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Future coral reefs are expected to be subject to higher pCO2 and temperature due to anthropogenic greenhouse gas emissions. Such global stressors are often paired with local stressors thereby potentially modifying the response of organisms. Benthic macroalgae are strong competitors to corals and are assumed to do well under future conditions. The present study aimed to assess the impact of past and future CO2 emission scenarios as well as nutrient enrichment on the growth, productivity, pigment, and tissue nutrient content of the common tropical brown alga Chnoospora implexa. Two experiments were conducted to assess the differential impacts of the manipulated conditions in winter and spring. Chnoospora implexa's growth rate averaged over winter and spring declined with increasing pCO2 and temperature. Furthermore, nutrient enrichment did not affect growth. Highest growth was observed under spring pre-industrial (PI) conditions, while slightly reduced growth was observed under winter A1FI (“business-as-usual”) scenarios. Productivity was not a good proxy for growth, as net O2 flux increased under A1FI conditions. Nutrient enrichment, whilst not affecting growth, led to luxury nutrient uptake that was greater in winter than in spring. The findings suggest that in contrast with previous work, C. implexa is not likely to show enhanced growth under future conditions in isolation or in conjunction with nutrient enrichment. Instead, the results suggest that greatest growth rates for this species appear to be a feature of the PI past, with A1FI winter conditions leading to potential decreases in the abundance of this species from present day levels.
Macroalgae are an integral part of coral reef ecosystems, providing shelter and substratum for many organisms, and food for herbivorous fish and invertebrates (Diaz-Pulido et al. 2007). However, increases in macro-algal production or growth, and biomass accumulation have the potential to destabilize these ecosystems (Nyström et al. 2000) as their ability to compete for space through shading, abrasion, and the release of secondary metabolites may be enhanced (McCook et al. 2001, Smith et al. 2006). Increases in seawater (SW) pCO2 associated with ocean acidification, and increases in eutrophication have both been identified as possible reasons for increased macroalgal productivity and growth (Done 1992, Hoegh-Guldberg et al. 2007, Hughes et al. 2007, 2010). However, algae belong to several different phyla and differ in many aspects of their anatomy and physiology, therefore, species specific approaches to algal ecology and eco-physiology are increasingly important for establishing the potential outlook for macroalgae on coral reefs (Schaffelke 1999, McCook et al. 2001, Jompa and McCook 2003, Bender et al. 2012, Cornwall et al. 2012).
Nutrients associated with eutrophication, especially nitrogen and phosphorus, are introduced to the Great Barrier Reef mainly by rivers and rain (Furnas 2003). Eutrophication, often experimentally simulated as daily/weekly pulses or as a single nutrient pulse, has been shown to increase macroalgal growth in some but not all algae (e.g., Lapointe 1987, Littler et al. 1991). In some algae, nutrients are incorporated, without stimulating either carbon fixation or growth (Gerloff and Krombholz 1966, Schaffelke 1999, Dailer et al. 2012), but with potential implications for palatability (Chan et al. 2012). Often, initial increases in production or growth only occur under typical present-day nutrient concentrations. Kleypas et al. (1999) found that nutrient levels occur between 0–3.34 μM for NO3 and 0–0.54 μM for PO42− for coral reefs worldwide. Others have shown that algal growth stagnates or decreases when concentrations exceed 3.5 μM NH4+ and 0.35 μM PO42− (Schaffelke and Klumpp 1998a, Dailer et al. 2012, Reef et al. 2012). Larger scale in situ experiments have shown mixed responses for biomass accumulation and productivity in response to nutrient enrichment (e.g., Larkum and Koop 1997, Miller et al. 1999, Koop et al. 2001, Smith et al. 2001), highlighting the complexity of the problem of nutrient enrichment and its ecological and physiological interactions.
Increases in atmospheric pCO2 increase (i) global temperature, due to the greenhouse effect of CO2 (IPCC 2007) and (ii) ocean acidification, as atmospheric CO2 equilibrates into the oceans. CO2 entering the oceans increases dissolved inorganic carbon, but due to the decrease in pH, CO2 and CO32− concentrations show the greatest percent change amongst the different carbon species with CO2 increasing and CO32− decreasing (Zeebe and Wolf-Gladrow 2001). Increasing ocean pCO2 has the potential to stimulate photosynthesis by providing more substrate to Ribulose-1,5-bisphosphate carboxylase oxygenase (RUBISCO), the enzyme that fixes CO2 into organic carbon (Beardall et al. 1998).
