The role of microbial biofilms in range shifts of marine habitat-forming organisms.

Marine species, such as corals and kelp, are responding to climate change by altering their distributions. Microbial biofilms underpin key processes that affect the establishment, maintenance, and function of these dominant habitat-formers. Climate-mediated changes to microbial biofilms can therefore strongly influence species' range shifts. Here, we review emerging research on the interactions between benthic biofilms and habitat-formers and identify two key areas of interaction where climate change can impact this dynamic: (i) via direct effects on biofilm composition, and (ii) via impacts on the complex feedback loops which exist between the biofilm microbes and habitat-forming organisms. We propose that these key interactions will be fundamental in driving the speed and extent of tropicalisation of coastal ecosystems under climate change.

Closing the gap between existing large-area imaging research and marine conservation needs.

Emerging technology has immense potential to increase the scale and efficiency of marine conservation. One such technology is large-area imaging (LAI), which relies on structure-from-motion photogrammetry to create composite products, including 3-dimensional (3-D) environmental models, that are larger in spatial extent than the individual images used to create them. Use of LAI has become widespread in certain fields of marine science, primarily to measure the 3D structure of benthic ecosystems and track change over time. However, the use of LAI in the field of marine conservation appears limited. We conducted a review of the coral reef literature on the use of LAI to identify research themes and regional trends in applications of this technology. We also surveyed 135 coral reef scientists and conservation practitioners to determine community familiarity with LAI, evaluate barriers practitioners face in using LAI, and identify applications of LAI believed to be most exciting or relevant to coral conservation. Adoption of LAI was limited primarily to researchers at institutions based in advanced economies and was applied infrequently to conservation, although conservation practitioners and survey respondents from emerging economies indicated they expect to use LAI in the future. Our results revealed disconnect between current LAI research topics and conservation priorities identified by practitioners, highlighting the need for more diverse, conservation-relevant research using LAI. We provide recommendations for how early adopters of LAI (typically Global North scientists from well-resourced institutions) can facilitate access to this conservation technology. These recommendations include developing training resources, creating partnerships for data storage and analysis, publishing standard operating procedures for LAI workflows, standardizing methods, developing tools for efficient data extraction from LAI products, and conducting conservation-relevant research using LAI.

Reducción de la brecha entre la investigación actual de imágenes de gran superficie y las necesidades de la conservación marina Resumen Las nuevas tecnologías tienen un enorme potencial para aumentar la escala y la eficiencia de la conservación marina. Una de ellas son las imágenes de gran superficie (IGS), que se basan en la fotogrametría de estructura a partir del movimiento para crear productos compuestos, incluidos modelos ambientales tridimensionales (3D), cuya extensión espacial es mayor que la de las imágenes individuales utilizadas para crearlos. El uso de las IGS se ha generalizado en determinados campos de las ciencias marinas, principalmente para medir la estructura tridimensional de los ecosistemas bentónicos y realizar un seguimiento de los cambios a lo largo del tiempo. Sin embargo, el uso de las IGS en el campo de la conservación marina parece limitado. Realizamos una revisión de la bibliografía sobre el uso de las IGS en los arrecifes de coral para identificar temas de investigación y tendencias regionales en las aplicaciones de esta tecnología. También encuestamos a 135 científicos de arrecifes de coral y profesionales de la conservación para determinar la familiaridad de la comunidad con las IGS, evaluar las barreras a las que se enfrentan los profesionales en el uso de las IGS e identificar sus aplicaciones consideradas como las más interesantes o relevantes para la conservación del coral. La adopción de las IGS se limitó principalmente a los investigadores de las instituciones con sede en las economías avanzadas y se aplicó con poca frecuencia a la conservación, aunque los profesionales de la conservación y los encuestados de las economías emergentes indicaron que esperan utilizar las IGS en el futuro. Nuestros resultados revelaron una desconexión entre los actuales temas de investigación de las IGS y las prioridades de conservación identificadas por los profesionales, lo que subraya la necesidad de una investigación más diversa y relevante para la conservación mediante el uso de las IGS.

Optimising sampling of fish assemblages on intertidal reefs using remote underwater video.

