Reproductive phenology and morphology of Macrocystis pyrifera (Laminariales, Ochrophyta) from southern New Zealand in relation to wave exposure1.

Macrocystis pyrifera is a major habitat forming kelp in coastal ecosystems of temperate regions of the northern and southern hemispheres. We investigated the seasonal occurrence of adult sporophytes, morphological characteristics, and reproductive phenology at two sites within a wave-protected harbour and two wave-exposed sites in southern New Zealand every 3-4 months between 2012 and 2013. Seasonality in reproduction was assessed via the number of sporophylls, the occurrence of sori on sporophylls, and non-sporophyllous laminae (fertile pneumatocyst-bearing blades and fertile apical scimitars), meiospore release, and germination. We found that M. pyrifera was present and reproductive year-round in three of the four sites, and patterns were similar for the wave-exposure conditions. Sori were found on pneumatocyst-bearing blades and apical scimitars in addition to the sporophylls, and viable meiospores were released from all three types of laminae. Morphological variations between sites with different wave exposure indicate that sporophytes from wave-protected sites have bigger blades and holdfasts and are longer than those from wave-exposed sites. We discuss the implications of these biological variables for the ecology of M. pyrifera inhabiting different wave exposure environments in southern New Zealand.

Nitrogen sufficiency enhances thermal tolerance in habitat-forming kelp: implications for acclimation under thermal stress.

Local and global changes associated with anthropogenic activities are impacting marine and terrestrial ecosystems. Macroalgae, especially habitat-forming species like kelp, play critical roles in temperate coastal ecosystems. However, their abundance and distribution patterns have been negatively affected by warming in many regions around the globe. Along with global change, coastal ecosystems are also impacted by local drivers such as eutrophication. The interaction between global and local drivers might modulate kelp responses to environmental change. This study examines the regulatory effect of NO3- on the thermal plasticity of the giant kelp Macrocystis pyrifera. To do this, thermal performance curves (TPCs) of key temperature-dependant traits-growth, photosynthesis, NO3- assimilation and chlorophyll a fluorescence-were examined under nitrate replete and deplete conditions in a short-term incubation. We found that thermal plasticity was modulated by NO3- but different thermal responses were observed among traits. Our study reveals that nitrogen, a local driver, modulates kelp responses to high seawater temperatures, ameliorating the negative impacts on physiological performance (i.e. growth and photosynthesis). However, this effect might be species-specific and vary among biogeographic regions - thus, further work is needed to determine the generality of our findings to other key temperate macroalgae that are experiencing temperatures close to their thermal tolerance due to climate change.

Responses of macroalgae to CO2 enrichment cannot be inferred solely from their inorganic carbon uptake strategy.

Increased plant biomass is observed in terrestrial systems due to rising levels of atmospheric CO2, but responses of marine macroalgae to CO2 enrichment are unclear. The 200% increase in CO2 by 2100 is predicted to enhance the productivity of fleshy macroalgae that acquire inorganic carbon solely as CO2 (non-carbon dioxide-concentrating mechanism [CCM] species-i.e., species without a carbon dioxide-concentrating mechanism), whereas those that additionally uptake bicarbonate (CCM species) are predicted to respond neutrally or positively depending on their affinity for bicarbonate. Previous studies, however, show that fleshy macroalgae exhibit a broad variety of responses to CO2 enrichment and the underlying mechanisms are largely unknown. This physiological study compared the responses of a CCM species (Lomentaria australis) with a non-CCM species (Craspedocarpus ramentaceus) to CO2 enrichment with regards to growth, net photosynthesis, and biochemistry. Contrary to expectations, there was no enrichment effect for the non-CCM species, whereas the CCM species had a twofold greater growth rate, likely driven by a downregulation of the energetically costly CCM(s). This saved energy was invested into new growth rather than storage lipids and fatty acids. In addition, we conducted a comprehensive literature synthesis to examine the extent to which the growth and photosynthetic responses of fleshy macroalgae to elevated CO2 are related to their carbon acquisition strategies. Findings highlight that the responses of macroalgae to CO2 enrichment cannot be inferred solely from their carbon uptake strategy, and targeted physiological experiments on a wider range of species are needed to better predict responses of macroalgae to future oceanic change.

