Amelioration of ocean acidification and warming effects through physiological buffering of a macroalgae

Concurrent anthropogenic global climate change and ocean acidification are expected to have a negative impact on calcifying marine organisms. While knowledge of biological responses of organisms to oceanic stress has emerged from single-species experiments, these do not capture ecologically relevant scenarios where the potential for multi-organism physiological interactions is assessed. Marine algae provide an interesting case study, as their photosynthetic activity elevates pH in the surrounding microenvironment, potentially buffering more acidic conditions for associated epiphytes. We present findings that indicate increased tolerance of an important epiphytic for aminifera, Marginopora vertebralis, to the effects of increased temperature (+/- 3 degrees C) and p CO2(similar to 1,000 mu atm) when associated with its common algal host, Laurencia intricata. Specimens of M. vertebralis were incubated for 15 days in flow-through aquaria simulating current and end-of-century temperature and pH conditions. Physiological measures of growth (change in wet weight), calcification (measured change in total alkalinity in closed bottles), photochemical efficiency (Fv/Fm), total chlorophyll, photosynthesis (oxygen flux), and respiration were determined. When incubated in isolation,M. vertebralis-exhibited reduced growth in end-of-century projections of ocean acidification conditions, while calcification rates were lowest in the high-temperature, low-pH treatment. Interestingly, association with L. intricata ameliorated these stress effects with the growth and calcification rates ofM. vertebralis being similar to those observed in ambient conditions. Total chlorophyll levels in M. vertebral is decreased when in association with L. intricata, while maximum photochemical efficiency increased in ambient conditions. Net production estimates remained similar between M. vertebralis in isolation and in association with L. intricata, although both production and respiration rates ofM. vertebralis were significantly higher when associated with L. intricata. These results indicate that the association with L. intricata increases the resilience ofM. vertebralis to climate change stress, providing one of the first examples of physiological buffering by a marine alga that can ameliorate the negative effects of changing ocean conditions

Ocean warming has greater and more consistent negative effects than ocean acidification on the growth and health of subtropical macroalgae

Macroalgae are the major habitat-forming organisms in many coastal temperate and subtropical marine systems. Although climate change has been identified as a major threat to the persistence of macroalgal beds, the combined effects of ocean warming and ocean acidification on algal performance are poorly understood. Here we investigate the effects of increased temperature and acidification on the growth, calcification and nutritional content of 6 common subtropical macroalgae; Sargassum linearifolium, Ulva sp., Amphiroa anceps, Corallina officinalis, Delisea pulchra and Laurencia decussata. Algae were reared in a factorial cross of 3 temperatures (23°C [ambient], 26°C and 28°C) and 3 pH levels (8.1 [ambient], 7.8 and 7.6) for 2 wk. The highest (28°C) temperature decreased the growth of all 6 macroalgal species, irrespective of the pH levels. In contrast, the effect of decreased pH on growth was variable. The growth of Ulva sp. and C. officinalis increased, L. decussata decreased, while the remaining 3 species were unaffected. Interestingly, the differential responses of macroalgae to ocean acidification were unrelated to whether or not a species was a calcifying alga, or their carbon-uptake mechanism—2 processes that are predicted to be sensitive to decreased pH. The growth of the calcifying algae (C. officinalis and A. anceps) was not affected by reduced pH but calcification of these 2 algae was reduced when exposed to a combination of reduced pH and elevated temperature. The 3 species capable of uptake of bicarbonate, S. linearifolium, L. decussata and Ulva sp., displayed positive, negative and neutral changes in growth, respectively, in response to reduced pH. The C:N ratio for 5 of the 6 species was unaffected by either pH or temperature. The consistent and predictable negative effects of temperature on the growth and calcification of subtropical macroalgae suggests that this stressor poses a greater threat to the persistence of subtropical macroalgal populations than ocean acidification under ongoing and future climate change

Habitat and fishing control grazing potential on coral reefs

Herbivory is a key process on coral reefs, which, through grazing of algae, can help sustain coral‐dominated states on frequently disturbed reefs and reverse macroalgal regime shifts on degraded ones. Our understanding of herbivory on reefs is largely founded on feeding observations at small spatial scales, yet the biomass and structure of herbivore populations is more closely linked to processes which can be highly variable across large areas, such as benthic habitat turnover and fishing pressure. Though our understanding of spatiotemporal variation in grazer biomass is well developed, equivalent macroscale approaches to understanding bottom‐up and top‐down controls on herbivory are lacking. Here, we integrate underwater survey data of fish abundances from four Indo‐Pacific island regions with herbivore feeding observations to estimate grazing rates for two herbivore functions, cropping (which controls turf algae) and scraping (which promotes coral settlement by clearing benthic substrate), for 72 coral reefs. By including a range of reef states, from coral to algal dominance and heavily fished to remote wilderness areas, we evaluate the influences of benthic habitat and fishing on the grazing rates of fish assemblages. Cropping rates were primarily influenced by benthic condition, with cropping maximized on structurally complex reefs with high substratum availability and low macroalgal cover. Fishing was the primary driver of scraping function, with scraping rates depleted at most reefs relative to remote, unfished reefs, though scraping did increase with substratum availability and structural complexity. Ultimately, benthic and fishing conditions influenced herbivore functioning through their effect on grazer biomass, which was tightly correlated to grazing rates. For a given level of biomass, we show that grazing rates are higher on reefs dominated by small‐bodied fishes, suggesting that grazing pressure is greatest when grazer size structure is truncated. Stressors which cause coral declines and clear substrate for turf algae will likely stimulate increases in cropping rates, in both fished and protected areas. In contrast, scraping functions are already impaired at reefs inhabited by people, particularly where structural complexity has collapsed, indicating that restoration of these key processes will require scraper biomass to be rebuilt towards wilderness levels