Background: Assessing fish assemblages in subtidal and intertidal habitats is challenging due to the structural complexity of many of these systems. Trapping and collecting are regarded as optimal ways to sample these assemblages, but this method is costly and destructive, so researchers also use video techniques. Underwater visual census and baited remote underwater video stations are commonly used to characterise fish communities in these systems. More passive techniques such as remote underwater video (RUV) may be more appropriate for behavioural studies, or for comparing proximal habitats where the broad attraction caused by bait plumes could be an issue. However, data processing for RUVs can be time consuming and create processing bottlenecks. Methods: Here, we identified the optimal subsampling method to assess fish assemblages on intertidal oyster reefs using RUV footage and bootstrapping techniques. We quantified how video subsampling effort and method (systematic vs random) affect the accuracy and precision of three different fish assemblage metrics; species richness and two proxies for the total abundance of fish, MaxNT and MeanCountT, which have not been evaluated previously for complex intertidal habitats. Results: Results suggest that MaxNT and species richness should be recorded in real time, whereas optimal sampling for MeanCountT is every 60 s. Systematic sampling proved to be more accurate and precise than random sampling. This study provides valuable methodology recommendations which are relevant for the use of RUV to assess fish assemblages in a variety of shallow intertidal habitats.

No apparent trade-offs associated with heat tolerance in a reef-building coral.

As marine species adapt to climate change, their heat tolerance will likely be under strong selection. Yet trade-offs between heat tolerance and other life history traits could compromise natural adaptation or assisted evolution. This is particularly important for ecosystem engineers, such as reef-building corals, which support biodiversity yet are vulnerable to heatwave-induced mass bleaching and mortality. Here, we exposed 70 colonies of the reef-building coral Acropora digitifera to a long-term marine heatwave emulation experiment. We tested for trade-offs between heat tolerance and three traits measured from the colonies in situ - colony growth, fecundity, and symbiont community composition. Despite observing remarkable within-population variability in heat tolerance, all colonies were dominated by Cladocopium C40 symbionts. We found no evidence for trade-offs between heat tolerance and fecundity or growth. Contrary to expectations, positive associations emerged with growth, such that faster-growing colonies tended to bleach and die at higher levels of heat stress. Collectively, our results suggest that these corals exist on an energetic continuum where some high-performing individuals excel across multiple traits. Within populations, trade-offs between heat tolerance and growth or fecundity may not be major barriers to natural adaptation or the success of assisted evolution interventions.

Evaluating the effectiveness of drones for quantifying invasive upside-down jellyfish (Cassiopea sp.) in Lake Macquarie, Australia.

Upside-down jellyfish (Cassiopea sp.) are mostly sedentary, benthic jellyfish that have invaded estuarine ecosystems around the world. Monitoring the spread of this invasive jellyfish must contend with high spatial and temporal variability in abundance of individuals, especially around their invasion front. Here, we evaluated the utility of drones to survey invasive Cassiopea in a coastal lake on the east coast of Australia. To assess the efficacy of a drone-based methodology, we compared the densities and counts of Cassiopea from drone observations to conventional boat-based observations and evaluated cost and time efficiency of these methods. We showed that there was no significant difference in Cassiopea density measured by drones compared to boat-based methods along the same transects. However, abundance estimates of Cassiopea derived from scaling-up transect densities were over-inflated by 319% for drones and 178% for boats, compared to drone-based counts of the whole site. Although conventional boat-based survey techniques were cost-efficient in the short-term, we recommend doing whole-of-site counts using drones. This is because it provides a time-saving and precise technique for long-term monitoring of the spatio-temporally dynamic invasion front of Cassiopea in coastal lakes and other sheltered marine habitats with relatively clear water.

Photogrammetry as a tool to improve ecosystem restoration.

Ecosystem restoration has been practiced for over a century and is increasingly supported by the emergent applied science of restoration ecology. A prerequisite for successful ecosystem restoration is determining meaningful and measurable goals. This requires tools to monitor success in a standardized way. Photogrammetry uses images to reconstruct landscapes and organisms in three dimensions, enabling non-invasive measurement of key success indicators with unprecedented accuracy. We propose photogrammetry can improve restoration success by: (i) facilitating measurable goals; (ii) innovating and standardizing indicators of success; and (iii) standardizing monitoring. While the case we present is specific to coral reefs, photogrammetry has enormous potential to improve restoration practice in a wide range of ecosystems.

Genetic and phenotypic variation exhibit both predictable and stochastic patterns across an intertidal fish metapopulation.

