Multiscale stability of an intertidal kelp (Postelsia palmaeformis) near its northern range edge through a period of prolonged heatwaves.

BACKGROUND AND AIMS: Climate change, including gradual changes and extreme weather events, is driving widespread species losses and range shifts. These climatic changes are felt acutely in intertidal ecosystems, where many organisms live close to their thermal limits and experience the extremes of both marine and terrestrial environments. A recent series of multiyear heatwaves in the northeast Pacific Ocean might have impacted species even towards their cooler, northern range edges. Among them, the high intertidal kelp Postelsia palmaeformis has traits that could make it particularly vulnerable to climate change, but it is critically understudied. METHODS: In 2021 and 2022, we replicated in situ and aerial P. palmaeformis surveys that were conducted originally in 2006 and 2007, in order to assess the state of northern populations following recent heatwaves. Changes in P. palmaeformis distribution, extent, density and morphometrics were assessed between these two time points over three spatial scales, ranging from 250 m grid cells across the entire 167 km study region, to within grid cells and the individual patch. KEY RESULTS: We found evidence consistent with population stability at all three scales: P. palmaeformis remained present in all 250 m grid cells in the study region where it was previously found, and neither the extent within cells nor the patch density changed significantly between time points. However, there was evidence of slight distributional expansion, increased blade lengths and a shift to earlier reproductive timing. CONCLUSIONS: We suggest that apparent long-term stability of P. palmaeformis might be attributable to thermal buffering near its northern range edge and from the wave-exposed coastlines it inhabits, which may have decreased the impacts of heatwaves. Our results highlight the importance of multiscale assessments when examining changes within species and populations, in addition to the importance of dispersal capability and local conditions in regulating the responses of species to climate change.

Marine protected areas can be useful but are not a silver bullet for kelp conservation.

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.

Tipping points and interactive effects of chronic human disturbance and acute heat stress on coral diversity.

Multiple anthropogenic stressors co-occur ubiquitously in natural ecosystems. However, multiple stressor studies often produce conflicting results, potentially because the nature and direction of stressor interactions depends upon the strength of the underlying stressors. Here, we first examine how coral α- and ß-diversities vary across sites spanning a gradient of chronic local anthropogenic stress before and after a prolonged marine heatwave. Developing a multiple stressor framework that encompasses non-discrete stressors, we then examine interactions between the continuous and discrete stressors. We provide evidence of additive effects, antagonistic interactions (with heatwave-driven turnover in coral community composition diminishing as the continuous stressor increased), and tipping points (at which the response of coral Hill-richness to stressors changed from additive to near synergistic). We show that community-level responses to multiple stressors can vary, and even change qualitatively, with stressor intensity, underscoring the importance of examining complex, but realistic continuous stressors to understand stressor interactions and their ecological impacts.

Whole genome population structure of North Atlantic kelp confirms high-latitude glacial refugia.

Coastal refugia during the Last Glacial Maximum (~21,000 years ago) have been hypothesized at high latitudes in the North Atlantic, suggesting marine populations persisted through cycles of glaciation and are potentially adapted to local environments. Here, whole-genome sequencing was used to test whether North Atlantic marine coastal populations of the kelp Alaria esculenta survived in the area of southwestern Greenland during the Last Glacial Maximum. We present the first annotated genome for A. esculenta and call variant positions in 54 individuals from populations in Atlantic Canada, Greenland, Faroe Islands, Norway and Ireland. Differentiation across populations was reflected in ~1.9 million single nucleotide polymorphisms, which further revealed mixed ancestry in the Faroe Islands individuals between putative Greenlandic and European lineages. Time-calibrated organellar phylogenies suggested Greenlandic populations were established during the last interglacial period more than 100,000 years ago, and that the Faroe Islands population was probably established following the Last Glacial Maximum. Patterns in population statistics, including nucleotide diversity, minor allele frequencies, heterozygosity and linkage disequilibrium decay, nonetheless suggested glaciation reduced Canadian Atlantic and Greenlandic populations to small effective sizes during the most recent glaciation. Functional differentiation was further reflected in exon read coverage, which revealed expansions unique to Greenland in 337 exons representing 162 genes, and a modest degree of exon loss (103 exons from 56 genes). Altogether, our genomic results provide strong evidence that A. esculenta populations were resilient to past climatic fluctuations related to glaciations and that high-latitude populations are potentially already adapted to local conditions as a result.

