Organisms at hydrothermal vents inhabit discontinuous chemical "islands" along mid-ocean ridges, ... more Organisms at hydrothermal vents inhabit discontinuous chemical "islands" along mid-ocean ridges, a scenario that may promote genetic divergence among populations. The 2003 discovery of mussels at the Lost City Hydrothermal Field provided a means of evaluating factors that govern the biogeography of symbiotic bacteria in the deep-sea. The unusual chemical composition of vent fluids, the remote location, and paucity of characteristic vent macrofauna at the site, raised the question of whether microbial symbioses existed at the extraordinary Lost City. And if so, how did symbiotic bacteria therein relate to those hosted by invertebrates at the closest known hydrothermal vents along the Mid-Atlantic Ridge (MAR)? To answer these questions, we performed microscopic and molecular analyses on the bacteria found within the gill tissue of Bathymodiolus mussels (Mytilidae, Bathymodiolinae) that were discovered at the Lost City. Here we show that Lost City mussels harbour chemoautotrophic and methanotrophic endosymbionts simultaneously. Furthermore, populations of the chemoautotrophic symbionts from the Lost City and two sites along the MAR are genetically distinct from each other, which suggests spatial isolation of bacteria in the deep-sea. These findings provide new insights into the processes that drive diversification of bacteria and evolution of symbioses at hydrothermal vents.
Habitat selection by 3 Juan de Fuca Ridge gastropod species relates to their thermal environment.... more Habitat selection by 3 Juan de Fuca Ridge gastropod species relates to their thermal environment. Both collections and images taken along transects document the small-scale abundance patterns of each species with respect to temperature and distance from vent flows. Lepetodrilus fucensis and Depressigyra globulus were most abundant at distances from vent flows of 0 to 25 cm in warm fluids with high temperature variability (10 ± 5°C) over several time scales. Both species were also abundant at 26 to 50 cm, where temperatures were lower with less variability (4 ± 1°C). Provanna variabilis was most abundant from 51 to 75 cm, where temperatures were stable (3 ± 0.5°C). All species were absent where maximum fluid temperatures reached 18°C and their substratum coverage was related to temperature. When presented with a choice in vent fluids from 10 to 2°C, L. fucensis and D. globulus moved to areas with temperatures above 5°C, while P. variabilis showed no preference. In species-specific temperature preference experiments, L. fucensis and D. globulus aggregated between 5 and 13°C, while P. variabilis occupied areas with significantly lower temperatures from 4 to 11°C. These experimental temperature preferences correspond with their thermal environments. Upper temperature limits are moderate; extreme abiotic variability in higher temperature fluids may constrain these 3 species. We conclude thermal conditions are a primary determinant of habitat selection, thereby driving gastropod abundance patterns. However, other factors likely contribute. Space competition nearest vent flows may result in the displacement of individuals of these species to low quality habitats. KEY WORDS: Thermal variability • Abundance patterns • Hydrothermal vent • Lepetodrilus fucensis • Depressigyra globulus • Provanna variabilis • Preferences Resale or republication not permitted without written consent of the publisher Hydrothermal vent limpets form prominent stacks at densities as high as 300 000 ind. m -2 in the mixing zone between hydrothermal and deep-sea fluids. Although mean temperatures at their habitat are moderate, the limpets are exposed to haphazard fluctuations between 5 and 15°C.
Hydrothermal vent gastropods use diverse feeding mechanisms and can gain nutrition from symbionts... more Hydrothermal vent gastropods use diverse feeding mechanisms and can gain nutrition from symbionts. The Juan de Fuca Ridge limpet Lepetodrilus fucensis forms conspicuous stacks in hydrothermal flows and hosts filamentous bacterial episymbionts on its gill. The present study investigates whether its feeding strategy differs from those of several Lepetodrilus species without epibionts. A comparative approach was used to detect morphological features of the gill and digestive tissues that would indicate feeding specialisation. The gill lamellae of L. fucensis possess distinct features that are shared by several suspension-feeding gastropod genera: dense spacing of enlarged, unattached lamellae that do not narrow towards the tip and are stabilised by ciliary junctions. These modifications increase surface area and fluid velocities across the gill. Furthermore, the radular ribbon length, tooth cusp area and stomach volume of adult L. fucensis are significantly reduced, indicating that grazing may not be as efficient a feeding mechanism in comparison to non-symbiotic Lepetodrilus. Next, the feeding abilities of L. fucensis were evaluated using carmine red as a tracer for particle uptake in shipboard pressure vessels. Occasional grazing and active suspension feeding were documented. Dissections of animals and microscopy revealed that bacterium-like filaments accumulate at the lamellar tips, are formed into a cylindrical mass that is moved by cilia to the neck, and are sorted into accepted (passes to the mouth) and rejected material. The morphological specialisations of L. fucensis gills allow effective processing of suspended particles and provide a pathway whereby the episymbionts can be cultivated and ingested. The reduction in the radula and stomach are consistent with the hypothesis that adult L. fucensis primarily suspension feed and/or farm their gill symbionts. However, in peripheral locations, where suspended particle concentrations and chemical fluxes are low, grazing may be the only feasible option. Thus, L. fucensis can survive in a variety of habitats by using multiple feeding mechanisms.