Copper pollution exacerbates the effects of ocean acidification and warming on kelp microscopic early life stages.

Ocean warming (OW), ocean acidification (OA) and their interaction with local drivers, e.g., copper pollution, may negatively affect macroalgae and their microscopic life stages. We evaluated meiospore development of the kelps Macrocystis pyrifera and Undaria pinnatifida exposed to a factorial combination of current and 2100-predicted temperature (12 and 16 °C, respectively), pH (8.16 and 7.65, respectively), and two copper levels (no-added-copper and species-specific germination Cu-EC50). Meiospore germination for both species declined by 5-18% under OA and ambient temperature/OA conditions, irrespective of copper exposure. Germling growth rate declined by >40%·day-1, and gametophyte development was inhibited under Cu-EC50 exposure, compared to the no-added-copper treatment, irrespective of pH and temperature. Following the removal of copper and 9-day recovery under respective pH and temperature treatments, germling growth rates increased by 8-18%·day-1. The exception was U. pinnatifida under OW/OA, where growth rate remained at 10%·day-1 before and after copper exposure. Copper-binding ligand concentrations were higher in copper-exposed cultures of both species, suggesting that ligands may act as a defence mechanism of kelp early life stages against copper toxicity. Our study demonstrated that copper pollution is more important than global climate drivers in controlling meiospore development in kelps as it disrupts the completion of their life cycle.

Growth, ammonium metabolism, and photosynthetic properties of Ulva australis (Chlorophyta) under decreasing pH and ammonium enrichment.

The responses of macroalgae to ocean acidification could be altered by availability of macronutrients, such as ammonium (NH4+). This study determined how the opportunistic macroalga, Ulva australis responded to simultaneous changes in decreasing pH and NH4+ enrichment. This was investigated in a week-long growth experiment across a range of predicted future pHs with ambient and enriched NH4+ treatments followed by measurements of relative growth rates (RGR), NH4+ uptake rates and pools, total chlorophyll, and tissue carbon and nitrogen content. Rapid light curves (RLCs) were used to measure the maximum relative electron transport rate (rETRmax) and maximum quantum yield of photosystem II (PSII) photochemistry (Fv/Fm). Photosynthetic capacity was derived from the RLCs and included the efficiency of light harvesting (α), slope of photoinhibition (ß), and the light saturation point (Ek). The results showed that NH4+ enrichment did not modify the effects of pH on RGRs, NH4+ uptake rates and pools, total chlorophyll, rETRmax, α, ß, Fv/Fm, tissue C and N, and the C:N ratio. However, Ek was differentially affected by pH under different NH4+ treatments. Ek increased with decreasing pH in the ambient NH4+ treatment, but not in the enriched NH4+ treatment. NH4+ enrichment increased RGRs, NH4+ pools, total chlorophyll, rETRmax, α, ß, Fv/Fm, and tissue N, and decreased NH4+ uptake rates and the C:N ratio. Decreased pH increased total chlorophyll content, rETRmax, Fv/Fm, and tissue N content, and decreased the C:N ratio. Therefore, the results indicate that U. australis growth is increased with NH4+ enrichment and not with decreasing pH. While decreasing pH influenced the carbon and nitrogen metabolisms of U. australis, it did not result in changes in growth.

Ocean acidification and kelp development: Reduced pH has no negative effects on meiospore germination and gametophyte development of Macrocystis pyrifera and Undaria pinnatifida.

