Ecology

Quantifying heating of coastal ecosystemsA variety of metrics have been developed to quantify MHWs, but to date, they have mainly focused on surface heating evident from SST. Surface MHWs have been defined based on exceedance of 90% confidence intervals calculated seasonally from historical SST10,11. Defined in this way, the threshold temperature for quantifying a MHW is likely to vary seasonally from, for example, winter to summer. However, the physiological and ecological relevance of seasonally changing thresholds remains unclear, especially for tropical biota such as corals that typically inhabit a relatively narrow range of temperatures close to their physiological thermal limits12,13,14. Assessing heating in the specific context of temperature-induced coral bleaching has instead focused on calculating cumulative degree heating, sensitive to both the magnitude and duration of heating, above a fixed, putative ‘bleaching threshold’ defined by the local Maximum Monthly Mean SST (MMM); i.e., the mean summer-time peak temperature predicted to initiate coral stress and bleaching. Such heat accumulation has most commonly been expressed as Degree Heating Weeks (DHW in °C-weeks) accumulated over a 12-week period15,16, or sometimes using monthly SST data to compute Degree Heating Months (DHM in °C-months) over 3 months17,18. Numerous studies have documented coral bleaching in shallow water linked to periods of anomalously high SST and accumulated DHW, especially during El Niño events1,2,4,19,20,21. However, DHW generally only explain a limited proportion of the observed variation in bleaching, even for communities in very shallow water (e.g., 50% of bleaching variation at 2 m depth7). A number of studies have documented bleaching that was less than that predicted based on contemporaneous SST and DHW. This discrepancy has sometimes been hypothesised to reflect ongoing coral acclimatisation to increasing temperatures and/or shifts in community composition towards more heat-tolerant genotypes and species22,23,24,25,26. Bleaching rates higher than predicted by SST, under limited DHW, have also been documented, and can be species-specific and more pronounced in heat-intolerant cryptic species27. It is unclear to what extent the relatively limited power of SST metrics such as DHW to predict coral bleaching results from an incomplete description of environmental conditions, a lack of nuance in describing biological thresholds and organisms’ reactions to elevated temperatures, genetic variation and cryptic species27,28, or, most likely, a combination of factors.Estimates of surface MHW severity are also highly sensitive to both the spatial and temporal scales of SST data considered. Present-day satellite products allow degree heating to be calculated at relatively fine spatial and temporal resolution using SST data measured daily over pixels of ~25 km2 size (e.g., NOAA Coral Reef Watch29). While many heating assessments in the context of coral bleaching continue to focus on long-term heating based on temperature anomalies accumulated across months (12 weeks or 3 months for DHW or DHM, respectively)18,20,30, here we focus on higher-resolution heating calculated as Degree Heating Days (DHD in °C-days) using daily SST data. Calculation of DHD over 12-day windows is analogous to the more coarse resolution DHW (i.e., weekly data over 12 weeks)31 but with different units, finer temporal resolution, and shorter time lags between the actual elevation of environmental temperatures and the resulting accumulated heating metric (see the DHD and DHW comparison in Fig. S5).To investigate the role of spatial scale in characterising MHWs, we analysed SST at a range of scales around Moorea between 1985 and 2019: 2° × 2° (~50,000 km2), 1° × 1° (~12,300 km2) and 0.1° × 0.1° (~100 km2) (see Fig. S1). The importance of spatial scales in heating severity apparent at the surface is reinforced by the regional heterogeneity in SST (see Fig. 2 and data animations in the Supplementary Information). Considering heating at local scales and finer temporal resolutions maximises the potential to detect, characterise and compare heating events at the surface in a way that is relevant to in situ MHW conditions (see also Guo et al.32. for the importance of scales in MHW assessments). For instance, when assessed using NOAA’s ‘Regional Bleaching Heat Stress Gauges’ for the Society Islands, DHW reached 4.54 °C-weeks in April 2016 and 5.35 °C-weeks in May 201933, indicating moderate likelihood of bleaching during both events, although inherent to calculations of accumulated DHW, the maximum heating was centred multiple weeks after the in situ heating events actually occurred (e.g., see Fig. S5e, f). Heat accumulation using higher resolution DHD across 12-day windows around Moorea itself (2° × 2°) was more closely aligned temporally to the heating events, suggesting a much higher bleaching risk in 2016 (6.83 °C-days) than 2019 (2.10 °C-days; Table S3). This likely reflects the localised heterogeneity in SST during the 2019 MHW, when hotter surface conditions prevailed north of Moorea (Fig. 1b). At a local scale, assessed using SST within a ~10 × 10 km area north of Moorea (see Fig. S1), heating was similar to regional estimates in 2016 (5.73 °C-days), but in 2019 revealed an intense, localised heatwave over Moorea’s north shore (15.4 °C-days; see Fig. 1e, f; Table S1). Because of these demonstrated advantages of higher temporal-resolution analysis, we rely on DHD rather than DHW for our analysis of MHW patterns among years at Moorea.Fig. 2: