Authors: Giulia Ghedini, Craig R White, and Dustin J Marshall

Published in: Ecology (early view)


Changes in population density alter the availability, acquisition and expenditure of resources by individuals, and consequently their contribution to the flux of energy in a system.

Whilst both negative and positive density-dependence have been well studied in natural populations, we are yet to estimate the underlying energy flows that generate these patterns and the ambivalent effects of density make prediction difficult.

Ultimately, density-dependence should emerge from the effects of conspecifics on rates of energy intake (feeding) and expenditure (metabolism) at the organismal level, thus determining the discretionary energy available for growth.

Using a model system of colonial marine invertebrates, we measured feeding and metabolic rates across a range of population densities to calculate how discretionary energy per colony changes with density and test whether this energy predicts observed patterns in organismal size across densities.

We found that both feeding and metabolic rates decline with density but that feeding declines faster, and that this discrepancy is the source of density-dependent reductions in individual growth. Importantly, we could predict the size of our focal organisms after 8 weeks in the field based on our estimates of energy intake and expenditure.

The effects of density on both energy intake and expenditure overwhelmed the effects of body size; even though higher density populations had smaller colonies (with higher mass-specific biological rates), density effects meant that these smaller colonies had lower mass-specific rates overall.

Thus, to predict the contribution of organisms to the flux of energy in populations it seems necessary not only to quantify how rates of energy intake and expenditure scale with body size, but also how they scale with density given that this ecological constraint can be a stronger driver of energy use than the physiological constraint of body size.


Ghedini G, White CR, Marshall DJ (2017) Does energy flux predict density-dependence? An empirical field test. Ecology, PDF 580 KB doi:10.1002/ecy.2032

Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects

Authors: Rolanda Lange and Dustin Marshall

Published in: Scientific Reports


Stressors associated with global change will be experienced simultaneously and may act synergistically, so attempts to estimate the capacity of marine systems to cope with global change requires a multi-stressor approach.

Because recent evidence suggests that stressor effects can be context-dependent, estimates of how stressors are experienced in ecologically realistic settings will be particularly valuable.

To enhance our understanding of the interplay between environmental effects and the impact of multiple stressors from both natural and anthropogenic sources, we conducted a field experiment. We explored the impact of multiple, functionally varied stressors from both natural and anthropogenic sources experienced during early life history in a common sessile marine invertebrate, Bugula neritina.

Natural spatial environmental variation induced differences in conspecific densities, allowing us to test for density-driven context-dependence of stressor effects. We indeed found density-dependent effects. Under high conspecific density, individual survival increased, which offset part of the negative effects of experiencing stressors.

Experiencing multiple stressors early in life history translated to a decreased survival in the field, albeit the effects were not as drastic as we expected: our results are congruent with antagonistic stressor effects. We speculate that when individual stressors are more subtle, stressor synergies become less common.


Lange R, Marshall D (2017) Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects. Scientific reports, PDF 1 MB doi:10.1038/s41598-017-06373-y

Should mothers provision their offspring equally? A manipulative field test

Authors: Hayley Cameron, Keyne Monro, and Dustin J Marshall

Published in: Ecology Letters, volume 20, issue 8 (August 2017)


Within-brood variation in offspring size is universal, but its causes are unclear. Theoretical explanations for within-brood variation commonly invoke bet-hedging, although alternatives consider the role of sibling competition. Despite abundant theory, empirical manipulations of within-brood variation in offspring size are rare.

Using a field experiment, we investigate the consequences of unequal maternal provisioning for both maternal and offspring fitness in a marine invertebrate. We create experimental broods of siblings with identical mean, but different variance, in offspring size, and different sibling densities.

Overall, more-variable broods had higher mean performance than less-variable broods, suggesting benefits of unequal provisioning that arise independently of bet-hedging. Complementarity effects drove these benefits, apparently because offspring-size variation promotes resource partitioning.

We suggest that when siblings compete for the same resources, and offspring size affects niche usage, the production of more-variable broods can provide greater fitness returns given the same maternal investment; a process unanticipated by the current theory.


Cameron H, Monro K, Marshall DJ (2017) Should mothers provision their offspring equally? A manipulative field test. Ecology Letters, PDF 799 KB  doi:10.1111/ele.12800

Do invasive species live faster? Mass-specific metabolic rate depends on growth form and invasion status

Authors: Marcelo E Lagos, Craig R White, and Dustin J Marshall

Published in: Functional Ecology


Invasive organisms often share characteristics that make them successful. Traits such as rapid growth and short generation times are classic “weed” phenotypes, such that invasive species often have r-selected rather than k-selected life histories. Given that invasive species often display “fast” life histories, invasive species may have relatively higher metabolic rates but systematic tests across taxa are lacking.

We compared metabolic rate across 14 sessile invasive and native marine invertebrates. We also investigated the influence of growth form (erect vs. flat species) on the metabolic rate of these species, since growth form can also affect metabolic rate.

