Publications by authors named "Philip W Boyd"

50 Publications

Rate and fate of dissolved organic carbon release by seaweeds: a missing link in the coastal ocean carbon cycle.

J Phycol 2021 Jul 21. Epub 2021 Jul 21.

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart Tasmania, 7001, Australia.

Dissolved organic carbon (DOC) release by seaweeds (marine macroalgae) is a critical component of the coastal oceans biogeochemical carbon cycle but is an aspect of seaweed carbon physiology that we know relatively little about. Seaweed-derived DOC is found throughout coastal ecosystems and supports multiple food web linkages. Here we discuss the mechanisms of DOC release by seaweeds and group them into passive (leakage, requires no energy) and active release (exudation, requires energy) with particular focus on the photosynthetic 'overflow' hypothesis. The release of DOC from seaweeds was first studied in the 1960's but subsequent studies use a range of units hindering evaluation: we convert published values to a common unit (μmol C · g DW · h ) allowing comparisons between seaweed phyla, functional groups, biogeographic region, and an assessment of the environmental regulation of DOC production. The range of DOC release rates by seaweeds from each phylum under ambient environmental conditions was: 0 - 266.44 μmol C · g DW · h (Chlorophyta), 0 - 89.92 μmol C · g DW · h (Ochrophyta) and 0 - 41.28 μmol C · g DW · h (Rhodophyta). DOC release rates increased under environmental factors such as desiccation, high irradiance, non-optimal temperatures, altered salinity and elevated dissolved carbon dioxide (CO ) concentrations. Importantly DOC release was highest by seaweeds which were desiccated (<90 times greater DOC release compared to ambient). We discuss the impact of future ocean scenarios (ocean acidification, seawater warming, altered irradiance) on DOC release rates by seaweeds, the role of seaweed-derived DOC in carbon sequestration models, and how they inform future research directions.
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http://dx.doi.org/10.1111/jpy.13198DOI Listing
July 2021

Nanomolar phosphate supply and its recycling drive net community production in the subtropical North Pacific.

Nat Commun 2021 06 8;12(1):3462. Epub 2021 Jun 8.

Meteorological Research Institute, Japan Meteorological Agency, Ibaraki, Japan.

Seasonal drawdown of dissolved inorganic carbon (DIC) in the subtropical upper ocean makes a significant contribution to net community production (NCP) globally. Although NCP requires macronutrient supply, surface macronutrients are chronically depleted, and their supply has been unable to balance the NCP demand. Here, we report nanomolar increases in surface nitrate plus nitrite (N+N, ~20 nM) and phosphate (PO, ~15 nM) from summer to winter in the western subtropical North Pacific. Molar ratios of upward fluxes of DIC:N+N:PO to the euphotic zone (< 100 m) were in near-stoichiometric balance with microbial C:N:P ratios (107~243:16~35:1). Comparison of these upward influxes with other atmospheric and marine sources demonstrated that total supply is largely driven by the other sources for C and N (93~96%), but not for P (10%), suggesting that nanomolar upward supply of P and its preferential recycling play a vital role in sustaining the NCP.
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http://dx.doi.org/10.1038/s41467-021-23837-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8187552PMC
June 2021

Testing the climate intervention potential of ocean afforestation using the Great Atlantic Sargassum Belt.

Nat Commun 2021 05 7;12(1):2556. Epub 2021 May 7.

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia.

Ensuring that global warming remains <2 °C requires rapid CO emissions reduction. Additionally, 100-900 gigatons CO must be removed from the atmosphere by 2100 using a portfolio of CO removal (CDR) methods. Ocean afforestation, CDR through basin-scale seaweed farming in the open ocean, is seen as a key component of the marine portfolio. Here, we analyse the CDR potential of recent re-occurring trans-basin belts of the floating seaweed Sargassum in the (sub)tropical North Atlantic as a natural analogue for ocean afforestation. We show that two biogeochemical feedbacks, nutrient reallocation and calcification by encrusting marine life, reduce the CDR efficacy of Sargassum by 20-100%. Atmospheric CO influx into the surface seawater, after CO-fixation by Sargassum, takes 2.5-18 times longer than the CO-deficient seawater remains in contact with the atmosphere, potentially hindering CDR verification. Furthermore, we estimate that increased ocean albedo, due to floating Sargassum, could influence climate radiative forcing more than Sargassum-CDR. Our analysis shows that multifaceted Earth-system feedbacks determine the efficacy of ocean afforestation.
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http://dx.doi.org/10.1038/s41467-021-22837-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105394PMC
May 2021

Implications for the mesopelagic microbial gardening hypothesis as determined by experimental fragmentation of Antarctic krill fecal pellets.

Ecol Evol 2021 Jan 28;11(2):1023-1036. Epub 2020 Dec 28.

Institute for Marine and Antarctic Studies University of Tasmania Battery Point TAS Australia.

