Christopher D. Hepburn

TESTING THE EFFECTS OF OCEAN ACIDIFICATION ON ALGAL METABOLISM: CONSIDERATIONS FOR EXPERIMENTAL DESIGNS(1).

Ocean acidification describes changes in the carbonate chemistry of the ocean due to the increased absorption of anthropogenically released CO2. Experiments to elucidate the biological effects of ocean acidification on algae are not straightforward because when pH is altered, the carbon speciation in seawater is altered, which has implications for photosynthesis and, for calcifying algae, calcification. Furthermore, photosynthesis, respiration, and calcification will themselves alter the pH of the seawater medium. In this review, algal physiologists and seawater carbonate chemists combine their knowledge to provide the fundamental information on carbon physiology and seawater carbonate chemistry required to comprehend the complexities of how ocean acidification might affect algae metabolism. A wide range in responses of algae to ocean acidification has been observed, which may be explained by differences in algal physiology, timescales of the responses measured, study duration, and the method employed to alter pH. Two methods have been widely used in a range of experimental systems: CO2 bubbling and HCl/NaOH additions. These methods affect the speciation of carbonate ions in the culture medium differently; we discuss how this could influence the biological responses of algae and suggest a third method based on HCl/NaHCO3 additions. We then discuss eight key points that should be considered prior to setting up experiments, including which method of manipulating pH to choose, monitoring during experiments, techniques for adding acidified seawater, biological side effects, and other environmental factors. Finally, we consider incubation timescales and prior conditioning of algae in terms of regulation, acclimation, and adaptation to ocean acidification.

CARBON-USE STRATEGIES IN MACROALGAE: DIFFERENTIAL RESPONSES TO LOWERED PH AND IMPLICATIONS FOR OCEAN ACIDIFICATION1

Ocean acidification (OA) is a reduction in oceanic pH due to increased absorption of anthropogenically produced CO2. This change alters the seawater concentrations of inorganic carbon species that are utilized by macroalgae for photosynthesis and calcification: CO2 and HCO3− increase; CO32− decreases. Two common methods of experimentally reducing seawater pH differentially alter other aspects of carbonate chemistry: the addition of CO2 gas mimics changes predicted due to OA, while the addition of HCl results in a comparatively lower [HCO3−]. We measured the short‐term photosynthetic responses of five macroalgal species with various carbon‐use strategies in one of three seawater pH treatments: pH 7.5 lowered by bubbling CO2 gas, pH 7.5 lowered by HCl, and ambient pH 7.9. There was no difference in photosynthetic rates between the CO2, HCl, or pH 7.9 treatments for any of the species examined. However, the ability of macroalgae to raise the pH of the surrounding seawater through carbon uptake was greatest in the pH 7.5 treatments. Modeling of pH change due to carbon assimilation indicated that macroalgal species that could utilize HCO3− increased their use of CO2 in the pH 7.5 treatments compared to pH 7.9 treatments. Species only capable of using CO2 did so exclusively in all treatments. Although CO2 is not likely to be limiting for photosynthesis for the macroalgal species examined, the diffusive uptake of CO2 is less energetically expensive than active HCO3− uptake, and so HCO3−‐using macroalgae may benefit in future seawater with elevated CO2.

Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification

Coastal ecosystems that are characterized by kelp forests encounter daily pH fluctuations, driven by photosynthesis and respiration, which are larger than pH changes owing to ocean acidification (OA) projected for surface ocean waters by 2100. We investigated whether mimicry of biologically mediated diurnal shifts in pH—based for the first time on pH time-series measurements within a kelp forest—would offset or amplify the negative effects of OA on calcifiers. In a 40-day laboratory experiment, the calcifying coralline macroalga, Arthrocardia corymbosa, was exposed to two mean pH treatments (8.05 or 7.65). For each mean, two experimental pH manipulations were applied. In one treatment, pH was held constant. In the second treatment, pH was manipulated around the mean (as a step-function), 0.4 pH units higher during daylight and 0.4 units lower during darkness to approximate diurnal fluctuations in a kelp forest. In all cases, growth rates were lower at a reduced mean pH, and fluctuations in pH acted additively to further reduce growth. Photosynthesis, recruitment and elemental composition did not change with pH, but δ13C increased at lower mean pH. Including environmental heterogeneity in experimental design will assist with a more accurate assessment of the responses of calcifiers to OA.

