Effect of marine heatwaves and warming on kelp microbiota influence trophic interactions.

The range-expansion of tropical herbivores due to ocean warming can profoundly alter temperate reef communities by overgrazing the seaweed forests that underpin them. Such ecological interactions may be mediated by changes to seaweed-associated microbiota in response to warming, but empirical evidence demonstrating this is rare. We experimentally simulated ocean warming and marine heatwaves (MHWs) to quantify effects on two dominant temperate seaweed species and their microbiota, as well as grazing by a tropical herbivore. The kelp Ecklonia radiata's microbiota in sustained warming and MHW treatments was enriched with microorganisms associated with seaweed disease and tissue degradation. In contrast, the fucoid Sargassum linearifolium's microbiota was unaffected by temperature. Consumption by the tropical sea-urchin Tripneustes gratilla was greater on Ecklonia where the microbiota had been altered by higher temperatures, while Sargassum's consumption was unaffected. Elemental traits (carbon, nitrogen), chemical defences (phenolics) and tissue bleaching of both seaweeds were generally unaffected by temperature. Effects of warming and MHWs on seaweed holobionts (host plus its microbiota) are likely species-specific. The effect of increased temperature on Ecklonia's microbiota and subsequent increased consumption suggest that changes to kelp microbiota may underpin kelp-herbivore interactions, providing novel insights into potential mechanisms driving change in species' interactions in warming oceans.

Tropicalization shifts herbivore pressure from seagrass to rocky reef communities.

Climate-driven species redistributions are reshuffling the composition of marine ecosystems. How these changes alter ecosystem functions, however, remains poorly understood. Here we examine how impacts of herbivory change across a gradient of tropicalization in the Mediterranean Sea, which includes a steep climatic gradient and marked changes in plant nutritional quality and fish herbivore composition. We quantified individual feeding rates and behaviour of 755 fishes of the native Sarpa salpa, and non-native Siganus rivulatus and Siganus luridus. We measured herbivore and benthic assemblage composition across 20 sites along the gradient, spanning 30° of longitude and 8° of latitude. We coupled patterns in behaviour and composition with temperature measurements and nutrient concentrations to assess changes in herbivory under tropicalization. We found a transition in ecological impacts by fish herbivory across the Mediterranean from a predominance of seagrass herbivory in the west to a dominance of macroalgal herbivory in the east. Underlying this shift were changes in both individual feeding behaviour (i.e. food choice) and fish assemblage composition. The shift in feeding selectivity was consistent among temperate and warm-affiliated herbivores. Our findings suggest herbivory can contribute to the increased vulnerability of seaweed communities and reduced vulnerability of seagrass meadows in tropicalized ecosystems.

Resilience of seagrass populations to thermal stress does not reflect regional differences in ocean climate.

The prevalence of local adaptation and phenotypic plasticity among populations is critical to accurately predicting when and where climate change impacts will occur. Currently, comparisons of thermal performance between populations are untested for most marine species or overlooked by models predicting the thermal sensitivity of species to extirpation. Here we compared the ecological response and recovery of seagrass populations (Posidonia oceanica) to thermal stress throughout a year-long translocation experiment across a 2800-km gradient in ocean climate. Transplants in central and warm-edge locations experienced temperatures > 29°C, representing thermal anomalies > 5°C above long-term maxima for cool-edge populations, 1.5°C for central and < 1°C for warm-edge populations. Cool-edge, central and warm-edge populations differed in thermal performance when grown under common conditions, but patterns contrasted with expectations based on thermal geography. Cool-edge populations did not differ from warm-edge populations under common conditions and performed significantly better than central populations in growth and survival. Our findings reveal that thermal performance does not necessarily reflect the thermal geography of a species. We demonstrate that warm-edge populations can be less sensitive to thermal stress than cooler, central populations suggesting that Mediterranean seagrasses have greater resilience to warming than current paradigms suggest.

Host genetics, phenotype and geography structure the microbiome of a foundational seaweed.