Detritivores need to upgrade their food to increase its nutritional value. One method is to fragment detritus promoting the colonization of nutrient-rich microbes, which consumers then ingest along with the detritus; so-called microbial gardening. Observations and numerical models of the detritus-dominated ocean mesopelagic zone have suggested microbial gardening by zooplankton is a fundamental process in the ocean carbon cycle leading to increased respiration of carbon-rich detritus. However, no experimental evidence exists to demonstrate that microbial respiration rates are higher on recently fragmented sinking detrital particles.Using aquaria-reared Antarctic krill fecal pellets, we showed fragmentation increased microbial particulate organic carbon (POC) turnover by 1.9×, but only on brown fecal pellets, formed from the consumption of other pellets. Microbial POC turnover on un- and fragmented green fecal pellets, formed from consuming fresh phytoplankton, was equal. Thus, POC content, fragmentation, and potentially nutritional value together drive POC turnover rates.Mesopelagic microbial gardening could be a risky strategy, as the dominant detrital food source is settling particles; even though fragmentation decreases particle size and sinking rate, it is unlikely that an organism would remain with the particle long enough to nutritionally benefit from attached microbes. We propose "communal gardening" occurs whereby additional mesopelagic organisms nearby or below the site of fragmentation consume the particle and the colonized microbes.To determine how fragmentation impacts the remineralization of sinking carbon-rich detritus and to parameterize microbial gardening in mesopelagic carbon models, three key metrics from further controlled experiments and observations are needed; how particle composition (here, pellet color/krill diet) impacts the response of microbes to the fragmentation of particles; the nutritional benefit to zooplankton from ingesting microbes after fragmentation along with identification of which essential nutrients are being targeted; how both these factors vary between physical (shear) and biological particle fragmentation.
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http://dx.doi.org/10.1002/ece3.7119DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7820144PMC
January 2021

Resource Colimitation Drives Competition Between Phytoplankton and Bacteria in the Southern Ocean.

Geophys Res Lett 2021 Jan 12;48(1):e2020GL088369. Epub 2021 Jan 12.

Department of Earth Ocean and Ecological Sciences School of Environmental Sciences University of Liverpool Liverpool UK.

Across the Southern Ocean, phytoplankton growth is governed by iron and light, while bacterial growth is regulated by iron and labile dissolved organic carbon (LDOC). We use a mechanistic model to examine how competition for iron between phytoplankton and bacteria responds to changes in iron, light, and LDOC. Consistent with experimental evidence, increasing iron and light encourages phytoplankton dominance, while increasing LDOC and decreasing light favors bacterial dominance. Under elevated LDOC, bacteria can outcompete phytoplankton for iron, most easily under lower iron. Simulations reveal that bacteria are major iron consumers and suggest that luxury storage plays a key role in competitive iron uptake. Under seasonal conditions typical of the Southern Ocean, sources of LDOC besides phytoplankton exudation modulate the strength of competitive interactions. Continued investigations on the competitive fitness of bacteria in driving changes in primary production in iron-limited systems will be invaluable in refining these results.
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http://dx.doi.org/10.1029/2020GL088369DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7816276PMC
January 2021

Exploring biogeochemical and ecological redundancy in phytoplankton communities in the global ocean.

Glob Chang Biol 2021 Mar 5;27(6):1196-1213. Epub 2021 Jan 5.

GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.

Climate-change-induced alterations of oceanic conditions will lead to the ecological niches of some marine phytoplankton species disappearing, at least regionally. How will such losses affect the ecosystem and the coupled biogeochemical cycles? Here, we couch this question in terms of ecological redundancy (will other species be able to fill the ecological roles of the extinct species) and biogeochemical redundancy (can other species replace their biogeochemical roles). Prior laboratory and field studies point to a spectrum in the degree of redundancy. We use a global three-dimensional computer model with diverse planktonic communities to explore these questions further. The model includes 35 phytoplankton types that differ in size, biogeochemical function and trophic strategy. We run two series of experiments in which single phytoplankton types are either partially or fully eliminated. The niches of the targeted types were not completely reoccupied, often with a reduction in the transfer of matter from autotrophs to heterotrophs. Primary production was often decreased, but sometimes increased due to reduction in grazing pressure. Complex trophic interactions (such as a decrease in the stocks of a predator's grazer) led to unexpected reshuffling of the community structure. Alterations in resource utilization may cause impacts beyond the regions where the type went extinct. Our results suggest a lack of redundancy, especially in the 'knock on' effects on higher trophic levels. Redundancy appeared lowest for types on the edges of trait space (e.g. smallest) or with unique competitive strategies. Though highly idealized, our modelling findings suggest that the results from laboratory or field studies often do not adequately capture the ramifications of functional redundancy. The modelled, often counterintuitive, responses-via complex food web interactions and bottom-up versus top-down controls-indicate that changes in planktonic community will be key determinants of future ocean global change ecology and biogeochemistry.
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http://dx.doi.org/10.1111/gcb.15493DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7986797PMC
March 2021

Effects of multiple drivers of ocean global change on the physiology and functional gene expression of the coccolithophore Emiliania huxleyi.

Glob Chang Biol 2020 Oct 30;26(10):5630-5645. Epub 2020 Jul 30.

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tas., Australia.

