Insights into the nitrogen ecophysiology of Macrocystis pyrifera
Low nitrogen availability is one of the major environmental factors limiting macroalgal growth in temperate marine ecosystems. Macroalgae have overcome the fluctuating nature of nitrogen supply via adjustments to their life-history (e.g. opportunistic versus perennial) and/or their morphophysiology (e.g. type of growth, use of reserves). Fast-growing species dominate when nutrients are elevated but are typically absent in nutrient-poor systems; Macrocystis pyrifera, however, is an exception because it is a perennial species as well as fast-growing. Although its nutrient demands are inherently high (due to its size and productivity), it remains a cosmopolitan species even when nitrogen concentrations are low. The primary objective of this collective work is to refine current knowledge on how the ecophysiology of Macrocystis helps mitigate nitrogen limitation. This is investigated within small communities (i.e. intra-bed mass-transfer) and also within individuals (i.e. endogenous nitrogen use and storage). Nitrogen uptake is enhanced by increased rates of water mass-transfer, which is largely dictated by water flow. Macrocystis beds modify their physical environment so that flow rates are reduced in the bed's interior. To better understand how macroalgae influence mass-transfer rates within kelp beds, the architecture of a model kelp bed is described, highlighting dominant canopy and subcanopy species. These biogenic structures significantly influenced the rates of mass-transfer throughout the bed – rates were highest at the exterior edge and at the surface of the bed, decreasing towards the interior and with depth. Growth and tissue chemistry (e.g. pigmentation, soluble nitrate) of Macrocystis paralleled the intra-bed variability in mass-transfer. This work also provides evidence that the influence of mass-transfer on nitrogen acquisition is a particularly important mechanism when ambient nitrogen is limiting. Growth is described as Macrocystis' first and primary response to nitrogen enrichment. Enrichment studies, however, typically fertilise experimental kelp beyond naturally occurring nitrogen concentrations and the nuances in physiological responses to realistic nitrogen enhancement (e.g. upwelling) are likely masked. To determine how Macrocystis prioritises the use of nitrogen when concentrations are low, the seawater immediately surrounding fronds were enhanced with ecologically relevant pulses of nitrate. The immediate response to fertilisation was not growth, but instead reduced blade erosion and increased pigmentation in canopy tissues. This work suggests that when nitrogen-stressed, Macrocystis first stabilises tissues important to photosynthesis and that growth responses can be delayed for at least one month after initial nitrate pulses. Due to localised increases in pigmentation and soluble nitrate within fronds, this work also highlights potential functional differentiation across tissues. Extended periods of low nitrogen can be mitigated using reserves. The reserve dynamics within whole Macrocystis fronds are poorly understood but suggested to be small. This work aimed to determine which compounds (pigments, soluble nitrate, amino acids) are important nitrogen reserves, in which tissues these pools are stored (six distinct tissues analysed), and how they explain growth. Ultimately, the data suggest that pigments are not an important nitrogen reserve in Macrocystis because maximum concentrations are low compared to other potential reserves, and because they fluctuate in synchrony with ambient seawater nitrate (i.e. no lag time). Soluble nitrate pools in mature blades, however, accrue to high concentrations when ambient nitrogen is replete (winter/early spring) and then nitrate is slowly disseminated to canopy tissues to fuel spring/early summer growth. When ambient nitrogen is low (summer), there is evidence that amino acids are reabsorbed from canopy blades and translocated to basal tissues, perhaps acting as reserve pools for growth in the autumn. This thesis addresses aspects of Macrocystis ecophysiology that are important in mitigating nitrogen limitation. The main findings are (1) that mass-transfer rates within kelp beds are highly variable and that increased mass-transfer is critical in ameliorating limitation events, (2) that Macrocystis uses nitrogen towards tissue maintenance before growth when nitrogen-stressed, facilitating continued nutrient uptake and photosynthesis, and (3) that soluble nitrate and amino acids are important nitrogen reserves, but that the former is more important for spring growth and the latter more important for autumn growth.
Advisor: Hepburn, Christopher
Degree Name: Doctor of Philosophy
Degree Discipline: Marine Science
Publisher: University of Otago
Keywords: kelp; nitrogen; physiology; ecology; ecophysiology; Macrocystis; stable; isotopes; amino; acids; nitrate; temperate reef; New Zealand
Research Type: Thesis