Temperate species underfill their tropical thermal potentials on land.

Understanding how temperature determines the distribution of life is necessary to assess species' sensitivities to contemporary climate change. Here, we test the importance of temperature in limiting the geographic ranges of ectotherms by comparing the temperatures and areas that species occupy to the temperatures and areas species could potentially occupy on the basis of their physiological thermal tolerances. We find that marine species across all latitudes and terrestrial species from the tropics occupy temperatures that closely match their thermal tolerances. However, terrestrial species from temperate and polar latitudes are absent from warm, thermally tolerable areas that they could potentially occupy beyond their equatorward range limits, indicating that extreme temperature is often not the factor limiting their distributions at lower latitudes. This matches predictions from the hypothesis that adaptation to cold environments that facilitates survival in temperate and polar regions is associated with a performance trade-off that reduces species' abilities to contend in the tropics, possibly due to biotic exclusion. Our findings predict more direct responses to climate warming of marine ranges and cool range edges of terrestrial species.

Half a century of thermal tolerance studies in springtails (Collembola): A review of metrics, spatial and temporal trends.

Global changes in soil surface temperatures are altering the abundances and distribution ranges of invertebrate species worldwide, including effects on soil microarthropods such as springtails (Collembola), which are vital for maintaining soil health and providing ecosystem services. Studies of thermal tolerance limits in soil invertebrates have the potential to provide information on demographic responses to climate change and guide assessments of possible impacts on the structure and functioning of ecosystems. Here, we review the state of knowledge of thermal tolerance limits in Collembola. Thermal tolerance metrics have diversified over time, which should be taken into account when conducting large-scale comparative studies. A temporal trend shows that the estimation of 'Critical Thermal Limits' (CTL) is becoming more common than investigations of 'Supercooling Point' (SCP), despite the latter being the most widely used metric. Indeed, most studies (66%) in Collembola have focused on cold tolerance; fewer have assessed heat tolerance. The majority of thermal tolerance data are from temperate and polar regions, with fewer assessments from tropical and subtropical latitudes. While the hemiedaphic life form represents the majority of records at low latitudes, euedaphic and epedaphic groups remain largely unsampled in these regions compared to the situation in temperate and high latitude regions, where sampling records show a more balanced distribution among the different life forms. Most CTL data are obtained during the warmest period of the year, whereas SCP and 'Lethal Temperature' (LT) show more variation in terms of the season when the data were collected. We conclude that more attention should be given to understudied zoogeographical regions across the tropics, as well as certain less-studied clades such as the family Neanuridae, to identify the role of thermal tolerance limits in the redistribution of species under changing climates.

The evolution of critical thermal limits of life on Earth.

Understanding how species' thermal limits have evolved across the tree of life is central to predicting species' responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary 'attractors' that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change.

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.

Ecophysiological responses of a threatened red alga to increased irradiance in an in situ transplant experiment.

The red alga Gelidium corneum is a dominant foundation species in the south-eastern Bay of Biscay, where a decline in its populations has been documented in the few last decades. We investigated the ecophysiological responses of G. corneum to different light conditions by means of an in situ transplant experiment. We found that the stress response measured by physiological and biochemical approaches was higher in G. corneum at higher irradiance levels, for both transplanted and control specimens, than under lower light intensities. In the former case the specimens showed a decrease in maximum quantum yield (Fv/Fm), maximum electron transport rate (ETRmax), photosynthetic efficiency (αETR), photosynthetic pigment contents, nitrogen content and thallus length, whereas the C:N ratio, MAAs and bleaching cover increased. In general terms, these responses were more evident in the apical parts of the thallus than in middle ones. Our results suggest that high light stress at depths of 3 m triggered photobiological changes in G. corneum, involving ineffective photoprotection and the occurrence of chronic photoinhibition. Therefore, considering the upward trend in summer mean surface solar radiation in the study area since the 80s, high light conditions may have played a role in the declines observed in G. corneum beds from the south-eastern Bay of Biscay.

Physiological responses to variations in grazing and light conditions in native and invasive fucoids.