Ongoing ocean global change due to anthropogenic activities is causing multiple chemical and physical seawater properties to change simultaneously, which may affect the physiology of marine phytoplankton. The coccolithophore Emiliania huxleyi is a model species often employed in the study of the marine carbon cycle. The effect of ocean acidification (OA) on coccolithophore calcification has been extensively studied; however, physiological responses to multiple environmental drivers are still largely unknown. Here we examined two-way and multiple driver effects of OA and other key environmental drivers-nitrate, phosphate, irradiance, and temperature-on the growth, photosynthetic, and calcification rates, and the elemental composition of E. huxleyi. In addition, changes in functional gene expression were examined to understand the molecular mechanisms underpinning the physiological responses. The single driver manipulation experiments suggest decreased nitrate supply being the most important driver regulating E. huxleyi physiology, by significantly reducing the growth, photosynthetic, and calcification rates. In addition, the interaction of OA and decreased nitrate supply (projected for year 2100) had more negative synergistic effects on E. huxleyi physiology than all other two-way factorial manipulations, suggesting a linkage between the single dominant driver (nitrate) effects and interactive effects with other drivers. Simultaneous manipulation of all five environmental drivers to the conditions of the projected year 2100 had the largest negative effects on most of the physiological metrics. Furthermore, functional genes associated with inorganic carbon acquisition (RubisCO, AEL1, and δCA) and calcification (CAX3, AEL1, PATP, and NhaA2) were most downregulated by the multiple driver manipulation, revealing linkages between responses of functional gene expression and associated physiological metrics. These findings together indicate that for more holistic projections of coccolithophore responses to future ocean global change, it is necessary to understand the relative importance of environmental drivers both individually (i.e., mechanistic understanding) and interactively (i.e., cumulative effect) on coccolithophore physiology.
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http://dx.doi.org/10.1111/gcb.15259DOI Listing
October 2020

Remote assessment of the fate of phytoplankton in the Southern Ocean sea-ice zone.

Nat Commun 2020 06 19;11(1):3108. Epub 2020 Jun 19.

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, 7001, Australia.

In the Southern Ocean, large-scale phytoplankton blooms occur in open water and the sea-ice zone (SIZ). These blooms have a range of fates including physical advection, downward carbon export, or grazing. Here, we determine the magnitude, timing and spatial trends of the biogeochemical (export) and ecological (foodwebs) fates of phytoplankton, based on seven BGC-Argo floats spanning three years across the SIZ. We calculate loss terms using the production of chlorophyll-based on nitrate depletion-compared with measured chlorophyll. Export losses are estimated using conspicuous chlorophyll pulses at depth. By subtracting export losses, we calculate grazing-mediated losses. Herbivory accounts for ~90% of the annually-averaged losses (169 mg C m d), and phytodetritus POC export comprises ~10%. Furthermore, export and grazing losses each exhibit distinctive seasonality captured by all floats spanning 60°S to 69°S. These similar trends reveal widespread patterns in phytoplankton fate throughout the Southern Ocean SIZ.
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http://dx.doi.org/10.1038/s41467-020-16931-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7305117PMC
June 2020

Metrics that matter for assessing the ocean biological carbon pump.

Proc Natl Acad Sci U S A 2020 05 6;117(18):9679-9687. Epub 2020 Apr 6.

Earth Research Institute and Department of Geography, University of California, Santa Barbara, CA 93106.

The biological carbon pump (BCP) comprises wide-ranging processes that set carbon supply, consumption, and storage in the oceans' interior. It is becoming increasingly evident that small changes in the efficiency of the BCP can significantly alter ocean carbon sequestration and, thus, atmospheric CO and climate, as well as the functioning of midwater ecosystems. Earth system models, including those used by the United Nation's Intergovernmental Panel on Climate Change, most often assess POC (particulate organic carbon) flux into the ocean interior at a fixed reference depth. The extrapolation of these fluxes to other depths, which defines the BCP efficiencies, is often executed using an idealized and empirically based flux-vs.-depth relationship, often referred to as the "Martin curve." We use a new compilation of POC fluxes in the upper ocean to reveal very different patterns in BCP efficiencies depending upon whether the fluxes are assessed at a fixed reference depth or relative to the depth of the sunlit euphotic zone (Ez). We find that the fixed-depth approach underestimates BCP efficiencies when the Ez is shallow, and vice versa. This adjustment alters regional assessments of BCP efficiencies as well as global carbon budgets and the interpretation of prior BCP studies. With several international studies recently underway to study the ocean BCP, there are new and unique opportunities to improve our understanding of the mechanistic controls on BCP efficiencies. However, we will only be able to compare results between studies if we use a common set of Ez-based metrics.
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http://dx.doi.org/10.1073/pnas.1918114117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7211944PMC
May 2020

Distinct iron cycling in a Southern Ocean eddy.

Nat Commun 2020 02 11;11(1):825. Epub 2020 Feb 11.

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Australia.