Microclimate predicts kelp forest extinction in the face of direct and indirect marine heatwave effects.

Marine heatwaves threaten the persistence of kelp forests globally. However, the observed responses of kelp forests to these events have been highly variable on local scales. Here, we synthesize distribution data from an environmentally diverse region to examine spatial patterns of canopy kelp persistence through an unprecedented marine heatwave. We show that, although often overlooked, temperature variation occurring at fine spatial scales (i.e., a few kilometers or less) can be a critical driver of kelp forest persistence during these events. Specifically, though kelp forests nearly all persisted toward the cool outer coast, inshore areas were >3°C warmer at the surface and experienced extensive kelp loss. Although temperatures remained cool at depths below the thermocline, kelp persistence in these thermal refugia was strongly constrained by biotic interactions, specifically urchin populations that increased during the heatwave and drove transitions to urchin barrens in deeper rocky habitat. Urchins were, however, largely absent from mixed sand and cobble benthos, leading to an unexpected association between bottom substrate and kelp forest persistence at inshore sites with warm surface waters. Our findings demonstrate both that warm microclimates increase the risk of habitat loss during marine heatwaves and that biotic interactions modified by these events will modulate the capacity of cool microclimates to serve as thermal refugia.

Trophic control of cryptic coralline algal diversity.

Understanding how trophic dynamics drive variation in biodiversity is essential for predicting the outcomes of trophic downgrading across the world's ecosystems. However, assessing the biodiversity of morphologically cryptic lineages can be problematic, yet may be crucial to understanding ecological patterns. Shifts in keystone predation that favor increases in herbivore abundance tend to have negative consequences for the biodiversity of primary producers. However, in nearshore ecosystems, coralline algal cover increases when herbivory is intense, suggesting that corallines may uniquely benefit from trophic downgrading. Because many coralline algal species are morphologically cryptic and their diversity has been globally underestimated, increasing the resolution at which we distinguish species could dramatically alter our conclusions about the consequences of trophic dynamics for this group. In this study, we used DNA barcoding to compare the diversity and composition of cryptic coralline algal assemblages at sites that differ in urchin biomass and keystone predation by sea otters. We show that while coralline cover is greater in urchin-dominated sites (or "barrens"), which are subject to intense grazing, coralline assemblages in these urchin barrens are significantly less diverse than in kelp forests and are dominated by only 1 or 2 species. These findings clarify how food web structure relates to coralline community composition and reconcile patterns of total coralline cover with the widely documented pattern that keystone predation promotes biodiversity. Shifts in coralline diversity and distribution associated with transitions from kelp forests to urchin barrens could have ecosystem-level effects that would be missed by ignoring cryptic species' identities.

Multiple stressors drive convergent evolution of performance properties in marine macrophytes.

Extreme environments have driven the evolution of some of the most inspiring adaptations in nature. In the intertidal zone of wave-swept shores, organisms face physical forces comparable to hurricanes and must further endure thermal and desiccation stress during low tides, compromising their physiological and biomechanical performance. We examine how these multiple stressors have influenced the evolution of tissue properties during desiccation using eight phylogenetically independent pairs of intertidal and subtidal macrophytes. Intertidal species generally lost water more slowly than their subtidal counterparts, presumably as an adaption to regular emersion. Under partial desiccation, breaking force, strength, and extensibility of intertidal species generally exceeded those of subtidal species, although important differences existed among phylogenetic pairs. This was often true even when subtidal relatives resisted greater forces or were more extensible under full hydration. The interacting effects of mechanical forces and desiccation during low tide are likely a major selective agent in determining macrophyte performance and fitness. Overall, we found that lineages that have independently evolved to occupy the wave-swept intertidal have converged on performance metrics that are likely to be adaptive to the interacting stressors associated with their extreme niches.