Interactions among selection, gene flow, and drift affect the trajectory of adaptive evolution. In natural populations, the direction and magnitude of these processes can be variable across different spatial, temporal, or ontogenetic scales. Consequently, variability in evolutionary processes affects the predictability or stochasticity of microevolutionary outcomes. We studied an intertidal fish, Bathygobius cocosensis (Bleeker, 1854), to understand how space, time, and life stage structure genetic and phenotypic variation in a species with potentially extensive dispersal and a complex life cycle (larval dispersal preceding benthic recruitment). We sampled juvenile and adult life stages, at three sites, over three years. Genome-wide SNPs uncovered a pattern of chaotic genetic patchiness, that is, weak-but-significant patchy spatial genetic structure that was variable through time and between life stages. Outlier locus analyses suggested that targets of spatially divergent selection were mostly temporally variable, though a significant number of spatial outlier loci were shared between life stages. Head shape, a putatively ecologically responsive (adaptive) phenotype in B. cocosensis also exhibited high temporal variability within sites. However, consistent spatial relationships between sites indicated that environmental similarities among sites may generate predictable phenotype distributions across space. Our study highlights the complex microevolutionary dynamics of marine systems, where consideration of multiple ecological dimensions can reveal both predictable and stochastic patterns in the distributions of genetic and phenotypic variation. Such considerations probably apply to species that possess short, complex life cycles, have large dispersal potential and fecundities, and that inhabit heterogeneous environments.

Opposing life stage-specific effects of ocean warming at source and sink populations of range-shifting coral-reef fishes.

Climate change is altering the latitudinal distributions of species, with their capacity to keep pace with a shifting climate depending on the stochastic expression of population growth rates, and the influence of compensatory density feedback on age-specific survival rates. We use population-abundance time series at the leading edge of an expanding species' range to quantify the contribution of stochastic environmental drivers and density feedbacks to the dynamics of life stage-specific population growth. Using a tropical, range-shifting Indo-Pacific damselfish (Abudefduf vaigiensis) as a model organism, we applied variants of the phenomenological Gompertz-logistic model to a 14-year dataset to quantify the relative importance of density feedback and stochastic environmental drivers on the separate and aggregated population growth rates of settler and juvenile life stages. The top-ranked models indicated that density feedback negatively affected the growth of tropical settlers and juveniles. Rates of settlement were negatively linked to temperatures experienced by parents at potential source populations in the tropics, but their subsequent survival and that of juveniles increased with the temperatures experienced at the temperate sink. Including these stochastic effects doubled the deviance explained by the models, corroborating an important role of temperature. By incorporating sea-surface temperature projections for the remainder of this century into these models, we anticipate improved conditions for the population growth of juvenile coral-reef fishes, but not for settlers in temperate ecosystems. Previous research has highlighted the association between temperature and the redistribution of species. Our analyses reveal the contrasting roles of different life stages in the dynamics of range-shifting species responding to climate change, as they transition from vagrancy to residency in their novel ranges.

Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia.

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high-latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage-scale and genus-level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long-term mean temperatures during the hottest month of each year (SSTLTMAX ), and annual fluctuations in water temperature (SSTVAR ) and solar irradiance (PARZVAR ). The most severely-bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SSTLTMAX was low or PARZVAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally-abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage-scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage-scale bleaching was associated with local differences in species abundance and taxon-specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high-latitude endemics, point to climate-driven simplification of assemblage structures and progressive homogenisation of reef functions at these high-latitude locations.

Understanding interactions between plasticity, adaptation and range shifts in response to marine environmental change.

Climate change is leading to shifts in species geographical distributions, but populations are also probably adapting to environmental change at different rates across their range. Owing to a lack of natural and empirical data on the influence of phenotypic adaptation on range shifts of marine species, we provide a general conceptual model for understanding population responses to climate change that incorporates plasticity and adaptation to environmental change in marine ecosystems. We use this conceptual model to help inform where within the geographical range each mechanism will probably operate most strongly and explore the supporting evidence in species. We then expand the discussion from a single-species perspective to community-level responses and use the conceptual model to visualize and guide research into the important yet poorly understood processes of plasticity and adaptation. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Larval traits show temporally consistent constraints, but are decoupled from postsettlement juvenile growth, in an intertidal fish.

