An invasive foundation species enhances multifunctionality in a coastal ecosystem.

While invasive species often threaten biodiversity and human well-being, their potential to enhance functioning by offsetting the loss of native habitat has rarely been considered. We manipulated the abundance of the nonnative, habitat-forming seaweed Gracilaria vermiculophylla in large plots (25 m2) on southeastern US intertidal landscapes to assess impacts on multiple ecosystem functions underlying coastal ecosystem services. We document that in the absence of native habitat formers, this invasion has an overall positive, density-dependent impact across a diverse set of ecosystem processes (e.g., abundance and richness of nursery taxa, flow attenuation). Manipulation of invader abundance revealed both thresholds and saturations in the provisioning of ecosystem functions. Taken together, these findings call into question the focus of traditional invasion research and management that assumes negative effects of nonnatives, and emphasize the need to consider context-dependence and integrative measurements when assessing the impact of an invader, including density dependence, multifunctionality, and the status of native habitat formers. This work supports discussion of the idea that where native foundation species have been lost, invasive habitat formers may be considered as sources of valuable ecosystem functions.

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.

Long-term community shifts driven by local extinction of an iconic foundation species following an extreme marine heatwave.

Gradual ocean warming combined with stronger marine heatwaves (MHWs) can reduce abundances of foundation species that control community structures, biodiversity, and ecosystem functioning. However, few studies have documented long-term succession trajectories following the more extreme events that cause localized extinctions of foundation species. Here, we documented long-term successional changes to marine benthic communities in Pile Bay, New Zealand, following the Tasman 2017/18 MHW, which caused localized extinctions of dominant southern bull kelp (Durvillaea sp.). Six years on, multiscale annual and seasonal surveys show no sign of Durvillaea recolonization. Instead, the invasive annual kelp (Undaria pinnatifida), rapidly colonized areas previously dominated by Durvillaea, followed by large changes to the understory community, as Durvillaea holdfasts and encrusting coralline algae were replaced by coralline turf. Between 3 and 6 years after the total loss of Durvillaea, smaller native fucoids colonized in high densities. Although Undaria initially colonized plots throughout Durvillaea's tidal range, later in the succession Undaria only retained dominance in the lower intertidal zone and only in spring. Ultimately, the tidal zone was slowly replaced by alternative foundation species, composed of different canopy-forming brown seaweeds that dominated different intertidal elevations, resulting in a net increase in canopy and understory diversity. This study is a rare example of long-term effects following an extreme MHW that caused extinctions of a locally dominant canopy-former, but these events and their associated dramatic changes to community structures and biodiversity are expected to become increasingly common as MHWs continue to increase in strength, frequency, and duration.

Spatiotemporal stressors, not secondary structures or small temperature increases, control rapid facilitation of intertidal epifauna.

Small animals (epifauna) are ubiquitous in marine systems. Epifauna have high secondary production and provide trophic linkages between primary producers and higher-order consumers, like fish. Despite their importance, little is known about how these animals respond to warming or how their communities vary across spatiotemporal gradients. Here we use mimics of turf seaweed and invasive kelp holdfast to test, in a 5-factorial field experiment, whether intertidal epifauna are facilitated by different habitat structures, temperature conditions, and along cooccurring spatiotemporal gradients. We found that facilitation of epifauna by intertidal turf seaweed peaked in summer, at low elevation, in older habitats and at a less wave-exposed site. However, epifauna were not affected by the presence of a secondary structure like kelp holdfast mimics or small temperature increases from passive solar heating of black and white mimics. There were many significant two-way, but few higher order interactions, showing stronger facilitation under specific environmental conditions, like at low elevation in summer, or low elevation in old habitats. These results highlight that turf-associated epifauna are controlled by vertical elevation, season, hydrodynamics, and habitat age, and appear to be resilient to small temperature increases. Findings are important to better understand linkages between primary producers and higher order consumers and system-wide productivity, and because fast growing turf, facilitated by global warming and eutrophication, are increasingly outcompeting slower growing large perennial canopy forming seaweeds, like kelp and rockweeds.

