Catriona L. Hurd

WATER MOTION, MARINE MACROALGAL PHYSIOLOGY, AND PRODUCTION

Water motion is a key determinant of marine macroalgal production, influencing directly or indirectly physiological rates and community structure. Our understanding of how marine macroalgae interact with their hydrodynamic environment has increased substantially over the past 20 years, due to the application of tools such as flow visualization to aquatic vegetation, and in situ measurements of seawater velocity and turbulence. This review considers how the hydrodynamic environment in which macroalgae grow influences their ability to acquire essential resources and how macroalgae might respond physiologically to fluctuations in their hydrodynamic regime with a focus on: (1) the biochemical processes occurring within the diffusion boundary layer (DBL) that might reduce rates of macroalgal production; (2) time scales over which measurements of velocity and DBL processes should be made, discussing the likelihood of in situ mass transfer limitation; (3) if and how macroalgal morphology influences resource acquisition in slow flows; and (4) ecobiomechanics and how hydrodynamic drag might influence resource acquisition and allocation. Finally, the concept that macroalgal production is enhanced in wave‐exposed versus sheltered habitats is discussed.

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.

Effect of seawater velocity on inorganic nitrogen uptake by morphologically distinct forms of Macrocystis integrifolia from wave-sheltered and exposed sites

In conditions of low water motion (<0.06 ms−1), the availability of essential nutrients to macroalgae, and thus their potential productivity, may be limited by thick diffusion boundary-layers at the thallus surface. The ability of macroalgae to take up nutrients in slow moving water may be related to how their blade morphology affects diffusion boundarylayer thickness. For the giant kelp, Macrocystis integrifolia Bory, morphological measurements indicate that blades of plants from a site exposed to wave action are thick, narrow and have a heavily corrugated surface. In contrast, blades from a site with a low degree of water motion are relatively thin, with few surface corrugations and large undulations along their edges. The aim of our work was to test the hypothesis that morphological features of M. integrifolia blades from a sheltered site allow enhanced inorganic nitrogen uptake at low seawater velocities compared to blades with a wave-exposed morphology. The rate of nitrate and ammonium uptake by morphologically distinct blades of M. integrifolia, from sites that were sheltered from and exposed to wave action, were measured in the laboratory at a range of seawater velocities (0.01 to 0.16 ms−1), between March and May 1993. For both sheltered and exposed blade morphologies, nitrate and ammonium uptake rates increased with increasing seawater velocity, reaching a maximum rate at 0.04 to 0.06 ms−1. Uptake parameters Vmax (maximum uptake rate) and U0.37 (the velocity at which the uptake rate is 37% of the maximum rate) were estimated using an exponential decay formula. These parameters were similar for both blade morphologies, at all seawater velocities tested. Additional measurements suggest that the nitrogen status of M. integrifolia blades from wavesheltered and exposed sites were similar throughout the experimental period, and thus nitrogen status did not affect the rate of nitrogen uptake in these experiments. on the basis of these results, we conclude that blade morphology does not enhance nitrogen uptake by M. integrifolia in conditions of low water motion. Potential effects of diffusion boundary-layers on kelp productivity are discussed.

An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta)

Direct comparisons between photosynthetic O2 evolution rate and electron transport rate (ETR) were made in situ over 24 h using the benthic macroalga Ulva lactuca (Chlorophyta), growing and measured at a depth of 1.8 m, where the midday irradiance rose to 400–600 μmol photons m−2 s−1. O2 exchange was measured with a 5-chamber data-logging apparatus and ETR with a submersible pulse amplitude modulated (PAM) fluorometer (Diving-PAM). Steady-state quantum yield ((Fm′−Ft)/Fm′) decreased from 0.7 during the morning to 0.45 at midday, followed by some recovery in the late afternoon. At low to medium irradiances (0–300 μmol photons m−2 s−1), there was a significant correlation between O2 evolution and ETR, but at higher irradiances, ETR continued to increase steadily, while O2 evolution tended towards an asymptote. However at high irradiance levels (600–1200 μmol photons m−2 s−1) ETR was significantly lowered. Two methods of measuring ETR, based on either diel ambient light levels and fluorescence yields or rapid light curves, gave similar results at low to moderate irradiance levels. Nutrient enrichment (increases in [NO3−], [NH4+] and [HPO42-] of 5- to 15-fold over ambient concentrations) resulted in an increase, within hours, in photosynthetic rates measured by both ETR and O2 evolution techniques. At low irradiances, approximately 6.5 to 8.2 electrons passed through PS II during the evolution of one molecule of O2, i.e., up to twice the theoretical minimum number of four. However, in nutrient-enriched treatments this ratio dropped to 5.1. The results indicate that PAM fluorescence can be used as a good indication of the photosynthetic rate only at low to medium irradiances.