The thermal characteristics of an organism ' s environment affect a multitude of parameters, from... more The thermal characteristics of an organism ' s environment affect a multitude of parameters, from biochemical to evolutionary processes. Hydrothermal vents on mid-ocean ridges are created when warm hydrothermal fl uids are ejected from the seafl oor and mixed with cold bottom seawater; many animals thrive along these steep temperature and chemical gradients. Twodimensional temperature maps at vent sites have demonstrated order of magnitude thermal changes over centimetre distances and at time intervals from minutes to hours. To investigate whether animals adapt to this extreme level of environmental variability, we examined differences in the thermal behaviour of mobile invertebrates from aquatic habitats that vary in thermal regime. Vent animals were highly responsive to heat and preferred much cooler fl uids than their upper thermal limits, whereas invertebrates from other aquatic environments risked exposure to warmer temperatures. Avoidance of temperatures well within their tolerated range may allow vent animals to maintain a safety margin against rapid temperature fl uctuations and concomitant toxicity of hydrothermal fl uids.
Changing biodiversity alters ecosystem functioning in nature, but the degree to which this relati... more Changing biodiversity alters ecosystem functioning in nature, but the degree to which this relationship depends on the taxonomic identities rather than the number of species remains untested at broad scales. Here, we partition the effects of declining species richness and changing community composition on fish community biomass across >3000 coral and rocky reef sites globally. We find that high biodiversity is 5.7x more important in maximizing biomass than the remaining influence of other ecological and environmental factors. Differences in fish community biomass across space are equally driven by both reductions in the total number of species and the disproportionate loss of larger-than-average species, which is exacerbated at sites impacted by humans. Our results confirm that sustaining biomass and associated ecosystem functions requires protecting diversity, most importantly of multiple large-bodied species in areas subject to strong human influences.
Thermal physiological tolerances of N. deaurata were mismatched to experienced environment. • A c... more Thermal physiological tolerances of N. deaurata were mismatched to experienced environment. • A cold climate legacy makes N. deaurata vulnerable to climate change. • N. deaurata physiology suggests it is suited to "invade" the Southern Ocean. • This study shows how evolutionary constraints can confound macrophysiological expectations.
Extrapolating patterns from individuals to populations informs climate vulnerability models, yet ... more Extrapolating patterns from individuals to populations informs climate vulnerability models, yet biological responses to warming are uncertain at both levels. Here we contrast data on the heating tolerances of fishes from laboratory experiments with abundance patterns of wild populations. We find that heating tolerances in terms of individual physiologies in the lab and abundance in the wild decline with increasing temperature at the same rate. However, at a given acclimation temperature or optimum temperature, tropical individuals and populations have broader heating tolerances than temperate ones. These congruent relationships implicate a tight coupling between physiological and demographic processes underpinning macroecological patterns, and identify vulnerability in both temperate and tropical species.
Climate change and other anthropogenic drivers of biodiversity change are unequally distributed a... more Climate change and other anthropogenic drivers of biodiversity change are unequally distributed across the world. Overlap in the distributions of different drivers have important implications for biodiversity change attribution and the potential for interactive effects. However, the spatial relationships among different drivers and whether they differ between the terrestrial and marine realm has yet to be examined. We compiled global gridded datasets on climate change, land‐use, resource exploitation, pollution, alien species potential and human population density. We used multivariate statistics to examine the spatial relationships among the drivers and to characterize the typical combinations of drivers experienced by different regions of the world. We found stronger positive correlations among drivers in the terrestrial than in the marine realm, leading to areas with high intensities of multiple drivers on land. Climate change tended to be negatively correlated with other drivers...
Climate change is reshaping global biodiversity as species respond to changing temperatures. Howe... more Climate change is reshaping global biodiversity as species respond to changing temperatures. However, the net effects of climate-driven species redistribution on local assemblage diversity remain unknown. Here, we relate trends in species richness and abundance from 21,500 terrestrial and marine assemblage time series across temperate regions (23.5-60.0°) to changes in air or sea surface temperature. We find a strong coupling between biodiversity and temperature changes in the marine realm, which is conditional on the baseline climate. We detect increases in species richness with increasing temperature that is twice as pronounced in warmer locations, while abundance declines with warming in the warmest marine locations. In contrast, we did not detect systematic temperature-related richness or abundance trends on land, despite a greater magnitude of warming. We also found no evidence for an interaction between biodiversity change and latitude, further emphasizing the importance of ba...
