• Energy Research

Climate change is rapidly altering the distributions of species and the composition of communities that have evolved over evolutionary time scales. Quantifying changes in species distributions and abundance in response to warming is critical to understanding how these changes modify structure, function and services provided by recipient communities. Changes in size structure of warm- and cool-affiliated species is an important indicator for climate-driven species redistributions over time, and has received relatively little attention. We quantified changes in length and biomass distributions of 25 species of Labridae fishes from 112 sites spanning 2000 km across a warm-cool temperate transition zone in south Western Australia. Length and biomass data were collected in 2005-2006 and 2014-2015 using diver operated stereo-video. In the decade between sampling events, south Western Australia experienced an extreme marine heatwave followed by repeated summers of anomalously warm ocean temperatures. Biomass of tropical and subtropical species increased 10-fold and 3-fold, respectively, between 2006 and 2015, whereas temperate species biomass remained relatively stable. In 2014-2015, the abundance and biomass of tropical species (e.g. Scarus ghobban) increased in the warmest regions and established multiple size classes poleward of their recorded 2005-2006 distributions, suggesting successful overwintering and recruitment where viable populations were not recorded in 2005-2006. Large, slow-growing temperate species such as Achoerodus gouldii and Bodianus frenchii decreased in small and medium size classes in warm regions. Our findings report a substantial change in the size structure and composition of labrid assemblages over a decade of climatic variability.

Vertical migration to reach cooler waters is a suitable strategy for some marine organisms to adapt to ocean warming. Here, we calculate that realized vertical isotherm migration rates averaged -6.6 + 18.8 m dec-1 across the global ocean between 1980 and 2015. Throughout this century (2006-2100), surface isotherms are projected to deepen at an increasing rate across the globe, averaging -32.3 m dec-1 under the representative concentration pathway (RCP)8.5 'business as usual' emissions scenario, and -18.7 m dec-1 under the more moderate RCP4.5 scenario. The vertical redistribution required by organisms to follow surface isotherms over this century is three to four orders of magnitude less than the equivalent horizontal redistribution distance. However, the seafloor depth and the depth of the photic layer pose ultimate limits to the vertical migration possible by species. Both limits will be reached by the end of this century across much of the ocean, leading to a rapid global compression of the three-dimensional (3D) habitat of many marine organisms. Phytoplankton diversity may be maintained but displaced toward the base of the photic layer, whereas highly productive benthic habitats, especially corals, will have their suitable 3D habitat rapidly reduced.

[Experimental design: thermal performance experiments] All experiments were run in climate-controlled incubation facilities of the Institut Mediterrani d’Estudis Avançats (Mallorca, Spain). Following 48 hrs under ambient (collection site) conditions, samples were transferred to individual experimental aquaria, which consisted of a double layered transparent plastic bag filled with 2 L of filtered seawater (60 μm) (following Savva et al. 2018). 16 experimental bags were suspended within 80L temperature-controlled baths. In total, ten baths were used, one for each experimental temperature treatment. Bath temperatures were initially set to the acclimatization temperature (i.e. in situ temperatures) and were subsequently increased or decreased by 1 °C every 24 hours until the desired experimental temperature was achieved. Experimental temperatures were: 15, 18, 21, 24, 26, 28, 30, 32, 34 and 36°C (Table S2). For each species, four replicate aquarium bags were used for each temperature treatment with three individually marked seagrass shoots or three algal fragments placed into each bag. For P. oceanica, each marked plant was a single shoot including leaves, vertical rhizome and roots. For C. nodosa, each marked individual consisted of a 10 cm fragment of horizontal rhizome containing three vertical shoots. Individually marked seaweeds contained the holdfast, and 4-5 fronds of P. pavonica (0.98 ± 0.06 g FW; mean ± SE) or a standardised 5-8 cm fragment with meristematic tip for C. compressa (3.67 ± 0.1 g FW; mean ± SE). Experimental plants were cleaned of conspicuous epiphytes. Once the targeted temperatures were reached in all of the baths, experiments ran for 14 days for the algal species and 21 days for seagrasses to allow for measurable growth in all species at the end of the experiment. Experiments