Whole-genome sequencing reveals forgotten lineages and recurrent hybridizations within the kelp genus Alaria (Phaeophyceae).

The genomic era continues to revolutionize our understanding of the evolution of biodiversity. In phycology, emphasis remains on assembling nuclear and organellar genomes, leaving the full potential of genomic datasets to answer long-standing questions about the evolution of biodiversity largely unexplored. Here, we used whole-genome sequencing (WGS) datasets to survey species diversity in the kelp genus Alaria, compare phylogenetic signals across organellar and nuclear genomes, and specifically test whether phylogenies behave like trees or networks. Genomes were sequenced from across the global distribution of Alaria (including Alaria crassifolia, A. praelonga, A. crispa, A. marginata, and A. esculenta), representing over 550 GB of data and over 2.2 billion paired reads. Genomic datasets retrieved 3,814 and 4,536 single-nucleotide polymorphisms (SNPs) for mitochondrial and chloroplast genomes, respectively, and upwards of 148,542 high-quality nuclear SNPs. WGS revealed an Arctic lineage of Alaria, which we hypothesize represents the synonymized taxon A. grandifolia. The SNP datasets also revealed inconsistent topologies across genomic compartments, and hybridization (i.e., phylogenetic networks) between Pacific A. praelonga, A. crispa, and putative A. grandifolia, and between some lineages of the A. marginata complex. Our analysis demonstrates the potential for WGS data to advance our understanding of evolution and biodiversity beyond amplicon sequencing, and that hybridization is potentially an important mechanism contributing to novel lineages within Alaria. We also emphasize the importance of surveying phylogenetic signals across organellar and nuclear genomes, such that models of mixed ancestry become integrated into our evolutionary and taxonomic understanding.

A comprehensive kelp phylogeny sheds light on the evolution of an ecosystem.

Reconstructing phylogenetic topologies and divergence times is essential for inferring the timing of radiations, the appearance of adaptations, and the historical biogeography of key lineages. In temperate marine ecosystems, kelps (Laminariales) drive productivity and form essential habitat but an incomplete understanding of their phylogeny has limited our ability to infer their evolutionary origins and the spatial and temporal patterns of their diversification. Here, we reconstruct the diversification of habitat-forming kelps using a global genus-level phylogeny inferred primarily from organellar genome datasets, and investigate the timing of kelp radiation. We resolve several important phylogenetic features, including relationships among the morphologically simple kelp families and the broader radiation of complex kelps, demonstrating that the initial radiation of the latter resulted from an increase in speciation rate around the Eocene-Oligocene boundary. This burst in speciation rate is consistent with a possible role of recent climatic cooling in triggering the kelp radiation and pre-dates the origin of benthic-foraging carnivores. Historical biogeographical reconstructions point to a northeast Pacific origin of complex kelps, with subsequent colonization of new habitats likely playing an important role in driving their ecological diversification. We infer that complex morphologies associated with modern kelp forests (e.g. branching, pneumatocysts) evolved several times over the past 15-20 MY, highlighting the importance of morphological convergence in establishing modern upright kelp forests. Our phylogenomic findings provide new insights into the geographical and ecological proliferation of kelps and provide a timeline along which feedbacks between kelps and their food-webs could have shaped the structure of temperate ecosystems.

An empirical test of 'universal' biomass scaling relationships in kelps: evidence of convergence with seed plants.

Biomass allocation patterns have received substantial consideration, leading to the recognition of several 'universal' interspecific trends. Despite efforts to understand biomass partitioning among embryophytes, few studies have examined macroalgae that evolved independently, yet function ecologically in much the same ways as plants. Kelps allocate photosynthate among three organs (the blade(s), stipe(s) and holdfast) that are superficially convergent with organs of land plants, providing a unique opportunity to test the limits of 'universal' trends. In this study, we used an allometric approach to quantify interspecific biomass partitioning patterns in kelps and assess whether embryophyte-based predictions of biomass scaling can be applied to marine macrophytes that lack root-to-leaf hydraulic transport. Photosynthetic area and dry mass were found to scale to approximately the ¾ power and kelp biomass allocation patterns were shown to match closely to empirical measures of allometric scaling among woody plants. Larger kelp species were found to have increased relative stipe and holdfast mass than smaller species, highlighting important consequences of size for marine macroalgae. Our study provides insights into the evolution of size in the largest marine macrophytes and corroborates previous work suggesting that the morphology of divergent lineages of photoautotrophs may reflect similar selective pressures.

