BUSCADOR RECOLECTA

Usage Notes: dataset of Generation and maintenance of predation hotspots of a functionally important herbivore in a patchy habitat mosaic Data file contains values for each patch of the accumulated predation rate after 5 days and 10 days of the experiment (response variable) and of the attributes at patch and landscape levels (z-score of HSA) used as predictor in the Multi-model averaging selection. Bold numbers evidence patches where high aggregations of predation risk occurred (predation hotspots). dataset.xlsx, 1. By modifying how critical ecosystem functions are distributed across the landscape, the spatial configuration and characteristics of patches can play a strong role in structuring communities. In strongly predator-controlled ecosystems, this patchy distribution of function can have complex downstream consequences, subjecting some areas to disproportionately high rates of predation, leaving other areas susceptible to herbivore outbreaks. 2. In this study we assess how spatial attributes at patch and landscape scales potentially influence the spatial and temporal distribution of predation on a functionally important herbivore in a patchy Mediterranean marine macrophyte community characterized by strong top-down control. 3. We experimentally tracked how predation risk of tethered sea urchins varied across space over a 10-day period in a patchy seagrass meadow. We related these patterns with patch and landscape-level attributes across the habitat mosaic. 4. At the level of the patch, predation risk was highest in seagrass patches with low canopies, without access to sheltering rocks. Scaling up to the landscape mosaic however, predation risk increased in dense aggregations of patches with high perimeter-to-area ratios close to rocky habitats. Predation aggregated in spatially-explicit hotspots and coldspots that were maintained through time. Interestingly, this pattern of predation risk correlated well with the natural abundance of sea urchins. 5. Our results show that spatial patch configuration can be a strong mediator of top trophic functions in marine ecosystems, causing significant clumping in the way predation – and therefore herbivory – are distributed across space. Given the importance of top-down control for these shallow marine ecosystems, it is crucial to incorporate landscape attributes in understanding the impact of functionally important herbivores on highly fragmented habitats., Peer reviewed

Densities OIKOS Sea urchin densities per size class in two different habitats (macroalgal communities on rocky substrates and Posidonia oceanica seagrass meadows). Data were collected by SCUBA in the NW Mediterranean (Catalan Coast, NE Spain) in 8 different sites and 2 periods., Herbivore outbreaks often trigger catastrophic overgrazing events in marine macrophyte ecosystems. The sea urchin Paracentrotus lividus, the dominant herbivore of shallow Mediterranean seascapes, is capable of precipitating shifts to barrens when its populations explode. P. lividus is found ubiquitously in rocky macroalgal communities and in sandy seagrass meadows of Posidonia oceanica, two of the most important subtidal habitats in the Mediterranean. We explored if habitat-specific regulation across the principal stages of the urchin life cycle could help explain the persistence of these populations in connected mosaics. We measured each of three relevant ecological process (i.e. settlement, post-settlement survival and predation) across a wide stretch of the Mediterranean coast (ca. 600km). Our results show that habitat-specific regulation is critical in determining urchin populations: each habitat limited urchin sub-populations at different life stages. Settlement was never limiting; urchins settled at similar rates in both habitats across the coast. Post-settlement survival was a clear bottleneck, particularly in seagrass meadows where no juvenile urchins were recorded. Despite this bottleneck in seagrasses, adult urchin populations were very similar in both seagrass and macroalgal habitats indicating that other processes (potentially migration) could be key in determining adult distributions across the mosaic. The fact that population regulation is clearly habitat-specific suggests that sea urchin populations may be significantly buffered from bottlenecks in mixed seascapes where both habitats co-occur. Sea urchin populations can therefore persist across the seascape despite strong habitat-specific regulation either by maintaining reproductive output in one habitat or by migrating between them. By affording these regulatory escapes to habitat-modifying species, patchy mosaics may be much more prone to herbivore outbreaks and a host of cascading effects that come in their wake., Peer reviewed

