Temporal variability of sea surface temperature affects marine macrophytes range retractions as well as gradual warming.

Record mean sea surface temperatures (SST) during the past decades and marine heatwaves have been identified as responsible for severe impacts on marine ecosystems, but the role of changes in the patterns of temporal variability under global warming has been much less studied. We compare descriptors of two time series of SST, encompassing extirpations (i.e. local extinctions) of six cold-temperate macroalgae species at their trailing range edge. We decompose the effects of gradual warming, extreme events and intrinsic variability (e.g. seasonality). We also relate the main factors determining macroalgae range shifts with their life cycles characteristics and thermal tolerance. We found extirpations of macroalgae were related to stretches of coast where autumn SST underwent warming, increased temperature seasonality, and decreased skewness over time. Regardless of the species, the persisting populations shared a common environmental domain, which was clearly differentiated from those experiencing local extinction. However, macroalgae species responded to temperature components in different ways, showing dissimilar resilience. Consideration of multiple thermal manifestations of climate change is needed to better understand local extinctions of habitat-forming species. Our study provides a framework for the incorporation of unused measures of environmental variability while analyzing the distributions of coastal species.

Are clam-seagrass interactions affected by heatwaves during emersion?

The increased frequency of heatwaves expected in the context of global warming will affect socio-ecological systems such as shellfish beds at intertidal seagrass meadows. A mesocosm experiment was performed to assess the effects of a simulated atmospheric heatwave during low tide on the bioturbation indicators and growth of the commercial juvenile native Ruditapes decussatus and the introduced clam R. philippinarum, and on their interactions with the seagrass Zostera noltei. Under the heatwave, heat dissipation at 5 cm depth was significantly greater in the sediments below Z. noltei than below bare sand, the photosynthetic efficiency (Fv/Fm) of Z. noltei decreased and the clams tended to grow less. Furthermore, after the heatwave clams below bare sand tended to burrow deeper than those below Z. noltei, indicating that seagrass provided a refuge for clams. Ruditapes philippinarum grew less, and did not burrow as deeply as R. decussatus, which may imply greater vulnerability to desiccation and heat at low tide. The particle displacement coefficient (PDC) of R. philippinarum indicated lower bioturbation values in Z. noltei than in bare sand and was a suitable bioturbation indicator for juvenile Ruditapes spp. clams. In Z. noltei coexisting with R. philippinarum, the Fv/Fm values were higher than without clams after a recovery period, which may be linked to the assimilation of phosphate excreted by the clams and suggests a facilitative interaction. No such interaction was observed with R. deccusatus, probably because of its deeper burrowing depth. The findings suggest reciprocal facilitative interactions between R. philippinarum and Z. noltei and the potential contribution of Z. noltei to the sustainability of clams under global warming scenarios, which may support management actions aimed at enhancing the coexistence between shellfishing activities and seagrass conservation.

A regime shift in intertidal assemblages triggered by loss of algal canopies: A multidecadal survey.

Canopy-forming macroalgae recently experienced a worldwide decline. This is relevant, because canopies sustain complex food webs in temperate coasts. We assessed the die-back of the canopy-forming alga Fucus serratus in N Spain, at its warm distributional range boundary, and its effects on associated assemblages. We combined long-term descriptive surveys with canopy-removal experiments. Results showed that rapid shifts to turf-forming communities were mostly the direct consequence of the canopy loss, rather than a concurrent process directly triggered by climate change. The switch alters the whole food web, as the prominent role of F.serratus and other cold-temperate intertidal fucoids is not being replaced by functionally equivalent species. Canopy loss caused a rapid biotic homogenization at regional scale which is spreading towards the west, from the edge to the central part of the former distributional range of F.serratus in N Spain. The most obvious effect is the ecological and functional impoverishment of the coastal system.

Removal of an established invader can change gross primary production of native macroalgae and alter carbon flow in intertidal rock pools.

The impact of invasive species on recipient communities can vary with environmental context and across levels of biological complexity. We investigated how an established invasive seaweed species affected the biomass, eco-physiology, carbon and nitrogen storage capacity of native seaweeds at sites with a different environmental setting due to a persistent upwelling in northern Spain. We removed the invasive Japanese wireweed Sargassum muticum from intertidal rock pools once every month during a one-year period and used an in-situ stable isotope pulse-chase labeling to estimate gross primary production (GPP), nitrogen uptake rate, 13C-carbon and 15N-nitrogen storage capacities. Following the addition of 13C-enriched bicarbonate and 15N-enriched nitrate to the seawater in the rock pools during the period of the low tide, we sampled macroalgal thalli at incoming tide to determine label uptake rate. After four days, we sampled macroalgal assemblages to determine both label storage capacity and biomass. After one year of removal there was no change in the macroalgal assemblage. However, both the GPP and 13C-carbon storage capacity were higher in the turf-forming Corallina spp. and, sometimes, in the canopy-forming Bifurcaria bifurcata. Nitrogen uptake rate followed similar, but more variable results. Although S. muticum inhibited carbon storage capacity of native species, the assemblage-level 13C-carbon storage was similar in the S. muticum-removed and control rock pools because the presence of the invasive species compensated for the functional loss of native species, particularly at sites where it was most abundant. No obvious effects were observed in relation to the environmental setting. Overall, the effect of the invasive S. muticum on carbon flow appeared to be mediated both by the effects on resource-use efficiency of native species and by its own biomass. Integrating physiological and assemblage-level responses can provide a broad understanding of how invasive species affect recipient communities and ecosystem functioning.

