ABSTRACT Marine heatwaves (MHWs) are among the most important threats to forest‐forming seaweeds and the ecological functions and services they underpin. Responses of seaweeds to MHWs are likely to vary across life‐stages, along their distribution and among populations with differing genetic structure. The effects of MHWs on early life‐stages and genetically distinct populations have rarely been tested experimentally. We used germlings and juveniles of the forest‐forming fucoid Phyllospora comosa from four genetically distinct populations, two at the warm‐edge (31° S) and two at the centre of its latitudinal distribution (34° S) in eastern Australia to examine their responses (i.e., survival, growth, photosynthetic efficiency, condition) to MHWs. Two MHW scenarios were tested: strong (23°C–23.5°C) and extreme (26°C), which would occur ~100 days and ~50 days per year, respectively, by 2100 under the RCP4.5 scenario (SSP2‐4.5). Survival under the extreme MHW was generally low for all populations and life‐stages (< 20% for juveniles; 20%–30% for germlings). The extreme MHW also negatively affected growth, photosynthesis and condition (e.g., loss of structural integrity in juveniles) over time. In contrast, responses of germlings and juveniles to the strong MHW did not differ from the control for either population. However, germlings from the warm‐edge population grew longer under the extreme and strong MHWs than those from the central population. Our results indicate only minor differences in responses to MHWs between genetically distinct populations of Phyllospora. While some Phyllospora individuals within each population appear able to resist strong MHWs, they are likely to be significantly affected by extreme MHWs that will be more common in the future. Given observed variation in responses among individuals within populations, finding, selecting, breeding and introducing resistant individuals (i.e., survivors to the extreme MHW) may allow increasing the resilience of Phyllospora forests into the future.
Global habitat degradation has prompted an urgent need for efficient restoration strategies at appropriate spatial scales. "Applied nucleation" is a restoration technique used in terrestrial forests, which starts with planting small vegetation patches that set the trajectory for natural propagation and recovery, resulting in large-scale restoration outcomes that require fewer resources. This concept could provide a framework for the restoration of marine seaweed forests, which are declining at unprecedented scales. We used the loss and 13-year restoration efforts of crayweed (Phyllospora comosa) forests along 70 km of Sydney's coastline, Australia, to determine the feasibility and challenges of applied nucleation in marine forests. After transplanting events at 14 sites, 43% of transplanted sites led to the establishment and expansion of crayweed, covering similar to 19,000 m(2) along Sydney's coastline. Recruitment 9 months post-transplantation was negatively associated with grazing and positively related to survival of transplanted adults-a source of propagules and canopy cover in the short-term. In the longer term, crayweed expansion was positively associated with other canopy-forming seaweed species, suggesting canopy provision as an important factor influencing recovery. Small-scale efforts, such as applied nucleation, that consider factors influencing seaweed establishment and expansion can help re-establish marine forests at relevant scales.
Kelp forests are among the most extensive and productive coastal ecosystems, yet they remain underrepresented in global conservation policy despite widespread declines driven by interacting global- (i.e., ocean warming, marine heatwaves) to local-scale stressors. At the same time, kelp conservation and restoration efforts are expanding rapidly across regions, but measures of success and syntheses tend to primarily focus on ecological conditions and trends, not on conservation and restoration actions. To fill this gap, we developed a comparative global dataset of kelp conservation initiatives based on expert-derived regional narratives from 209 participants spanning 35 regions with kelp forests. We applied a structured presence–absence scoring framework across six domains: conservation actions, restoration approaches, governance actors, conservation objectives, social dimensions, and funding structures, supplemented by regional expert knowledge to enable cross-regional comparison. Across regions, conservation was characterised by strong emphasis on monitoring (86
Climate-driven shifts in the abundance and distribution of habitat-forming species are transforming how ecosystems produce and cycle carbon, nutrients and energy. Temperate kelp forests are increasingly being replaced by tropical or warm-affinity habitat-forming species like turf seaweeds and corals, i.e. 'tropicalized'. These changes can have cascading effects on associated species such as calcifying organisms, which contribute to sediment generation and carbon cycling via the production of calcium carbonate. This study quantified carbonate production and erosion across a temperate kelp forest and three tropicalized reef states following the 2011 marine heatwave: kelp-turf mix, warmer affinity seaweeds and coral-turf dominance. Results show that gross carbonate production was the highest in coral-turf reefs (1.85 ± 0.65 kg m-2 yr-1), lowest in warmer affinity seaweed reefs (0.04 ± 0.02 kg m-2 yr-1) and intermediate in temperate kelp forests (0.60 ± 0.19 kg m-2 yr-1). These differences were linked to the abundance of corals in coral-turf state and scarce calcifying algae in the warmer affinity seaweed state. Bioerosion played a moderate role in the overall budget, but the dominant bioeroders differed between habitats: urchins in temperate reefs contributed 80% less than parrotfishes in tropicalized reefs. Overall, tropicalization can either increase or decrease carbonate availability, depending on the dominant habitat formers. These shifts may significantly impact inorganic carbon cycling and the structural and functional integrity of coastal reef ecosystems.