The absorption of anthropogenic CO2 by the oceans is causing a reduction in the pH of the surface waters termed ocean acidification (OA). This could have substantial effects on marine coastal environments where fleshy (non-calcareous) macroalgae are dominant primary producers and ecosystem engineers. Few OA studies have focused on the early life stages of large macroalgae such as kelps. This study evaluated the effects of seawater pH on the ontogenic development of meiospores of the native kelp Macrocystis pyrifera and the invasive kelp Undaria pinnatifida, in south-eastern New Zealand. Meiospores of both kelps were released into four seawater pH treatments (pHT 7.20, extreme OA predicted for 2300; pHT 7.65, OA predicted for 2100; pHT 8.01, ambient pH; and pHT 8.40, pre-industrial pH) and cultured for 15 d. Meiospore germination, germling growth rate, and gametophyte size and sex ratio were monitored and measured. Exposure to reduced pHT (7.20 and 7.65) had positive effects on germling growth rate and gametophyte size in both M. pyrifera and U. pinnatifida, whereas, higher pHT (8.01 and 8.40) reduced the gametophyte size in both kelps. Sex ratio of gametophytes of both kelps was biased toward females under all pHT treatments, except for U. pinnatifida at pHT 7.65. Germling growth rate under OA was significantly higher in M. pyrifera compared to U. pinnatifida but gametophyte development was equal for both kelps under all seawater pHT treatments, indicating that the microscopic stages of the native M. pyrifera and the invasive U. pinnatifida will respond similarly to OA.

Seawater pH, and not inorganic nitrogen source, affects pH at the blade surface of Macrocystis pyrifera: implications for responses of the giant kelp to future oceanic conditions.

Ocean acidification (OA), the ongoing decline in seawater pH, is predicted to have wide-ranging effects on marine organisms and ecosystems. For seaweeds, the pH at the thallus surface, within the diffusion boundary layer (DBL), is one of the factors controlling their response to OA. Surface pH is controlled by both the pH of the bulk seawater and by the seaweeds' metabolism: photosynthesis and respiration increase and decrease pH within the DBL (pHDBL ), respectively. However, other metabolic processes, especially the uptake of inorganic nitrogen (Ni ; NO3- and NH4+ ) may also affect the pHDBL . Using Macrocystis pyrifera, we hypothesized that (1) NO3- uptake will increase the pHDBL , whereas NH4+ uptake will decrease it, (2) if NO3- is cotransported with H+ , increases in pHDBL would be greater under an OA treatment (pH = 7.65) than under an ambient treatment (pH = 8.00), and (3) decreases in pHDBL will be smaller at pH 7.65 than at pH 8.00, as higher external [H+ ] might affect the strength of the diffusion gradient. Overall, Ni source did not affect the pHDBL . However, increases in pHDBL were greater at pH 7.65 than at pH 8.00. CO2 uptake was higher at pH 7.65 than at pH 8.00, whereas HCO3- uptake was unaffected by pH. Photosynthesis and respiration control pHDBL rather than Ni uptake. We suggest that under future OA, Macrocystis pyrifera will metabolically modify its surface microenvironment such that the physiological processes of photosynthesis and Ni uptake will not be affected by a reduced pH.

Meiospores produced in sori of nonsporophyllous laminae of Macrocystis pyrifera (Laminariales, Phaeophyceae) may enhance reproductive output.

Different lamina of Macrocystis pyrifera sporophytes (i.e., sporophylls, pneumatocyst-bearing blades, and apical scimitars) in a wave-sheltered site were found to be fertile. We quantified their sorus surface area, reproductive output (number of spores released) and the viability of released spores (germination rate). Sorus area was greatest on the sporophylls, with sporangia developing on >57% of the total area and smallest on the pneumatocyst-bearing blades with 21% of the total area bearing sporangia. The apical scimitar released the greatest number of meiospores (cells · mL(-1)  · cm(-2) ) and the sporophylls the least. Meiospores produced from all types of fertile laminae were equally viable. This reproductive plasticity may enhance reproductive output, and contribute to short and long-distance spore dispersal and the cryptic gametophyte propagule bank for the next generation of sporophytes.