were conducted inside a temperature-controlled chamber at constant humidity and air temperature (15 °C). Bags were arranged in a 4x4 grid within each bath, enabling four species/population treatments to be run simultaneously. Bags were mixed within each bath so that one replicate bag was in each row and column of the grid, to minimise any potential within bath effects of bag position. Replicate bags were suspended with their surface kept open to allow gas exchange and were illuminated with a 14h light:10h dark photoperiod through fluorescent aquarium growth lamps. The water within the bags were mixed with aquaria pumps. The light intensity within each bag was measured via a photometric bulb sensor (LI-COR) and ranged between 180-258 μmol m-2 s-1. Light intensity was constant between experiments and did not significantly differ between experimental treatments (p > 0.05). The temperature in the baths was controlled and recorded with an IKS-AQUASTAR system, which was connected to heaters and thermometers. The seawater within the bags was renewed every 72 hrs and salinity was monitored daily with an YSI multi-parameter meter. Distilled water was added when necessary to ensure salinity levels remained within the range of 36-39 PSU, typical of the study region. Carbon and Nitrogen concentrations in the leaf tissue were measured at the end of the experiment for triplicates of the 24ºC treatment for each species and location (Fig. S2) at Unidade de Técnicas Instrumentais de Análise (University of Coruña, Spain) with an elemental analyser FlashEA112 (ThermoFinnigan). [Species description and distribution] The species used in this study are all common species throughout the Mediterranean Sea, although differ in their biological traits, evolutionary histories and thermo-geographic affinities (Fig. S1). P. oceanica is endemic to the Mediterranean Sea with the all other Posidonia species found in temperate Australia (Aires et al. 2011). The distribution of P. oceanica is restricted to the Mediterranean, spanning from Gibraltar in the west to Cyprus in the east and north into the Aegean and Adriatic seas (Telesca et al. 2015) (Fig. S1A). C. nodosa distribution extends across the Mediterranean Sea and eastern Atlantic Ocean, where it is found from south west Portugal, down the African coast to Mauritania and west to Macaronesia (Alberto et al. 2008) (Fig. S1B). Congeneric species of C. nodosa are found in tropical waters of the Red Sea and Indo-Pacific, suggesting origins in the region at least prior to the closure of the Suez Isthmus, approximately 10Mya. Like C. nodosa, Cystoseira compressa has a distribution that extends across the Mediterranean and into the eastern Atlantic, where it is found west to Macaronesia and south to northwest Africa (Fig. S1C). The genus Cystoseira has recently been reclassified to include just four species with all congeneric Cystoseira spp. having warm-temperate distributions from the Mediterranean to the eastern Atlantic (Orellana et al. 2019). The distribution of Padina pavonica is conservatively considered to resemble C. nodosa and C. compressa, spanning throughout the Mediterranean and into the eastern Atlantic. We considered the poleward distribution limit of P. pavonica to be the British Isles 50ºN (Herbert et al. 2016). P. pavonica was previously thought to have a global distribution, but molecular analysis of the genus has found no evidence to support this (Silberfeld et al. 2013). Instead it has been suggested that P. pavonica was potentially misclassified outside of the Mediterranean, due to morphological similarity with congeneric species (Silberfeld et al. 2013). Padina is a monophyletic genus with a worldwide distribution from tropical to cold temperate waters (Silberfeld et al. 2013). Most species have a regional distribution, with few confirmed examples of species spanning beyond a single marine realm (sensu Spalding et al. 2007). [Metabolic rates] Net production (NP), gross primary production (GPP) and respiration (R) were measured for all species from the four sites for five different experimental temperatures containing the in-situ temperature during sampling up to a 6ºC warming (see SM Table S3 for details). Individuals of the different species were moved to methacrylate cylinders containing seawater treated with UV radiation to remove bacteria and phytoplankton, in incubation tanks at the 5 selected temperatures. Cylinders were closed using gas-tight lids that prevent gas exchange with the atmosphere, containing an optical dissolved oxygen sensor (ODOS® IKS), with a measuring range from 0-200 % saturation and accuracy at 25ºC of 1% saturation, and magnetic stirrers inserted to ensure mixing along the height of the core. Triplicates were measured for each species and location, along with controls consisting in cylinders filled with the UV-treated seawater, in order to account for any