Facilitation of animals is stronger during summer marine heatwaves and around morphologically complex foundation species.

Foundation species create biogenic habitats, modify environmental conditions, augment biodiversity, and control animal community structures. In recent decades, marine heatwaves (MHWs) have affected the ecology of foundation species worldwide, and perhaps also their associated animal communities. However, no realistic field experiment has tested how MHWs affect animals that live in and around these foundation species. We therefore tested, in a four-factorial field experiment, if colonisation by small mobile marine animals (epifauna) onto plates with attached single versus co-occurring foundation species of different morphological complexities, were affected by 3-5°C heating (that mirrored a recent extreme MHW in the study area) and if the heating effect on the epifauna varied within and between seasons. For this experiment mimics of turf seaweed represented the single foundation species and holdfasts of seven common canopy-forming seaweed represented the co-occurring foundation species with different morphological complexities. We found that the taxonomic richness and total abundance of epifauna, dominated by copepods, generally were higher on heated plates with complex seaweed holdfasts in warmer summer trials. Furthermore, several interactions between test-factors were significant, e.g., epifaunal abundances, were, across taxonomic groups, generally higher in warmer than colder summer trials. These results suggest that, in temperate ecosystems, small, mobile, short-lived, and fast-growing marine epifauna can be facilitated by warmer oceans and morphologically complex foundation species, implying that future MHWs may increase secondary production and trophic transfers between primary producers and fish. Future studies should test whether these results can be scaled to other ecological species-interactions, across latitudes and biogeographical regions, and if similar results are found after longer MHWs or within live foundation species under real MHW conditions.

Biological Impacts of Marine Heatwaves.

Climatic extremes are becoming increasingly common against a background trend of global warming. In the oceans, marine heatwaves (MHWs)-discrete periods of anomalously warm water-have intensified and become more frequent over the past century, impacting the integrity of marine ecosystems globally. We review and synthesize current understanding of MHW impacts at the individual, population, and community levels. We then examine how these impacts affect broader ecosystem services and discuss the current state of research on biological impacts of MHWs. Finally, we explore current and emergent approaches to predicting the occurrence andimpacts of future events, along with adaptation and management approaches. With further increases in intensity and frequency projected for coming decades, MHWs are emerging as pervasive stressors to marine ecosystems globally. A deeper mechanistic understanding of their biological impacts is needed to better predict and adapt to increased MHW activity in the Anthropocene.

Herbivory limits success of vegetation restoration globally.

Restoring vegetation in degraded ecosystems is an increasingly common practice for promoting biodiversity and ecological function, but successful implementation is hampered by an incomplete understanding of the processes that limit restoration success. By synthesizing terrestrial and aquatic studies globally (2594 experimental tests from 610 articles), we reveal substantial herbivore control of vegetation under restoration. Herbivores at restoration sites reduced vegetation abundance more strongly (by 89%, on average) than those at relatively undegraded sites and suppressed, rather than fostered, plant diversity. These effects were particularly pronounced in regions with higher temperatures and lower precipitation. Excluding targeted herbivores temporarily or introducing their predators improved restoration by magnitudes similar to or greater than those achieved by managing plant competition or facilitation. Thus, managing herbivory is a promising strategy for enhancing vegetation restoration efforts.

Unravelling seasonal trends in coastal marine heatwave metrics across global biogeographical realms.