Ongoing and predicted range loss of kelp forests in response to climatic stressors is pressing marine managers to look into the adaptive capacity of populations to inform conservation strategies. Characterising how adaptive genetic diversity and structure relate to present and future environmental variation represents an emerging approach to quantifying kelp vulnerability to environmental change and identifying populations with genotypes that potentially confer an adaptive advantage in future ocean conditions. The dominant Australian kelp, Ecklonia radiata, was genotyped from 10 locations spanning 2000 km of coastline and a 9.5°C average temperature gradient along the east coast of Australia, a global warming hotspot. ddRAD sequencing generated 10,700 high-quality single nucleotide polymorphisms (SNPs) and characterized levels of neutral and adaptive genomic diversity and structure. The adaptive dataset, reflecting portions of the genome putatively under selection, was used to infer genomic vulnerability by 2050 under the RCP 8.5 scenario. There was strong neutral genetic differentiation between Australia mainland and Tasmanian populations, but only weak genetic structure among mainland populations within the main path of the East Australian Current. Genetic diversity was highest in the center of the range and lowest in the warm-edge population. The adaptive SNP candidates revealed similar genetic structure patterns, with a spread of adaptive alleles across most warm (northern) populations. The lowest, but most unique, adaptive genetic diversity values were found in both warm and cool population edges, suggesting local adaptation but low evolutionary potential. Critically, genomic vulnerability modeling identified high levels of vulnerability to future environmental conditions in Tasmanian populations. Populations of kelp at range edges are unlikely to adapt and keep pace with predicted climate change. Ensuring the persistence of these kelp forests, by boosting resilience to climate change, may require active management strategies with assisted adaptation in warm-edge (northern) populations and assisted gene flow in cool-edge (Tasmania) populations.
A critical component of ecosystem restoration projects involves using genetic data to select source material that will enhance success under current and future climates. However, the complexity and expense of applying genetic data is a barrier to its use outside of specialised scientific contexts. To help overcome this barrier, we developed Reef Adapt ( www.reefadapt.org ), an innovative, globally applicable and expandable web platform that incorporates genetic, biophysical and environmental prediction data into marine restoration and assisted gene flow planning. The Reef Adapt tool provides maps that identify areas with populations suited to user-specified restoration/recipient sites under current and future climate scenarios. We demonstrate its versatility and practicality with four case studies of ecologically and evolutionarily diverse taxa: the habitat-forming corals Pocillopora damicornis and Acropora kenti, and macroalgae Phyllospora comosa and Ecklonia radiata. Reef Adapt is a management-ready tool to aid restoration and conservation efforts amidst ongoing habitat degradation and climate change. Aiming to accelerate research in the field of marine restoration, ‘Reef Adapt’ integrates genetic, environmental, and biophysical data to predict populations suited to ‘local’ and ‘future’ climates for marine restoration
IntroductionTo counteract the rapid loss of marine forests globally and meet international commitments of the UN Decade on Ecosystem Restoration and the Convention on Biological Diversity ‘30 by 30’ targets, there is an urgent need to enhance our capacity for macroalgal restoration. The Green Gravel Action Group (GGAG) is a global network of 67 members that are working on the restoration of a diverse range of macroalgal forests and it aims to facilitate knowledge exchange to fast-track innovation and implementation of outplanting approaches worldwide. MethodsHere, we overview 25 projects conducted by members of the group that are focused on testing and developing techniques for macroalgal restoration. Based on these projects, we summarise the major challenges associated with scaling up the area of marine forests restored. ResultsWe identify several critical challenges that currently impede more widespread rollout of effective large-scale macroalgal restoration worldwide: 1) funding and capacity limitations, 2) difficulties arising from conditions at restoration sites, 3) technical barriers, and 4) challenges at the restoration-policy interface. DiscussionDespite these challenges, there has been substantial progress, with an increasing number of efforts, community engagement and momentum towards scaling up activities in recent years. Drawing on the collective expertise of the GGAG, we outline key recommendations for the scaling up of restoration efforts to match the goals of international commitments. These include the establishment of novel pathways to fund macroalgal restoration activities, building skills and capacity, harnessing emerging innovations in mobile hatchery and seeding technologies, and the development of the scientific and governance frameworks necessary to implement and monitor macroalgal restoration projects at scale.