Evidence of an evolutionary-developmental trade-off between drag avoidance and tolerance strategies in wave-swept intertidal kelps (Laminariales, Phaeophyceae).

Kelps are a clade of morphologically diverse, ecologically important habitat-forming species. Many kelps live in wave-swept environments and are exposed to chronic flow-induced stress. In order to grow and survive in these harsh environments, kelps can streamline (reducing drag coefficient) to avoid drag or to increase attachment and breakage force to tolerate it. We aimed to quantify the drag tolerance and streamlining strategies of kelps from wave-swept intertidal habitats. We measured drag coefficient and tenacity of populations from eight kelp species over a wide range of sizes to determine whether kelps avoid dislodgement by reducing drag coefficient or by increasing tenacity as they grow, and whether these traits are traded off. We employed phylogenetic comparative methods to rule out potentially confounding effects of species' relatedness. There was a significant negative relationship between drag avoidance and tolerance strategies, even after incorporating phylogeny. Kelps that were more tenacious were less able to reduce drag, resulting in a continuum from "tolerators" to "streamliners," with some species demonstrating intermediate, mixed strategies. Drag and tenacity were correlated with geometric properties (i.e., second moment of area) of the stipe in large kelps. Results presented in this study suggest that kelps are either strong or streamlined, but not both. This continuum is consistent with avoidance and tolerance trade-offs that have been documented in many different biological systems and may have widespread implications for the evolution of large macroalgae, perhaps driving morphological diversity within this group.

Biomechanical consequences of branching in flexible wave-swept macroalgae.

Wave-swept macroalgae present an excellent system for studying the effects of chronic physical stress on the morphological evolution of plants. Wave-induced water velocities impose great drag forces, leading to a morphological tradeoff between light interception and drag reduction/tolerance. What are the hydrodynamic consequences of morphological diversification, such as increased branching? Drag was measured on artificial macroalgae of constant 'photosynthetic' area, but differing branching patterns, in a high-speed flume at water velocities up to 3.5 m s(-1). A meta-analysis was used to compare dislodgement forces of branched and unbranched species of comparable sizes in the field to determine if drag-prone morphologies had greater attachment strengths. Branched fronds experienced greater drag than unbranched fronds of the same size. Greater drag in branched forms was not the result of increased projected area but probably resulted from greater pressure or friction drag. In the field, branched species resisted greater dislodgement forces than unbranched species of comparable size, suggesting that branched species compensate for increased drag with stronger attachment to the substratum. Branching has clear biomechanical consequences, increasing drag and the need for increased attachment. This raises questions about physiological and ecological advantages that may have driven the repeated evolution of biomechanically costly, branched morphologies.

Impacts of Climate Change on Marine Foundation Species.

Marine foundation species are the biotic basis for many of the world's coastal ecosystems, providing structural habitat, food, and protection for myriad plants and animals as well as many ecosystem services. However, climate change poses a significant threat to foundation species and the ecosystems they support. We review the impacts of climate change on common marine foundation species, including corals, kelps, seagrasses, salt marsh plants, mangroves, and bivalves. It is evident that marine foundation species have already been severely impacted by several climate change drivers, often through interactive effects with other human stressors, such as pollution, overfishing, and coastal development. Despite considerable variation in geographical, environmental, and ecological contexts, direct and indirect effects of gradual warming and subsequent heatwaves have emerged as the most pervasive drivers of observed impact and potent threat across all marine foundation species, but effects from sea level rise, ocean acidification, and increased storminess are expected to increase. Documented impacts include changes in the genetic structures, physiology, abundance, and distribution of the foundation species themselves and changes to their interactions with other species, with flow-on effects to associated communities, biodiversity, and ecosystem functioning. We discuss strategies to support marine foundation species into the Anthropocene, in order to increase their resilience and ensure the persistence of the ecosystem services they provide.