Mesoscale eddies are ubiquitous in the iron-limited Southern Ocean, controlling ocean-atmosphere exchange processes, however their influence on phytoplankton productivity remains unknown. Here we probed the biogeochemical cycling of iron (Fe) in a cold-core eddy. In-eddy surface dissolved Fe (dFe) concentrations and phytoplankton productivity were exceedingly low relative to external waters. In-eddy phytoplankton Fe-to-carbon uptake ratios were elevated 2-6 fold, indicating upregulated intracellular Fe acquisition resulting in a dFe residence time of ~1 day. Heavy dFe isotope values were measured for in-eddy surface waters highlighting extensive trafficking of dFe by cells. Below the euphotic zone, dFe isotope values were lighter and coincident with peaks in recycled nutrients and cell abundance, indicating enhanced microbially-mediated Fe recycling. Our measurements show that the isolated nature of Southern Ocean eddies can produce distinctly different Fe biogeochemistry compared to surrounding waters with cells upregulating iron uptake and using recycling processes to sustain themselves.
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http://dx.doi.org/10.1038/s41467-020-14464-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7012851PMC
February 2020

How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes?

Glob Chang Biol 2020 02 24;26(2):343-354. Epub 2019 Dec 24.

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tas., Australia.

Extreme heat wave events are now causing ecosystem degradation across marine ecosystems. The consequences of this heat-induced damage range from the rapid loss of habitat-forming organisms, through to a reduction in the services that ecosystems support, and ultimately to impacts on human health and society. How we tackle the sudden emergence of ecosystem-wide degradation has not yet been addressed in the context of marine heat waves. An examination of recent marine heat waves from around Australia points to the potential important role that respite or refuge from environmental extremes can play in enabling organismal survival. However, most ecological interventions are being devised with a target of mid to late-century implementation, at which time many of the ecosystems, that the interventions are targeted towards, will have already undergone repeated and widespread heat wave induced degradation. Here, our assessment of the merits of proposed ecological interventions, across a spectrum of approaches, to counter marine environmental extremes, reveals a lack preparedness to counter the effects of extreme conditions on marine ecosystems. The ecological influence of these extremes are projected to continue to impact marine ecosystems in the coming years, long before these interventions can be developed. Our assessment reveals that approaches which are technologically ready and likely to be socially acceptable are locally deployable only, whereas those which are scalable-for example to features as large as major reef systems-are not close to being testable, and are unlikely to obtain social licence for deployment. Knowledge of the environmental timescales for survival of extremes, via respite or refuge, inferred from field observations will help test such intervention tools. The growing frequency of extreme events such as marine heat waves increases the urgency to consider mitigation and intervention tools that support organismal and ecosystem survival in the immediate future, while global climate mitigation and/or intervention are formulated.
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http://dx.doi.org/10.1111/gcb.14901DOI Listing
February 2020

Assessment of leaching protocols to determine the solubility of trace metals in aerosols.

Talanta 2020 Feb 19;208:120377. Epub 2019 Sep 19.

Institute for Marine and Antarctic Studies, University of Tasmania, Battery Point, Tasmania, Australia; Antarctic Climate and Ecosystems CRC, University of Tasmania, Battery Point, Tasmania, Australia.

Atmospheric deposition of aerosols to the ocean provides an important pathway for the supply of vital micronutrients, including trace metals. These trace metals are essential for phytoplankton growth, and therefore their delivery to marine ecosystems can strongly influence the ocean carbon cycle. The solubility of trace metals in aerosols is a key parameter to better constrain their potential impact on phytoplankton growth. To date, a wide range of experimental approaches and nomenclature have been used to define aerosol trace metal solubility, making data comparison between studies difficult. Here we investigate and discuss several laboratory leaching protocols to determine the solubility of key trace metals in aerosol samples, namely iron, cobalt, manganese, copper, lead, vanadium, titanium and aluminium. Commonly used techniques and tools are also considered such as enrichment factor calculations and air mass back-trajectory projections and recommendations are given for aerosol field sampling, laboratory processing (including leaching and digestion) and analytical measurements. Finally, a simple 3-step leaching protocol combining commonly used protocols is proposed to operationally define trace metal solubility in aerosols. The need for standard guidelines and protocols to study the biogeochemical impact of atmospheric trace metal deposition to the ocean has been increasingly emphasised by both the atmospheric and oceanographic communities. This lack of standardisation currently limits our understanding and ability to predict ocean and climate interactions under changing environmental conditions.
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http://dx.doi.org/10.1016/j.talanta.2019.120377DOI Listing
February 2020

The interplay between regeneration and scavenging fluxes drives ocean iron cycling.

Nat Commun 2019 10 31;10(1):4960. Epub 2019 Oct 31.

Institute for Marine and Antarctic Studies and Antarctic Climate and Ecosystems CRC, University of Tasmania, Hobsart, TAS, Australia.

Despite recent advances in observational data coverage, quantitative constraints on how different physical and biogeochemical processes shape dissolved iron distributions remain elusive, lowering confidence in future projections for iron-limited regions. Here we show that dissolved iron is cycled rapidly in Pacific mode and intermediate water and accumulates at a rate controlled by the strongly opposing fluxes of regeneration and scavenging. Combining new data sets within a watermass framework shows that the multidecadal dissolved iron accumulation is much lower than expected from a meta-analysis of iron regeneration fluxes. This mismatch can only be reconciled by invoking significant rates of iron removal  to balance iron regeneration, which imply generation of authigenic particulate iron pools. Consequently, rapid internal cycling of iron, rather than its physical transport, is the main control on observed iron stocks within intermediate waters globally and upper ocean iron limitation will be strongly sensitive to subtle changes to the internal cycling balance.
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http://dx.doi.org/10.1038/s41467-019-12775-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6823497PMC
October 2019

Biogeochemical controls of surface ocean phosphate.