Brown algae, inclusive of Chnoospora implexa J.Agardh, most likely employ carbon concentrating mechanisms (CCM) involving either direct HCO3− uptake, or uptake of CO2 following conversion from HCO3− by an external carbonic anhydrase (CA), to ultimately increase CO2 concentration at the site of fixation (Surif and Raven 1989, Maberly 1990, Badger et al. 1998, Axelsson et al. 2000, Raven and Hurd 2012). The form of RUBISCO present in brown algae (type 1D) also shows a relatively high selectivity factor for CO2 over O2 (Raven 1997). Both CCM and type 1D RUBISCO should therefore ensure that carbon fixation is sustained at relatively high levels through RUBISCO carboxylase activity, even within an ocean deplete of CO2. Despite this, photorespiration is still active (Larkum et al. 2004). Increasing ocean pCO2 may eliminate some costs associated with the conversion of HCO3− to CO2 (Cornwall et al. 2012), but is unlikely to further enrich CO2 at RUBISCO because photoprotective mechanisms, such as photorespiration, whilst immediately costly in terms of carbon gain, are optimal for carbon gain over the long term in variable natural environments (Murchie and Niyogi 2011).
Within physiological limits, elevated temperatures increase the Vmax of both carboxylase and oxygenase reactions of RUBISCO similarly. However, elevated temperatures also reduce RUBISCO's affinity for CO2 while increasing its relative affinity for O2 (Badger and Collatz 1977, Jordan and Ogren 1984, Badger et al. 2000). As a consequence, the elevation of temperature has the potential to negate or counterbalance potential changes in the rate of carbon fixation by algae residing in CO2 enriched oceans. Outside physiologically acceptable temperature and pH ranges, cellular metabolism is negatively impacted. Often, these physiologically acceptable ranges tend to be associated with local adaptation to the long-term dynamics of a specific habitat and coral reef algae may be living relatively close to their upper thresholds (Humphrey 1975, Mathieson and Dawes 1986). Organisms of the future will have to deal with both warmer and more acidified oceans that may take them outside physiologically acceptable ranges for all or part of the year. Future scenarios based on “reduced” CO2 emission or “business-as-usual” CO2 emission profiles over the next decades tend to define warming as offsets from past or present temperature (IPCC 2007); likewise, it is possible to do the same for future ocean pCO2. By jointly applying these offsets to diurnally and seasonally variable local present conditions, it becomes possible to make relatively sound prediction regarding the fate of these organisms under the different scenarios. Such predictions are needed to inform risk assessments concerning current CO2 emission levels (Harvey et al. 2013).
The present study aimed to assess the response of C. implexa, a brown alga common to the GBR (Rogers 1997, Schaffelke 1999) to combined ocean warming and acidification levels. C. implexa is a mat-forming, corticated and relatively unpalatable alga (Jones 1968) whose main impact on corals is likely to be due to smothering of adult corals and/or inhibition of coral recruits (Birrell et al. 2008). Few herbivores appear to eat it (Jones 1968) making growth rates the most significant feature with respect to its effect on coral reef ecosystems. C. implexa is therefore a good representative for an algae associated with deleterious effects on reefs, irrespective of fishing impacts on herbivores. For the present study, this species was subjected to pre-industrial (PI) conditions and two future IPCC scenarios: a “reduced” CO2 emission scenario (B1); and a “business-as-usual” CO2 emission scenario such as A1FI (IPCC 2007). The study was conducted under ambient levels of inorganic nitrogen and phosphorus, and under elevated levels periodically associated with flood plumes. The experiment was conducted in two different seasons to account for possible temporal differences, as a first step toward understanding the potential annual response of this common macroalga to predicted changes in its local environment.
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In the present study, the response of the brown alga C. implexa to predicted changes in ocean temperature and acidification was explored. The future growth rate of C. implexa was found to be either unchanged, or significantly reduced from present, depending on whether the experiment was performed in the spring month of November or in the winter month of August. Significantly, the results further suggested that optimal growth conditions for this mat-forming alga occurred in the PI past, countering suggestions that algae will “bloom” in the future (e.g., Hoegh-Guldberg et al. 2007, Hughes et al. 2010). Therefore, it seems that not all macroalgal species have similar responses to ocean acidification and warming.
