Cross-basin and cross-taxa patterns of marine community tropicalization and deborealization in warming European seas.

Ocean warming and acidification, decreases in dissolved oxygen concentrations, and changes in primary production are causing an unprecedented global redistribution of marine life. The identification of underlying ecological processes underpinning marine species turnover, particularly the prevalence of increases of warm-water species or declines of cold-water species, has been recently debated in the context of ocean warming. Here, we track changes in the mean thermal affinity of marine communities across European seas by calculating the Community Temperature Index for 65 biodiversity time series collected over four decades and containing 1,817 species from different communities (zooplankton, coastal benthos, pelagic and demersal invertebrates and fish). We show that most communities and sites have clearly responded to ongoing ocean warming via abundance increases of warm-water species (tropicalization, 54%) and decreases of cold-water species (deborealization, 18%). Tropicalization dominated Atlantic sites compared to semi-enclosed basins such as the Mediterranean and Baltic Seas, probably due to physical barrier constraints to connectivity and species colonization. Semi-enclosed basins appeared to be particularly vulnerable to ocean warming, experiencing the fastest rates of warming and biodiversity loss through deborealization.

The genome sequence of the common limpet, Patella vulgata (Linnaeus, 1758).

We present a genome assembly from an individual Patella vulgata (the common limpet; Mollusca; Gastropoda; Patellogastropoda; Patellidae). The genome sequence is 695.4 megabases in span. Most of the assembly is scaffolded into 9 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 14.93 kilobases in length. Gene annotation of this assembly on Ensembl identified 19,378 protein coding genes.

Genome sequence for the thick topshell, Phorcus lineatus (da Costa, 1778).

We present a genome assembly from an individual Phorcus lineatus (the thick topshell; Mollusca; Gastropoda; Trochida; Trochidae). The genome sequence is 958 megabases in span. Most of the assembly (99.9%) is scaffolded into 18 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 19.1 kilobases in length.

Shoreline sentinels of global change show the consequences of extreme events.

Anthropogenic climate change along with the more frequent extreme weather it prompts, are having direct and indirect effects on distributions and abundance of species with consequence for community structure-especially if habitat providers are lost. Rocky shores have long been recognized as tractable experimental arenas for ecology contributing to theory. They have also emerged as important sentinel systems for tracking climate change responses of marine biodiversity and ecosystems, capitalizing on both historic broadscale surveys and time series. Combining these twin traditions is a powerful approach for better understanding and forecasting climate change impacts. Sustained observing allows extreme events to be detected and explored by in-parallel experimentation.

Applying landscape metrics to species distribution model predictions to characterize internal range structure and associated changes.

Distributional shifts in species ranges provide critical evidence of ecological responses to climate change. Assessments of climate-driven changes typically focus on broad-scale range shifts (e.g. poleward or upward), with ecological consequences at regional and local scales commonly overlooked. While these changes are informative for species presenting continuous geographic ranges, many species have discontinuous distributions-both natural (e.g. mountain or coastal species) or human-induced (e.g. species inhabiting fragmented landscapes)-where within-range changes can be significant. Here, we use an ecosystem engineer species (Sabellaria alveolata) with a naturally fragmented distribution as a case study to assess climate-driven changes in within-range occupancy across its entire global distribution. To this end, we applied landscape ecology metrics to outputs from species distribution modelling (SDM) in a novel unified framework. SDM predicted a 27.5% overall increase in the area of potentially suitable habitat under RCP 4.5 by 2050, which taken in isolation would have led to the classification of the species as a climate change winner. SDM further revealed that the latitudinal range is predicted to shrink because of decreased habitat suitability in the equatorward part of the range, not compensated by a poleward expansion. The use of landscape ecology metrics provided additional insights by identifying regions that are predicted to become increasingly fragmented in the future, potentially increasing extirpation risk by jeopardising metapopulation dynamics. This increased range fragmentation could have dramatic consequences for ecosystem structure and functioning. Importantly, the proposed framework-which brings together SDM and landscape metrics-can be widely used to study currently overlooked climate-driven changes in species internal range structure, without requiring detailed empirical knowledge of the modelled species. This approach represents an important advancement beyond predictive envelope approaches and could reveal itself as paramount for managers whose spatial scale of action usually ranges from local to regional.

Cold-induced [Ca2+]cyt elevations function to support osmoregulation in marine diatoms.