In December 2022, the United Nations Convention on Biological Diversity (CBD) adopted the Kunming-Montreal Global Biodiversity Framework, in which 196 Parties, for the first time, committed to report on the status of genetic diversity for all species. To facilitate this reporting, three genetic diversity indicators were developed, two of which focus on the processes contributing to genetic diversity loss: the loss of genetically distinct populations (measured by complementary indicator “proportion of populations maintained within species”) and populations being too small to maintain genetic diversity (measured by headline indicator A4, “The proportion of populations within species with an effective population size > 500”). The major advantage of these indicators is that they can be estimated without DNA-based data. However, demonstrating the feasibility of this approach to all Parties for their national reporting, requires addressing methodological challenges of using empirical data gathered from diverse sources, across diverse taxonomic groups and for countries of varying socio-economic status and biodiversity levels. Here, we assess the genetic indicators for 919 taxa, representing 5,271 populations across nine countries, including megadiverse and developing economies. Data were available to calculate indicators for each country and taxonomic group (765 taxa [83%] had data for at least one indicator). Additionally, 41% of taxa (n=518) have lost at least one-tenth of their populations (complementary indicator [populations maintained] value < 0.9), while 58% of taxa (n=568) have all populations too small to sustain genetic diversity (headline indicator [Ne 500] value = 0). By comparing taxon indicator values to their GlobalRed List status, range size, and other factors, we found the loss of genetic diversity shown by these indicators would go unnoticed by other biodiversity assessments, highlighting the critical importance of monitoring and conserving genetic diversity using these indicators.
Kelp forests are among the most valuable ecosystems on Earth, but they are increasingly being degraded and lost due to a range of human-related stressors, leading to recent calls for their improved management and conservation. One of the primary tools to conserve marine species and biodiversity is the establishment of marine protected areas (MPAs). International commitments to protect 30% of the world's ecosystems are gaining momentum, offering a promising avenue to secure kelp forests into the Anthropocene. However, a clear understanding of the efficacy of MPAs for conserving kelp forests in a changing ocean is lacking. In this perspective, we question whether strengthened global protection will create meaningful conservation outcomes for kelp forests. We explore the benefits of MPAs for kelp conservation under a suite of different stressors, focusing on empirical evidence from protected kelp forests. We show that MPAs can be effective against some drivers of kelp loss (e.g., overgrazing, kelp harvesting), particularly when they are maintained in the long-term and enforced as no-take areas. There is also some evidence that MPAs can reduce impacts of climate change through building resilience in multi-stressor situations. However, MPAs also often fail to provide protection against ocean warming, marine heatwaves, coastal darkening, and pollution, which have emerged as dominant drivers of kelp forest loss globally. Although well-enforced MPAs should remain an important tool to protect kelp forests, successful kelp conservation will require implementing an additional suite of management solutions that target these accelerating threats.
