The effects of ocean acidification on zooplankton: Using natural CO2 seeps as windows into the future

Since the beginning of the Industrial Revolution, carbon dioxide (CO2) has been emitted into the atmosphere at rates unprecedented to Earth’s history. Nearly 30% of the anthropogenic CO2 in the atmosphere has been absorbed in surface waters of the ocean, pushing carbonate chemistry towards increased bicarbonate ions and hydrogen protons and decreased carbonate ions. Consequently, seawater pH has decreased from pre-Industrial Revolution levels of 8.2 to current levels of 8.1, and it is expected to continue to drop to 7.8 by the year 2100 if carbon emissions continue as predicted. The combination of these effects is referred to as ocean acidification. It is at the forefront of marine research as it poses a serious threat to several marine organisms and ecosystems. Ocean acidification has the most notable direct effect on calcifying organisms with calcium carbonate skeletons and shells, because fewer carbonate ions in the water column result in reduced calcification. Coral reefs are especially vulnerable to ocean acidification since reefs are composed of complex carbonate structures. Coral reefs have a high biodiversity; thus, not only will the corals themselves be affected by ocean acidification, but so will many of the animals that dwell in them.

The primary objective of this thesis was to examine the effects of ocean acidification on demersal zooplankton that reside in coral reefs. Ocean acidification research on zooplankton has primarily been single- species experiments on calcifying species or generalist copepod species. Scaling-up to experiments examining ocean acidification effects on entire zooplankton communities is logistically difficult, thus the ability to predict community changes in zooplankton due to ocean acidification has been rather limited. However, a few locations around the world have submarine volcanic CO2 seeps that can be used as natural laboratories to study ecosystem effects of ocean acidification. Two CO2 seeps located in coral reefs in Papua New Guinea were used as windows into the future to examine the effects of ocean acidification on entire zooplankton communities while they live naturally in their environment. Over three expeditions to two CO2 seeps, nocturnal plankton were sampled with horizontal net tows and emergence traps. Additional experiments were also conducted, and collectively this work is summarized in chapters 2-5 as outlined below.

Chapter 2 reports on the observed changes in zooplankton abundance and community composition between control and high-CO2 sites. Consistent results between seep sites and expeditions showed that zooplankton abundances were reduced three-fold under high-CO2 conditions. The abundance loss was partially attributed to habitat change within the coral reef, from more structurally complex corals in the control sites to a replacement of massive bouldering corals in the high-CO2 sites. The loss of structural complexity in the reef meant there were fewer hiding spaces for the zooplankton to seek refuge in during the day. All zooplankton taxa were reduced under high-CO2 conditions but to varying levels, suggesting that each taxon reacts differently to ocean acidification. Since each taxonomic group within the zooplankton communities was reduced to varying levels under ocean acidification, the copepod genus with the largest reduction in abundance was investigated in more detail. Labidocera spp. are pontellid copepods that are generally considered surface-dwellers and are not known to inhabit coral reefs. Therefore, as a preface to the ocean acidification study, the new discovery of these copepods living in coral reefs is first described (Chapter 3). Not only were they found to be residential to the reef, but Labidocera spp. living at the control reefs preferred to reside in coral rubble, macroalgae, and turf algae. Labidocera spp. were one of the most sensitive copepods to high-CO2 conditions and were reduced by nearly 70% in abundance, prompting a more detailed investigation about the effect of ocean acidification on their physiology and habitat preference (Chapter 4). Physiological parameters, e.g. size, feeding, and oocyte development, were unaffected by ocean acidification. Unlike the zooplankton community as a whole, the main cause for the abundance loss of Labidocera spp. was not a shift in the habitat because their preferred substrata were of equal percent coverage across high-CO2 and control sites. Instead, Labidocera spp. were no longer associated with any substrata type. Multiple direct and indirect effects of ocean acidification will act on each zooplankton taxa separately, and their collective response will contribute to the community response. The effects of ocean acidification on zooplankton communities were then scaled up to potential impacts on entire ecosystems. Zooplankton are the primary food source for corals, fish, and other zooplanktivores. The impacts of ocean acidification on zooplankton communities will have cascade effects on the food chain via the pathway of zooplanktivorous organisms. A case study on the stony coral Galaxea fascicularis explored the effects of ocean acidification on the ability of corals, which had lived their entire lives under high-CO2 conditions, to feed on zooplankton (Chapter 5). Under anthropogenic changes, whether it is from bleaching, high turbidity, or ocean acidification, some corals rely more on heterotrophy and consume more zooplankton. Contrary to expectation, this study showed that when given equal quantities of food particles these corals consumed less zooplankton under ocean acidification. Corals rely on heterotrophy for essential nutrients, like nitrogen and phosphorus, which they cannot otherwise obtain from autotrophy and their symbiotic zooxanthellae.

