Terminal blades in Macrocystis and their unexplored links to functional biology

Understanding patterns of growth and primary productivity of the giant kelp, Macrocystis pyrifera, is of significant ecological and commercial value. Not only does the biogenic structure of this species provide food and shelter for a multitude of organisms (North 1971), but the floating canopies also allow harvest by boat of tissues for economic pursuits (V asquez et al. 2014). Interest in predicting its productivity is, therefore, not surprising (Jackson 1987, Hadley et al. 2015). Success in doing so is challenged by the inherent difficulty in characterizing the biomass and rates of tissue turnover in a subtidal species as large and complex as Macrocystis. That whole fronds within a thallus are progressively senesced and replaced is widely recognized (North 1971, Lobban 1978, van T€ ussenbroek 1989) and recent work suggests that frond age is an important predictor for rates of frond loss (Rodriguez et al. 2013). Monitoring age structure in Macrocystis, however, is an indirect metric for predicting fluxes in biomass because age is a construct of time without biological input: other factors that interact with time (e.g., abiotic conditions, growth rate) may modulate rates of senescence (Kirkwood and Melov 2011, Mencuccini and Munn e-Bosch 2017). In terrestrial plants, determinate growth is frequently a biological precurser to senescence of the determinate organ and/or initiation of activity in adjacent organs (see Thomas 2013). Although determinate growth in Macrocystis is identifiable via morphological characteristics (North 1971, Arzee et al. 1985, North 1994), the phenomenon has been given minimal attention. In this note, I share observations of the prevalence of determinate growth in Macrocystis and comment on potential research directions that would advance our understanding of giant kelp development, ecophysiology, and predictions of biomass turnover. In 2013 and 2014, I conducted a series of field-based studies, all of which monitored growth rates ofMacrocystis fronds in southeast New Zealand (see Stephens 2015:95; Stephens and Hepburn 2014, 2016). While selecting appropriate fronds to tag and monitor, many of the existing mature fronds (defined as fronds reaching the surface of the water) displayed malformed pneumatocysts (air bladders) at the end of the stipe where the apical meristem is typically located. Instead of the stipe and new blade divisions reducing in thickness and size, asymptotically, towards a cluster of meristematic cells at the stipe apex (Fig. 1a), an elongated or bulbous pneumatocyst (with blade) formed (Fig. 1b–f). It was later determined that these “abnormalities” were likely terminal blades (see North 1971:27; Fig. 1g), which can sometimes lack terminal pneumatocysts (Fig. 1h,i; Arzee et al. 1985). In addition to the suspected terminal blades in my studies, tissues throughout these fronds were often darker (Fig. 1f). Although I did not measure the biomechanical properties of these tissues, they also appeared more brittle (personal observation) compared to tissues in adjacent fronds within the same thallus. Due to the distinct morphology, fronds with putative terminal blades were initially excluded from growth measurements. Despite selecting only Macrocystis fronds with indeterminate apical meristems, numerous tagged kelp developed terminal blades after 30-d of growth. I assessed whether these stipe ends (Fig. 1b–f) reflect terminal blades, and thus determinate growth, by comparing the rates of adult blade elongation, stipe elongation, and new blade production in putative determinate fronds to those that were indeterminate (Fig. 1a). This was necessary because only once has growth in fronds with terminal blade morphology been empirically tested (Arzee et al. 1985), demonstrating a depression in growth in terminal frond tips. Unpublished data from Stephens and Hepburn (2014) show that blade and stipe elongation rates of indeterminate fronds were 1.5-fold and 1.3-fold higher in the summer, respectively, than those of determinate fronds (nested ANOVA, df = 5, P < 0.001; df = 5, P < 0.001), and that the production of new blades was 3.5-fold higher in indeterminate fronds (t test, df = 5, P < 0.001. Note: only indeterminate fronds were tagged for observation and the development of terminal blades occurred sometime during the 30-d period, thus allowing for the formation of new blades prior to determinate transformation). During the winter, blade and stipe elongation rates within indeterminate fronds were 2.1-fold and 0.32-fold higher, respectively (nested ANOVA, df = 5, P < 0.001; df = 5, P = 0.041), and the production of new blades was also higher by 2.3-fold (nested ANOVA, df = 5, P = 0.013). These data support the notion that the terminal blades are, in fact, indicative of determinate growth in Macrocystis. In addition to growth metrics, the expression of terminal blades may not be randomly distributed across time. In one study (Hepburn and Stephens 2014; unpublished data), frond growth was measured across a water motion gradient in two geographically distinct regions (three sites each, n = 90 per site) and across two seasons. Terminal