Sci Adv 2019 08 28;5(8):eaax0341. Epub 2019 Aug 28.

Department of Earth System Science, University of California, Irvine, Irvine, CA 92697, USA.

Surface ocean phosphate is commonly below the standard analytical detection limits, leading to an incomplete picture of the global variation and biogeochemical role of phosphate. A global compilation of phosphate measured using high-sensitivity methods revealed several previously unrecognized low-phosphate areas and clear regional differences. Both observational climatologies and Earth system models (ESMs) systematically overestimated surface phosphate. Furthermore, ESMs misrepresented the relationships between phosphate, phytoplankton biomass, and primary productivity. Atmospheric iron input and nitrogen fixation are known important controls on surface phosphate, but model simulations showed that differences in the iron-to-macronutrient ratio in the vertical nutrient supply and surface lateral transport are additional drivers of phosphate concentrations. Our study demonstrates the importance of accurately quantifying nutrients for understanding the regulation of ocean ecosystems and biogeochemistry now and under future climate conditions.
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http://dx.doi.org/10.1126/sciadv.aax0341DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6713502PMC
August 2019

Evolution, Microbes, and Changing Ocean Conditions.

Ann Rev Mar Sci 2020 01 26;12:181-208. Epub 2019 Aug 26.

Climate Change Cluster, University of Technology Sydney, Sydney, New South Wales 2007, Australia; email:

Experimental evolution and the associated theory are underutilized in marine microbial studies; the two fields have developed largely in isolation. Here, we review evolutionary tools for addressing four key areas of ocean global change biology: linking plastic and evolutionary trait changes, the contribution of environmental variability to determining trait values, the role of multiple environmental drivers in trait change, and the fate of populations near their tolerance limits. Wherever possible, we highlight which data from marine studies could use evolutionary approaches and where marine model systems can advance our understanding of evolution. Finally, we discuss the emerging field of marine microbial experimental evolution. We propose a framework linking changes in environmental quality (defined as the cumulative effect on population growth rate) with population traits affecting evolutionary potential, in order to understand which evolutionary processes are likely to be most important across a range of locations for different types of marine microbes.
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http://dx.doi.org/10.1146/annurev-marine-010318-095311DOI Listing
January 2020

Scientists' warning to humanity: microorganisms and climate change.

Nat Rev Microbiol 2019 09 18;17(9):569-586. Epub 2019 Jun 18.

School of BioSciences, The University of Melbourne, Parkville, VIC, Australia.

In the Anthropocene, in which we now live, climate change is impacting most life on Earth. Microorganisms support the existence of all higher trophic life forms. To understand how humans and other life forms on Earth (including those we are yet to discover) can withstand anthropogenic climate change, it is vital to incorporate knowledge of the microbial 'unseen majority'. We must learn not just how microorganisms affect climate change (including production and consumption of greenhouse gases) but also how they will be affected by climate change and other human activities. This Consensus Statement documents the central role and global importance of microorganisms in climate change biology. It also puts humanity on notice that the impact of climate change will depend heavily on responses of microorganisms, which are essential for achieving an environmentally sustainable future.
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http://dx.doi.org/10.1038/s41579-019-0222-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7136171PMC
September 2019

Multi-faceted particle pumps drive carbon sequestration in the ocean.

Nature 2019 04 17;568(7752):327-335. Epub 2019 Apr 17.

Department of Earth and Environmental Sciences, University of Rochester, Rochester, NY, USA.

The ocean's ability to sequester carbon away from the atmosphere exerts an important control on global climate. The biological pump drives carbon storage in the deep ocean and is thought to function via gravitational settling of organic particles from surface waters. However, the settling flux alone is often insufficient to balance mesopelagic carbon budgets or to meet the demands of subsurface biota. Here we review additional biological and physical mechanisms that inject suspended and sinking particles to depth. We propose that these 'particle injection pumps' probably sequester as much carbon as the gravitational pump, helping to close the carbon budget and motivating further investigation into their environmental control.
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http://dx.doi.org/10.1038/s41586-019-1098-2DOI Listing
April 2019

Photosynthetic adaptation to low iron, light, and temperature in Southern Ocean phytoplankton.

Proc Natl Acad Sci U S A 2019 03 20;116(10):4388-4393. Epub 2019 Feb 20.

Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599.

