Restore or Redefine:Future Trajectories for Restoration

Global habitat deterioration of marine ecosystems has led to a need for active interventions to halt or reverse the loss of ecological function. Restoration has historically been a key tool to reverse habitat loss and restore functions, but the extent to which this will be sufficient under future climates is uncertain. Emerging genetic technologies now provide the ability for restoration to proactively match adaptability of target species to predicted future environmental conditions, which opens up the possibility of boosting resistance to future stress in degraded and threatened habitats. As such, the choice of whether to restore to historical baselines or anticipate the future remains a key decision that will influence restoration success in the face of environmental and climate change. Here, we present an overview of the different motives for restoration – to recover or revive lost or degraded habitats to extant or historical states, or to reinforce or redefine for future conditions. We focus on the genetic and adaptive choices that underpin each option and subsequent consequences for restoration success. These options span a range of possible trajectories, technological advances and societal acceptability, and represent a framework for progressing restoration of marine habitat forming species into the future

A communal catalogue reveals Earth’s multiscale microbial diversity

Our growing awareness of the microbial world’s importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth’s microbial diversity

A communal catalogue reveals Earth's multiscale microbial diversity

Our growing awareness of the microbial world's importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth's microbial diversity.Peer reviewe

Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed

Macroalgal surfaces support abundant and diverse microorganisms within biofilms, which are often involved in fundamental functions relating to the health and defence of their seaweed hosts, including algal development, facilitation of spore release and chemical antifouling. Given these intimate and important interactions, environmental changes have the potential to negatively impact macroalgae by disrupting seaweed-microbe interactions. We used the disappearance of the dominant canopy-forming fucoid Phyllospora comosa from the metropolitan coast of Sydney, Australia as a model system to study these interactions. We transplanted Phyllospora individuals from nearby, extant populations back onto reefs in Sydney to test whether bacterial assemblages associated with seaweed surfaces would be influenced by (i) the host itself, independently of where it occurs, (ii) the type of habitat where the host occurs or (iii) site-specific differences. Analyses of bacterial DNA fingerprints (TRFLPs) indicated that assemblages of bacteria on Phyllospora were not habitat-specific. Rather, they were primarily influenced by local, site-specific conditions with some evidence for host-specificity in some cases. This could suggest a lottery model of host-surface colonisation, by which hosts are colonised by ‘suitable’ bacteria available in the local species pool, resulting in high variability in assemblage structure across sites, but where some species in the community are specific to the host and possibly influenced by differences in host traits

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.Published versionThis work was funded by the Australian Research Council through a Linkage Project to P.D.S., E.M.M., A.V., A.H.C. and M.A.C. (LP160100836), Discovery Projects to A.V. and P.D.S. (DP170100023) and P.D.S. and E.M.M. (DP180104041), and the Ecological Society of Australia through a Holsworth Wildlife Research Endowment to G.W. and E.M.M. Open access publishing facilitated by The University of Sydney, as part of the Wiley - The University of Sydney agreement via the Council of Australian University Librarians

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.SS was supported by an Australian Government Research Training Program (RTP) Scholarship. Funding was provided by the Australian Research Council (DP160100114, DP200100201, TW, MC; DP170100023, TW, AV; DP180104041, EM; DP190102030, AV; LP160100836, EM, AV, MC; DP150104263, BK)

Coastal urbanisation affects microbial communities on a dominant marine holobiont

Host-associated microbial communities play a fundamental role in the life of eukaryotic hosts. It is increasingly argued that hosts and their microbiota must be studied together as 'holobionts' to better understand the effects of environmental stressors on host functioning. Disruptions of host–microbiota interactions by environmental stressors can negatively affect host performance and survival. Substantial ecological impacts are likely when the affected hosts are habitat-forming species (e.g., trees, kelps) that underpin local biodiversity. In marine systems, coastal urbanisation via the addition of artificial structures is a major source of stress to habitat formers, but its effect on their associated microbial communities is unknown. We characterised kelp-associated microbial communities in two of the most common and abundant artificial structures in Sydney Harbour—pier-pilings and seawalls—and in neighbouring natural rocky reefs. The kelp Ecklonia radiata is the dominant habitat-forming species along 8000 km of the temperate Australian coast. Kelp-associated microbial communities on pilings differed significantly from those on seawalls and natural rocky reefs, possibly due to differences in abiotic (e.g., shade) and biotic (e.g., grazing) factors between habitats. Many bacteria that were more abundant on kelp on pilings belonged to taxa often associated with macroalgal diseases, including tissue bleaching in Ecklonia. There were, however, no differences in kelp photosynthetic capacity between habitats. The observed differences in microbial communities may have negative effects on the host by promoting fouling by macroorganisms or by causing and spreading disease over time. This study demonstrates that urbanisation can alter the microbiota of key habitat-forming species with potential ecological consequences.Published versio