Poor physiological acclimatization to climate change has led to shifts in the distributional ranges of various species and to biodiversity loss. However, evidence also suggests the relevance of non-climatic physical factors, such as light, and biotic factors, which may act in interactive or additive way. We used a mechanistic approach to evaluate the ecophysiological responses of four seaweed species (three dominant intertidal fucoids, Fucus serratus, Ascophyllum nodosum, Bifurcaria bifurcata, and the invasive Sargassum muticum) to different conditions of grazing, light irradiance and ultraviolet (UV) radiation. We performed a large-scale mesocosm experiment with a total of 800 individual thalli of macroalgae. The factorial experimental design included major algal traits, photoacclimation, nutrient stoichiometry and chemical defence as response variables. Few significant effects of the factors acting alone or in combination were observed, suggesting a good capacity for acclimatization in all four species. The significant effects were generally additive and there were no potentially deleterious synergistic effects between factors. Fucus serratus, a species currently undergoing a drastic contraction of its southern distribution limit in Europe, was the most strongly affected species, showing overall lower photosynthetic efficiency than the other species. The growth rate of F. serratus decreased when UV radiation was filtered out, but only in the presence of grazers. Moreover, more individuals of this species tended to reach maturity in the absence of grazers, and the nitrogen content of tissues decreased under full-spectrum light. Only the phlorotannin content of tissues of B. bifurcata and of exudates of A. nodosum, both slow-growing species, were positively affected by respectively removal of UVB radiation and the presence of grazers. The findings for S. muticum, a well-established invasive seaweed across European coasts, suggested similar physiological response of this fast-growing species to different levels of grazing activity and light quality/intensity. As expected, this species grew faster than the other species. Bifurcaria bifurcata and A. nodosum only showed minor effects of light quality and grazing on phlorotannins content, which suggests good resistance of these two long-lived species to the experimental conditions. Mechanistic approaches that are designed to analyse interactive effects of physical and biotic factors provide an understanding of physiological responses of species and help to improve the confidence of predictive distribution models.

GlobTherm, a global database on thermal tolerances for aquatic and terrestrial organisms.

How climate affects species distributions is a longstanding question receiving renewed interest owing to the need to predict the impacts of global warming on biodiversity. Is climate change forcing species to live near their critical thermal limits? Are these limits likely to change through natural selection? These and other important questions can be addressed with models relating geographical distributions of species with climate data, but inferences made with these models are highly contingent on non-climatic factors such as biotic interactions. Improved understanding of climate change effects on species will require extensive analysis of thermal physiological traits, but such data are both scarce and scattered. To overcome current limitations, we created the GlobTherm database. The database contains experimentally derived species' thermal tolerance data currently comprising over 2,000 species of terrestrial, freshwater, intertidal and marine multicellular algae, plants, fungi, and animals. The GlobTherm database will be maintained and curated by iDiv with the aim to keep expanding it, and enable further investigations on the effects of climate on the distribution of life on Earth.

Photoprotective responses in a brown macroalgae Cystoseira tamariscifolia to increases in CO2 and temperature.

Global warming and ocean acidification are increasingly affecting coastal ecosystems, with impacts that vary regionally depending upon local biogeography. Ocean acidification drives shifts in seaweed community dominance that depend on interactions with other factors such as light and nutrients. In this study, we investigated the photophysiological responses in the brown macroalgae species Cystoseira tamariscifolia (Hudson) Papenfuss with important structural role in the coastal Mediterranean communities. These algae were collected in the Cabo de Gata-Nijar Natural Park in ultraoligotrophic waters (algae exposed under high irradiance and less nutrient conditions) vs. those collected in the La Araña beach in oligotrophic waters (algae exposed at middle nutrient and irradiance conditions) in the Mediterranean Sea. They were incubated in mesocosms, under two levels of CO2; ambient (400-500 ppm) and high CO2 (1200-1300 ppm), combined with two temperatures (ambient temperature; 20 °C and ambient temperature + 4 °C; 24 °C) and the same nutrient conditions of the waters of the origin of macroalgae. Thalli from two sites on the Spanish Mediterranean coast were significantly affected by increases in pCO2 and temperature. The carotenoids (fucoxanthin, violaxanthin and ß-carotene) contents were higher in algae from oligotrophic than that from ultraoligotrophic water, i.e., algae collected under higher nutrient conditions respect to less conditions, increase photoprotective pigments content. Thalli from both locations upregulated photosynthesis (as Fv/Fm) at increased pCO2 levels. Our study shows that ongoing ocean acidification and warming can increase photoprotection and photosynthesis in intertidal macroalgae.

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.

Physiological response of fucoid algae to environmental stress: comparing range centre and southern populations.

