Adaptive Capacity of the Habitat Modifying Sea Urchin Centrostephanus rodgersii to Ocean Warming and Ocean Acidification: Performance of Early Embryos

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Abstract

Background

Predicting effects of rapid climate change on populations depends on measuring the effects of climate stressors on performance, and potential for adaptation. Adaptation to stressful climatic conditions requires heritable genetic variance for stress tolerance present in populations.

Methodology/Principal Findings

We quantified genetic variation in tolerance of early development of the ecologically important sea urchin Centrostephanus rodgersii to near-future (2100) ocean conditions projected for the southeast Australian global change hot spot. Multiple dam-sire crosses were used to quantify the interactive effects of warming (+2–4°C) and acidification (−0.3−0.5 pH units) across twenty-seven family lines. Acidification, but not temperature, decreased the percentage of cleavage stage embryos. In contrast, temperature, but not acidification decreased the percentage of gastrulation. Cleavage success in response to both stressors was strongly affected by sire identity. Sire and dam identity significantly affected gastrulation and both interacted with temperature to determine developmental success. Positive genetic correlations for gastrulation indicated that genotypes that did well at lower pH also did well in higher temperatures.

Conclusions/Significance

Significant genotype (sire) by environment interactions for both stressors at gastrulation indicated the presence of heritable variation in thermal tolerance and the ability of embryos to respond to changing environments. The significant influence of dam may be due to maternal provisioning (maternal genotype or environment) and/or offspring genotype. It appears that early development in this ecologically important sea urchin is not constrained in adapting to the multiple stressors of ocean warming and acidification. The presence of tolerant genotypes indicates the potential to adapt to concurrent warming and acidification, contributing to the resilience of C. rodgersii in a changing ocean.

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Most cited references 11

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Larval experience and latent effects--metamorphosis is not a new beginning.

Jan A. Pechenik (2006)

For many years ecologists have documented the remarkable within-species variation inherent in natural systems-for example, variability in juvenile growth rates, mortality rates, fecundities, time to reproductive maturity, the outcomes of competitive interactions, and tolerance to pollutants. Over the past 20 years, it has become increasingly apparent that at least some of this variation may reflect differences in embryonic or larval experiences. Such experiences may include delayed metamorphosis, short term starvation, short term salinity stress, or exposure to sublethal concentrations of pollutants or sublethal levels of ultra violet irradiation. Latent effects-effects that have their origins in early development but that are first exhibited in juveniles or adults-have now been documented among gastropods, bivalves, echinoderms, polychaetes, crustaceans, bryozoans, urochordates, and vertebrates. The extent to which latent effects alter ecological outcomes in natural populations in the field, and the mechanisms through which they are mediated are largely unexplored.

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Adaptive phenotypic plasticity and the successful colonization of a novel environment.

Christopher T D Price, Andrew Yeh (2004)

Behavior and other forms of phenotypic plasticity potentially enable individuals to deal with novel situations. This implies that establishment of a population in a new environment is aided by plastic responses, as first suggested by Baldwin (1896). In the early 1980s, a small population of dark-eyed juncos from a temperate, montane environment became established in a Mediterranean climate in coastal San Diego. The breeding season of coastal juncos is more than twice as long as that of the ancestral population, and they fledge approximately twice as many young. We investigated the adaptive significance of the longer breeding season and its consequences for population persistence. Within the coastal population, individuals with longer breeding seasons have higher offspring production and recruitment, with no measured detrimental effects such as higher mortality or lower reproductive success the following year. Population size has remained approximately constant during the 6 years of study (1998-2003). The increase in reproductive effort in the coastal population contributes substantially to the persistence of this population because there is no evidence of density-dependent recruitment, which would otherwise negate the effects of increased fledgling production. These results provide the first quantitative support of Baldwin's proposition that plasticity can be crucial for population persistence during the early stages of colonization.

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Impact of Ocean Warming and Ocean Acidification on Larval Development and Calcification in the Sea Urchin Tripneustes gratilla

Hannah Sheppard Brennand, Natalie Soars, Symon A. Dworjanyn … (2010)

Background As the oceans simultaneously warm, acidify and increase in P CO2, prospects for marine biota are of concern. Calcifying species may find it difficult to produce their skeleton because ocean acidification decreases calcium carbonate saturation and accompanying hypercapnia suppresses metabolism. However, this may be buffered by enhanced growth and metabolism due to warming. Methodology/Principal Findings We examined the interactive effects of near-future ocean warming and increased acidification/P CO2 on larval development in the tropical sea urchin Tripneustes gratilla. Larvae were reared in multifactorial experiments in flow-through conditions in all combinations of three temperature and three pH/P CO2 treatments. Experiments were placed in the setting of projected near future conditions for SE Australia, a global change hot spot. Increased acidity/P CO2 and decreased carbonate mineral saturation significantly reduced larval growth resulting in decreased skeletal length. Increased temperature (+3°C) stimulated growth, producing significantly bigger larvae across all pH/P CO2 treatments up to a thermal threshold (+6°C). Increased acidity (-0.3-0.5 pH units) and hypercapnia significantly reduced larval calcification. A +3°C warming diminished the negative effects of acidification and hypercapnia on larval growth. Conclusions and Significance This study of the effects of ocean warming and CO2 driven acidification on development and calcification of marine invertebrate larvae reared in experimental conditions from the outset of development (fertilization) shows the positive and negative effects of these stressors. In simultaneous exposure to stressors the dwarfing effects of acidification were dominant. Reduction in size of sea urchin larvae in a high P CO2 ocean would likely impair their performance with negative consequent effects for benthic adult populations.

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Author and article information

Contributors

: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2012

Publication date (Electronic): 3 August 2012

Volume: 7

Issue: 8

Electronic Location Identifier: e42497

Affiliations

[1 ]School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia

[2 ]National Marine Science Centre, Southern Cross University, Coffs Harbour, New South Wales, Australia

[3 ]Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia

[4 ]Schools of Medical and Biological Sciences, The University of Sydney, Sydney, New South Wales, Australia

National Institute of Water & Atmospheric Research, New Zealand

Author notes

* E-mail: shawna@ 123456anatomy.usyd.edu.au

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: SAF SAD AGBP MB. Performed the experiments: SAF SAD. Analyzed the data: AGBP. Contributed reagents/materials/analysis tools: SAD AGBP MB. Wrote the paper: SAF.

Article

Publisher ID: PONE-D-12-11849

DOI: 10.1371/journal.pone.0042497

PMC ID: 3411790

PubMed ID: 22880005

SO-VID: 9f40f54f-4c24-4462-ad2b-7ab25412daf1

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 25 April 2012

Date accepted : 9 July 2012

Page count

Pages: 9

Funding

This research was supported by grants from the Australian Research Council ( http://www.arc.gov.au/), New South Wales Environment Research trust ( http://www.environment.nsw.gov.au/grants/research.htm) and the National Climate Change Adaptation Research Facility ( http://www.nccarf.edu.au/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Adaptive Capacity of the Habitat Modifying Sea Urchin Centrostephanus rodgersii to Ocean Warming and Ocean Acidification: Performance of Early Embryos

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Abstract

Background

Methodology/Principal Findings

Conclusions/Significance

Related collections

Climate Change: Open Access

Most cited references 11

Larval experience and latent effects--metamorphosis is not a new beginning.

Adaptive phenotypic plasticity and the successful colonization of a novel environment.

Impact of Ocean Warming and Ocean Acidification on Larval Development and Calcification in the Sea Urchin Tripneustes gratilla

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