Urchin and Algal cover survey This file contains information on macroalgal cover to urchin biomasses from field surveys in two regions in the Mediterranean. Region 1 (high nutrient regions) and region 2 (low nutrient region). This data was obtained from 50x50cm quadrats in several locations in each region. Algae_Urchin_2013 (TRBase).txt Code R This file contains the R code used to determine thresholds, Predicting where state-changing thresholds lie can be inherently complex in ecosystems characterized by nonlinear dynamics. Unpacking the mechanisms underlying these transitions can help considerably reduce this unpredictability. We used empirical observations, field and laboratory experiments, and mathematical models to examine how differences in nutrient regimes mediate the capacity of macrophyte communities to sustain sea urchin grazing. In relatively nutrient-rich conditions, macrophyte systems were more resilient to grazing, shifting to barrens beyond 1 800 g m−2 (urchin biomass), more than twice the threshold of nutrient-poor conditions. The mechanisms driving these differences are linked to how nutrients mediate urchin foraging and algal growth: controlled experiments showed that low-nutrient regimes trigger compensatory feeding and reduce plant growth, mechanisms supported by our consumer–resource model. These mechanisms act together to halve macrophyte community resilience. Our study demonstrates that by mediating the underlying drivers, inherent conditions can strongly influence the buffer capacity of nonlinear systems., Peer reviewed

Data from: Matrix composition and patch edges influence plant-herbivore interactions in marine landscapes Ecological data from seagrass meadows located in the NW Mediterranean Sea. herbivory_seascape.zip, The functioning of ecosystems can be strongly driven by landscape attributes. Despite its importance, however, our understanding of how landscape influences ecosystem function derives mostly from species richness and abundance patterns, with few studies assessing how these relate to actual functional rates. We examined the influence of landscape attributes on the rates of herbivory in seagrass meadows, where herbivory has been identified as a key process structuring these relatively simple systems. The study was conducted in three representative Posidonia oceanica meadows. The principal herbivores in these meadows are the fish Sarpa salpa and the sea urchin Paracentrotus lividus, and we hypothesised that differences in their interaction with landscape attributes would significantly influence herbivory rates. We measured herbivore abundance, herbivory rates, primary production and plant quality (C:N) in seagrass patches embedded either in rock or in sand (matrix attribute), in patches either near or far from a rocky reef (distance attribute) and at the edges and interior of meadows. Our results show that matrix and meadow edges significantly affected the actual levels of herbivory. Herbivory rates were higher in seagrass patches embedded in a rocky matrix compared to those on sand, and herbivory at the centre of seagrass meadows was higher than at the edges. In contrast, patch distance to rocky reefs did not affect herbivory. Neither herbivore abundance nor food quality explained the patterns across different landscape attributes. This suggests that variation in herbivory across the landscape may be related much more to behavioural differences between species in their evaluation of risk, movement, and food preference in relation to the landscape structure. Our results indicate that richness and abundance patterns may mask critical interactions between landscape attributes and species responses, which result in considerable heterogeneity in the way key functional processes like herbivory are distributed across the ecosystem mosaic., Peer reviewed