Interactions between hosts and their microbiota are vital to the functioning and resilience of macro-organisms. Critically, for hosts that play foundational roles in communities, understanding what drives host-microbiota interactions is essential for informing ecosystem restoration and conservation. We investigated the relative influence of host traits and the surrounding environment on microbial communities associated with the foundational seaweed Phyllospora comosa. We quantified 16 morphological and functional phenotypic traits, including host genetics (using 354 single nucleotide polymorphisms) and surface-associated microbial communities (using 16S rRNA gene amplicon sequencing) from 160 individuals sampled from eight sites spanning Phyllospora's entire latitudinal distribution (1,300 km). Combined, these factors explained 54% of the overall variation in Phyllospora's associated microbial community structure, much of which was related to the local environment (~32%). We found that putative "core" microbial taxa (i.e., present on all Phyllospora individuals sampled) exhibited slightly higher associations with host traits when compared to "variable" taxa (not present on all individuals). We identified several key genetic loci and phenotypic traits in Phyllospora that were strongly related to multiple microbial amplicon sequence variants, including taxa with known associations to seaweed defence, disease and tissue degradation. This information on how host-associated microbial communities vary with host traits and the environment enhances our current understanding of how "holobionts" (hosts plus their microbiota) are structured. Such understanding can be used to inform management strategies of these important and vulnerable habitats.

Persistent thermally driven shift in the functional trait structure of herbivorous fishes: Evidence of top-down control on the rebound potential of temperate seaweed forests?

Extreme climatic events can reshape the functional structure of ecological communities, potentially altering ecological interactions and ecosystem functioning. While these shifts have been widely documented, evidence of their persistence and potential flow-on effects on ecosystem structure following relaxation of extreme events remains limited. Here, we investigate changes in the functional trait structure - encompassing dimensions of resource use, thermal affinity, and body size - of herbivorous fishes in a temperate reef system that experienced an extreme marine heatwave (MHW) and subsequent return to cool conditions. We quantify how changes in the trait structure modified the nature and intensity of herbivory-related functions (macroalgae, turf, and sediment removal), and explored the potential flow-on effects on the recovery dynamics of macroalgal foundation species. The trait structure of the herbivorous fish assemblage shifted as a result of the MHW, from dominance of cool-water browsing species to increased evenness in the distribution of abundance among temperate and tropical guilds supporting novel herbivory roles (i.e. scraping, cropping, and sediment sucking). Despite the abundance of tropical herbivorous fishes and intensity of herbivory-related functions declined following a period of cooling after the MHW, the underlying trait structure displayed limited recovery. Concomitantly, algal assemblages displayed a lack of recovery of the formerly dominant foundational species, the kelp Ecklonia radiata, transitioning to an alternative state dominated by turf and Sargassum spp. Our study demonstrates a legacy effect of an extreme MHW and exemplified the value of monitoring phenotypic (trait mediated) changes in the nature of core ecosystem processes to predict and adapt to the future configurations of changing reef ecosystems.

Persistence of seaweed forests in the anthropocene will depend on warming and marine heatwave profiles.

Marine heatwaves (MHWs), discrete periods of extreme warm water temperatures superimposed onto persistent ocean warming, have increased in frequency and significantly disrupted marine ecosystems. While field observations on the ecological consequences of MHWs are growing, a mechanistic understanding of their direct effects is rare. We conducted an outdoor tank experiment testing how different thermal stressor profiles impacted the ecophysiological performance of three dominant forest-forming seaweeds. Four thermal scenarios were tested: contemporary summer temperature (22°C), low persistent warming (24°C), a discrete MHW (22-27°C), and temperature variability followed by a MHW (22-24°C, 22-27°C). The physiological performance of seaweeds was strongly related to thermal profile and varied among species, with the highest temperature not always having the strongest effect. MHWs were highly detrimental for the fucoid Phyllospora comosa, whereas the laminarian kelp Ecklonia radiata showed sensitivity to extended thermal stress and demonstrated a cumulative temperature threshold. The fucoid Sargassum linearifolium showed resilience, albeit with signs of decline with bleached and degraded fronds, under all conditions, with stronger decline under stable control and warming conditions. The varying responses of these three co-occurring forest-forming seaweeds under different temperature scenarios suggests that the impact of ocean warming on near shore ecosystems may be complex and will depend on the specific thermal profile of rising water temperatures relative to the vulnerability of different species.

Genomic vulnerability of a dominant seaweed points to future-proofing pathways for Australia's underwater forests.