residual production or respiration derived from microorganisms (changes in oxygen in controls was subtracted from treatments). Oxygen was measured continuously and recorded every 15 minutes for 24 hours. Changes in the dissolved oxygen (DO) were assumed to result from the biological metabolic processes and represent NP. During the night, changes in DO are assumed to be driven by R, as in the absence of light, no photosynthetic production can occur. R was calculated from the rate of change in oxygen at night, from half an hour after lights went off to half an hour before light went on (NP in darkness equalled R). NP was calculated from the rate of change in DO, at 15 min intervals, accumulated over each 24 h period. Assuming that daytime R equals that during the night, GPP was estimated as the sum of NP and R. To derive daily metabolic rates, we accumulated individual estimates of GPP, NP, and R resolved at 15 min intervals over each 24 h period during experiments and reported them in mmol O2 m−3 day−1. A detailed description of calculation of metabolic rates can be found at Vaquer-Sunyer et al. (Vaquer-Sunyer et al. 2015). [Thermal distribution and thermal safety margins] We estimated the realised thermal distribution for the four experimental species by downloading occurrence records from the Global Biodiversity Information Facility (GBIF.org (11/03/2020) GBIF Occurrence Download). Occurrence records from GBIF were screened for outliers and distributions were verified from the primary literature (Alberto et al. 2008, Draisma et al. 2010, Ni-Ni-Win et al. 2010, Silberfeld et al. 2013, Telesca et al. 2015, Orellana et al. 2019) and Enrique Ballesteros (pers. comms) (Fig. S1). Mean, 1st and 99th percentiles of daily SST’s were downloaded for each occurrence site for the period between 1981-2019 using the SST products described above (Table S4). Thermal range position of species at each experimental site were standardised by their global distribution using a Range Index (RI; Sagarin & Gaines 2002). Median SST at the experimental collection sites were standardized relative to the thermal range observed across a species realized distribution, using the equation: RI = 2(SM- DM)/DB where SM = the median temperature at the experimental collection site, Dm = the thermal midpoint of the species global thermal distribution and DB = range of median temperatures (ºC) that a species experiences across its distribution. The RI scales from -1 to 1, whereby ‘-1’ represents the cool, leading edge of a species distribution, ‘0’ represents the thermal midpoint of a species distribution and ‘1’ represents the warm, trailing edge of a species distribution (Sagarin & Gaines 2002). Thermal safety margins for each population were calculated as the difference between empirically derived upper thermal limits for each population and the maximum long term habitat temperatures recorded at collection sites. Each population’s thermal safety margin was plotted against its range position to examine patterns in thermal sensitivity across a species distribution. [Growth measurements and statistical analyses] Net growth rate of seagrass shoots was measured using leaf piercing-technique (Short & Duarte 2001). At the beginning of the experiment seagrass shoots were pierced just below the ligule with a syringe needle and shoot growth rate was estimated as the elongation of leaf tissue in between the ligule and the mark position of all leaves in a shoot at the end of the experiment, divided by the experimental duration. Net growth rate of macroalgae individuals was measured as the difference in wet weight at the end of the experiment from the beginning of the experiment divided by the duration of the experiment. Moisture on macroalgae specimens was carefully removed before weighing them. Patterns of growth in response to temperature were examined for each experimental population using a gaussian function: g = ke[-0.5(TMA-μ)2/σ2], where k = amplitude, μ = mean and σ = standard deviation of the curve. Best fit values for each parameter were determined using a non-linear least squares regression using the ‘nlstools’ package (Baty et al. 2015) in R (Team 2020). 