[Methods] Experiment locations and climate Trans-Mediterranean translocation of Posidonia oceanica fragments took place between Catalunya (Spain), Mallorca (Spain) and Cyprus in July 2018 and were monitored until July 2019 (Fig. 1). Sea surface temperature data for each transplant 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 the transplant sites in Catalunya, Mallorca and Cyprus and recorded hourly temperatures throughout the duration of the experiment (one year). In order to obtain an extended time series of temperature at transplant sites, 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. Local climate data was also compared to the global thermal distribution of P. oceanica to assess how representative experimental sites were of the thermal distribution of the species (Supplementary materials). Collectively, seawater temperatures from the three locations span the 16th - 99th percentile of temperatures observed across the global thermal distribution of P. oceanica. As such Catalunya, Mallorca and Cyprus are herein considered to represent the cool-edge, centre and warm-edge of P. oceanica distribution, respectively. Transplantation took place toward warmer climates and procedural controls were conducted within each source location, resulting in six source-to-recipient combinations (i.e. treatments, Fig. 1). Initial collection of P. oceanica, handling and transplantation was carried out simultaneously by coordinated teams in July 2018 (Table S1). Each recipient location was subsequently resampled four times over the course of the experiment, in August/September 2018 (T1), October 2018 (T2), April 2019 (T3) and May/June 2019 (T4, Table S1). Between 60-100 fragments were collected for each treatment. A fragment was defined as a section of P. oceanica containing one apical shoot connected with approximately five vertical shoots by approximately 10-15 cm of rhizome with intact roots. Collection occurred at two sites within each location, separated by approximately 1 km. Within sites, collections were conducted between 4 – 5 m depth and were spaced across the meadow to minimise the dominance of a single clone and damage to the meadow. Upon collection, fragments were transported for up to one hour back to the nearest laboratory in shaded seawater. Handling methods In the laboratory, fragments were placed into holding tanks with aerated seawater, at ambient temperature and a 14:10 light-dark cycle. All shoots were clipped to 25 cm length (from meristem to the tip of the longest leaves), to standardise initial conditions and reduce biomass for transportation. For transport by plane or ferry between locations, fragments were packed in layers within cool-boxes. Each layer was separated by frozen cool-packs wrapped in wet tea towels (rinsed in sea water). All fragments spent 12 hrs inside a cool-box irrespective of their recipient destination, including procedural controls (i.e. cool-cool, centre-centre and warm-warm) to simulate the transit times of the plants travelling furthest from their source location (Fig. 1a). On arrival at the destination, fragments were placed in holding tanks with aerated seawater at ambient temperature as described above in their recipient location for 48 hrs, prior to field transplantation. Measurement methods One day prior to transplantation, fragments were tagged with a unique number and attached to U-shaped peg with cable-ties. Morphological traits for each fragment were measured and included: 1) length of the longest apical leaf, width and number of leaves 2) total number of bite marks on leaves of three vertical shoots per fragment, 3) number of vertical shoots, 4) leaf count of three vertical shoots per fragment and 5) overall horizontal rhizome length. A subset (n=10) of fragments per treatment were marked prior transplantation to measure shoot growth. To do this, all shoots within a single fragment were pierced using a hypodermic needle. Two holes were pierced side-by-side at the base of the leaf/top of the meristem. Transplant methods All transplant sites were located in 4 – 5 m depth in area of open dead-matte, surrounded by P. oceanica meadow. In Mallorca and Cyprus, fragments were distributed between two sites, separated by approximately 1 km. In Catalunya, a lack of suitable dead matte habitat, meant that all fragments were placed in one site. Fragments were planted along parallel transects at 50 cm intervals and with a 50 cm gap between parallel transects (Fig. S1). Different treatments were mixed and deployed haphazardly along each transect. Resampling methods and herbivory On day 10 of the experiment, a severe herbivory event was recorded at both warm-edge translocation sites. Scaled photos of all fragments were taken at this time to record the effects of herbivory on transplants. At the end of each main sampling period (T0 – T1, T1-T2 and T3 – T4), all pierced fragments were collected and taken back to the laboratory to measure shoot growth. At T1, T2 and T3, additional sets of fragments (n = 10 per treatment) were marked using the piercing method to record growth in the subsequent time period. In addition, at T1 and T3, n = 20 shoots within the natural meadow at each site were marked to compare growth rates between the native meadow and transplants. Underwater shoot counts and a scaled photo was taken to record fragment survivorship, shoot mortality, bite marks, and shoot length among all remaining fragments within each site and sampling time. In the laboratory, morphological measurements (described above) were repeated on the collected fragments and growth of transplant and natural meadow shoots was measured. Growth (shoot elongation, cm d-1) of the marked shoots was obtained by measuring the length from the base of meristem to marked holes of each leaf (new growth) of the shoot and dividing the leaf elongation per shoot by the marking period (in days). For each shoot, total leaf length (cm shoot-1) and the number of new leaves was also recorded. The rate of new leaf production (new leaves shoot-1 d-1) was estimated dividing the number of new leaves produced per shoot and the marking period. New growth was dried at 60 ºC for 48 hrs to determine carbon and nitrogen content of the leaves, and carbon to nitrogen (C:N) ratios. Carbon and nitrogen concentrations in the new growth leaf tissue was measured at the beginning of the experiment and each subsequent time point for each treatment. Nutrient analyses were conducted at Unidade de Técnicas Instrumentais de Análise (University of Coruña, Spain) with an elemental analyser FlashEA112 (ThermoFinnigan). Underwater photos of shoots were analysed using ImageJ software (https://imagej.net). Maximum leaf length on each shoot in warm-edge transplant sites (cool-warm, centre-warm and warm-warm) were recorded for the initial (day 10) herbivore impact, T1, T2 and T3 time-points and related to transplant nutrient concentrations. Herbivore impact was estimated as the proportional change in length of the longest leaf relative to initial length at T0. Thermal stress Long term maximum temperatures were recorded as the average of annual maximum daily temperatures in each transplant site, averaged between years from 1981-2019. Maximum thermal anomalies were calculated as the difference between daily temperatures in a recipient site over the course of the experiment and the long-term maximum temperature in the source site for each corresponding population. ‘Heat stress’ and ‘recovery’ growth periods of the experiment were defined as T0 -T2 (July-October) and T2-T4 (November-June), respectively, corresponding to periods of positive and negative maximum thermal anomalies. Thermal anomalies experienced by the different transplant treatments were plotted using the ‘geom_flame’, function in the ‘HeatwavesR’ package (Schlegel & Smit 2018) of R (version 3.6.1, 2019) ., 1. The prevalence of local adaptation and phenotypic plasticity among populations is critical to accurately predicting when and where climate change impacts will occur. Currently, comparisons of thermal performance between populations are untested for most marine species or overlooked by models predicting the thermal sensitivity of species to extirpation. 2. Here we compared the ecological response and recovery of seagrass populations (Posidonia oceanica) to thermal stress throughout a year-long translocation experiment across a 2800 km gradient in ocean climate. Transplants in central and warm-edge locations experienced temperatures >29 ºC, representing thermal anomalies >5ºC above long-term maxima for cool-edge populations, 1.5ºC for central and <1ºC for warm-edge populations. 3. Cool, central and warm-edge populations differed in thermal performance when grown under common conditions, but patterns contrasted with expectations based on thermal geography. Cool-edge populations did not differ from warm-edge populations under common conditions and performed significantly better than central populations in growth and survival. 4. Our findings reveal that thermal performance does not necessarily reflect the thermal geography of a species. We demonstrate that warm-edge populations can be less sensitive to thermal stress than cooler, central populations suggesting that Mediterranean seagrasses have greater resilience to warming than current paradigms suggest., Australian Research Council, Award: DE200100900. Horizon 2020 Framework Programme, Award: 659246. Fundación BBVA., Peer reviewed