Among the most enduring ecological challenges is an integrated theory explaining the latitudinal ... more Among the most enduring ecological challenges is an integrated theory explaining the latitudinal biodiversity gradient, including discrepancies observed at different spatial scales. Analysis of Reef Life Survey data for 4127 marine species at 2406 coral and rocky sites worldwide confirms that the total ecoregion richness peaks in low latitudes, near +15°N and -15°S. However, although richness at survey sites is maximal near the equator for vertebrates, it peaks at high latitudes for large mobile invertebrates. Site richness for different groups is dependent on abundance, which is in turn correlated with temperature for fishes and nutrients for macroinvertebrates. We suggest that temperature-mediated fish predation and herbivory have constrained mobile macroinvertebrate diversity at the site scale across the tropics. Conversely, at the ecoregion scale, richness responds positively to coral reef area, highlighting potentially huge global biodiversity losses with coral decline. Improve...
Shifts in the abundance and location of species are restructuring life on the Earth, presenting t... more Shifts in the abundance and location of species are restructuring life on the Earth, presenting the need to build resilience into our natural systems. Here, we tested if protection from fishing promotes community resilience in temperate reef communities undergoing rapid warming in Tasmania. Regardless of protection status, we detected a signature of warming in the brown macroalgae, invertebrates and fishes, through increases in the local richness and abundance of warm-affinity species. Even so, responses in protected communities diverged from exploited communities. At the local scale, the number of cool-affinity fishes and canopy-forming algal species increased following protection, even though the observation window fell within a period of warming. At the same time, exploited communities gained turf algal and sessile invertebrate species. We further found that the recovery of predator populations following protection leads to marked declines in mobile invertebrates-this trend could...
Reporting progress against targets for international biodiversity agreements is hindered by a sho... more Reporting progress against targets for international biodiversity agreements is hindered by a shortage of suitable biodiversity data. We describe a cost-effective system involving Reef Life Survey citizen scientists in the systematic collection of quantitative data covering multiple phyla that can underpin numerous marine biodiversity indicators at high spatial and temporal resolution. We then summarize the findings of a continentaland decadal-scale State of the Environment assessment for rocky and coral reefs based on indicators of ecosystem state relating to fishing, ocean warming, and invasive species and describing the distribution of threatened species. Fishing impacts are widespread, whereas substantial warming-related change affected some regions between 2005 and 2015. Invasive species are concentrated near harbors in southeastern Australia, and the threatened-species index is highest for the Great Australian Bight and Tasman Sea. Our approach can be applied globally to improve reporting against biodiversity targets and enhance public and policymakers' understanding of marine biodiversity trends.
In an era of rapid global change, conservation managers urgently need improved tools to track and... more In an era of rapid global change, conservation managers urgently need improved tools to track and counter declining ecosystem conditions. This need is particularly acute in the marine realm, where threats are out of sight, inadequately mapped, cumulative, and often poorly understood, thereby generating impacts that are inefficiently managed. Recent advances in macroecology, statistical analysis, and the compilation of global data will play a central role in improving conservation outcomes, provided that global, regional, and local data streams can be integrated to produce locally relevant and interpretable outputs. Progress will be assisted by (a) expanded rollout of systematic surveys that quantify species patterns, including some carried out with help from citizen scientists; (b) coordinated experimental research networks that utilize large-scale manipulations to identify mechanisms underlying these patterns; (c) improved understanding of consequences of threats through the applic...
of calcified invertebrates (bivalves, gastropods, urchins and brachiopods), using a single consis... more of calcified invertebrates (bivalves, gastropods, urchins and brachiopods), using a single consistent methodology, including 11 species whose SMR was described for the first time. SMR of 15 out of 17 species had a mass-scaling exponent between 2/3 and 1, with no greater support for a 3/4 rather than a 2/3 scaling exponent. After accounting for taxonomy and variability in parameter estimates among species using variance-weighted linear mixed effects modelling, temperature sensitivity of SMR had an activation energy (Ea) of 0.16 for both Northern and Southern Hemisphere species which was lower than predicted under the metabolic theory of ecology (Ea 0.2-1.2 eV). Northern Hemisphere species, however, had a higher SMR at each habitat temperature, but a lower mass-scaling exponent relative to SMR. Evolutionary trade-offs that may be driving Abstract Metabolic rate is a key component of energy budgets that scales with body size and varies with largescale environmental geographical patterns. Here we conduct an analysis of standard metabolic rates (SMR) of marine ectotherms across a 70° latitudinal gradient in both hemispheres that spanned collection temperatures of 0-30 °C. To account for latitudinal differences in the size and skeletal composition between species, SMR was mass normalized to that of a standard-sized (223 mg) ash-free dry mass individual. SMR was measured for 17 species Communicated by Craig Osenberg.