95% CI for each of the parameters were calculated using non-parametric bootstrapping of the mean centred residuals. The relationship between growth metrics and the best-fit model was determined by comparing the sum of squared deviations (SS) of the observed data from the model, to the SS of 104 randomly resampled datasets. Growth metrics were considered to display a significant relationship to the best-fit model if the observed SS was smaller than the 5th percentile of randomised SS. Upper thermal limits were defined as the optimal temperature + 2 standard deviations (95th percentile of curve) or where net growth = 0. Samples that had lost all pigment or structural integrity by the end of the experiment were considered dead and any positive growth was treated as zero. Comparative patterns in thermal performance between populations have fundamental implications for a species thermal sensitivity to warming and extreme events. Despite this, within-species variation in thermal performance is seldom measured. Here we compare thermal performance between-species variation within communities, for two species of seagrass (Posidonia oceanica and Cymodocea nodosa) and two species of seaweed (Padina pavonica and Cystoseira compressa). Experimental populations from four locations spanning approximately 75% of each species global distribution and a 6ºC gradient in summer temperatures were exposed to 10 temperature treatments (15ºC to 36ºC), reflecting median, maximum and future temperatures. Experimental thermal performance displayed the greatest variability between species, with optimal temperatures differing by over 10ºC within the same location. Within-species differences in thermal performance were also important for P. oceanica which displayed large thermal safety margins within cool and warm-edge populations and small safety margins within central populations. Our findings suggest patterns of thermal performance in Mediterranean seagrasses and seaweeds retain deep ‘pre-Mediterranean’ evolutionary legacies, suggesting marked differences in sensitivity to warming within and between benthic marine communities. [Sample collection] Sample collections were conducted at two sites, separated by approximately 1 km, within each location. Collections were conducted at the same depth (1-3 m) at each location and were spaced across the reef or meadow to try and minimise relatedness between shoots or fragments. Upon collection, fragments were placed into a mesh bag and transported back to holding tanks in cool, damp, dark conditions (following Bennett et al. 2021). Fragments were kept in aerated holding tanks in the collection sites at ambient seawater temperature and maintained under a 14:10 light-dark cycle until transport back to Mallorca, where experiments were performed. Prior to transport, P. oceanica shoots were clipped to 25 cm length (from meristem to tip), to standardise initial conditions and remove old tissue for transport. For transport back to Mallorca, fragments were packed in layers within cool-boxes. Cool-packs were wrapped in damp tea towels (rinsed in seawater) and placed between layers of samples. Samples from Catalonia, Crete and Cyprus experienced approximately 12hrs of transit time. On arrival at the destination, samples were returned to holding tanks with aerated seawater and a 14:10 light-dark cycle. [Sea temperature measurements and reconstruction] Sea surface temperature data for each collection site were based on daily SST maps with a spatial resolution of 1/4°, obtained from the National Center for Environmental Information (NCEI, https://www.ncdc.noaa.gov/oisst (Reynolds et al. 2007). These maps have been generated through the optimal interpolation of Advanced Very High Resolution Radiometer (AVHRR) data for the period 1981-2019. Underwater temperature loggers (ONSET Hobo pro v2 Data logger) were deployed at each site and recorded hourly temperatures throughout one year. In order to obtain an extended time series of temperature at each collection site, a calibration procedure was performed comparing logger data with sea surface temperature from the nearest point on SST maps. In particular, SST data were linearly fitted to logger data for the common period. Then, the calibration coefficients were applied to the whole SST time series to obtain corrected-SST data and reconstruct daily habitat temperatures from 1981-2019. [Field collections] Thermal tolerance experiments were conducted on two seagrass species (P. oceanica and Cymodocea nodosa) and two brown seaweed species (Cystoseira compressa and P. pavonica) from four locations spanning 8 degrees in latitude and 30 degrees in longitude across the Mediterranean (Fig. 1, Table S1). These four species were chosen as they are dominant foundation species and cosmopolitan across the Mediterranean Sea. Thermal performance experiments from Catalonia and Mallorca were conducted simultaneously in June 2016 for seaweeds (P. pavonica and C. compressa) and in August 2016 for seagrasses (P. oceanica and C. nodosa). Experiments for all four species were conducted in July 2017 for Crete and in September 2017 for Cyprus. Horizon 2020 Framework Programme, Award: 659246; Juan de la Cierva Formacion, Award: FJCI-2016-30728; Spanish Ministry of Economy, Industry and Competitiveness, Award: MedShift, CGL2015-71809-P; Spanish Ministry of Science, Innovation and Universities, Award: SUMAECO, RTI2018-095441-B-C21