The expanding range of Undaria pinnatifida in southern New Zealand: distribution, dispersal mechanisms and the invasion of wave-exposed environments

Very few studies have addressed how the invasive kelp Undaria pinnatifida (Harvey) Suringar spreads beyond initial founding populations in harbours. Surveys of the harbours and accessible areas of open coast throughout southern New Zealand were conducted to determine how far U. pinnatifida populations had extended since initial incursions. Our findings clearly demonstrate that U. pinnatifida is capable of invading native communities and can establish reproductive populations in locations subjected to significant and consistent wave action. The extent of spread from source populations differs between harbours in which it has established. Dispersal is greatest in harbours with long established populations, those where populations have not been strategically managed, harbours with high water exchange with surrounding coastal waters, and where prevailing currents allow establishment of U. pinnatifida on suitable substrata close to harbour entrances. Dispersal along the open coast is primarily achieved by drifting adult sporophytes that are washed up in the rocky intertidal zone. Founding populations are most often found in the intertidal zone, primarily within rockpools. Subtidal transects and observations indicate that U. pinnatifida is well adapted to invade exposed coastlines and can establish within a broad range of niches in wave-exposed areas including rockpools, the low intertidal, shallow subtidal, Macrocystis pyrifera kelp forests, and in low light areas beyond the vertical extent of large native macroalgae. The current range of U. pinnatifida is much greater than expected and appears to be expanding. Due to its ability to grow in a broad range of environments and to form dense monospecific stands, U. pinnatifida has the potential to strongly modify almost all rocky subtidal and intertidal communities in temperate locations.

Colony Structure and Seasonal Differences in Light and Nitrogen Modify the Impact of Sessile Epifauna on the Giant Kelp Macrocystis pyrifera (L.) C Agardh

The presence of the stoloniferous hydroid Obelia geniculata (L.) had no effect on the pigment concentration or nitrogen status of underlying blade tissue of the giant kelp Macrocystis pyrifera (L.) C. Agardh. The sheet-like colonies of the bryozoan Membranipora membranacea (L.) markedly reduced the pigment concentration of colonized blade tissue, but only during winter. Reductions in pigment concentration are most likely a result of damage to underlying tissue due to some factor related to the presence of bryozoan colonies on blade surfaces. Blade tissue colonized by M. membranacea also had higher δ15N signatures than surrounding bryozoan-free tissue, possibly indicating the provision of nitrogen to M. pyrifera by bryozoan colonies. Results show that seasonal changes in nitrogen and colony size can strongly modify the effect of epifauna on macroalgae they colonize. Unlike bryozoans, hydroid colonies provided no barrier to nitrogen uptake by colonized M. pyrifera tissue and enhanced ammonium uptake was observed for tissue colonized by O. geniculata during nitrogen limitation. Epifauna with stoloniferous growth forms such as hydroids are more likely to have benign or even mutualistic relationships with macroalgae they colonize than the sheet-like colonies of bryozoans.

Light Limitation within Southern New Zealand Kelp Forest Communities

Light is the fundamental driver of primary productivity in the marine environment. Reduced light availability has the potential to alter the distribution, community composition, and productivity of key benthic primary producers, potentially reducing habitat and energy provision to coastal food webs. We compared the underwater light environment of macroalgal dominated shallow subtidal rocky reef habitats on a coastline modified by human activities with a coastline of forested catchments. Key metrics describing the availability of photosynthetically active radiation (PAR) were determined over 295 days and were related to macroalgal depth distribution, community composition, and standing biomass patterns, which were recorded seasonally. Light attenuation was more than twice as high in shallow subtidal zones along the modified coast. Macroalgal biomass was 2–5 times greater within forested sites, and even in shallow water (2m) a significant difference in biomass was observed. Long-term light dose provided the best explanation for differences in observed biomass between modified and forested coasts, with light availability over the study period differing by 60 and 90 mol photons m−2 at 2 and 10 metres, respectively. Higher biomass on the forested coast was driven by the presence of larger individuals rather than species diversity or density. This study suggests that commonly used metrics such as species diversity and density are not as sensitive as direct measures of biomass when detecting the effects of light limitation within macroalgal communities.