Climate change has led to alterations in assemblage composition. Species of temperate macroalgae at their southern limits in the Iberian Peninsula have shown shifts in geographical range and a decline in abundance ultimately related to climate, but with the proximate factors largely unknown. We performed manipulative experiments to compare physiological responses of Fucus vesiculosus and Fucus spiralis from Portugal and Wales (UK), representing, respectively, southern and central areas of their distribution, to different intensities of solar radiation and different air temperatures. Following exposure to stressful emerged conditions, Portuguese and Welsh individuals of both fucoid species showed increased frond temperature, high desiccation levels and reduced photophysiological performance that was evident even after a 16 h recovery period, with light and temperature acting in an additive, not an interactive, manner. The level of physiological decline was influenced by geographical origin of populations and species identity, with algae from the south and those living higher on the shore coping better with stressful conditions. The negative effect of summer conditions on photophysiology may contribute to changes in fucoid abundance and distribution in southern Europe. Our results emphasise how physiological performance of geographically distinct populations can differ, which is particularly relevant when predicting responses to climate change.

Physical factors driving intertidal macroalgae distribution: physiological stress of a dominant fucoid at its southern limit.

Climate change is driving species range shifts worldwide. However, physiological responses related to distributional changes are not fully understood. Oceanographers have reported an increase in ocean temperature in the northwest Iberian Peninsula that is potentially related to the decline in some cold-temperate intertidal macroalgae in the Cantabrian Sea, namely Fucus serratus. Low tide stress could also play a role in this decline. We performed one mensurative (in situ) and two manipulative (in culture) experiments designed to evaluate the interactive effects of some physical factors. The first experiment analysed field response to low tide stress in marginal (mid-Cantabrian Sea and northern Portugal) versus central (Galicia) populations of F. serratus. Then a second experiment was performed that utilized either harsh or mild summer conditions of atmospheric temperature, irradiance, humidity, and wind velocity to compare the responses of individuals from one marginal and one central population to low tide stress. Finally, the combined effect of sea temperature and the other factors was evaluated to detect interactive effects. Changes in frond growth, maximal photosynthetic quantum yield (F(v)/F(m)), temperature, and desiccation were found. Three additive factors (solar irradiation, ocean and air temperatures) were found to drive F. serratus distribution, except under mildly humid conditions that ameliorated atmospheric thermal stress (two additive factors). Mid-Cantabrian Sea temperatures have recently increased, reaching the inhibitory levels suggested in this study of F. serratus. We also expect an additive secondary contribution of low tide stress to this species decline. On the northern Portugal coast, ocean warming plus low tide stress has not reached this species' inhibition threshold. No significant differential responses attributed to the population of origin were found. Mechanistic approaches that are designed to analyse the interactive effects of physical stressors may improve the levels of confidence in predicted range shifts of species.

CHANGES IN NUTRIENT CONTENT OF PALMARIA PALMATA IN RESPONSE TO VARIABLE LIGHT AND UPWELLING IN NORTHERN SPAIN(1).

Light has been identified as one of the main factors affecting seaweed ecophysiology. We investigated the dependence of nutrient metabolism on sun and shade light conditions and whether episodes of upwelling of nutrient-rich subsuperficial water could reduce the summer nutrient limitation driving physiological changes in Palmaria palmata (L.) Kuntze. We measured the major nutrient pools, photosynthetic pigments, and light curves, under sun and shade conditions during a summer period when one upwelling was recorded. The redundancy analysis (RDA) produced two clear groups: sun- and shade-acclimated algae. Light was the major predictive factor. Sun-acclimated algae exhibited higher carbon (C) and lower nitrogen (N) and phosphorus (P) content in association with the storage of floridoside (main C reserve) to benefit from higher irradiance (under nutrient limitation). Among N pools, N reserves (phycoerythrin, nitrate) were a lower proportion of the total N in sun-acclimated algae, suggesting their degradation to fulfill the N demands of the cell. The orthophosphate content was also lower in sun-acclimated algae, indicating its utilization as a nutrient reserve. In contrast, N within cell walls and membranes and chl a contributed to a similar proportion of the total N in sun- and shade-acclimated algae, suggesting a response to sustain cell integrity. Transient high nutrient concentration due to the upwelling was unrelated to the nutrient content of the thallus. The storage of C as floridoside from high light exposure was shown to be the driving force for the metabolic adjustment of P. palmata at the end of summer before the onset of dormancy.