Density and height of Sargassum influence rabbitfish (f. Siganidae) settlement on inshore reef flats of the Great Barrier Reef

Macroalgal beds have been suggested to be an important settlement habitat for a diversity of reef fishes, yet few studies have considered how the composition or structure of macroalgal beds may influence fish settlement. The aim of this study was to investigate how the physical characteristics of Sargassum beds, a common macroalga on inshore coral reefs, influence the abundance of recently-settled rabbitfishes (Siganidae) on Orpheus Island, Great Barrier Reef. The abundance of recently-settled rabbitfish (< 3 cm total length), the density and height of Sargassum thalli, and benthic composition were quantified within replicate 1-m(2) quadrats across 15 mid-reef flat sites. A total of 419 recently-settled rabbitfish from three species (Siganus doliatus, S. lineatus and S. canaliculatus) were recorded across 150 quadrats (range 0-16 individuals m(-2)), with S. doliatus accounting for the majority (85.2%) of individuals recorded. The abundance of S. doliatus and S. lineatus was greatest at moderate Sargassum densities (ca. 20-30 holdfasts m(-2)) and generally increased with Sargassum height and the cover of 'other' macroalgae. These findings demonstrate the potential importance of the physical characteristics of macroalgal beds to the settlement of rabbitfishes on inshore reef flats

Larval phenotypic plasticity in the boom-and-bust crown-of-thorns seastar, Acanthaster planci

Many echinoderm larvae exhibit phenotypic plasticity: a change in phenotype in response to environmental food levels. We investigated phenotypic plasticity in the larvae of the crown-of-thorns seastar Acanthaster planci, an opportunistic boom-and-bust species with larvae that have a strong response to food conditions. The increased predation pressure resulting from outbreaks (population explosions) of A. planci is deleterious to coral reefs, but the link between population outbreaks and larval ecology is poorly understood. We hypothesised that the larvae of A. planci would have a different morphological profile in the oligotrophic conditions typical of tropical waters than in the eutrophic conditions associated with increased nutrients. We predicted that larvae reared in low food conditions would increase their ciliated band length to enhance feeding potential. Larvae were fed algal concentrations representing starvation (0 cells ml-1), low food (oligotrophic; 1000 cells ml-1), high food (eutrophic; 10000 cells ml-1) or excessive food (100000 cells ml-1) conditions. A phenotypic response was evident. Larvae in the 2 high food treatments had a shorter ciliated band length relative to body size. Conversely, larvae in the starvation and low food treatments had longer ciliated bands relative to body size, a change that would enhance particle capture capacity and facilitate larval success. This plastic response of the larvae of A. planci could have flow-on effects to adult populations, potentially facilitating population outbreaks

Superstars: assessing nutrient thresholds for enhanced larval success of Acanthaster planci, a review of the evidence

Crown-of-thorns starfish, Acanthaster planci (COTS), predation is a major cause of coral reef decline, but the factors behind their population outbreaks remain unclear. Increased phytoplankton food resulting from eutrophication is suggested to enhance larval survival. We addressed the hypothesis that larval success is associated with particular chl-a levels in tightly controlled larval:algal conditions. We used chl-a conditions found on coral reefs (0.1-5.0μgchl-aL(-1)), including nominal threshold levels for disproportionate larval success (≥1.0μgchl-aL(-1)). High success to the juvenile occurred across an order of magnitude of chl-a concentrations (0.5-5.0μgchl-aL(-1)), suggesting there may not be a narrow value for optimal success. Oligotrophic conditions (0.1μgchl-aL(-1)) appeared to be a critical limit. With a review of the evidence, we suggest that opportunistic COTS larvae may be more resilient to low food levels than previously appreciated. Initiation of outbreak populations need not require eutrophic conditions

Regions on the Great Barrier Reef where hotspots of <i>Acanthaster planci</i> outbreaks occur (Wet Tropics, Burdekin, Fitzroy), with indication of coastal, mid-shelf and offshore reefs.

<p>The ‘initiation box’ for <i>A</i>. <i>planci</i> outbreaks between Cooktown and Cairns [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122010#pone.0122010.ref012" target="_blank">12</a>] is indicated by the rectangle.</p

Levels of chl <i>a</i> (μg L^-1) on the Great Barrier Reef where hotspots of <i>Acanthaster planci</i> outbreaks occur (Wet Tropics, Burdekin and Fitzroy), when larvae would be expected in the plankton (November-March).

<p>Average (a) natural chl <i>a</i> from 2011–2014 (n = 20; ±se), and (b) mean and (c) maximum chl <i>a</i> recorded for the week following major cyclone or flood events between 2009–2014 (n = 7; ±se). Data sourced from eReefs (<a href="http://www.bom.gov.au/marinewaterquality/" target="_blank">http://www.bom.gov.au/marinewaterquality/</a>).</p

Average (a) percent settlement and (b) size of recently settled <i>Acanthaster planci</i> juveniles at day 18, following rearing larval rearing in five algal concentrations represented as chl <i>a</i> concentration (μg L^-1) across all settlement assays (±se).

<p>Tukey’s HSD test: levels not connected by the same letter are significantly different.</p

Larval (a) length and (b) width for <i>Acanthaster planci</i> reared in five algal concentrations, represented as chl <i>a</i> concentration (μg L^-1) on days 4, 7 and 10 (n = 10).

<p>Boxes represent the interquartile range (25 and 75^th percentile), the horizontal line is the median, and the whiskers represent the data range. Tukey’s HSD test: levels not connected by the same letter are significantly different (within each day).</p