For species with an erect growth form, we found an effect of invasive status on mass-specific metabolic rate. Invasive species had much higher mass-specific metabolic rates than native species and this was particularly pronounced for organisms with smaller body masses.

Given that smaller-bodied invasive organisms are typically early-successional, “fugitive” species, a higher metabolic rate may allow a faster pace of life, enhancing their capacity to invade and reproduce in newly created disturbed habitats.


Lagos ME, White CR, Marshall DJ (2017) Do invasive species live faster? Mass-specific metabolic rate depends on growth form and invasion status. Functional Ecology, PDF 644 KB DOI:10.1111/1365-2435.12913

Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions

Authors: Marcelo E Lagos, Diego R Barneche, Craig R White, and Dustin J Marshall

Published in: Global Change Biology (early view)


Biological invasions are one of the biggest threats to global biodiversity.

Marine artificial structures are proliferating worldwide and provide a haven for marine invasive species. Such structures disrupt local hydrodynamics, which can lead to the formation of oxygen-depleted microsites.

The extent to which native fauna can cope with such low oxygen conditions, and whether invasive species, long associated with artificial structures in flow-restricted habitats, have adapted to these conditions remains unclear.

We measured water flow and oxygen availability in marinas and piers at the scales relevant to sessile marine invertebrates (mm). We then measured the capacity of invasive and native marine invertebrates to maintain metabolic rates under decreasing levels of oxygen using standard laboratory assays.

We found that marinas reduce water flow relative to piers, and that local oxygen levels can be zero in low flow conditions. We also found that for species with erect growth forms, invasive species can tolerate much lower levels of oxygen relative to native species.

Integrating the field and laboratory data showed that up to 30% of available microhabitats within low flow environments are physiologically stressful for native species, while only 18% of the same habitat is physiologically stressful for invasive species.

These results suggest that invasive species have adapted to low oxygen habitats associated with manmade habitats, and artificial structures may be creating niche opportunities for invasive species.


Lagos ME, Barneche DR, White CR, Marshall DJ (2017) Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions. Global Change Biology PDF 1 MB doi:10.1111/gcb.13668

Field manipulations of resources mediate the transition from intraspecific competition to facilitation

Authors: Karin Svanfeldt, Keyne Monro, and Dustin J Marshall

Published in: Journal of Animal Ecology, volume 86, issue 3 (May 2017)


Population density affects individual performance, though its effects are often mixed. For sessile species, increases in population density typically reduce performance. Still, cases of positive density-dependence do occur in sessile systems and demand explanation. The stress gradient hypothesis (SGH) predicts that under stressful conditions, positive effects of facilitation may outweigh the negative effects of competition.

While some elements of the SGH are well studied, its potential to explain intraspecific facilitation has received little attention. Further, there have been questions regarding whether the SGH holds if the stressor is a resource. Most studies of interactions between the environment and intraspecific facilitation have relied on natural environmental gradients; manipulative studies are much rarer.

To test the effects of intraspecific density and resources, we manipulated resource availability over natural population densities for the marine bryozoan Watersipora subtorquata.

We found negative effects of density on colony performance in low resource environments, but mainly positive density-dependence in high resource environments. By adding resources, competition effects were reduced and the positive effects of facilitation were revealed.

Our results suggest that resource availability mediates the relative strength of competition and facilitation in our system. We also suggest that intraspecific facilitation is more common than may be appreciated and that environmental variation may mediate the balance between negative and positive density-dependence.


Svanfeldt K, Monro K, Marshall DJ (2017) Field manipulations of resources mediate the transition from intraspecific competition to facilitation. Journal of Animal Ecology, PDF 233 KB doi:10.1111/1365-2656.12644

Estimating monotonic rates from biological data using local linear regression

Authors: Colin Olito, Craig R White, Dustin J Marshall and Diego R Barneche

Published in: Journal of Experimental Biology, volume 220, number 5 (March 2017)


Accessing many fundamental questions in biology begins with empirical estimation of simple monotonic rates of underlying biological processes. Across a variety of disciplines, ranging from physiology to biogeochemistry, these rates are routinely estimated from non-linear and noisy time series data using linear regression and ad hoc manual truncation of non-linearities.

Here, we introduce the R package LoLinR, a flexible toolkit to implement local linear regression techniques to objectively and reproducibly estimate monotonic biological rates from non-linear time series data, and demonstrate possible applications using metabolic rate data.

LoLinR provides methods to easily and reliably estimate monotonic rates from time series data in a way that is statistically robust, facilitates reproducible research and is applicable to a wide variety of research disciplines in the biological sciences.