Other studies have investigated the effects of acidification on brown algal growth and have come to opposing conclusions. For example, Diaz-Pulido et al. (2011) found that A1FI-like acidification levels led to decreased growth in Lobophora papenfussii, while Israel and Hophy (2002) found no effect on Sargassum vulgare. It is not clear whether the different responses are species specific or associated with different, but undefined background temperatures, nutrient, and light conditions. Our data, however, suggest that limited or no differential responses between A1FI and present-day are derived because growth has already been significantly impacted since PI times. In the present study, C. implexa, experienced slight reductions in growth in winter under the dual impact of future A1FI warming and acidification. The data suggest, that prior to industrialization, C. implexa potentially exhibited much greater seasonal dynamics than it does today, potentially flourishing in November and hence at a time when its impact on coral recruitment may be at its greatest (Babcock et al. 1986). Clearly, further experiments need to be conducted at more time points and nested within seasons to gather a more accurate picture. The assumption that these algae will be relatively resilient to future conditions, however, appears based on an already shifted baseline.
In contrast with other studies on brown algae, inclusive of C. implexa (e.g., Larned 1998, Schaffelke and Klumpp 1998a,b, Schaffelke 1999), nutrient enrichment appeared to play no role in the elevated growth rates. This disparity may be due to the different experimental designs used: in previous studies nutrients were added as pulses and the experimental period was considerably shorter, whereas in the present study, press nutrient treatments were applied over 1 month. The mean growth rates of C. implexa under enriched November-PI scenarios over nonenriched treatments are slightly but not significantly elevated. This difference in growth rate between enriched- and ambient-PI scenarios is surpassed by the stimulation of growth observed in November-PI scenarios compared with all other scenarios. Potentially, it is the interaction between light, temperature and SW pCO2 that is driving the response, with light levels 20% greater in November than those observed in August, but the photosynthetic apparatus seemingly only able to take advantage of the greater light availability when temperature and pCO2 are both relatively low. At present, C. implexa cover at the study site is highest in the month of December (Rogers 1997), but the present data also suggest that the late spring period is not necessarily also the period of greater growth under present-day conditions.
The importance of the timing of the experiment as well as the applied scenario conditions is reflected in all productivity measurements (dark-adapted Fv/Fm, Pnmax and Rdark). The dark-adapted Fv/Fm showed a similar trend as the growth data, due to its tendency to be elevated in the November-PI scenario and relatively low in the August-A1FI scenario. The opposing patterns observed for dark-adapted Fv/Fm and O2 flux (Pnmax and Pgross, Pgross not shown) are unexpected. In the short term, dark-adapted Fv/Fm is typically reduced following closure of reaction centers (RC) and under conditions that lead to an imbalance between light harvested and photochemical quenching capability (Genty et al. 1989). Frequently, the response to such conditions is to increase nonphotochemical quenching (NPQ); rerouting captured light energy to heat prior to its activation of the RC and hence O2 evolution (Müller et al. 2001). Both the closure of RCs and the activation of NPQ should reduce O2 evolution, that is, Fv/Fm and O2 evolution should work in concert. Decoupling of dark-adapted Fv/Fm and O2 flux responses has previously been observed for Palmaria palmata, in this case constant O2 flux gave way to decreased O2 flux only when Fv was reduced by 40% (Hanelt and Nultsch 1995). In the present case, however, the relationship between Fv/Fm and O2 flux are opposite for different PI- and A1FI-scenarios in different seasons and established over a 4 week period, suggesting the establishment of significant differences in photosystem dynamics between treatments. Furthermore, the disparity between fluorescent and O2 flux measurement is not solved by reference to respiration rates (Rdark or Light-enhanced dark respiration, results not shown for the latter) as they follow a similar trend as Pnmax and Pgross.
C. implexa grew profusely under November-PI conditions, but, Pnmax was greatest under November-A1FI conditions. An uncoupling between biomass accumulation and growth rate has been observed in other studies (e.g., Israel et al. 1999 and Xu and Gao 2012) and in at least one species this has been attributed to changes in carbon allocation (Gordillo et al. 2001). Likewise, changes in resource allocation may have occurred in C. implexa, where Rdark tended to be greater under November-A1FI, suggesting that much of the carbon accumulated by day is respired by night, as opposed to converted into biomass for growth. Furthermore, there is a tendency for the amount of carbon per dry weight of tissue to be less in the PI and present-day treatments than in the B1 or A1FI treatments, suggesting a bias against the formation of carbon storage compounds such as laminarin and fatty acids (Michel et al. 2010, Gardner et al. 2013). This bias is especially noticeable in the contrast between nutrient-enriched versus ambient treatments. In this case, algal tissue from enriched treatments, irrespective of experimental time point or scenario, are relatively deplete in carbon and enriched in both nitrogen and phosphorus, clearly demonstrating that the enrichment was assimilated by the algae, even if it did not lead to differential growth. The reduction in tissue carbon content observed under nutrient addition may have been caused by its release as dissolved organic carbon; this has been suggested for various other tropical algal species under seasonal nutrient enrichment (Wild et al. 2008).