Aim Ocean warming and marine heatwaves are rapidly reconfiguring the composition of seaweed forests-the world's largest coastal vegetated biome. Seaweed forest responses to climate change in remote locations, which constitute the majority of the forest biome, remain however poorly quantified. Here, we examine the temporal stability of the seaweed forests across a global seaweed biodiversity hotspot where several species are predicted to undergo severe range contractions in this century. Location Western south coast of Australia. Methods Seaweed forest canopies were censused at 18 shallow (< 10 m) sheltered reefs between 1997 and 2006 and again between 2021 and 2024 (six sites per location). We also surveyed 24 sites to examine whether temporal changes differed over gradients of wave exposure and depth. Results Seaweed forest canopies across all locations showed surprisingly little change in biomass, cover, stand density and species composition over two decades, with strong spatial structuring across depth and exposure gradients persisting over time. The average thermal affinity of forest canopies (i.e., the community temperature index, CTI) did not track warming, suggesting that factors other than temperature (e.g., wave exposure and depth) are more important drivers of forest stand structure and/or that key thermal thresholds have not yet been crossed. Forests in the location with the most pronounced warming exhibited increased thermal bias over time (total bias of 0.8 degrees C-2.2 degrees C), indicating they were dominated by species with cooler affinities than their local temperatures. Main Conclusions The greater thermal bias in forests at the warmer edge of southern Australia suggests these will be more susceptible to future warming-related compositional changes than forests in cooler locations. The relative stability we found contrasts with a current context of rapidly changing seaweed forests nationally and globally, highlighting the need to deepen our ecological understanding of the region so that future changes to its unique biodiversity and ecosystem services can be predicted and mitigated.
Marine kelp forests cover 1/3 of our world's coastlines, are heralded as a nature-based solution to address socio-environmental issues, connect hundreds of millions of people with the ocean, and support a rich web of biodiversity throughout our oceans. But they are increasingly threatened with some areas reporting over 90% declines in kelp forest cover in living memory. Despite their importance and the threats they face, kelp forests are entirely absent from the international conservation dialogue. No international laws, policies, or targets focus on kelp forests and very few countries consider them in their national policy. The Kelp Forest Challenge addresses that gap. Together with 252 kelp experts, professionals, and citizens from 25 countries, the Kelp Forest Challenge was developed as a grassroots vision of what the world can achieve for kelp forest conservation. It is a global call to restore 1 million and protect 3 million hectares of kelp forests by 2040. This is a monumental challenge, that will require coordination across multiple levels of society and the mobilization of immense resources. Pledges may therefore include area for protection or restoration, enabling pledges which assist in conservation (funding, equipment, professional expertise, capacity building), or awareness-based pledges which increase awareness or education about kelp forests. Correspondingly, participants may be from government, scientific institutions, private sector, NGOs, community groups, or individuals. This challenge is the beginning of a 17-year mission to save our kelp forests and anyone and any organisation is invited to participate.
Marine heatwaves (MHWs), increasing in duration and intensity because of climate change, are now a major threat to marine life and can have lasting effects on the structure and function of ecosystems. However, the responses of marine taxa and ecosystems to MHWs can be highly variable, making predicting and interpreting biological outcomes a challenge. Here, we review how biological responses to MHWs, from individuals to ecosystems, are mediated by fine-scale spatial variability in the coastal marine environment (hereafter, local gradients). Viewing observed responses through a lens of ecological theory, we present a simple framework of three ‘resilience processes’ (RPs) by which local gradients can influence the responses of marine taxa to MHWs. Local gradients (1) influence the amount of stress directly experienced by individuals, (2) facilitate local adaptation and acclimatization of individuals and populations, and (3) shape community composition which then influences responses to MHWs. We then synthesize known examples of fine-scale gradients that have affected responses of benthic foundation species to MHWs, including kelp forests, coral reefs, and seagrass meadows and link these varying responses to the RPs. We present a series of case studies from various marine ecosystems to illustrate the differential impacts of MHWs mediated by gradients in both temperature and other co-occurring drivers. In many cases, these gradients had large effect sizes with several examples of local gradients causing a 10-fold difference in impacts or more (e.g., survival, coverage). This review highlights the need for high-resolution environmental data to accurately predict and manage the consequences of MHWs in the context of ongoing climate change. While current tools may capture some of these gradients already, we advocate for enhanced monitoring and finer scale integration of local environmental heterogeneity into climate models. This will be essential for developing effective conservation strategies and mitigating future marine biodiversity loss.