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 role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae)

Abstract The Asian kelp Undaria pinnatifida (Laminariales, Phaeophyceae) was first recorded in New Zealand in 1987 and has since spread via shipping traffic and other vectors to a number of ports and harbours. Here we report the results of laboratory and fieldstudies devised to assess the potential for natural dispersal of Undaria from a founding population. Under laboratory conditions, > 90% of Undaria spores were viable in seawater for at least 5 days, with some viable after 14 days. Spores artificially released into a tidal current resulted later in sporophytes appearing on artificial surfaces positioned 10 m down-current of the release point. Field monitoring of a founding population within the Marlborough Sounds, New Zealand, suggested that natural populations spread at least 100 m yr−1. Reasons for the differences between the dispersal distances of the artificially released spores (10 m) and natural populations (100 m) are discussed. We propose that spore dispersal from fixed stands of Undaria results primarily in short-range spread (metres to hundreds of metres), with dispersal of fragments or whole sporophytes facilitating spread at scales of hundreds of metres to kilometres.

BEFORE OCEAN ACIDIFICATION: CALCIFIER CHEMISTRY LESSONS(1).

Ocean Acidification (OA) has been an important research topic for a decade. Scientists have focused on how the predicted 56% decline in the seawater carbonate ion () concentration will dramatically impair the ability of calcifiers, ranging from coccolithophores to shellfish, to form calcium carbonate (CaCO3) structures, and the implications of the reduced carbonate saturation state (Ω) for increased dissolution of such structures. However, many published OA studies have overlooked a fundamental issue: most calcifying organisms do not rely on carbonate from seawater to calcify; they use either bicarbonate () or metabolically‐produced CO2. The ability of important primary (corals, coralline seaweeds, and coccolithophores) and secondary (mollusks) producers to modify their local carbonate chemistry suggests that the primary threat to them from OA is by dissolution rather than impaired calcification. Here, we draw on calcification research from an era before OA and combine it with recent studies that question the source of the carbonate ion, to provide new insights into how OA might affect calcifying organisms. Organismal modification of local carbonate chemistry may enable some calcifiers to successfully form calcareous structures despite OA.

Short- and long-term conditioning of a temperate marine diatom community to acidification and warming

Ocean acidification and greenhouse warming will interactively influence competitive success of key phytoplankton groups such as diatoms, but how long-term responses to global change will affect community structure is unknown. We incubated a mixed natural diatom community from coastal New Zealand waters in a short-term (two-week) incubation experiment using a factorial matrix of warming and/or elevated pCO2 and measured effects on community structure. We then isolated the dominant diatoms in clonal cultures and conditioned them for 1 year under the same temperature and pCO2 conditions from which they were isolated, in order to allow for extended selection or acclimation by these abiotic environmental change factors in the absence of interspecific interactions. These conditioned isolates were then recombined into ‘artificial’ communities modelled after the original natural assemblage and allowed to compete under conditions identical to those in the short-term natural community experiment. In general, the resulting structure of both the unconditioned natural community and conditioned ‘artificial’ community experiments was similar, despite differences such as the loss of two species in the latter. pCO2 and temperature had both individual and interactive effects on community structure, but temperature was more influential, as warming significantly reduced species richness. In this case, our short-term manipulative experiment with a mixed natural assemblage spanning weeks served as a reasonable proxy to predict the effects of global change forcing on diatom community structure after the component species were conditioned in isolation over an extended timescale. Future studies will be required to assess whether or not this is also the case for other types of algal communities from other marine regimes.

Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata

Ocean acidification (OA) is the reduction in seawater pH due to the absorption of human-released CO2 by the world’s oceans. The average surface oceanic pH is predicted to decline by 0.4 units by 2100. However, kelp metabolically modifies seawater pH via photosynthesis and respiration in some temperate coastal systems, resulting in daily pH fluctuations of up to ±0.45 units. It is unknown how these fluctuations in pH influence the growth and physiology of the kelp, or how this might change with OA. In laboratory experiments that mimicked the most extreme pH fluctuations measured within beds of the canopy-forming kelp Ecklonia radiata in Tasmania, the growth and photosynthetic rates of juvenile E. radiata were greater under fluctuating pH (8.4 in the day, 7.8 at night) than in static pH treatments (8.4, 8.1, 7.8). However, pH fluctuations had no effect on growth rates and a negative effect on photosynthesis when the mean pH of each treatment was reduced by 0.3 units. Currently, pH fluctuations have a positive effect on E. radiata but this effect could be reversed in the future under OA, which is likely to impact the future ecological dynamics and productivity of habitats dominated by E. radiata.