The nitrogen assimilated into the tissue of C. implexa can be stored as inorganic nitrogen, used in nitrogen rich pigments such as Chl a, or amino acids and proteins (Chapman and Craigie 1977, Wheeler and North 1980, Bird et al. 1982). The present results suggest that the additional nitrogen is not used for Chl a synthesis in C. implexa because (i) no increase was observed with nutrient addition and (ii) winter Chl a concentration decreased under nutrient addition. This leaves proteins, amino acids, and inorganic nitrogen storage as possible nutrient sinks. The relative xanthophyll pool, that does not include nitrogen as a component, increased with nutrient enrichment, but this response was principally driven by the reduction in Chl a levels, rather than an increase in xanthophyll synthesis. Interestingly, neither reduction in Chl a nor the increase in the relative xanthophyll pool appeared to have consistent effects on either dark-adapted Fv/Fm or Pnmax. This possibly suggests that NPQ in the light-harvesting antennae may not be the dominant photoprotective mechanism employed by this alga (Niyogi 1999). The increase in β-carotene concentration may be related to several factors such as light intensity and quality and has also been correlated with the biosynthesis of chlorophylls (Bohne and Linden 2002).
The nutritional status of the algal tissue not only alters concentrations of inorganic and organic compounds within the organism, but also changes its nutritional value. In C. implexa, the addition of ammonium and phosphate mainly led to more tissue nitrogen and phosphorus in both experiments, indicating luxury nutrient uptake as opposed to investment into new tissue as observed by Schaffelke (1999). A trade-off between new tissue synthesis (growth) versus nutrient enrichment of current tissue was observed between November and August experiments with growth promoted in November and tissue enrichment promoted in August. Higher nutrient content in algae has also been correlated with higher palatability for herbivores and even species with relatively low palatability have recently been shown to follow this trend (Diaz-Pulido 2003, Chan et al. 2012). Therefore, it is possible that this species may be increasingly grazed upon following nutrient enrichment and this may be more pronounced in winter than in spring. Further studies involving behavioral feeding experiments with herbivores are required to support this hypothesis.
Growth is the key response variable examined in this study on the effect of CO2 emission scenarios and nutrient enrichment on C. implexa. Growth was greatest under past spring conditions, a finding that is in contrast with current predictions (Hoegh-Guldberg et al. 2007, Hughes et al. 2010). This suggests that C. implexa is not likely to pose an increasing threat in the future. Furthermore, nutrient enrichment led to comparatively small changes in the measured parameters and did not cause significant biomass increases. Under A1FI conditions, winter growth rates were further reduced from PD and B1 scenarios, suggesting further reductions to the threat posed to reefs by this alga. Clearly, other coral competitors may fill the void, either other algae such as cyanobacteria (Paerl and Huisman 2009, Diaz-Pulido et al. 2011), or potentially other organisms such as soft corals, or sponges, inclusive of bioeroding sponges, that may have even greater negative impacts on aspects of reefs such as their carbonate balance (Nyström et al. 2008, Wisshak et al. 2012, Gabay et al. 2013, Fang et al. 2013). The assumed persistence of macroalgae as a group and their inferred superiority to cope with future conditions is not universal, and needs to be reassessed relative to other competitor groups to more reliably predict the fate of future reefs.
The present results provide insights into the way C. implexa may be affected by future changes, whilst highlighting the importance of temporal effects. In light of this study, it is important to expand the scope of future studies to include all seasons, as impacts and interactions are likely to vary throughout the year. Interactions amongst environmental factors appear to dominate the response of this alga, highlighting the necessity to investigate the impact of environmental factors in conjunction, rather than in an isolated fashion, especially if our aim is to gain insight into the future fate of coral reefs (Harvey et al. 2013).