Phytoplankton productivity in the polar Southern Ocean (SO) plays an important role in the transfer of carbon from the atmosphere to the ocean's interior, a process called the biological carbon pump, which helps regulate global climate. SO productivity in turn is limited by low iron, light, and temperature, which restrict the efficiency of the carbon pump. Iron and light can colimit productivity due to the high iron content of the photosynthetic photosystems and the need for increased photosystems for low-light acclimation in many phytoplankton. Here we show that SO phytoplankton have evolved critical adaptations to enhance photosynthetic rates under the joint constraints of low iron, light, and temperature. Under growth-limiting iron and light levels, three SO species had up to sixfold higher photosynthetic rates per photosystem II and similar or higher rates per mol of photosynthetic iron than temperate species, despite their lower growth temperature (3 vs. 18 °C) and light intensity (30 vs. 40 μmol quanta⋅m⋅s), which should have decreased photosynthetic rates. These unexpectedly high rates in the SO species are partly explained by their unusually large photosynthetic antennae, which are among the largest ever recorded in marine phytoplankton. Large antennae are disadvantageous at low light intensities because they increase excitation energy loss as heat, but this loss may be mitigated by the low SO temperatures. Such adaptations point to higher SO production rates than environmental conditions should otherwise permit, with implications for regional ecology and biogeochemistry.
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http://dx.doi.org/10.1073/pnas.1810886116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410794PMC
March 2019

Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review.

Glob Chang Biol 2018 06 31;24(6):2239-2261. Epub 2018 Mar 31.

Helmholtz Centre for Polar and Marine Research, Alfred Wegener Institute, Bremerhaven, Germany.

Marine life is controlled by multiple physical and chemical drivers and by diverse ecological processes. Many of these oceanic properties are being altered by climate change and other anthropogenic pressures. Hence, identifying the influences of multifaceted ocean change, from local to global scales, is a complex task. To guide policy-making and make projections of the future of the marine biosphere, it is essential to understand biological responses at physiological, evolutionary and ecological levels. Here, we contrast and compare different approaches to multiple driver experiments that aim to elucidate biological responses to a complex matrix of ocean global change. We present the benefits and the challenges of each approach with a focus on marine research, and guidelines to navigate through these different categories to help identify strategies that might best address research questions in fundamental physiology, experimental evolutionary biology and community ecology. Our review reveals that the field of multiple driver research is being pulled in complementary directions: the need for reductionist approaches to obtain process-oriented, mechanistic understanding and a requirement to quantify responses to projected future scenarios of ocean change. We conclude the review with recommendations on how best to align different experimental approaches to contribute fundamental information needed for science-based policy formulation.
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http://dx.doi.org/10.1111/gcb.14102DOI Listing
June 2018

Coastal ocean and shelf-sea biogeochemical cycling of trace elements and isotopes: lessons learned from GEOTRACES.

Philos Trans A Math Phys Eng Sci 2016 Nov;374(2081)

Physics Department-ICTA, Universitat Autònoma de Barcelona, Barcelona 08193, Spain.

Continental shelves and shelf seas play a central role in the global carbon cycle. However, their importance with respect to trace element and isotope (TEI) inputs to ocean basins is less well understood. Here, we present major findings on shelf TEI biogeochemistry from the GEOTRACES programme as well as a proof of concept for a new method to estimate shelf TEI fluxes. The case studies focus on advances in our understanding of TEI cycling in the Arctic, transformations within a major river estuary (Amazon), shelf sediment micronutrient fluxes and basin-scale estimates of submarine groundwater discharge. The proposed shelf flux tracer is 228-radium ( = 5.75 yr), which is continuously supplied to the shelf from coastal aquifers, sediment porewater exchange and rivers. Model-derived shelf Ra fluxes are combined with TEI/ Ra ratios to quantify ocean TEI fluxes from the western North Atlantic margin. The results from this new approach agree well with previous estimates for shelf Co, Fe, Mn and Zn inputs and exceed published estimates of atmospheric deposition by factors of approximately 3-23. Lastly, recommendations are made for additional GEOTRACES process studies and coastal margin-focused section cruises that will help refine the model and provide better insight on the mechanisms driving shelf-derived TEI fluxes to the ocean.This article is part of the themed issue 'Biological and climatic impacts of ocean trace element chemistry'.
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http://dx.doi.org/10.1098/rsta.2016.0076DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5069537PMC
November 2016

Developing a test-bed for robust research governance of geoengineering: the contribution of ocean iron biogeochemistry.

Philos Trans A Math Phys Eng Sci 2016 Nov;374(2081)

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.

Geoengineering to mitigate climate change has long been proposed, but remains nebulous. Exploration of the feasibility of geoengineering first requires the development of research governance to move beyond the conceptual towards scientifically designed pilot studies. Fortuitously, 12 mesoscale (approx. 1000 km) iron enrichments, funded to investigate how ocean iron biogeochemistry altered Earth's carbon cycle in the geological past, provide proxies to better understand the benefits and drawbacks of geoengineering. The utility of these iron enrichments in the geoengineering debate is enhanced by the GEOTRACES global survey. Here, we outline how GEOTRACES surveys and process studies can provide invaluable insights into geoengineering. Surveys inform key unknowns including the regional influence and magnitude of modes of iron supply, and stimulate iron biogeochemical modelling. These advances will enable quantification of interannual variability of iron supply to assess whether any future purposeful multi-year iron-fertilization meets the principle of 'additionality' ( Kyoto protocol). Process studies address issues including upscaling of geoengineering, and how differing iron-enrichment strategies could stimulate wide-ranging biogeochemical outcomes. In summary, the availability of databases on both mesoscale iron-enrichment studies and the GEOTRACES survey, along with modelling, policy initiatives and legislation have positioned the iron-enrichment approach as a robust multifaceted test-bed to assess proposed research into climate intervention.This article is part of the themed issue 'Biological and climatic impacts of ocean trace element chemistry'.
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http://dx.doi.org/10.1098/rsta.2015.0299DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5069533PMC
November 2016

The integral role of iron in ocean biogeochemistry.