Variation in the density and body size of a threatened foundation species across multiple spatial scales

Population characteristics (e.g. density and body sizes) of foundation species can affect their own persistence and provisioning of ecosystem functions. Understanding the drivers of population characteristics of foundation species at multiple spatial scales is therefore critical for maximizing ecosystem functions of restored habitats. We analyzed variation in population characteristics (densities, 95th percentile, and median lengths of live oysters) of the Sydney rock oyster, Saccostrea glomerata, on remnant oyster reefs at regional scales (among three estuaries) along an approximately 250 km of coastline in New South Wales, Australia. We then analyzed how population characteristics were further related to spatial attributes at smaller spatial scales including within-patches (rugosity, distance to patch-edge, and elevation), whole-patches (size and shape), and among-patch (connectivity) within each estuary. The densities and body sizes of S. glomerata were related to spatial attributes occurring within-patch (e.g. elevation), whole-patch (e.g. shape), and landscape (i.e. connectivity) scales, but these relationships varied among estuaries. The greatest variation in oyster density and size occurred at regional scales, suggesting that processes acting at larger spatial scales (e.g. water quality and/or climate) set the context for smaller scale influences on oyster characteristics. Our results highlight the potential importance of incorporating site-specific, spatial attributes in the design of restored oyster reefs to maximize ecosystem services and functions provided by restoration efforts.Published versionResearch was funded by an Australian Research Council Linkage Grant LP180100732, in collaboration with The Nature Conservancy, NSW DPI, NSW Department of Planning, Industry, and Environment, and the Sydney Institute of Marine Science Foundation. R.C.L. was supported by a University of New South Wales University International Postgraduate Award (UIPA) during this research. Open access publishing facilitated by University of New South Wales, as part of the Wiley - University of New South Wales agreement via the Council of Australian University Librarians

Playing to the positives : using synergies to enhance kelp forest restoration

Kelp forests are highly productive foundation species along much of the world’s coastline. As a result, kelp are crucial to the ecological, social, and economic well-being of coastal communities. Yet, due to a combination of acute and chronic stressors, kelp forests are under threat and have declined in many locations worldwide. Active restoration of kelp ecosystems is an emerging field that aims to reverse these declines by mitigating negative stressors and then, if needed, introducing biotic material into the environment. To date, few restoration efforts have incorporated positive species interactions. This gap presents a potential shortcoming for the field as evidence from other marine ecosystems illustrates that the inclusion of positive species interactions can enhance restoration success. Additionally, as the climate continues to warm, this approach will be particularly pertinent as positive interactions can also expand the range of physical conditions under which species can persist. Here, we highlight how practitioners can use positive density dependence within and amongst kelp species to increase the chances of restoration success. At higher trophic levels, we emphasize how co-restoring predators can prime ecosystems for restoration. We also investigate how emerging technologies in genetic and microbial selection and manipulation can increase the tolerance of target species to warming and other stressors. Finally, we provide examples of how we can use existing anthropogenic activities to facilitate restoration while performing alternative purposes. As kelp forests continue to decline and the field of kelp restoration continues to develop, it is also important that we monitor these potential advancements and ensure they do not have unintended ecosystem effects, particularly with untested techniques such as genetic and microbial manipulations. Nevertheless, incorporating positive species interactions into future restoration practice stands to promote a more holistic form of restoration that also increases the likelihood of success in a shifting seascape.Published versio

Financial and Institutional Support Are Important for Large-Scale Kelp Forest Restoration

Kelps form extensive underwater forests that underpin valuable ecosystem goods and services in temperate and polar rocky coastlines globally. Stressors, such as ocean warming and pollution are causing regional declines of kelp forests and their associated services worldwide. Kelp forest restoration is becoming a prominent management intervention, but we have little understanding of what drives restoration success at appropriate spatial scales. Though most restoration guidelines stress the importance of planning, stressor mitigation and ecological knowledge, other factors, such as lack of resources or institutional support are rarely discussed despite being potentially critical to achieving desired restoration outcomes. In this paper, we work to understand the importance of finances and institutions in the context of four of the world’s largest kelp restoration projects. These projects span four countries, six kelp genera and were initiated in response to different causes of decline. We argue that to restore kelp at desired scales, adequate financing, and institutional support are critical to overcome ecological and environmental limitations. Acknowledging limitations, we outline ways to mobilize resources and encourage institutions to support kelp restoration.publishedVersio