Diatoms are a group of microalgae that are important primary producers in a range of open ocean, freshwater, and intertidal environments. The latter can experience substantial long- and short-term variability in temperature, from seasonal variations to rapid temperature shifts caused by tidal immersion and emersion. As temperature is a major determinant in the distribution of diatom species, their temperature sensory and response mechanisms likely have important roles in their ecological success. We examined the mechanisms diatoms use to sense rapid changes in temperature, such as those experienced in the intertidal zone. We found that the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana exhibit a transient cytosolic Ca2+ ([Ca2+]cyt) elevation in response to rapid cooling, similar to those observed in plant and animal cells. However, [Ca2+]cyt elevations were not observed in response to rapid warming. The kinetics and magnitude of cold-induced [Ca2+]cyt elevations corresponded with the rate of temperature decrease. We did not find a role for the [Ca2+]cyt elevations in enhancing cold tolerance but showed that cold shock induces a Ca2+-dependent K+ efflux and reduces mortality of P. tricornutum during a simultaneous hypo-osmotic shock. As intertidal diatom species may routinely encounter simultaneous cold and hypo-osmotic shocks during tidal cycles, we propose that cold-induced Ca2+ signaling interacts with osmotic signaling pathways to aid in the regulation of cell volume. Our findings provide insight into the nature of temperature perception in diatoms and highlight that cross-talk between signaling pathways may play an important role in their cellular responses to multiple simultaneous stressors.

The genome sequence of the scale worm, Lepidonotus clava (Montagu, 1808).

We present a genome assembly from an individual Lepidonotus clava (scale worm; Annelida; Polychaeta; Phyllodocida; Polynoidae). The genome sequence is 1,044 megabases in span. Most of the assembly is scaffolded into 18 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 15.6 kilobases in length.

On the diversity and distribution of a data deficient habitat in a poorly mapped region: The case of Sabellaria alveolata L. in Ireland.

Data that can be used to monitor biodiversity through time are essential for conservation and management. The reef-forming worm, Sabellaria alveolata (L. 1767) is currently classed as 'Data Deficient' due to an imbalance in the spread of data on its distribution. Little is known about the distribution of this species around Ireland. Using data archaeology, we collated past and present distribution records and discovered that S. alveolata has a discontinuous distribution with large gaps between populations. Many regions lack data and should be targeted for sampling. Biodiversity surveys revealed that S. alveolata supported diverse epibiotic algal communities. Retrograding (declining) reefs supported greater infaunal diversity than prograding (growing) reefs or sand, suggesting that S. alveolata is a dynamic ecosystem engineer that has a lasting legacy effect. Similar research should be carried out for other Data Deficient species, habitats and regions. Such data are invaluable resources for management and conservation.

Long-term environmental tolerance of the non-indigenous Pacific oyster to expected contemporary climate change conditions.

The current global redistribution of biota is often attributed to two main drivers: contemporary climate change (CCC) and non-indigenous species (NIS). Despite evidence of synergetic effects, however, studies assessing long-term effects of CCC conditions on NIS fitness remain rare. We examined the interactive effects of warming, ocean acidification and reduced salinity on the globally distributed marine NIS Magallana gigas (Pacific oyster) over a ten-month period. Growth, clearance and oxygen consumption rates were measured monthly to assess individual fitness. Lower salinity had a significant, permanent effect on M. gigas, reducing and increasing clearance and oxygen consumption rates, respectively. Neither predicted increases in seawater temperature nor reduced pH had a long-term physiological effect, indicating conditions predicted for 2100 will not affect adult physiology and survival. These results suggest that M. gigas will remain a globally successful NIS and predicted CCC will continue to facilitate their competitive dominance in the near future.

Evolutionary Phycology: Toward a Macroalgal Species Conceptual Framework.

Species concepts formalize evolutionary and ecological processes, but often conflict with one another when considering the mechanisms that ultimately lead to species delimitation. Evolutionary biologists are, however, recognizing that the conceptualization of a species is separate and distinct from the delimitation of species. Indeed, if species are generally defined as separately evolving metapopulation lineages, then characteristics, such as reproductive isolation or monophyly, can be used as evidence of lineage separation and no longer conflict with the conceptualization of a species. However, little of this discussion has addressed the formalization of this evolutionary conceptual framework for macroalgal species. This may be due to the complexity and variation found in macroalgal life cycles. While macroalgal mating system variation and patterns of hybridization and introgression have been identified, complex algal life cycles generate unique eco-evolutionary consequences. Moreover, the discovery of frequent macroalgal cryptic speciation has not been accompanied by the study of the evolutionary ecology of those lineages, and, thus, an understanding of the mechanisms underlying such rampant speciation remain elusive. In this perspective, we aim to further the discussion and interest in species concepts and speciation processes in macroalgae. We propose a conceptual framework to enable phycological researchers and students alike to portray these processes in a manner consistent with dialogue at the forefront of evolutionary biology. We define a macroalgal species as an independently evolving metapopulation lineage, whereby we can test for reproductive isolation or the occupation of distinct adaptive zones, among other mechanisms, as secondary lines of supporting evidence.