Restricting human activities through Marine Protected Areas (MPAs) is assumed to create more resi... more Restricting human activities through Marine Protected Areas (MPAs) is assumed to create more resilient biological communities with a greater capacity to resist and recover following climate events. Here we review the evidence linking protection from local pressures (e.g., fishing and habitat destruction) with increased resilience. Despite strong theoretical underpinnings, studies have only rarely attributed resilience responses to the recovery of food webs and habitats, and increases in the diversity of communities and populations. When detected, resistance to ocean warming and recovery after extreme events in MPAs have small effect sizes against a backdrop of natural variability. By contrast, large die-offs are well described from MPAs following climate stress events. This may be in part because protection from one set of pressures or drivers (such as fishing) can select for species that are highly sensitive to others (such as warming), creating a 'Protection Paradox'. Given that climate change is overwhelming the resilience capacity of marine ecosystems, the only primary solution is to reduce carbon emissions. High-quality monitoring data in both space and time can also identify emergent resilience signals that do exist, in combination with adequate reference data to quantify the initial system state. This knowledge will allow networks of diverse protected areas to incorporate spatial refugia against climate change, and identify resilient biological components of natural systems. Sufficient spatial replication further offers insurance against losses in any given MPA, and the possibility for many weak signals of resilience to accumulate.
This study investigates wasting disease in the northeast Pacific keystone predatory sea star Pisa... more This study investigates wasting disease in the northeast Pacific keystone predatory sea star Pisaster ochraceus on the outer west coast of Vancouver Island (British Columbia, Canada). To quantify the effects of temperature, season and locality on the vulnerability of P. ochraceus to wasting disease, we conducted surveys and experiments in early and late summer. To test the prediction that a small increase in temperature would result in heightened infection intensities, we housed sea stars at different temperatures in the laboratory and caged sea stars subtidally at 2 depths. Prevalence and infection intensity were always higher in warm temperature treatments and did not differ between the sexes or with increasing size. Disease effects also varied with season and locality. Specimens held in aquaria displayed significantly higher disease prevalence and infection intensity in June versus August. Furthermore, sea stars from a sheltered inlet showed markedly higher prevalence of the disease in late summer, while wave-exposed sites had consistently low disease prevalence. Seasonal changes in reproductive potential, host condition and/or physiological acclimation, as well as differences in environmental regime among localities, may impact the dynamics of wasting disease. These results demonstrate that small increases in temperature could drive mass mortalities of Pisaster due to wasting disease, with vulnerability possibly reaching a peak in spring and in populations from sheltered localities. This is the most northern report of wasting disease in the class Asteroidea on the west coast of North America.
The GEO Handbook on Biodiversity Observation Networks, 2016
Recognition of the threats to biodiversity and its importance to society has led to calls for glo... more Recognition of the threats to biodiversity and its importance to society has led to calls for globally coordinated sampling of trends in marine ecosystems. As a step to defining such efforts, we review current methods of collecting and managing marine biodiversity data. A fundamental component of marine biodiversity is knowing what, where, and when species are present. However, monitoring methods are invariably biased in what taxa, ecological guilds, and body sizes they collect.
Marine invertebrates hosting chemosynthetic bacterial symbionts are known from multiple phyla and... more Marine invertebrates hosting chemosynthetic bacterial symbionts are known from multiple phyla and represent remarkable diversity in form and function. The deep-sea hydrothermal vent limpet Lepetodrilus fucensis from the Juan de Fuca Ridge complex hosts a gill symbiosis of particular interest because it displays a morphology unique among molluscs: filamentous bacteria are found partially embedded in the host's gill epithelium and extend into the fluids circulating across the lamellae. Our objective was to investigate the phylogenetic affiliation of the limpet's primary gill symbionts for comparison with previously characterized bacteria. Comparative 16S rRNA sequence analysis identified one γ- and three ε-Proteobacteria as candidate symbionts. We used fluorescence in situ hybridization (FISH) to test which of these four candidates occur with the limpet's symbiotic gill bacteria. The γ-proteobacterial probes consistently hybridized to the entire area where symbiotic bacter...
Aims: Contemporary climate change and biological invasions are two main drivers of biodiversity r... more Aims: Contemporary climate change and biological invasions are two main drivers of biodiversity redistribution. Interactive effects between these drivers have been reported in a variety of studies, yet results are conflicting. Some studies find that contemporary climate change facilitates the spread and success of non-native species, especially those with broad physiological tolerances. Other studies conclude that non-natives are vulnerable to current and future changes in climatic conditions. Given that most studies have focused on terrestrial species, here we contribute to this debate by analysing responses of marine native and non-native fauna and flora to key climate-related stressors, namely increased temperature (warming) and decreased salinity (freshening).
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