5 pages. -- Table S1. Summary table with description of sites and fish species studied at four locations across the Mediterranean Sea. -- Fig. S1 Trend in minimum (1st percentile of daily temperatures) and maximum (99th percentile of daily temperatures) sea surface temperatures from 1981 to 2019. -- Fig. S2 Ivlev’s electivity index for herbivorous fishes across the Mediterranean Sea. Ivlev’s index standardizes food consumed by food availability within the habitat and scales from -1 (extreme selection against food source) to 1 (extreme selection for food source) (Jones & Norman 1986), Peer reviewed

Climate-driven species redistributions are reshuffling the composition of marine ecosystems. How these changes alter ecosystem functions, however, remains poorly understood. Here we examine how the impacts of herbivory change across a gradient of tropicalization in the Mediterranean Sea, which includes a steep climatic gradient and marked changes in plant nutritional quality and fish herbivore composition. We quantified individual feeding rates and behaviour of 755 fishes of the native Sarpa salpa, and non-native Siganus rivulatus and Siganus luridus. We measured herbivore and benthic assemblage composition across 20 sites along the gradient, spanning 30º of longitude and 8º of latitude. We coupled patterns in behaviour and composition with temperature measurements and nutrient concentrations to assess changes in herbivory under tropicalization. We found a transition in ecological impacts by fish herbivory across the Mediterranean from a predominance of seagrass herbivory in the west to a dominance of macroalgal herbivory in the east. Underlying this shift were changes in both individual feeding behaviour (i.e., food choice) and fish assemblage composition. The shift in feeding selectivity was consistent among temperate and warm-affiliated herbivores. Our findings suggest herbivory can contribute to the increased vulnerability of seaweed communities and reduced vulnerability of seagrass meadows in tropicalized ecosystems., Funding: Fundación BBVA, Award: Interbioclima; Ministry of Economy, Industry and Competitiveness, Award: CGL2015-71809-P, Fig._1_reconsructed_temperatures_by_location.csv, Fig._2_benthic_data_RAW.csv, Fig._2_herbivore_abundance_biomass.csv, Fig._3_Herbivore_bite_rates.csv, Fig._4b_C_and_N_Posidonia_Padina_turf.csv, Peer reviewed