Contributions of an annual invasive kelp to native algal assemblages: algal resource allocation and seasonal connectivity across ecotones

Abstract: The consequences of macroalgal invasions for coastal ecosystem structure and food webs remain poorly understood. We investigated the relative contribution of the invasive kelp Undaria pinnatifida (Heterokontophyta), which has an annual life cycle, to the composition of algal assemblages in subtidal rocky reefs and in the wrack of nearby surf zones and sandy beaches in southern New Zealand. Undaria pinnatifida made substantial contributions to the density and percent cover (up to 75%) of algal communities in the subtidal habitats studied, suggesting that it influences the living habitat and food resources in subtidal temperate reefs. In comparison, its contribution to the drift in the surf zone and algal wrack that accumulated on sandy beach habitats was low (usually < 25%) compared with native kelps, although it occasionally contributed up to 75% of the drift biomass. This difference likely reflects the lack of buoyancy of U. pinnatifida compared with native kelp species, limiting its capacity to act as a vector for the transfer of carbon across coastal landscapes. In contrast to the native perennial algae, U. pinnatifidas contribution to algal communities in subtidal habitats was inconsistent through time, with the greatest percent cover in early summer (December) and the lowest in early winter (April). Such a temporal pattern in the biomass of wrack and drift U. pinnatifida in beach and surf-zone habitats was, however, less apparent. Our findings suggest that the strongly seasonal and highly invasive U. pinnatifida has the potential to influence carbon fluxes and faunal communities in subtidal food webs, but that such effects are unlikely to be transferred across coastal habitats.

Survival in low light: photosynthesis and growth of a red alga in relation to measured in situ irradiance

Reduced light availability for benthic primary producers as a result of anthropogenic activities may be an important driver of change in coastal seas. However, our knowledge of the minimum light requirements for benthic macroalgae limits our understanding of how these changes may affect primary productivity and the functioning of coastal ecosystems. This knowledge gap is particularly acute in deeper water, where the impacts of increased light attenuation will be most severe. We examined the minimum light requirements of Anotrichium crinitum, which dominates near the maximum depth limit for macroalgae throughout New Zealand and Southern Australia, and is a functional analog of rhodophyte macroalgae in temperate low‐light (deep‐water) habitats throughout the world. These data show that A. crinitum is a shade‐adapted seaweed with modest light requirements for the initiation of net photosynthesis (1.49–2.25 μmol photons · m−2 · s−1) and growth (0.12–0.19 mol photons · m−2 · d−1). A. crinitum maintains high photosynthetic efficiency and pigment content and a low C:N ratio throughout the year and can maintain biomass under sub‐compensation (critical) light levels for at least 5 d. Nevertheless, in situ photon flux is less than the minimum light requirement for A. crinitum on at least 103 d per annum and is rarely sufficient to saturate growth. These findings reinforce the importance of understanding the physiological response of macroalgae at the extremes of environmental gradients and highlight the need to establish minimum thresholds that modification of the subtidal light environment should not cross.

Restricted use of nitrate and a strong preference for ammonium reflects the nitrogen ecophysiology of a light‐limited red alga

Ammonium and nitrate are important sources of inorganic nitrogen for coastal primary producers. Nitrate has higher energy requirement for uptake and assimilation, compared with ammonium, suggesting that it might be a more efficient nitrogen source for slow‐growing, light‐limited macroalgae. To address this hypothesis, we examined the nitrogen ecophysiology of Anotrichium crinitum, a rhodophyte macroalgae common in low‐light habitats in New Zealand. We measured seasonal changes in seawater nitrate and ammonium concentrations and the concentration of nitrate and ammonium stored internally by A. crinitum. We determined the maximal uptake rates of nitrate and ammonium seasonally and grew A. crinitum in the laboratory with these nitrogen sources under two ecologically relevant saturating light levels. Our results show that field‐harvested A. crinitum has a high affinity for ammonium and although it will grow when supplied exclusively with nitrate, internal nitrate pools are low and it is unable to take up nitrate without several days of acclimation to saturating light. Our data predict that A. crinitum would be able to sustain growth with ammonium as the sole source of nitrogen, a strategy that would help it survive under low‐light conditions that prevail in the field.

Ocean acidification in New Zealand waters: trends and impacts

ABSTRACT The threat posed by ocean acidification (OA) to the diversity and productivity of New Zealand marine ecosystems is assessed in a synthesis of published trends and impacts. A 20-year time series in Subantarctic water, and a national coastal monitoring programme, provide insight into pH variability, and context for experimental design, modelling and projections. A review of the potential impact of changes in the carbonate system on the major phyla in New Zealand waters confirms international observations that calcifying organisms, and particularly their early life-history stages, are vulnerable. The synthesis considers ecosystem and socio-economic impacts, and identifies current knowledge gaps and future research directions, including mechanistic studies of OA sensitivity. Advanced ecosystem models of OA, that incorporate the indirect effects of OA and interactions with other climate stressors, are required for robust projection of the future status of New Zealand marine ecosystems.