In conclusion, my thesis shows that not only is there fewer zooplankton available to consume, but the existing zooplankton is consumed with lower capture rates under high CO2 conditions. Coral reefs in future oceans will likely have reduced zooplankton abundances as an indirect effect of ocean acidification, partially caused by a change in habitat from branching corals to more massive bouldering corals. Zooplankton abundances were reduced yet the community composition was unaffected by ocean acidification. All zooplankton taxa were reduced yet present under high-CO2 conditions suggesting that the zooplankton are at least able to survive under ocean acidification. Fewer zooplankton will be available to zooplanktivores, but the fatty acid content and nutritional value of the zooplankton as a food source is expected to be similar to current food. Together this is expected to negatively impact the entire coral reef ecosystem, with some coral species unable to consume zooplankton at normal rates. In an ecosystem already highly vulnerable to ocean acidification, coral reefs may be even more threatened if the very basis of their food webs is reduced.

Continue reading ‘The effects of ocean acidification on zooplankton: Using natural CO2 seeps as windows into the future’

Conspecific aggregations mitigate the effects of ocean acidification on calcification of the coral Pocillopora verrucosa

In densely populated communities, such as coral reefs, organisms can modify the physical and chemical environment for neighbouring individuals. We tested the hypothesis that colony density (12 colonies each placed∼0.5 cm apart versus∼8 cm apart) can modulate the physiological response (measured through rates of calcification, photosynthesis, and respiration in the light and dark) of the coral Pocillopora verrucosa to pCO2 treatments (∼ 400 µatm and∼1200 µatm) by altering the seawater flow regimes experienced by colonies placed in aggregations within a flume at a single flow speed. While light calcification decreased 20% under elevated versus ambient pCO2 for colonies in low-density aggregations, light calcification of high-density aggregations increased 23% at elevated versus ambient pCO2. As a result, densely aggregated corals maintained calcification rates over 24 h that were comparable to those maintained under ambient pCO2, despite a 45% decrease in dark calcification at elevated versus ambient pCO2. Additionally, densely aggregated corals experienced reduced flow speeds and higher seawater retention times between colonies due to the formation of eddies. These results support recent indications that neighbouring organisms, such as the conspecific coral colonies in the present example, can create small-scale refugia from the negative effects of ocean acidification.

Continue reading ‘Conspecific aggregations mitigate the effects of ocean acidification on calcification of the coral Pocillopora verrucosa’

Genomic characterization of the evolutionary potential of the sea urchin Strongylocentrotus droebachiensis facing ocean acidification