Globally, critical habitats are in decline, threatening ecological, economic and social values and prompting calls for 'future proofing' efforts that enhance resilience to climate change. Such efforts rely on predicting how neutral and adaptive genomic patterns across a species' distribution will change under future climate scenarios, but data is scant for most species of conservation concern. Here, we use seascape genomics to characterise genetic diversity, structure and gene-environmental associations in a dominant forest-forming seaweed, Phyllospora comosa, along its entire latitudinal (12° latitude), and thermal (~14°C) range. Phyllospora showed high connectivity throughout its central range, with evidence of genetic structure and potential selection associated with sea surface temperatures (SSTs) at its rear and leading edges. Rear and leading-edge populations harboured only half the genetic diversity of central populations. By modelling genetic turnover as a function of SST, we assessed the genomic vulnerability across Phyllospora's distributional range under climate change scenarios. Despite low diversity, range-edge populations were predicted to harbour beneficial adaptations to marginal conditions and overall adaptability of the species may be compromised by their loss. Assisted gene flow from range edge populations may be required to enhance adaptation and increase resilience of central and leading-edge populations under warming oceans. Understanding genomic vulnerability can inform proactive restoration and future-proofing strategies for underwater forests and ensure their persistence in changing oceans.

Tropicalization and kelp loss shift trophic composition and lead to more winners than losers in fish communities.

Climate-mediated species redistributions are causing novel interactions and leading to profound regime shifts globally. For species that expand their distribution in response to warming, survival depends not only on their physiological capacity, but also on the ability to coexist or be competitive within the established community. In temperate marine reefs from around the world, the range expansion of tropical species, known as 'tropicalization', has been linked to the disappearance of temperate habitat-forming kelps and shifts to dominance by low-biomass turfing algae. The consequences of these range expansions and habitat changes on resident fish communities are, however, unclear. Here, we use data derived from baited remote underwater video (BRUV) surveys to analyse changes in diversity and abundance of marine fishes over a 17-year period in warming reefs that have experienced kelp loss (occurring c. 2009). Despite the loss of kelp, we found that species richness and overall abundance of fishes (measured as probability of occurrence and relative abundance), including both tropical and temperate species, increased through time. We also found dramatic shifts in the trophic composition of fish assemblages. Tropical herbivorous fish increased most markedly through time, and temperate-associated planktivores were the only group that declined, a potential consequence of tropicalization not previously identified. At the species level, we identified 22 tropical and temperate species from four trophic guilds that significantly increased in occurrence, while only three species (all temperate associated) declined. Morphological trait space models suggest increases in fish diversity and overall occurrence are unlikely to be driven by uniqueness of traits among tropical range expanders. Our results show more winners than losers and suggest that pathways of energy flow will change in tropicalized systems, as planktonic inputs become less important and a higher proportion of algal productivity gets consumed locally by increasingly abundant herbivores.

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.

Accelerating Tropicalization and the Transformation of Temperate Seagrass Meadows.

Climate-driven changes are altering production and functioning of biotic assemblages in terrestrial and aquatic environments. In temperate coastal waters, rising sea temperatures, warm water anomalies and poleward shifts in the distribution of tropical herbivores have had a detrimental effect on algal forests. We develop generalized scenarios of this form of tropicalization and its potential effects on the structure and functioning of globally significant and threatened seagrass ecosystems, through poleward shifts in tropical seagrasses and herbivores. Initially, we expect tropical herbivorous fishes to establish in temperate seagrass meadows, followed later by megafauna. Tropical seagrasses are likely to establish later, delayed by more limited dispersal abilities. Ultimately, food webs are likely to shift from primarily seagrass-detritus to more direct-consumption-based systems, thereby affecting a range of important ecosystem services that seagrasses provide, including their nursery habitat role for fishery species, carbon sequestration, and the provision of organic matter to other ecosystems in temperate regions.

Congruence of intraspecific variability in leaf traits for two co-occurring estuarine angiosperms.

Studies seeking to identify sources of variability and trade-offs in leaf traits have done so by assembling large databases of traits, across species and time points. It is unclear to what extent interspecific patterns derived in such a manner apply to intraspecific variation, particularly at regional scales, and the extent to which interspecific patterns vary temporally. We tested the hypothesis that the leaf traits of two foundation species, the mangrove Avicennia marina and the eelgrass Zostera muelleri, would display similar patterns of intraspecific variability across gradients of latitude and estuarine condition, that match previously reported interspecific patterns, and that persist through time. We found intraspecific patterns of decreasing carbon to nitrogen ratio and mechanical elasticity, and increasing nitrogen content with latitude that were consistent between the two plant species, and with previously reported interspecific patterns for other groups of species. Specific leaf area, leaf toughness and total phenolics, by contrast, displayed species-specific patterns that varied markedly through time. Relationships between estuarine condition and leaf traits were highly variable temporally, and also displayed markedly different patterns of intraspecific variability between the two species. Our study highlights the considerable within-species variation in leaf traits that should be accounted for in regional to biome scale analyses. Although some intraspecific patterns mirrored those found across species, at global scales, the considerable variability in other leaf traits between species and through time highlights the need to better understand the drivers and constraints of this intraspecific variation.

Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography.

Interactions between hosts and associated microbial communities can fundamentally shape the development and ecology of 'holobionts', from humans to marine habitat-forming organisms such as seaweeds. In marine systems, planktonic microbial community structure is mainly driven by geography and related environmental factors, but the large-scale drivers of host-associated microbial communities are largely unknown. Using 16S-rRNA gene sequencing, we characterized 260 seaweed-associated bacterial and archaeal communities on the kelp Ecklonia radiata from three biogeographical provinces spanning 10° of latitude and 35° of longitude across the Australian continent. These phylogenetically and taxonomically diverse communities were more strongly and consistently associated with host condition than geographical location or environmental variables, and a 'core' microbial community characteristic of healthy kelps appears to be lost when hosts become stressed. Microbial communities on stressed individuals were more similar to each other among locations than those on healthy hosts. In contrast to biogeographical patterns of planktonic marine microbial communities, host traits emerge as critical determinants of associated microbial community structure of these holobionts, even at a continental scale.

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.

Demographic consequences of disease in a habitat-forming seaweed and impacts on interactions between natural enemies.

Diseases affecting natural ecosystems are increasing in frequency and severity, but unless obviously catastrophic, the consequences of disease outbreaks are often overlooked, relative to other ecological processes (e.g., predation, competition). Disease can have profound effects on individuals and can also strongly influence interactions between infected hosts and their natural enemies. We investigated whether a novel bleaching disease affected the survival or performance of a habitat-forming red seaweed, Delisea pulchra. In addition, we investigated bidirectional, multipartite interactions between this seaweed host, its pathogens, and consumers. Although we found no negative impacts of disease on survival of D. pulchra, bleaching had substantial, negative consequences for affected individuals, including a dramatic drop in fecundity and a significant decrease in size. In the first direct demonstration of bacterial disease-mediated herbivory of seaweeds, herbivores generally preferred to consume bleached tissue in feeding trials, and we also found higher densities of herbivores on bleached than co-occurring, healthy algae at sites where herbivores were abundant. In a conceptually reciprocal test of the effects of herbivores on infection, we showed that simulated herbivory increased susceptibility to bleaching when algae were also exposed to cultures of a bacterial pathogen. Given the high proportions of D. pulchra affected by bleaching during peak periods, the impacts of this disease are likely to have important implications at the population level. This work highlights complex interactions between habitat-forming organisms and their natural enemies and further emphasizes the need to consider disease in ecological research.

The value of ecosystem services in global marine kelp forests.

While marine kelp forests have provided valuable ecosystem services for millennia, the global ecological and economic value of those services is largely unresolved. Kelp forests are diminishing in many regions worldwide, and efforts to manage these ecosystems are hindered without accurate estimates of the value of the services that kelp forests provide to human societies. Here, we present a global estimate of the ecological and economic potential of three key ecosystem services - fisheries production, nutrient cycling, and carbon removal provided by six major forest forming kelp genera (Ecklonia, Laminaria, Lessonia, Macrocystis, Nereocystis, and Saccharina). Each of these genera creates a potential value of between $64,400 and $147,100/hectare each year. Collectively, they generate between $465 and $562 billion/year worldwide, with an average of $500 billion. These values are primarily driven by fisheries production (mean $29,900, 904 Kg/Ha/year) and nitrogen removal ($73,800, 657 Kg N/Ha/year), though kelp forests are also estimated to sequester 4.91 megatons of carbon from the atmosphere/year highlighting their potential as blue carbon systems for climate change mitigation. These findings highlight the ecological and economic value of kelp forests to society and will facilitate better informed marine management and conservation decisions.

Differences in fish herbivory among tropical and temperate seaweeds and annual patterns in kelp consumption influence the tropicalisation of temperate reefs.

Climate change is leading to novel species interactions and profoundly altering ecosystems. In marine systems, tropical and subtropical species are increasing in higher latitudes. This has been linked to the deforestation of temperate coastlines, as direct effects of ocean warming combine with increased herbivory from tropical and sub-tropical fishes and lead to the decline of canopy-forming kelp. Here, we tested the hypothesis that this deforestation may be facilitated by greater palatability of temperate kelp and other canopy seaweeds compared to tropical taxa. We used multiple-choice filmed feeding field experiments and chemical analyses to measure the palatability of temperate and tropical seaweeds from Tosa Bay (southeastern Japan) and we used single-species feeding assays to measure changes in consumption of the kelp Ecklonia cava throughout the year. We found no evidence that temperate seaweeds are more palatable to herbivorous fish. In the multiple-choice assays, consumption was concentrated on both tropical and temperate Sargassum species, which are ephemeral and peak in abundance in the spring/early summer. Consumption of the kelp Ecklonia cava peaked during the autumn, when Sargassum species are absent. The highest levels of kelp herbivory coincide with the reproductive season for E. cava and may contribute to the long-term decline of these kelp forests in southern Japan.