Host-associated microbiota are critical for eukaryotic host functioning, to the extent that hosts and their associated microbial communities are often considered “holobionts”. Most studies of holobionts have focused on descriptive approaches or have used model systems, usually in the laboratory, to understand host-microbiome interactions. To advance our understanding of host-microbiota interactions and their wider ecological impacts, we need experimental frameworks that can explore causation in non-model hosts, which often have highly diverse microbiota, and in their natural ecological setting (i.e. in the field). We used a dominant habitat-forming seaweed, Hormosira banksii, to explore these issues and to experimentally test host-microbiota interactions in a non-model holobiont. The experimental protocols were aimed at trying to disentangle microbially mediated effects on hosts from direct effects on hosts associated with the methods employed to manipulate host-microbiota. This was done by disrupting the microbiome, either through removal/disruption using a combination of antimicrobial treatments, or additions of specific taxa via inoculations, or a combination of thew two. The experiments were done in mesocosms and in the field. Three different antibiotic treatments were used to disrupt seaweed-associated microbiota to test whether disturbances of microbiota, particularly bacteria, would negatively affect host performance. Responses of bacteria to these disturbances were complex and differed substantially among treatments, with some antibacterial treatments having little discernible effect. However, the temporal sequence of responses antibiotic treatments, changes in bacterial diversity and subsequent decreases in host performance, strongly suggested an effect of the microbiota on host performance in some treatments, as opposed to direct effects of the antibiotics. To further test these effects, we used 16S-rRNA-gene sequencing to identify bacterial taxa that were either correlated, or uncorrelated, with poor host performance following antibiotic treatment. These were then isolated and used in inoculation experiments, independently or in combination with the previously used antibiotic treatments. Negative effects on host performance were strongest where specific microbial antimicrobials treatments were combined with inoculations of strains that were correlated with poor host performance. For these treatments, negative host effects persisted the entire experimental period (12 days), even though treatments were only applied at the beginning of the experiment. Host performance recovered in all other treatments. These experiments provide a framework for exploring causation and disentangling microbially mediated vs. direct effects on hosts for ecologically important, non-model holobionts in the field. This should allow for better predictions of how these systems will respond to, and potentially mitigate, environmental disturbances in their natural context.
EDITORIAL article Front. Mar. Sci., 18 August 2023Sec. Marine Evolutionary Biology, Biogeography and Species Diversity Volume 10 - 2023 | https://doi.org/10.3389/fmars.2023.1273405
IntroductionThe collapse of macroalgal habitats is altering the structure of benthic communities on rocky shores globally. Nonetheless, how the loss of canopy-forming macroalgae influences the structure of epilithic microbial communities is yet to be explored. MethodsHere, we used experimental field manipulations and 16S-rRNA-gene amplicon sequencing to determine the effects of macroalgal loss on the understory bacterial communities and their relationship with epiphytic bacteria on macroalgae. Beds of the fucoid Hormosira banksii were exposed to different levels of disturbance resulting in five treatments: (i) 100% removal of Hormosira individuals, (ii) 50% removal, (iii) no removal, (iv) a procedural control that mimicked the removal process, but no Hormosira was removed and (v) adjacent bare rock. Canopy cover, bacterial communities (epilithic and epiphytic) and benthic macroorganisms were monitored for 16 months.ResultsResults showed that reductions in canopy cover rapidly altered understory bacterial diversity and composition. Hormosira canopies in 50% and 100% removal plots showed signs of recovery over time, but understory epilithic bacterial communities remained distinct throughout the experiment in plots that experienced full Hormosira removal. Changes in bacterial communities were not related to changes in other benthic macroorganisms.DiscussionThese results demonstrate that understory epilithic bacterial communities respond rapidly to environmental disturbances at small scales and these changes can be long-lasting. A deeper knowledge of the ecological role of understory epilithic microbial communities is needed to better understand potential cascading effects of disturbances on the functioning of macroalgal-dominated systems.
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.