Nature 2017 03;543(7643):51-59

Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA.

The micronutrient iron is now recognized to be important in regulating the magnitude and dynamics of ocean primary productivity, making it an integral component of the ocean's biogeochemical cycles. In this Review, we discuss how a recent increase in observational data for this trace metal has challenged the prevailing view of the ocean iron cycle. Instead of focusing on dust as the major iron source and emphasizing iron's tight biogeochemical coupling to major nutrients, a more complex and diverse picture of the sources of iron, its cycling processes and intricate linkages with the ocean carbon and nitrogen cycles has emerged.
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http://dx.doi.org/10.1038/nature21058DOI Listing
March 2017

Forecast ocean variability.

Nature 2016 11;539(7628):162-163

Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Australia.

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http://dx.doi.org/10.1038/539162aDOI Listing
November 2016

Biological responses to environmental heterogeneity under future ocean conditions.

Glob Chang Biol 2016 08 25;22(8):2633-50. Epub 2016 Apr 25.

Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tas., 7001, Australia.

Organisms are projected to face unprecedented rates of change in future ocean conditions due to anthropogenic climate-change. At present, marine life encounters a wide range of environmental heterogeneity from natural fluctuations to mean climate change. Manipulation studies suggest that biota from more variable marine environments have more phenotypic plasticity to tolerate environmental heterogeneity. Here, we consider current strategies employed by a range of representative organisms across various habitats - from short-lived phytoplankton to long-lived corals - in response to environmental heterogeneity. We then discuss how, if and when organismal responses (acclimate/migrate/adapt) may be altered by shifts in the magnitude of the mean climate-change signal relative to that for natural fluctuations projected for coming decades. The findings from both novel climate-change modelling simulations and prior biological manipulation studies, in which natural fluctuations are superimposed on those of mean change, provide valuable insights into organismal responses to environmental heterogeneity. Manipulations reveal that different experimental outcomes are evident between climate-change treatments which include natural fluctuations vs. those which do not. Modelling simulations project that the magnitude of climate variability, along with mean climate change, will increase in coming decades, and hence environmental heterogeneity will increase, illustrating the need for more realistic biological manipulation experiments that include natural fluctuations. However, simulations also strongly suggest that the timescales over which the mean climate-change signature will become dominant, relative to natural fluctuations, will vary for individual properties, being most rapid for CO2 (~10 years from present day) to 4 decades for nutrients. We conclude that the strategies used by biota to respond to shifts in environmental heterogeneity may be complex, as they will have to physiologically straddle wide-ranging timescales in the alteration of ocean conditions, including the need to adapt to rapidly rising CO2 and also acclimate to environmental heterogeneity in more slowly changing properties such as warming.
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http://dx.doi.org/10.1111/gcb.13287DOI Listing
August 2016

Ocean acidification increases the accumulation of toxic phenolic compounds across trophic levels.

Nat Commun 2015 Oct 27;6:8714. Epub 2015 Oct 27.

State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, China.

Increasing atmospheric CO2 concentrations are causing ocean acidification (OA), altering carbonate chemistry with consequences for marine organisms. Here we show that OA increases by 46-212% the production of phenolic compounds in phytoplankton grown under the elevated CO2 concentrations projected for the end of this century, compared with the ambient CO2 level. At the same time, mitochondrial respiration rate is enhanced under elevated CO2 concentrations by 130-160% in a single species or mixed phytoplankton assemblage. When fed with phytoplankton cells grown under OA, zooplankton assemblages have significantly higher phenolic compound content, by about 28-48%. The functional consequences of the increased accumulation of toxic phenolic compounds in primary and secondary producers have the potential to have profound consequences for marine ecosystem and seafood quality, with the possibility that fishery industries could be influenced as a result of progressive ocean changes.
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http://dx.doi.org/10.1038/ncomms9714DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4640080PMC
October 2015

Long-Term Conditioning to Elevated pCO2 and Warming Influences the Fatty and Amino Acid Composition of the Diatom Cylindrotheca fusiformis.

PLoS One 2015 13;10(5):e0123945. Epub 2015 May 13.

Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden.