A genome-wide investigation of the worldwide invader Sargassum muticum shows high success albeit (almost) no genetic diversity.

Twenty years of genetic studies of marine invaders have shown that successful invaders are often characterized by native and introduced populations displaying similar levels of genetic diversity. This pattern is presumably due to high propagule pressure and repeated introductions. The opposite pattern is reported in this study of the brown seaweed, Sargassum muticum, an emblematic species for circumglobal invasions. Albeit demonstrating polymorphism in the native range, microsatellites failed to detect any genetic variation over 1,269 individuals sampled from 46 locations over the Pacific-Atlantic introduction range. Single-nucleotide polymorphisms (SNPs) obtained from ddRAD sequencing revealed some genetic variation, but confirmed severe founder events in both the Pacific and Atlantic introduction ranges. Our study thus exemplifies the need for extreme caution in interpreting neutral genetic diversity as a proxy for invasive potential. Our results confirm a previously hypothesized transoceanic secondary introduction from NE Pacific to Europe. However, the SNP panel unexpectedly revealed two additional distinct genetic origins of introductions. Also, conversely to scenarios based on historical records, southern rather than northern NE Pacific populations could have seeded most of the European populations. Finally, the most recently introduced populations showed the lowest selfing rates, suggesting higher levels of recombination might be beneficial at the early stage of the introduction process (i.e., facilitating evolutionary novelties), whereas uniparental reproduction might be favored later in sustainably established populations (i.e., sustaining local adaptation).

Global-scale species distributions predict temperature-related changes in species composition of rocky shore communities in Britain.

Changes in rocky shore community composition as responses to climatic fluctuations and anthropogenic warming can be shown by changes in average species thermal affinities. In this study, we derived thermal affinities for European Atlantic rocky intertidal species by matching their known distributions to patterns in average annual sea surface temperature. Average thermal affinities (the Community Temperature Index, CTI) tracked patterns in sea surface temperature from Portugal to Norway, but CTI for communities of macroalgae and plant species changed less than those composed of animal species. This reduced response was in line with the expectation that communities with a smaller range of thermal affinities among species would change less in composition along thermal gradients and over time. Local-scale patterns in CTI over wave exposure gradients suggested that canopy macroalgae allow species with ranges centred in cooler than local temperatures ('cold-affinity') to persist in otherwise too-warm conditions. In annual surveys of rocky shores, communities of animal species in Shetland showed a shift in dominance towards warm-affinity species ('thermophilization') with local warming from 1980 to 2018 but the community of plant and macroalgal species did not. From 2002 to 2018, communities in southwest Britain showed the reverse trend in CTI: declining average thermal affinities over a period of modest temperature decline. Despite the cooling, trends in species abundance were in line with the general mechanism of direction and magnitude of long-term trends depending on the difference between species thermal affinities and local temperatures. Cold-affinity species increased during cooling and warm-affinity ones decreased. The consistency of responses across different communities and with general expectations based on species thermal characteristics suggests strong predictive accuracy of responses of community composition to anthropogenic warming.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

Historical comparisons reveal multiple drivers of decadal change of an ecosystem engineer at the range edge.

Biogenic reefs are important for habitat provision and coastal protection. Long-term datasets on the distribution and abundance of Sabellaria alveolata (L.) are available from Britain. The aim of this study was to combine historical records and contemporary data to (1) describe spatiotemporal variation in winter temperatures, (2) document short-term and long-term changes in the distribution and abundance of S. alveolata and discuss these changes in relation to extreme weather events and recent warming, and (3) assess the potential for artificial coastal defense structures to function as habitat for S. alveolata. A semi-quantitative abundance scale (ACFOR) was used to compare broadscale, long-term and interannual abundance of S. alveolata near its range edge in NW Britain. S. alveolata disappeared from the North Wales and Wirral coastlines where it had been abundant prior to the cold winter of 1962/1963. Population declines were also observed following the recent cold winters of 2009/2010 and 2010/2011. Extensive surveys in 2004 and 2012 revealed that S. alveolata had recolonized locations from which it had previously disappeared. Furthermore, it had increased in abundance at many locations, possibly in response to recent warming. S. alveolata was recorded on the majority of artificial coastal defense structures surveyed, suggesting that the proliferation of artificial coastal defense structures along this stretch of coastline may have enabled S. alveolata to spread across stretches of unsuitable natural habitat. Long-term and broadscale contextual monitoring is essential for monitoring responses of organisms to climate change. Historical data and gray literature can be invaluable sources of information. Our results support the theory that Lusitanian species are responding positively to climate warming but also that short-term extreme weather events can have potentially devastating widespread and lasting effects on organisms. Furthermore, the proliferation of coastal defense structures has implications for phylogeography, population genetics, and connectivity of coastal populations.

Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem.

Understanding long-term, ecosystem-level impacts of climate change is challenging because experimental research frequently focuses on short-term, individual-level impacts in isolation. We address this shortcoming first through an interdisciplinary ensemble of novel experimental techniques to investigate the impacts of 14-month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterize a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual-level responses, while acidification had a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual-level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large-scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local-environmental conditions and resource availability. Such changes in macro-scale distributions cannot be predicted by investigating individual-level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long-term, multiscale responses to multiple stressors, in an ecosystem context.

The future of the northeast Atlantic benthic flora in a high CO2 world.

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO2 emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf-forming seaweeds.

Climate change and adaptational impacts in coastal systems: the case of sea defences.

We briefly review how coastal ecosystems are responding to and being impacted by climate change, one of the greatest challenges facing society today. In adapting to rising and stormier seas associated with climate change, coastal defence structures are proliferating and becoming dominant coastal features, particularly in urbanised areas. Whilst the primary function of these structures is to protect coastal property and infrastructure, they inevitably have a significant secondary impact on the local environment and ecosystems. In this review we outline some of the negative and positive effects of these structures on physical processes, impacts on marine species, and the novel engineering approaches that have been employed to improve the ecological value of these structures in recent years. Finally we outline guidelines for an environmentally sensitive approach to design of such structures in the marine environment.

Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption.

Climate change may cause ecosystems to become trophically restructured as a result of primary producers and consumers responding differently to increasing CO2 and temperature. This study used an integrative approach using a controlled microcosm experiment to investigate the combined effects of CO2 and temperature on key components of the intertidal system in the UK, biofilms and their consumers (Littorina littorea). In addition, to identify whether pre-exposure to experimental conditions can alter experimental outcomes we explicitly tested for differential effects on L. littorea pre-exposed to experimental conditions for two weeks and five months. In contrast to predictions based on metabolic theory, the combination of elevated temperature and CO2 over a five-week period caused a decrease in the amount of primary productivity consumed by grazers, while the abundance of biofilms increased. However, long-term pre-exposure to experimental conditions (five months) altered this effect, with grazing rates in these animals being greater than in animals exposed only for two weeks. We suggest that the structure of future ecosystems may not be predictable using short-term laboratory experiments alone owing to potentially confounding effects of exposure time and effects of being held in an artificial environment over prolonged time periods. A combination of laboratory (physiology responses) and large, long-term experiments (ecosystem responses) may therefore be necessary to adequately predict the complex and interactive effects of climate change as organisms may acclimate to conditions over the longer term.

Dynamic species distribution models from categorical survey data.

1. Species distribution models are static models for the distribution of a species, based on Hutchinson's niche concept. They make probabilistic predictions about the distribution of a species, but do not have a temporal interpretation. In contrast, density-structured models based on categorical abundance data make it possible to incorporate population dynamics into species distribution modelling. 2. Using dynamic species distribution models, temporal aspects of a species' distribution can be investigated, including the predictability of future abundance categories and the expected persistence times of local populations, and how these may respond to environmental or anthropogenic drivers. 3. We built density-structured models for two intertidal marine invertebrates, the Lusitanian trochid gastropods Phorcus lineatus and Gibbula umbilicalis, based on 9 years of field data from around the United Kingdom. Abundances were recorded on a categorical scale, and stochastic models for year-to-year changes in abundance category were constructed with winter mean sea surface temperature (SST) and wave fetch (a measure of the exposure of a shore) as explanatory variables. 4. Both species were more likely to be present at sites with high SST, but differed in their responses to wave fetch. Phorcus lineatus had more predictable future abundance and longer expected persistence times than G. umbilicalis. This is consistent with the longer lifespan of P. lineatus. 5. Where data from multiple time points are available, dynamic species distribution models of the kind described here have many applications in population and conservation biology. These include allowing for changes over time when combining historical and contemporary data, and predicting how climate change might alter future abundance conditional on current distributions.