Olito C, White CR, Marshall DJ, Barneche DR (2017) Estimating monotonic rates from biological data using local linear regression, Journal of Experimental Biology, 220: 759‒764 PDF 617 KB doi: 10.1242/jeb.148775

Geographical gradients in selection can reveal genetic constraints for evolutionary responses to ocean acidification

Authors: Juan Diego Gaitán-Espitia, Dustin Marshall, Sam Dupont, Leonardo D Bacigalupe, Levente Bodrossy, and Alistair J Hobday

Published in: Biology Letters, volume 13, issue 2 (February 2017)


Geographical gradients in selection can shape different genetic architectures in natural populations, reflecting potential genetic constraints for adaptive evolution under climate change.

Investigation of natural pH/pCO₂ variation in upwelling regions reveals different spatio-temporal patterns of natural selection, generating genetic and phenotypic clines in populations, and potentially leading to local adaptation, relevant to understanding effects of ocean acidification (OA).

Strong directional selection, associated with intense and continuous upwellings, may have depleted genetic variation in populations within these upwelling regions, favouring increased tolerances to low pH but with an associated cost in other traits. In contrast, diversifying or weak directional selection in populations with seasonal upwellings or outside major upwelling regions may have resulted in higher genetic variances and the lack of genetic correlations among traits.

Testing this hypothesis in geographical regions with similar environmental conditions to those predicted under climate change will build insights into how selection may act in the future and how populations may respond to stressors such as OA.


Gaitán-Espitia JD, Marshall D, Dupont S, Bacigalupe LD, Bodrossy L, Hobday AJ (2017) Geographical gradients in selection can reveal genetic constraints for evolutionary responses to ocean acidification. Biology Letters, 13(2) PDF 333 KB
doi: 10.1098/rsbl.2016.0784

Limited evolutionary responses to harvesting regime in the intensive production of algae

Authors: Rebecca J Lawton, Nicholas A Paul, Dustin J Marshall and Keyne Monro

Published in: Journal of Applied Phycology, January 2017


Plastic changes in the growth and productivity of algae in response to environment and stocking density are well established. In contrast, the capacity for such changes to persist once environmental differences cease, potentially signalling an evolutionary response, have rarely been tested for algae in intensive production systems.

We tested whether continuous differences in harvesting regime (a high stocking density/low-yield regime versus low stocking density/high-yield regime) generated changes in biomass productivity and other growth metrics within several strains of the clonal macroalga Oedogonium (Chlorophyta, Oedogoniales) and whether such changes persisted once differential harvesting yields ceased.

We found considerable plasticity in growth rate and biomass productivity over a 12-week period of active selection (i.e. repeated high-yield and low-yield harvesting of clonal lineages within strains) and that strains responded differently to this selection pressure over time.

While small, but significant, differences in growth rates of clonal lineages exposed to high-yield vs low-yield harvesting regimes were maintained after prolonged culture under a common selection regime (i.e. medium-yield harvesting), differences in biomass productivity were not. There was no evidence for positive or negative effects of maintaining multiple strains in polyculture on growth and biomass productivity.

Overall, we detected limited potential for evolutionary responses to harvesting regime in the main commercial trait of interest — biomass productivity. This outcome is important for commercial cultivation in intensive production systems, since it identifies a low risk that harvesting practices will impact negatively on biomass productivity in the longer term.


Lawton RJ, Paul NA, Marshall DJ, Monro K (2017) Limited evolutionary responses to harvesting regime in the intensive production of algae. Journal of Applied Phycology PDF 1 MB doi:10.1007/s10811-016-1044-8

Temperature effects on mass-scaling exponents in colonial animals: a manipulative test

Authors: Diego R Barneche, Craig R White and Dustin J Marshall

Published in: Ecology, volume 98, issue 1 (January 2017)


Body size and temperature are fundamental drivers of ecological processes because they determine metabolic rates at the individual level. Whether these drivers act independently on individual-level metabolic rates remains uncertain.

Most studies of intraspecic scaling of unitary organisms must rely on pre-existing differences in size to examine its relationship with metabolic rate, thereby potentially confounding size-correlated traits (e.g., age, nutrition) with size, which can affect metabolic rate.

Here, we use a size manipulation approach to test whether metabolic mass scaling and temperature dependence interact in four species (two phyla) of colonial marine invertebrates. Size manipulation in colonial organisms allows tests of how ecological processes (e.g., predation) affect individual physiology and consequently population- and community-level energy flux.

Body mass and temperature interacted in two species, with one species exhibiting decreased and the other increased mass-scaling exponents with increasing temperature.

The allometric scaling of metabolic rate that we observe in three species contrasts with the isometric scaling of ingestion rates observed in some colonial marine invertebrates.

Thus, we suggest that the often observed competitive superiority of colonial over unitary organisms may arise because the difference between energy intake and expenditure increases more strongly with size in colonial organisms.


Barneche DR, White CR, Marshall DJ (2016) Temperature effects on mass-scaling exponents in colonial animals: a manipulative test, Ecology, 98(1), 2017, pp. 103–111 PDF 534 KB doi:10.1002/ecy.1624