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)

Abstract

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.

Citation

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)

Summary

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.

Citation

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)

Abstract

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.

Citation

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)

Abstract

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.

Citation

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

Abstract

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.

Citation

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)

Abstract

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.

Citation

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

The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change?

Authors: Evatt Chirgwin, Dustin J  Marshall, Carla M Sgrò, and Keyne Monro

Published in: Evolutionary Applications, volume 10, issue 3 (March 2017)

Abstract

Mounting research considers whether populations may adapt to global change based on additive genetic variance in fitness. Yet selection acts on phenotypes, not additive genetic variance alone, meaning that persistence and evolutionary potential in the near term, at least, may be influenced by other sources of fitness variation, including nonadditive genetic and maternal environmental effects. The fitness consequences of these effects, and their environmental sensitivity, are largely unknown.

Here, applying a quantitative genetic breeding design to an ecologically important marine tubeworm, we examined nonadditive genetic and maternal environmental effects on fitness (larval survival) across three thermal environments.

We found that these effects are nontrivial and environment dependent, explaining at least 44% of all parentally derived effects on survival at any temperature and 96% of parental effects at the most stressful temperature. Unlike maternal environmental effects, which manifested at the latter temperature only, nonadditive genetic effects were consistently significant and covaried positively across temperatures (i.e., parental combinations that enhanced survival at one temperature also enhanced survival at elevated temperatures).

Thus, while nonadditive genetic and maternal environmental effects have long been neglected because their evolutionary consequences are complex, unpredictable, or seen as transient, we argue that they warrant further attention in a rapidly warming world.

Citation

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2016) The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change? Evolutionary Applications, 10(3) PDF 445 KB doi: 10.1111/eva.12447

The evolution of reproductive phenology in broadcast spawners and the maintenance of sexually antagonistic polymorphism

Authors: , and Tim Connallon

Published in: The American Naturalist, volume 189, number 2 (February 2017)

Abstract

Reproductive phenology is a crucial life-history trait that evolves in response to external environmental conditions and frequency- and density-dependent interactions within species.

Broadcast spawners — which represent a large fraction of aquatic biodiversity — evolve phenologies that balance strong density-dependent fertilization success against abiotic environmental conditions that are required for successful reproduction. The overall balance between these processes may be particularly complex in dioecious species, where selection on reproductive timing potentially differs between the sexes.

Here, we develop a population genetic model of reproductive phenology in a dioecious broadcast spawning species and show that environmental variability and density-dependent fertilization dynamics naturally give rise to profound sex differences in selection on gamete release strategies.

The frequency-dependent nature of sperm competition generates sexually antagonistic selection on reproductive timing and facilitates the maintenance of genetic variation in phenological traits. Selection in females favors monomorphic spawning phenologies that maximize net fertilization success and offspring survival across environmental conditions, whereas selection in males often favors polymorphic phenologies that are primarily shaped by sperm competition.

Our model helps explain several well-documented empirical observations in aquatic species, including high intraspecific variance of reproductive phenologies, sex-specific spawning phenologies, and spawning during environmentally suboptimal times.

Citation

Olito C, Marshall DJ, Connallon T (2017) The evolution of reproductive phenology in broadcast spawners and the maintenance of sexually antagonistic polymorphism, The American Naturalist, 189(2) PDF 717 KB, doi:10.1086/690010

Why do larger mothers produce larger offspring? A test of classic theory

Authors: Hayley Cameron, Keyne Monro, Martino Malerba, Stephan Munch and Dustin Marshall

Published in: Ecology, volume 97, issue 12 (December 2016)

Abstract

Across a wide range of taxa, larger mothers produce larger offspring.

Theory assumes that larger, more fecund mothers create higher local densities of siblings, and so larger mothers produce larger offspring to offset sibling competition. This assumption has been debated for over 30 years, but direct empirical tests are surprisingly rare.

Here, we test two key assumptions of classic theories that predict sibling competition drives maternal-size–offspring-size (MSOS) correlations:

  1. independent effects of offspring size and sibling density on offspring performance or
  2. as a product of an interaction between these two factors.

To simultaneously test these alternative assumptions, we manipulate offspring size and sibling density in the marine invertebrate, Bugula neritina, and monitor offspring performance in the field.

We found that, depending on the fitness metric being considered, offspring size and sibling density can either independently or interactively affect offspring performance. Yet sibling density did not affect offspring performance in the ways that classic theories assume.

Given our results, it is unlikely that sibling competition drives the positive MSOS correlation observed in this species. Empirical support for these classic theories remains lacking, suggesting alternative explanations are necessary.

Citation

Cameron H, Monro K, Malerba M, Munch S, Marshall DJ (2016) Why do larger mothers produce larger offspring? A test of classic theory. Ecology, 97: 3452–3459. PDF 415 KB doi:10.1002/ecy.1590

Spatial pattern of distribution of marine invertebrates within a subtidal community: do communities vary more among patches or plots?

Authors: Chun‐Yi Chang and Dustin J Marshall

Published in: Ecology and Evolution, volume 6, issue 22 (November 2016)

Abstract

Making links between ecological processes and the scales at which they operate is an enduring challenge of community ecology.

Our understanding of ecological communities cannot advance if we do not distinguish larger scale processes from smaller ones.

Variability at small spatial scales can be important because it carries information about biological interactions, which cannot be explained by environmental heterogeneity alone.

Marine fouling communities are shaped by both the supply of larvae and competition for resources among colonizers—these two processes operate on distinctly different scales.

Here, we demonstrate how fouling community structure varies with spatial scale in a temperate Australian environment, and we identify the spatial scale that captures the most variability. Community structure was quantified with both univariate (species richness and diversity) and multivariate (similarity in species composition) indices.

Variation in community structure was unevenly distributed between the spatial scales that we examined. While variation in community structure within patch was usually greater than among patch, variation among patch was always significant.

Opportunistic taxa that rely heavily on rapid colonization of free space spread more evenly among patches during early succession. In contrast, taxa that are strong adult competitors but slow colonizers spread more evenly among patches only during late succession.

Our findings show significant patchiness can develop in a habitat showing no systematic environmental spatial variation, and this patchiness can be mediated through different biological factors at different spatial scales.

Citation

Chang CY, Marshall DJ (2016) Spatial pattern of distribution of marine invertebrates within a subtidal community: do communities vary more among patches or plots? Ecology and Evolution 6(22)83308337 PDF 522 KB doi: 10.1002/ece3.2462