Marine heatwaves (MHWs) can cause dramatic changes to ecologically, culturally, and economically important coastal ecosystems. To date, MHW studies have focused on geographically isolated regions or broad-scale global oceanic analyses, without considering coastal biogeographical regions and seasons. However, to understand impacts from MHWs on diverse coastal communities, a combined biogeographical-seasonal approach is necessary, because (1) bioregions reflect community-wide temperature tolerances and (2) summer or winter heatwaves likely affect communities differently. We therefore carried out season-specific Theil-Sen robust linear regressions and Pettitt change point analyses from 1982 to 2021 on the number of events, number of MHW days, mean intensity, maximum intensity, and cumulative intensity of MHWs, for each of the world's 12 major coastal biogeographical realms. We found that 70% of 240 trend analyses increased significantly, 5% decreased and 25% were unaffected. There were clear differences between trends in metrics within biogeographical regions, and among seasons. For the significant increases, most change points occurred between 1998 and 2006. Regression slopes were generally positive across MHW metrics, seasons, and biogeographical realms as well as being highest after change point detection. Trends were highest for the Arctic, Northern Pacific, and Northern Atlantic realms in summer, and lowest for the Southern Ocean and several equatorial realms in other seasons. Our analysis highlights that future case studies should incorporate break point changes and seasonality in MHW analysis, to increase our understanding of how future, more frequent, and stronger MHWs will affect coastal ecosystems.

Heterogeneity within and among co-occurring foundation species increases biodiversity.

Habitat heterogeneity is considered a primary causal driver underpinning patterns of diversity, yet the universal role of heterogeneity in structuring biodiversity is unclear due to a lack of coordinated experiments testing its effects across geographic scales and habitat types. Furthermore, key species interactions that can enhance heterogeneity, such as facilitation cascades of foundation species, have been largely overlooked in general biodiversity models. Here, we performed 22 geographically distributed experiments in different ecosystems and biogeographical regions to assess the extent to which variation in biodiversity is explained by three axes of habitat heterogeneity: the amount of habitat, its morphological complexity, and capacity to provide ecological resources (e.g. food) within and between co-occurring foundation species. We show that positive and additive effects across the three axes of heterogeneity are common, providing a compelling mechanistic insight into the universal importance of habitat heterogeneity in promoting biodiversity via cascades of facilitative interactions. Because many aspects of habitat heterogeneity can be controlled through restoration and management interventions, our findings are directly relevant to biodiversity conservation.

A broad framework to organize and compare ecological invasion impacts.

Invasive species have transformed local, regional and global biotas; however, few generalities about the mechanisms driving impacts of invaders have emerged. To explain variation in impacts among studies, we propose a broad framework that separates drivers of impacts into universal and unique attributes of the invasive species and the invaded habitat. Universal attributes are relevant to all invasions whereas unique attributes are distinct to a specific invasion. For example, impacts associated with the abundance of any invader or the properties of a specific invader (e.g., a rare toxin) represent a universal and unique impact attribute. Through meta-analyses of aquatic field experiments, we demonstrate the utility of our framework, documenting that both the abundance and the taxonomic identity of the invader significantly influence invasion outcomes for marine and freshwater plant and animal invaders. Our review also highlights that many more experiments are needed to test for universal attributes, such as priority effects, age and size, and how the attributes of the invaded habitat further modify invasion impacts. We hope that our framework will stimulate experimental invasion ecology and begin to reconcile the idiosyncrasies that currently impede the development of a unified framework for invasion impacts.

An invasive species erodes the performance of coastal wetland protected areas.

The world has increasingly relied on protected areas (PAs) to rescue highly valued ecosystems from human activities, but whether PAs will fare well with bioinvasions remains unknown. By analyzing three decades of seven of the largest coastal PAs in China, including World Natural Heritage and/or Wetlands of International Importance sites, we show that, although PAs are achieving success in rescuing iconic wetlands and critical shorebird habitats from once widespread reclamation, this success is counteracted by escalating plant invasions. Plant invasions were not only more extensive in PAs than non-PA controls but also undermined PA performance by, without human intervention, irreversibly replacing expansive native wetlands (primarily mudflats) and precluding successional formation of new native marshes. Exotic species are invading PAs globally. This study across large spatiotemporal scales highlights that the consequences of bioinvasions for humanity's major conservation tool may be more profound, far reaching, and critical for management than currently recognized.

Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future.

Successful mitigation of negative effects of global warming will depend on understanding the link between physiological and ecological responses of key species. We show that while metabolic adjustment may assist Australasian kelp beds to persist and maintain abundance in warmer waters, it also reduces the physiological responsiveness of kelps to perturbation, and suppresses canopy recovery from disturbances by reducing the ecological performance of kelp recruits. This provides a warning not to rely solely on inventories of distribution and abundance to evaluate ecosystem function. The erosion of resilience is mediated by a shift in adult-juvenile interactions from competitive under cool to facilitative under warm conditions, supporting the prediction that positive interactions may become increasingly important in a warmer future. Kelp beds may remain intact but with a lower threshold for where additional impacts (e.g., extreme storms or reduced water quality) will lead to persistent loss of habitat and ecological function.

Habitat provided by native species facilitates higher abundances of an invader in its introduced compared to native range.

The impacts invasive species have on biodiversity and ecosystem function globally have been linked to the higher abundances they often obtain in their introduced compared to native ranges. Higher abundances of invaders in the introduced range are often explained by a reduction in negative species interactions in that range, although results are equivocal. The role of positive interactions in explaining differences in  the abundance of invaders between native and invasive ranges has not been tested. Using biogeographic surveys, we showed that the rocky shore porcelain crab, Petrolisthes elongatus, was ~4 times more abundant in its introduced (Tasmania, Australia) compared to its native (New Zealand) range. The habitat of these crabs in the invaded range (underside of intertidal boulders) was extensively covered with the habitat-forming tubeworm Galeolaria caespitosa. We tested whether the habitat provided by the tubeworm facilitates a higher abundance of the invasive crab by creating mimics of boulders with and without the tubeworm physical structure and measured crab colonisation into these habitats at three sites in both Tasmania and New Zealand. Adding the tubeworm structure increased crab abundance by an average of 85% across all sites in both ranges. Our intercontinental biogeographic survey and experiment demonstrate that native species can facilitate invader abundance and that positive interactions can be important drivers of invasion success.

Genetic diversity and kelp forest vulnerability to climatic stress.

Genetic diversity confers adaptive capacity to populations under changing conditions but its role in mediating impacts of climate change remains unresolved for most ecosystems. This lack of knowledge is particularly acute for foundation species, where impacts may cascade throughout entire ecosystems. We combined population genetics with eco-physiological and ecological field experiments to explore relationships among latitudinal patterns in genetic diversity, physiology and resilience of a kelp ecosystem to climate stress. A subsequent 'natural experiment' illustrated the possible influence of latitudinal patterns of genetic diversity on ecosystem vulnerability to an extreme climatic perturbation (marine heatwave). There were strong relationships between physiological versatility, ecological resilience and genetic diversity of kelp forests across latitudes, and genetic diversity consistently outperformed other explanatory variables in contributing to the response of kelp forests to the marine heatwave. Population performance and vulnerability to a severe climatic event were thus strongly related to latitudinal patterns in genetic diversity, with the heatwave extirpating forests with low genetic diversity. Where foundation species control ecological structure and function, impacts of climatic stress can cascade through the ecosystem and, consequently, genetic diversity could contribute to ecosystem vulnerability to climate change.

Secondary foundation species enhance biodiversity.