AbstractThe Mediterranean Sea is warming at three times the rate of the global ocean raising concerns about the vulnerability of marine organisms to climate change. Macrophytes play a key role in coastal ecosystems, therefore predicting how warming will affect these key species is critical to understand the effects of climate change on Mediterranean coastal ecosystems. We measured the physiological performance of six dominant native Mediterranean macrophytes under ten temperature treatments ranging from 12 to 34°C to examine their thermal niche, and vulnerability to projected warming in the western Mediterranean up until 2100. Among the macrophytes tested, Cymodocea nodosa was the species with the highest thermal optima and it was beyond current summer temperature. Therefore, C. nodosa may benefit from projected warming over the coming century. The optimal temperature for growth of the other species (Posidonia oceanica, Cystoseira compressa, Padina pavonica, Caulerpa prolifera, and Halimeda tuna) was lower. Similarly, the species presented different upper lethal limits, spanning at least across 5.1°C between 28.9°C (P. oceanica) and >34°C (C. nodosa). Our results demonstrate the variable physiological responses of species within the same local community to temperature changes and highlight important potential differences in climate change vulnerability, among species within coastal marine ecosystems.

AbstractGenetic diversity confers adaptive capacity to populations under changing conditions but its role in mediating impacts of climate change remains unresolved for most ecosystems. This lack of knowledge is particularly acute for foundation species, where impacts may cascade throughout entire ecosystems. We combined population genetics with eco-physiological and ecological field experiments to explore relationships among latitudinal patterns in genetic diversity, physiology and resilience of a kelp ecosystem to climate stress. A subsequent ‘natural experiment’ illustrated the possible influence of latitudinal patterns of genetic diversity on ecosystem vulnerability to an extreme climatic perturbation (marine heatwave). There were strong relationships between physiological versatility, ecological resilience and genetic diversity of kelp forests across latitudes, and genetic diversity consistently outperformed other explanatory variables in contributing to the response of kelp forests to the marine heatwave. Population performance and vulnerability to a severe climatic event were thus strongly related to latitudinal patterns in genetic diversity, with the heatwave extirpating forests with low genetic diversity. Where foundation species control ecological structure and function, impacts of climatic stress can cascade through the ecosystem and, consequently, genetic diversity could contribute to ecosystem vulnerability to climate change.

Accurately forecasting the response of global biota to warming is a fundamental challenge for ecology in the Anthropocene. Within-species variation in thermal sensitivity, caused by phenotypic plasticity and local adaptation of thermal limits, is often overlooked in assessments of species responses to warming. Despite this, implicit assumptions of thermal niche conservatism or adaptation and plasticity at the species level permeate the literature with potentially important implications for predictions of warming impacts at the population level. Here we review how these attributes interact with the spatial and temporal context of ocean warming to influence the vulnerability of marine organisms. We identify a broad spectrum of thermal sensitivities among marine organisms, particularly in central and cool-edge populations of species distributions. These are characterized by generally low sensitivity in organisms with conserved thermal niches, to high sensitivity for organisms with locally adapted thermal niches. Important differences in thermal sensitivity among marine taxa suggest that warming could adversely affect benthic primary producers sooner than less vulnerable higher trophic groups. Embracing the spatial, temporal and biological context of within-species variation in thermal physiology helps explain observed impacts of ocean warming and can improve forecasts of climate change vulnerability in marine systems.This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.

No turning back? Ecosystems over time have endured much disturbance, yet they tend to remain intact, a characteristic we call resilience. Though many systems have been lost and destroyed, for systems that remain physically intact, there is debate as to whether changing temperatures will result in shifts or collapses. Wernburg et al. show that extreme warming of a temperate kelp forest off Australia resulted not only in its collapse, but also in a shift in community composition that brought about an increase in herbivorous tropical fishes that prevent the reestablishment of kelp. Thus, many systems may not be resilient to the rapid climate change that we face. Science , this issue p. 169