Ocean acidification (OA) is increasing due to anthropogenic CO2 emissions, and poses a threat to marine species and communities worldwide. To better project the effects of acidification on organisms’ health and persistence an understanding is needed of (1) the mechanisms underlying developmental and physiological tolerance, and (2) the potential populations have for rapid evolutionary adaptation. This is especially challenging in non-model species where targeted assays of metabolism and stress physiology may not be available or economical for large-scale assessments of genetic constraints. We used mRNA sequencing and a quantitative genetics breeding design to study mechanisms underlying genetic variability and tolerance to decreased seawater pH (-0.4 pH units) in larvae of the sea urchin Strongylocentrotus droebachiensis. We used a gene ontology-based approach to integrate expression profiles into indirect measures of cellular and biochemical traits underlying variation in larval performance (i.e., growth rates). Molecular responses to OA were complex, involving changes to several functions such as growth rates, cell division, metabolism, and immune activities. Surprisingly, the magnitude of pH effects on molecular traits tended to be small relative to variation attributable to segregating functional genetic variation in this species. We discuss how the application of transcriptomics and quantitative genetics approaches across diverse species can enrich our understanding of the biological impacts of climate change.

Continue reading ‘Genomic characterization of the evolutionary potential of the sea urchin Strongylocentrotus droebachiensis facing ocean acidification’

Coral calcifying fluid pH is modulated by seawater carbonate chemistry not solely seawater pH

Reef coral calcification depends on regulation of pH in the internal calcifying fluid (CF) in which the coral skeleton forms. However, little is known about calcifying fluid pH (pHCF) regulation, despite its importance in determining the response of corals to ocean acidification. Here, we investigate pHCF in the coral Stylophora pistillata in seawater maintained at constant pH with manipulated carbonate chemistry to alter dissolved inorganic carbon (DIC) concentration, and therefore total alkalinity (AT). We also investigate the intracellular pH of calcifying cells, photosynthesis, respiration and calcification rates under the same conditions. Our results show that despite constant pH in the surrounding seawater, pHCF is sensitive to shifts in carbonate chemistry associated with changes in [DIC] and [AT], revealing that seawater pH is not the sole driver of pHCF. Notably, when we synthesize our results with published data, we identify linear relationships of pHCF with the seawater [DIC]/[H+] ratio, [AT]/ [H+] ratio and [Embedded Image]. Our findings contribute new insights into the mechanisms determining the sensitivity of coral calcification to changes in seawater carbonate chemistry, which are needed for predicting effects of environmental change on coral reefs and for robust interpretations of isotopic palaeoenvironmental records in coral skeletons.

Continue reading ‘Coral calcifying fluid pH is modulated by seawater carbonate chemistry not solely seawater pH’

Community production modulates coral reef pH and the sensitivity of ecosystem calcification to ocean acidification

Coral reefs are built of calcium carbonate (CaCO3) produced biogenically by a diversity of calcifying plants, animals and microbes. As the ocean warms and acidifies, there is mounting concern that declining calcification rates could shift coral reef CaCO3 budgets from net accretion to net dissolution. We quantified net ecosystem calcification (NEC) and production (NEP) on Dongsha Atoll, northern South China Sea, over a two-week period that included a transient bleaching event. Peak daytime pH on the wide, shallow reef flat during the non-bleaching period was ∼8.5, significantly elevated above that of the surrounding open ocean (∼8.0-8.1) as a consequence of daytime NEP (up to 112 mmol C m−2 hr−1). Diurnal-averaged NEC was 390 ± 90 mmol CaCO3 m−2 day−1, higher than any other coral reef studied to date despite comparable calcifier cover (25%) and relatively high fleshy algal cover (19%). Coral bleaching linked to elevated temperatures significantly reduced daytime NEP by 29 mmol C m−2 hr−1. pH on the reef flat declined by 0.2 units, causing a 40% reduction in NEC in the absence of pH changes in the surrounding open ocean. Our findings highlight the interactive relationship between carbonate chemistry of coral reef ecosystems and ecosystem production and calcification rates, which are in turn impacted by ocean warming. As open-ocean waters bathing coral reefs warm and acidify over the 21st century, the health and composition of reef benthic communities will play a major role in determining on-reef conditions that will in turn dictate the ecosystem response to climate change. Continue reading ‘Community production modulates coral reef pH and the sensitivity of ecosystem calcification to ocean acidification’