Correction: Correction: Seagrass on the brink: Decline of threatened seagrass Posidonia australis continues following protection.

[This corrects the article DOI: 10.1371/journal.pone.0216107.].

How to quantify algal turf sediments and particulates on tropical and temperate reefs: An overview.

Algal turfs are the most abundant benthic covering on reefs in many shallow-water marine ecosystems. The particulates and sediments bound within algal turfs can influence a multitude of functions within these ecosystems. Despite the global abundance and importance of algal turfs, comparison of algal turf-bound sediments is problematic due to a lack of standardisation across collection methods. Here we provide an overview of three methods (vacuum sampling, airlift sampling, and TurfPods), and the necessary equipment (including construction suggestions), commonly employed to quantify sediments from algal turfs. We review the purposes of these methods (e.g. quantification of standing stock versus net accumulation) and how methods can vary depending on the research question or monitoring protocol. By providing these details in a readily accessible format we hope to encourage a standardised set of approaches for marine benthic ecologists, geologists and managers, that facilitates further quantification and global comparisons of algal turf sediments.

Global kelp forest restoration: past lessons, present status, and future directions.

Kelp forest ecosystems and their associated ecosystem services are declining around the world. In response, marine managers are working to restore and counteract these declines. Kelp restoration first started in the 1700s in Japan and since then has spread across the globe. Restoration efforts, however, have been largely disconnected, with varying methodologies trialled by different actors in different countries. Moreover, a small subset of these efforts are 'afforestation', which focuses on creating new kelp habitat, as opposed to restoring kelp where it previously existed. To distil lessons learned over the last 300 years of kelp restoration, we review the history of kelp restoration (including afforestation) around the world and synthesise the results of 259 documented restoration attempts spanning from 1957 to 2020, across 16 countries, five languages, and multiple user groups. Our results show that kelp restoration projects have increased in frequency, have employed 10 different methodologies and targeted 17 different kelp genera. Of these projects, the majority have been led by academics (62%), have been conducted at sizes of less than 1 ha (80%) and took place over time spans of less than 2 years. We show that projects are most successful when they are located near existing kelp forests. Further, disturbance events such as sea-urchin grazing are identified as regular causes of project failure. Costs for restoration are historically high, averaging hundreds of thousands of dollars per hectare, therefore we explore avenues to reduce these costs and suggest financial and legal pathways for scaling up future restoration efforts. One key suggestion is the creation of a living database which serves as a platform for recording restoration projects, showcasing and/or re-analysing existing data, and providing updated information. Our work establishes the groundwork to provide adaptive and relevant recommendations on best practices for kelp restoration projects today and into the future.

Plant defences and the role of epibiosis in mediating within-plant feeding choices of seagrass consumers.

Within-plant variation in susceptibility to herbivory can significantly influence the ecological and evolutionary consequences of plant-herbivore interactions. Seagrasses are marine angiosperms characterised by substantial intra-individual differences in multiple traits, such as nutrients, chemical and structural defences and epibiotic load, all of which can strongly influence herbivore preferences. We quantified the within-plant feeding choices of the two main consumers of the temperate seagrass Posidonia oceanica--the fish Sarpa salpa and the sea urchin Paracentrotus lividus--and determined the plant traits that explained their foraging strategies. We found strong within-plant heterogeneity in both seagrass susceptibility to herbivory and chemical composition, but different consumers exhibited contrasting feeding choices. S. salpa preferred the most nutritious and chemically defended younger leaves, suggesting a full adaptation to consuming this macrophyte and a greater impact of this herbivore on the plant. In contrast, P. lividus consistently preferred the older leaves covered by epibionts, probably attenuating the relative impact of this consumer and helping to explain the weak effects usually recorded for this echinoid in undisturbed meadows. Artificial diet experiments showed that morphology and fine-scale structural defences were the primary determinant of urchin feeding choices, with nutrient content and chemical defences being of secondary importance. Epibiosis did not strongly influence fish feeding, but it did have a strong 'shared-doom' effect on urchin consumption. This effect was driven by a distinct preference towards a mixed diet that included both host tissues and their epibiotic community.