Complex life cycles may evolve to dissociate distinct developmental phases in an organism's lifetime. However, genetic or environmental factors may restrict trait independence across life stages, constraining ontogenetic trajectories. Quantifying covariance across life stages and their temporal variability is fundamental in understanding life-history phenotypes and potential distributions and consequences for selection. We studied developmental constraints in an intertidal fish (Bathygobius cocosensis: Gobiidae) with a discrete pelagic larval phase and benthic juvenile phase. We tested whether traits occurring earlier in life affected those expressed later, and whether larval traits were decoupled from postsettlement juvenile traits. Sampling distinct cohorts from three annual breeding seasons afforded tests of temporally variability in trait covariance. From otoliths (fish ear stones), we measured hatch size, larval duration, pelagic growth (larval traits) and early postsettlement growth (juvenile trait) in 124 juvenile B. cocoensis. We used path analyses to model trait relationships with respect to their chronological expression, comparing models among seasons. We also modelled the effect of season and hatch date on each individual trait to quantify their inherent variability. Our path analyses demonstrated a decoupling of larval traits on juvenile growth. Within the larval phase, longer larval durations resulted in greater pelagic growth, and larger size-at-settlement. There was also evidence that larger hatch size might reduce larval durations, but this effect was only marginally significant. Although pelagic and postsettlement growth were decoupled, pelagic growth had postsettlement consequences: individuals with high pelagic growth were among the largest fish at settlement, and remained among the largest early postsettlement. We observed no evidence that trait relationships varied among breeding seasons, but larval duration differed among breeding seasons, and was shorter for larvae hatching later within each season. Overall, we demonstrate mixed support for the expectation that traits in different life stages are independent. While postsettlement growth was decoupled from larval traits, pelagic development had consequences for the size of newly settled juveniles. Temporal consistency in trait covariances implies that genetic and/or environmental factors influencing them were stable over our three-year study. Our work highlights the importance of individual developmental experiences and temporal variability in understanding population distributions of life-history traits.

Large-scale assessment of benthic communities across multiple marine protected areas using an autonomous underwater vehicle.

Marine protected areas (MPAs) are designed to reduce threats to biodiversity and ecosystem functioning from anthropogenic activities. Assessment of MPAs effectiveness requires synchronous sampling of protected and non-protected areas at multiple spatial and temporal scales. We used an autonomous underwater vehicle to map benthic communities in replicate 'no-take' and 'general-use' (fishing allowed) zones within three MPAs along 7o of latitude. We recorded 92 taxa and 38 morpho-groups across three large MPAs. We found that important habitat-forming biota (e.g. massive sponges) were more prevalent and abundant in no-take zones, while short ephemeral algae were more abundant in general-use zones, suggesting potential short-term effects of zoning (5-10 years). Yet, short-term effects of zoning were not detected at the community level (community structure or composition), while community structure varied significantly among MPAs. We conclude that by allowing rapid, simultaneous assessments at multiple spatial scales, autonomous underwater vehicles are useful to document changes in marine communities and identify adequate scales to manage them. This study advanced knowledge of marine benthic communities and their conservation in three ways. First, we quantified benthic biodiversity and abundance, generating the first baseline of these benthic communities against which the effectiveness of three large MPAs can be assessed. Second, we identified the taxonomic resolution necessary to assess both short and long-term effects of MPAs, concluding that coarse taxonomic resolution is sufficient given that analyses of community structure at different taxonomic levels were generally consistent. Yet, observed differences were taxa-specific and may have not been evident using our broader taxonomic classifications, a classification of mid to high taxonomic resolution may be necessary to determine zoning effects on key taxa. Third, we provide an example of statistical analyses and sampling design that once temporal sampling is incorporated will be useful to detect changes of marine benthic communities across multiple spatial and temporal scales.

3D photogrammetry quantifies growth and external erosion of individual coral colonies and skeletons.

Growth and contraction of ecosystem engineers, such as trees, influence ecosystem structure and function. On coral reefs, methods to measure small changes in the structure of microhabitats, driven by growth of coral colonies and contraction of skeletons, are extremely limited. We used 3D reconstructions to quantify changes in the external structure of coral colonies of tabular Acropora spp., the dominant habitat-forming corals in shallow exposed reefs across the Pacific. The volume and surface area of live colonies increased by 21% and 22%, respectively, in 12 months, corresponding to a mean annual linear extension of 5.62 cm yr-1 (±1.81 SE). The volume and surface area of dead skeletons decreased by 52% and 47%, respectively, corresponding to a mean decline in linear extension of -29.56 cm yr-1 (±7.08 SE), which accounted for both erosion and fragmentation of dead colonies. This is the first study to use 3D photogrammetry to assess fine-scale structural changes of entire individual colonies in situ, quantifying coral growth and contraction. The high-resolution of the technique allows for detection of changes on reef structure faster than other non-intrusive approaches. These results improve our capacity to measure the drivers underpinning ecosystem biodiversity, status and trajectory.

Global warming and recurrent mass bleaching of corals.

During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Variable responses of benthic communities to anomalously warm sea temperatures on a high-latitude coral reef.

