Vegetative Reproduction Is More Advantageous Than Sexual Reproduction in a Canopy-Forming Clonal Macroalga under Ocean Warming Accompanied by Oligotrophication and Intensive Herbivory

Ocean warming and the associated changes in fish herbivory have caused polarward distributional shifts in the majority of canopy-forming macroalgae that are dominant in temperate Japan, but have little effect on the alga Sargassum fusiforme. The regeneration ability of new shoots from holdfasts in this species may be advantageous in highly grazed environments. However, little is known about the factors regulating this in Sargassum species. Moreover, holdfast tolerance to high-temperature and nutrient-poor conditions during summer has rarely been evaluated. In the present study, S. fusiforme holdfast responses to the combined effects of temperature and nutrient availability were compared to those of sexually reproduced propagules. The combined effects of holdfast fragmentation and irradiance on regeneration were also evaluated. Propagule growth rate values changed from positive to negative under the combination of elevated temperature (20 °C–30 °C) and reduced nutrient availability, whereas holdfasts exhibited a positive growth rate even at 32 °C in nutrient-poor conditions. The regeneration rate increased with holdfast fragmentation (1 mm segments), but was unaffected by decreased irradiance. These results suggest that S. fusiforme holdfasts have a higher tolerance to high-temperature and nutrient-poor conditions during summer than propagules, and regenerate new shoots even if 1-mm segments remain in shaded refuges for fish herbivory avoidance.

First insights into the impacts of benthic cyanobacterial mats on fish herbivory functions on a nearshore coral reef

Benthic cyanobacterial mats (BCMs) are becoming increasingly common on coral reefs. In Fiji, blooms generally occur in nearshore areas during warm months but some are starting to prevail through cold months. Many fundamental knowledge gaps about BCM proliferation remain, including their composition and how they influence reef processes. This study examined a seasonal BCM bloom occurring in a 17-year-old no-take inshore reef area in Fiji. Surveys quantified the coverage of various BCM-types and estimated the biomass of key herbivorous fish functional groups. Using remote video observations, we compared fish herbivory (bite rates) on substrate covered primarily by BCMs (> 50%) to substrate lacking BCMs (< 10%) and looked for indications of fish (opportunistically) consuming BCMs. Samples of different BCM-types were analysed by microscopy and next-generation amplicon sequencing (16S rRNA). In total, BCMs covered 51 ± 4% (mean ± s.e.m) of the benthos. Herbivorous fish biomass was relatively high (212 ± 36 kg/ha) with good representation across functional groups. Bite rates were significantly reduced on BCM-dominated substratum, and no fish were unambiguously observed consuming BCMs. Seven different BCM-types were identified, with most containing a complex consortium of cyanobacteria. These results provide insight into BCM composition and impacts on inshore Pacific reefs.

Dynamics of carbonate sediment production by Halimeda: implications for reef carbonate budgets

Reef carbonate production and sediment generation are key processes for coral reef development and shoreline protection. The calcified green alga Halimeda is a major contributor of calcareous sediments, but rates of production and herbivory upon Halimeda are driven by biotic and environmental factors. Consequently, estimating rates of calcium carbonate (CaCO3) production and transformation into sediment requires the integration of Halimeda gains and losses across habitats and seasons, which is rarely considered in carbonate budgets. Using seasonal rates of recruitment, growth, senescence and herbivory derived from observations and manipulative experiments, we developed an individual-based model to quantify the annual cycle of Halimeda carbonate and sediment production at Heron Island, Great Barrier Reef. Halimeda population dynamics were simulated both within and outside branching Acropora canopies, which provide refuge from herbivory. Shelter from herbivory allowed larger Halimeda thalli to grow, leading to higher rates of carbonate accumulation (3.9 and 0.9 kg CaCO3 m-2 yr-1 within and outside Acropora canopies, respectively) and sediment production (2.5 versus 1.0 kg CaCO3 m-2 yr-1, respectively). Overall, 37% of the annual carbonate production was transformed into sediments through senescence (84%) and fish herbivory (16%), with important variations among seasons and habitats. Our model underlines that algal rates of carbonate production are likely to be underestimated if herbivory is not integrated into the carbonate budget, and reveals an important indirect pathway by which structurally complex coral habitats contribute to reef carbonate budgets, suggesting that coral losses due to climate change may lead to further declines in reef sediment production.

Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp

Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical–temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.

The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to ‘barrens’ when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.

Fifty million years of herbivory on coral reefs: fossils, fish and functional innovations

The evolution of ecological processes on coral reefs was examined based on Eocene fossil fishes from Monte Bolca, Italy and extant species from the Great Barrier Reef, Australia. Using ecologically relevant morphological metrics, we investigated the evolution of herbivory in surgeonfishes (Acanthuridae) and rabbitfishes (Siganidae). Eocene and Recent surgeonfishes showed remarkable similarities, with grazers, browsers and even specialized, long-snouted forms having Eocene analogues. These long-snouted Eocene species were probably pair-forming, crevice-feeding forms like their Recent counterparts. Although Eocene surgeonfishes likely played a critical role as herbivores during the origins of modern coral reefs, they lacked the novel morphologies seen in modern Acanthurus and Siganus (including eyes positioned high above their low-set mouths). Today, these forms dominate coral reefs in both abundance and species richness and are associated with feeding on shallow, exposed algal turfs. The radiation of these new forms, and their expansion into new habitats in the Oligocene–Miocene, reflects the second phase in the development of fish herbivory on coral reefs that is closely associated with the exploitation of highly productive short algal turfs.