The unabated rise in anthropogenic CO₂ emissions is predicted to strongly influence the ocean's environment, increasing the mean sea-surface temperature by 4°C and causing a pH decline of 0.3 units by the year 2100. These changes are likely to affect the nutritional value of marine food sources since temperature and CO₂ can influence the fatty (FA) and amino acid (AA) composition of marine primary producers. Here, essential amino (EA) and polyunsaturated fatty (PUFA) acids are of particular importance due to their nutritional value to higher trophic levels. In order to determine the interactive effects of CO₂ and temperature on the nutritional quality of a primary producer, we analyzed the relative PUFA and EA composition of the diatom Cylindrotheca fusiformis cultured under a factorial matrix of 2 temperatures (14 and 19°C) and 3 partial pressures of CO₂ (180, 380, 750 μatm) for >250 generations. Our results show a decay of ~3% and ~6% in PUFA and EA content in algae kept at a pCO₂ of 750 μatm (high) compared to the 380 μatm (intermediate) CO₂ treatments at 14°C. Cultures kept at 19°C displayed a ~3% lower PUFA content under high compared to intermediate pCO₂, while EA did not show differences between treatments. Algae grown at a pCO₂ of 180 μatm (low) had a lower PUFA and AA content in relation to those at intermediate and high CO₂ levels at 14°C, but there were no differences in EA at 19°C for any CO₂ treatment. This study is the first to report adverse effects of warming and acidification on the EA of a primary producer, and corroborates previous observations of negative effects of these stressors on PUFA. Considering that only ~20% of essential biomolecules such as PUFA (and possibly EA) are incorporated into new biomass at the next trophic level, the potential impacts of adverse effects of ocean warming and acidification at the base of the food web may be amplified towards higher trophic levels, which rely on them as source of essential biomolecules.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0123945PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4430207PMC
February 2016

Iron stable isotopes track pelagic iron cycling during a subtropical phytoplankton bloom.

Proc Natl Acad Sci U S A 2015 Jan 22;112(1):E15-20. Epub 2014 Dec 22.

National Institute of Water and Atmospheric Research Centre for Chemical and Physical Oceanography, Department of Chemistry, University of Otago, Dunedin 9012, New Zealand.

The supply and bioavailability of dissolved iron sets the magnitude of surface productivity for ∼ 40% of the global ocean. The redox state, organic complexation, and phase (dissolved versus particulate) of iron are key determinants of iron bioavailability in the marine realm, although the mechanisms facilitating exchange between iron species (inorganic and organic) and phases are poorly constrained. Here we use the isotope fingerprint of dissolved and particulate iron to reveal distinct isotopic signatures for biological uptake of iron during a GEOTRACES process study focused on a temperate spring phytoplankton bloom in subtropical waters. At the onset of the bloom, dissolved iron within the mixed layer was isotopically light relative to particulate iron. The isotopically light dissolved iron pool likely results from the reduction of particulate iron via photochemical and (to a lesser extent) biologically mediated reduction processes. As the bloom develops, dissolved iron within the surface mixed layer becomes isotopically heavy, reflecting the dominance of biological processing of iron as it is removed from solution, while scavenging appears to play a minor role. As stable isotopes have shown for major elements like nitrogen, iron isotopes offer a new window into our understanding of the biogeochemical cycling of iron, thereby allowing us to disentangle a suite of concurrent biotic and abiotic transformations of this key biolimiting element.
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http://dx.doi.org/10.1073/pnas.1421576112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4291648PMC
January 2015

Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa.

PLoS One 2014 13;9(5):e97235. Epub 2014 May 13.

Department of Botany, University of Otago, Dunedin, New Zealand; Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.

Anthropogenically-modulated reductions in pH, termed ocean acidification, could pose a major threat to the physiological performance, stocks, and biodiversity of calcifiers and may devalue their ecosystem services. Recent debate has focussed on the need to develop approaches to arrest the potential negative impacts of ocean acidification on ecosystems dominated by calcareous organisms. In this study, we demonstrate the role of a discrete (i.e. diffusion) boundary layer (DBL), formed at the surface of some calcifying species under slow flows, in buffering them from the corrosive effects of low pH seawater. The coralline macroalga Arthrocardia corymbosa was grown in a multifactorial experiment with two mean pH levels (8.05 'ambient' and 7.65 a worst case 'ocean acidification' scenario projected for 2100), each with two levels of seawater flow (fast and slow, i.e. DBL thin or thick). Coralline algae grown under slow flows with thick DBLs (i.e., unstirred with regular replenishment of seawater to their surface) maintained net growth and calcification at pH 7.65 whereas those in higher flows with thin DBLs had net dissolution. Growth under ambient seawater pH (8.05) was not significantly different in thin and thick DBL treatments. No other measured diagnostic (recruit sizes and numbers, photosynthetic metrics, %C, %N, %MgCO3) responded to the effects of reduced seawater pH. Thus, flow conditions that promote the formation of thick DBLs, may enhance the subsistence of calcifiers by creating localised hydrodynamic conditions where metabolic activity ameliorates the negative impacts of ocean acidification.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0097235PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4019523PMC
December 2014

Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota.

Glob Chang Biol 2014 Oct 30;20(10):3004-25. Epub 2014 Jun 30.

Australian Antarctic Division, Channel Highway, Kingston, Tasmania, 7050, Australia; Antarctic Climate and Ecosystems Cooperative Research Centre, Private Bag 80, Hobart, Tasmania, 7001, Australia.

Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.
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http://dx.doi.org/10.1111/gcb.12623DOI Listing
October 2014
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