High-latitude reefs support unique ecological communities occurring at the biogeographic boundaries between tropical and temperate marine ecosystems. Due to their lower ambient temperatures, they are regarded as potential refugia for tropical species shifting poleward due to rising sea temperatures. However, acute warming events can cause rapid shifts in the composition of high-latitude reef communities, including range contractions of temperate macroalgae and bleaching-induced mortality in corals. While bleaching has been reported on numerous high-latitude reefs, post-bleaching trajectories of benthic communities are poorly described. Consequently, the longer-term effects of thermal anomalies on high-latitude reefs are difficult to predict. Here, we use an autonomous underwater vehicle to conduct repeated surveys of three 625 m(2) plots on a coral-dominated high-latitude reef in the Houtman Abrolhos Islands, Western Australia, over a four-year period spanning a large-magnitude thermal anomaly. Quantification of benthic communities revealed high coral cover (>70%, comprising three main morphospecies) prior to the bleaching event. Plating Montipora was most susceptible to bleaching, but in the plot where it was most abundant, coral cover did not change significantly because of post-bleaching increases in branching Acropora. In the other two plots, coral cover decreased while macroalgal cover increased markedly. Overall, coral cover declined from 73% to 59% over the course of the study, while macroalgal cover increased from 11% to 24%. The significant differences in impacts and post-bleaching trajectories among plots underline the importance of understanding the underlying causes of such variation to improve predictions of how climate change will affect reefs, especially at high-latitudes.

Patterns of the non-indigenous isopod Cirolana harfordi in Sydney Harbour.

Biological introductions can alter the ecology of local assemblages and are an important driver of global environmental change. The first step towards understanding the impact of a non-indigenous species is to study its distribution and associations in the invaded area. In Sydney Harbour, the non-indigenous isopod Cirolana harfordi has been reported in densities up to 0.5 individuals per cm(2) in mussel-beds. Abundances of this species have, however, been largely overlooked in other key habitats. The first aim of this study was to evaluate the abundances and distribution of C. harfordi across different habitats representative of Sydney Harbour. Results showed that C. harfordi occurred in oyster and mussel-beds, being particularly abundant in oyster-beds. We also aimed to determine the role of C. harfordi as a predator, scavenger and detritus feeder by investigating the relationships between densities of C. harfordi and (i) the structure of the resident assemblages, and (ii) deposited organic matter in oyster-beds. Densities of C. harfordi were not related to the structure of the assemblages, nor amounts of deposited organic matter. These findings suggested little or no ecological impacts of C. harfordi in oyster-beds. These relationships may, however, affect other variables such as growth of individuals, or be disguised by high variability of assemblages among different locations. Future studies should, therefore, test the impacts of C. harfordi on the size of organisms in the assemblage and use manipulative experiments to control for spatial variation. This study is the first published work on the ecology of the invasion of C. harfordi and provides the starting-point for the study of the impacts of this species in Sydney Harbour.

Selective mortality of a coral reef damselfish: role of predator-competitor synergisms.

Phenotypic variability within cohorts of juvenile organisms can serve as the basis for selective mortality. Previous studies have demonstrated the important role that predators play in this process but not the impact of competitors on selective predation. We use a combination of lab and field studies to evaluate the effect of the presence of adult competitor damselfish (Dascyllus aruanus and Pomacentrus moluccensis; family Pomacentridae) on the selective mortality of newly-arrived (settled) lemon damselfish (P. moluccensis) by resident predator fishes (Pseudochromis fuscus Pseudochromidae and Cheilodipterus quinquelineatus Apogonidae). Lab trials consisted of mesocosm experiments in which the behaviour, mortality, and physiological condition (measured as lipid content) of surviving P. moluccensis settlers from each of three treatments: (1) predators absent, (2) predators present, and (3) predators and competitors present, were compared. The field study involved stocking newly settled P. moluccensis on natural bommies (patch reefs) which had either been subject to a partial removal of resident fish (predators and competitors) or left alone. Results indicated there was very strong condition-based selective mortality in both the lab and field trials. In both cases there was a strong positive relationship between mortality and the lipid content of surviving fish; implying low-condition fish were selectively removed. The mesocosm trials indicated that the strength of mortality as well as condition selectivity was higher when competitors were present than when they were absent. Behavioural observations in the mesocosm study suggest that attention by juvenile P. moluccensis to the movements and occasional chases of the competitors (especially D. aruanus) reduced their vigilance to the predators. These results suggest the important and interactive roles which condition of newly settled reef fish and interspecific competition can play in the outcomes of post-settlement predation.