A key marine diazotroph in a changing ocean: the interacting effects of temperature, CO2 and light on the growth of Trichodesmium erythraeum IMS101

Trichodesmium is a globally important marine diazotroph that accounts for approximately 60 − 80% of marine biological N2 fixation and as such plays a key role in marine N and C cycles. We undertook a comprehensive assessment of how the growth rate of Trichodesmium erythraeum IMS101 was directly affected by the combined interactions of temperature, pCO2 and light intensity. Our key findings were: low pCO2 affected the lower temperature tolerance limit (Tmin) but had no effect on the optimum temperature (Topt) at which growth was maximal or the maximum temperature tolerance limit (Tmax); low pCO2 had a greater effect on the thermal niche width than low-light; the effect of pCO2 on growth rate was more pronounced at suboptimal temperatures than at supraoptimal temperatures; temperature and light had a stronger effect on the photosynthetic efficiency (Fv/Fm) than did CO2; and at Topt, the maximum growth rate increased with increasing CO2, but the initial slope of the growth-irradiance curve was not affected by CO2. In the context of environmental change, our results suggest that the (i) nutrient replete growth rate of Trichodesmium IMS101 would have been severely limited by low pCO2 at the last glacial maximum (LGM), (ii) future increases in pCO2 will increase growth rates in areas where temperature ranges between Tmin to Topt, but will have negligible effect at temperatures between Topt and Tmax, (iii) areal increase of warm surface waters (> 18°C) has allowed the geographic range to increase significantly from the LGM to present and that the range will continue to expand to higher latitudes with continued warming, but (iv) continued global warming may exclude Trichodesmium spp. from some tropical regions by 2100 where temperature exceeds Topt.

Continue reading ‘A key marine diazotroph in a changing ocean: the interacting effects of temperature, CO2 and light on the growth of Trichodesmium erythraeum IMS101’

Ocean acidification and calcium carbonate saturation states in the coastal zone of the West Antarctic Peninsula

The polar oceans are particularly vulnerable to ocean acidification; the lowering of seawater pH and carbonate mineral saturation states due to uptake of atmospheric carbon dioxide (CO2). High spatial variability in surface water pH and saturation states (Ω) for two biologically-important calcium carbonate minerals calcite and aragonite was observed in Ryder Bay, in the coastal sea-ice zone of the West Antarctic Peninsula. Glacial meltwater and melting sea ice stratified the water column and facilitated the development of large phytoplankton blooms and subsequent strong uptake of atmospheric CO2 of up to 55 mmol m-2 day-1 during austral summer. Concurrent high pH (8.48) and calcium carbonate mineral supersaturation (Ωaragonite ~3.1) occurred in the meltwater-influenced surface ocean. Biologically-induced increases in calcium carbonate mineral saturation states counteracted any effects of carbonate ion dilution. Accumulation of CO2 through remineralisation of additional organic matter from productive coastal waters lowered the pH (7.84) and caused deep-water corrosivity (Ωaragonite ~0.9) in regions impacted by Circumpolar Deep Water. Episodic mixing events enabled CO2-rich subsurface water to become entrained into the surface and eroded seasonal stratification to lower surface water pH (8.21) and saturation states (Ωaragonite ~1.8) relative to all surface waters across Ryder Bay. Uptake of atmospheric CO2 of 28 mmol m-2 day-1 in regions of vertical mixing may enhance the susceptibility of the surface layer to future ocean acidification in dynamic coastal environments. Spatially-resolved studies are essential to elucidate the natural variability in carbonate chemistry in order to better understand and predict carbon cycling and the response of marine organisms to future ocean acidification in the Antarctic coastal zone.

Continue reading ‘Ocean acidification and calcium carbonate saturation states in the coastal zone of the West Antarctic Peninsula’

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Ocean acidification in the IPCC AR5 WG II

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