Heatwave restructures marine intertidal communities across a stress gradient.

Significant questions remain about how ecosystems that are structured by abiotic stress will be affected by climate change. Warmer temperatures are hypothesized to shift species along abiotic gradients such that distributions track changing environments where physical conditions allow. However, community-scale impacts of extreme warming in heterogeneous landscapes are likely to be more complex. We investigated the impacts of a multiyear marine heatwave on intertidal community dynamics and zonation on a wave-swept rocky coastline along the Central Coast of British Columbia, Canada. Leveraging an 8-year time series with high seaweed taxonomic resolution (116 taxa) that was established 3 years prior to the heatwave, we document major shifts in zonation and abundance of populations that led to substantial reorganization at the community level. The heatwave was associated with shifts in primary production away from upper elevations through declines in seaweed cover and partial replacement by invertebrates. At low elevations, seaweed cover remained stable or recovered rapidly following decline, being balanced by increases in some species and decreases in others. These results illustrate that, rather than shifting community zonation uniformly along abiotic stress gradients, intense and lasting warming events may restructure patterns of ecological dominance and reduce total habitability of ecosystems, especially at extreme ends of pre-existing abiotic gradients.

Marine heatwaves threaten cryptic coral diversity and erode associations among coevolving partners.

Climate change-amplified marine heatwaves can drive extensive mortality in foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter cryptic genetic structure. Heatwave impacts may be exacerbated in species that engage in obligate symbioses, where the genetics of multiple coevolving taxa may be affected. Here, we tracked the symbiotic associations of reef-building corals for 6 years through a prolonged heatwave, including known survivorship for 79 of 315 colonies. Coral genetics strongly predicted survival of the ubiquitous coral, Porites (massive growth form), with variable survival (15 to 61%) across three morphologically indistinguishable-but genetically distinct-lineages. The heatwave also disrupted strong associations between these coral lineages and their algal symbionts (family Symbiodiniaceae), with symbiotic turnover in some colonies, resulting in reduced specificity across lineages. These results highlight how heatwaves can threaten cryptic genotypes and decouple otherwise tightly coevolved relationships between hosts and symbionts.

Toward a conceptual framework for managing and conserving marine habitats: A case study of kelp forests in the Salish Sea.

Kelp forests are in decline across much of their range due to place-specific combinations of local and global stressors. Declines in kelp abundance can lead to cascading losses of biodiversity and productivity with far-reaching ecological and socioeconomic consequences. The Salish Sea is a hotspot of kelp diversity where many species of kelp provide critical habitat and food for commercially, ecologically, and culturally important fish and invertebrate species. However, like other regions, kelp forests in much of the Salish Sea are in rapid decline. Data gaps and limited long-term monitoring have hampered attempts to identify and manage for specific drivers of decline, despite the documented urgency to protect these important habitats. To address these knowledge gaps, we gathered a focus group of experts on kelp in the Salish Sea to identify perceived direct and indirect stressors facing kelp forests. We then conducted a comprehensive literature review of peer-reviewed studies from the Salish Sea and temperate coastal ecosystems worldwide to assess the level of support for the pathways identified by the experts, and we identified knowledge gaps to prioritize future research. Our results revealed major research gaps within the Salish Sea and highlighted the potential to use expert knowledge for making informed decisions in the region. We found high support for the pathways in the global literature, with variable consensus on the relationship between stressors and responses across studies, confirming the influence of local ecological, oceanographic, and anthropogenic contexts and threshold effects on stressor-response relationships. Finally, we prioritized areas for future research in the Salish Sea. This study demonstrates the value expert opinion has to inform management decisions. These methods are readily adaptable to other ecosystem management contexts, and the results of this case study can be immediately applied to kelp management.

Inconsistent Patterns of Microbial Diversity and Composition Between Highly Similar Sequencing Protocols: A Case Study With Reef-Building Corals.