Spatio-temporal dynamics of Codium populations along the rocky shores of N and NW Spain.

The green alga Codium fragile ssp. fragile (hereafter C. fragile) has long been assumed to outcompete and displace its native congeners via cryptic invasion. We analysed the population dynamics of the exotic C. fragile and native congeners and their relative abundance on intertidal shores in N-NW Spain. Our results did not support the existence of current competitive displacement by the exotic species. The presence of C. fragile was clearly seasonal, while the native C. tomentosum was more persistent throughout the year, due to a higher frequency of frond sprouting from perennial basal fragments. However, our results also indicated an increase in the proportion of C. fragile relative to native species towards inner areas of the Bay of Biscay, which was correlated with environmental gradients. The greater tolerance of C. fragile to environmental stress and its opportunistic abilities may favour establishment and spread of the species under a warming scenario.

Environmental and phenotypic heterogeneity of populations at the trailing range-edge of the habitat-forming macroalga Fucus serratus.

Empirical work on the dynamics of range limits of species distributions often lack replications of edge populations. We compared the local environment and performance of two groups of geographically peripheral populations of the foundation intertidal alga Fucus serratus L. at its southern range boundary in the NW Iberian Peninsula. Two populations were located on the Western Galician coast in large embayments or rias, and the other two on a Northern open coastal stretch in Lugo province. Sharp differences were detected in the local environment and performance of the two groups of populations. While recruitment was quite consistent throughout the year in rias, it was very limited and variable in Lugo. Furthermore, thalli from rias were severely damaged following their transplantation in Lugo, and poor conditions of local adult plants were detected there in subsequent years. These results suggest a higher vulnerability of Lugo populations under new climate conditions, while western rias, strongly influenced by upwelling events, feasibly act as contemporary refugia for this species. If sustained over time, these refugia may mitigate the retreat of the seaweed' rear-edge predicted by large spatial scale models.

Combining physiological threshold knowledge to species distribution models is key to improving forecasts of the future niche for macroalgae.

Species distribution models (SDM) are a useful tool for predicting species range shifts in response to global warming. However, they do not explore the mechanisms underlying biological processes, making it difficult to predict shifts outside the environmental gradient where the model was trained. In this study, we combine correlative SDMs and knowledge on physiological limits to provide more robust predictions. The thermal thresholds obtained in growth and survival experiments were used as proxies of the fundamental niches of two foundational marine macrophytes. The geographic projections of these species' distributions obtained using these thresholds and existing SDMs were similar in areas where the species are either absent-rare or frequent and where their potential and realized niches match, reaching consensus predictions. The cold-temperate foundational seaweed Himanthalia elongata was predicted to become extinct at its southern limit in northern Spain in response to global warming, whereas the occupancy of southern-lusitanic Bifurcaria bifurcata was expected to increase. Combined approaches such as this one may also highlight geographic areas where models disagree potentially due to biotic factors. Physiological thresholds alone tended to over-predict species prevalence, as they cannot identify absences in climatic conditions within the species' range of physiological tolerance or at the optima. Although SDMs tended to have higher sensitivity than threshold models, they may include regressions that do not reflect causal mechanisms, constraining their predictive power. We present a simple example of how combining correlative and mechanistic knowledge provides a rapid way to gain insight into a species' niche resulting in consistent predictions and highlighting potential sources of uncertainty in forecasted responses to climate change.

Coexistence of congeneric native and invasive species: the case of the green algae Codium spp. in northwestern Spain.

We examined the patterns of distribution and abundance, and reproductive traits (presence of gametophytes and size at time of reproduction) in the invasive Codium fragile ssp. fragile and the native C. tomentosum and C. vermilara on intertidal habitats of NW Spain at two dates. All three species coexist in the locations and habitats studied, although abundances were low. We found a greater proportion of C. fragile ssp. fragile towards the east of the Cantabrian coast and on upper levels on the shore, where conditions are more stressful. The proportion of thalli bearing gametangia in C. fragile ssp. fragile was greater than in the native species in all habitats. The presence of gametangia was size-dependent for all species, with the invasive species maturing at a smaller size, which combined with the previous features, might confer competitive advantages to this species over the native species. We also demonstrated that molecular analyses are necessary for the correct identification of C. fragile subspecies.