It has long been recognized that primary foundation species (FS), such as trees and seagrasses, enhance biodiversity. Among the species facilitated are secondary FS, including mistletoes and epiphytes. Case studies have demonstrated that secondary FS can further modify habitat-associated organisms ('inhabitants'), but their net effects remain unknown. Here we assess how inhabitants, globally, are affected by secondary FS. We extracted and calculated 2,187 abundance and 397 richness Hedges' g effect sizes from 91 and 50 publications, respectively. A weighted meta-analysis revealed that secondary FS significantly enhanced the abundance and richness of inhabitants compared to the primary FS alone. This indirect facilitation arising through sequential habitat formation was consistent across environmental and experimental conditions. Complementary unweighted analyses on log response ratios revealed that the magnitude of these effects was similar to the global average strength of direct facilitation from primary foundation species and greater than the average strength of trophic cascades, a widely recognized type of indirect facilitation arising through sequential consumption. The finding that secondary FS enhance the abundance and richness of inhabitants has important implications for understanding the mechanisms that regulate biodiversity. Integrating secondary FS into conservation practice will improve our ability to protect biodiversity and ecosystem function.

A review of three decades of research on the invasive kelp Undaria pinnatifida in Australasia: An assessment of its success, impacts and status as one of the world's worst invaders.

Marine invasive macroalgae can have severe local-scale impacts on ecological communities. The kelp Undaria pinnatifida is one of the most successful marine invasive species worldwide, and is widely regarded as one of the worst. Here, we review research on Undaria in Australasia, where the kelp is established throughout much of New Zealand and south-eastern Australia. The presence of Undaria for at least three decades in these locations makes Australasia one of the longest-invaded bioregions globally, and a valuable case study for considering Undaria's invasion success and associated impacts. In Australasia, Undaria has primarily invaded open spaces, turf communities, and gaps in native canopies within a relatively narrow elevation band on rocky shores. Despite its high biomass, Undaria has relatively few direct impacts on native species, and can increase community-wide attributes such as primary productivity and the provision of biogenic habitat. Therefore, Australasian Undaria research provides an example of a decoupling between the success and impact of an invasive species. Undaria will most likely continue to spread along thousands of kilometres of rocky coastline in temperate Australasia, due to its tolerance to large variations in temperature, ability to exploit disturbances to local communities, and the continued transfer among regions via vessel movements and aquaculture activities. However, the spread of Undaria remains difficult to manage as eradication is challenging and seldom successful. Therefore, understanding potential invasion pathways, maintaining native canopy-forming species that limit Undaria success, and effectively managing anthropogenic vectors of Undaria spread, should be key management priorities.

A sixth-level habitat cascade increases biodiversity in an intertidal estuary.

Many studies have documented habitat cascades where two co-occurring habitat-forming species control biodiversity. However, more than two habitat-formers could theoretically co-occur. We here documented a sixth-level habitat cascade from the Avon-Heathcote Estuary, New Zealand, by correlating counts of attached inhabitants to the size and accumulated biomass of their biogenic hosts. These data revealed predictable sequences of habitat-formation (=attachment space). First, the bivalve Austrovenus provided habitat for green seaweeds (Ulva) that provided habitat for trochid snails in a typical estuarine habitat cascade. However, the trochids also provided habitat for the nonnative bryozoan Conopeum that provided habitat for the red seaweed Gigartina that provided habitat for more trochids, thereby resetting the sequence of the habitat cascade, theoretically in perpetuity. Austrovenus is here the basal habitat-former that controls this "long" cascade. The strength of facilitation increased with seaweed frond size, accumulated seaweed biomass, accumulated shell biomass but less with shell size. We also found that Ulva attached to all habitat-formers, trochids attached to Ulva and Gigartina, and Conopeum and Gigartina predominately attached to trochids. These "affinities" for different habitat-forming species probably reflect species-specific traits of juveniles and adults. Finally, manipulative experiments confirmed that the amount of seaweed and trochids was important and consistent regulators of the habitat cascade in different estuarine environments. We also interpreted this cascade as a habitat-formation network that describes the likelihood of an inhabitant being found attached to a specific habitat-former. We conclude that the strength of the cascade increased with the amount of higher-order habitat-formers, with differences in form and function between higher and lower-order habitat-formers, and with the affinity of inhabitants for higher-order habitat-formers. We suggest that long habitat cascades are common where species traits allow for physical attachment to other species, such as in marine benthic systems and old forest.