16S rRNA gene profiling (amplicon sequencing) is a popular technique for understanding host-associated and environmental microbial communities. Most protocols for sequencing amplicon libraries follow a standardized pipeline that can differ slightly depending on laboratory facility and user. Given that the same variable region of the 16S gene is targeted, it is generally accepted that sequencing output from differing protocols are comparable and this assumption underlies our ability to identify universal patterns in microbial dynamics through meta-analyses. However, discrepant results from a combined 16S rRNA gene dataset prepared by two labs whose protocols differed only in DNA polymerase and sequencing platform led us to scrutinize the outputs and challenge the idea of confidently combining them for standard microbiome analysis. Using technical replicates of reef-building coral samples from two species, Montipora aequituberculata and Porites lobata, we evaluated the consistency of alpha and beta diversity metrics between data resulting from these highly similar protocols. While we found minimal variation in alpha diversity between platform, significant differences were revealed with most beta diversity metrics, dependent on host species. These inconsistencies persisted following removal of low abundance taxa and when comparing across higher taxonomic levels, suggesting that bacterial community differences associated with sequencing protocol are likely to be context dependent and difficult to correct without extensive validation work. The results of this study encourage caution in the statistical comparison and interpretation of studies that combine rRNA gene sequence data from distinct protocols and point to a need for further work identifying mechanistic causes of these observed differences.

Morphological complexity affects the diversity of marine microbiomes.

Large eukaryotes support diverse communities of microbes on their surface-epibiota-that profoundly influence their biology. Alternate factors known to structure complex patterns of microbial diversity-host evolutionary history and ecology, environmental conditions and stochasticity-do not act independently and it is challenging to disentangle their relative effects. Here, we surveyed the epibiota from 38 sympatric seaweed species that span diverse clades and have convergent morphology, which strongly influences seaweed ecology. Host identity explains most of the variation in epibiont communities and deeper host phylogenetic relationships (e.g., genus level) explain a small but significant portion of epibiont community variation. Strikingly, epibiota community composition is significantly influenced by host morphology and epibiota richness increases with morphological complexity of the seaweed host. This effect is robust after controlling for phylogenetic non-independence and is strongest for crustose seaweeds. We experimentally validated the effect of host morphology by quantifying bacterial community assembly on latex sheets cut to resemble three seaweed morphologies. The patterns match those observed in our field survey. Thus, biodiversity increases with habitat complexity in host-associated microbial communities, mirroring patterns observed in animal communities. We suggest that host morphology and structural complexity are underexplored mechanisms structuring microbial communities.

Genomic Rearrangements and Sequence Evolution across Brown Algal Organelles.

Organellar genomes serve as useful models for genome evolution and contain some of the most widely used phylogenetic markers, but they are poorly characterized in many lineages. Here, we report 20 novel mitochondrial genomes and 16 novel plastid genomes from the brown algae. We focused our efforts on the orders Chordales and Laminariales but also provide the first plastid genomes (plastomes) from Desmarestiales and Sphacelariales, the first mitochondrial genome (mitome) from Ralfsiales and a nearly complete mitome from Sphacelariales. We then compared gene content, sequence evolution rates, shifts in genome structural arrangements, and intron distributions across lineages. We confirm that gene content is largely conserved in both organellar genomes across the brown algal tree of life, with few cases of gene gain or loss. We further show that substitution rates are generally lower in plastid than mitochondrial genes, but plastomes are more variable in gene arrangement, as mitomes tend to be colinear even among distantly related lineages (with exceptions). Patterns of intron distribution across organellar genomes are complex. In particular, the mitomes of several laminarialean species possess group II introns that have T7-like ORFs, found previously only in mitochondrial genomes of Pylaiella spp. (Ectocarpales). The distribution of these mitochondrial introns is inconsistent with vertical transmission and likely reflects invasion by horizontal gene transfer between lineages. In the most extreme case, the mitome of Hedophyllum nigripes is ∼40% larger than the mitomes of close relatives because of these introns. Our results provide substantial insight into organellar evolution across the brown algae.