Regional sea-surface temperature (SST) variability during the peak of the 2016 and 2019 surface marine heatwaves around Moorea suggested hotter conditions during 2016.Panels show SST over a, b 20° × 20° and c, d 10° × 10° during 2016 and 2019, respectively, focusing on the date of peak SST observed over Moorea’s north shore (8 April 2016 and 4 April 2019). Dashed squares in (a, b) show extent of (c, d) and those in (c, d) the extent of data shown in Fig. 1a, b (2° × 2°). Coastlines based on Wessel and Smith77.Full size imageContrasting surface and subsurface heatingComparing surface and subsurface MHWs is challenging for many coastal ecosystems, even once SST data of appropriately fine spatial and temporal scale are obtained, due to a lack of long-term, in-situ temperature data through which to assess mean climatological patterns below the sea surface. Moorea represents one of the few coral reef systems with consistent in-situ observations over timescales (decades) and depths (sea surface to 40 m) relevant to understanding the oceanographic drivers of subsurface heating and their impacts on coral bleaching. Our analysis of long-term SST records indicates there have been 16 local-scale (0.1° × 0.1°) surface MHWs over the north shore of Moorea relative to a MMM-based bleaching threshold of 29.8 °C (Table S4), compared to 14 regional-scale (2° × 2°) events (Table S3). Localised heating over the north shore was often greater than regional SST would suggest, with the hottest event recorded in 2003 reaching 17.7 °C-days locally (Table S4), compared to 15.5 °C-days regionally (Table S3). Further details on historical events can be found in ‘Surface MHW history around Moorea’ in the Supplementary Information, which provides context for the six more recent surface MHWs that have occurred over the north shore since continuous in-situ, reef-level observations began at Moorea in 2005 (MHWs in 2007, 2012, 2015, 2016, 2017, and 2019; Table S4). Two recent, contrasting events in 2016 and 2019 demonstrate the extent to which thermal environments at depth, and the associated severity of coral bleaching, can vary substantially from predictions based on sea-surface conditions.MHW severity based only on SST can miss important information on the conditions experienced by organisms at depths greater than the surface skin layer quantified through remote sensing, which may only be few millimetres thick34. For example, although the localised peak in sea-surface temperatures were essentially identical between 2016 (30.1 °C; Fig. 1a) and 2019 (30.2 °C; Fig. 1b), and regional surface heating metrics and warnings were similar33, markedly different heat accumulation occurred due to the different duration that temperatures remained above the putative coral bleaching threshold (MMM + 1 = 29.8 °C; up to 2 days in April 2016 compared to up to 11 days in April 2019; Table S1). Yet these results from local SST—of similar SST maximums in 2016 and 2019, but longer durations above the threshold in 2019—only capture some of the significant differences that led to constating MHW severity and ecological outcomes between years and across depths.Daily average temperatures measured in situ at reef level in water depths of 10–40 m over ~15 years are well correlated with daily SST (r2 = 0.94–0.78 at 10–40 m). However, the strength of the relationship between SSTs and in situ temperatures declines with increasing water depth, even when in situ temperatures are averaged to a daily resolution31,35. The potential for subsurface attenuation of heating over coral reefs has previously been demonstrated using high-resolution in-situ water temperature data in the context of both regional upwelling and local internal-wave climates31,36,37, with observations of periodic transport of deeper, cooler water onto reef habitats at a large number of reefs globally31,35,38. The propagation of internal-wave energy is associated with significant vertical displacements of density isopycnals and isotherms; e.g., ~60 m displacements along the Hawaiian Ridge39. Upon encountering a sloping bottom, internal-wave dynamics become complex, and, for habitats on the fore reef slope, typically result in rapid, periodic cooling (rather than oscillations around a mean temperature) as water masses associated with e.g., 24–27 °C isotherms are vertically advected onto the reef and recede again31,40,41. In deeper reef habitats there may also be periodic heating associated with exposure to warmer surface water masses when internal waves lead to downward displacement of isotherms31, but the overall magnitude of any resulting net heating is small across the depth range considered here (i.e., no average heating at depths of 40 m and less; Fig. S4).To separate the effects of low- and high-frequency processes driving heating across the reef slope, we used a filtering approach specifically designed and validated by Wyatt et al.31. to estimate coral reef thermal regimes without internal waves. In situ temperatures were filtered to isolate variability at frequencies higher and lower than the local inertial period (~40.0 h), effectively removing the effects of internal waves from lower frequency processes (i.e., multi-day weather patterns and seasonal effects; see Fig. S3). Contrasting the observed and filtered in-situ temperature variations (black and white lines, respectively, in Fig. 3) highlights differences in the processes driving the 2016 and 2019 subsurface MHWs. During the 2019 MHW around Moorea, the filtered, or ‘non-internal wave’ (NIW), temperatures closely resembled the observed temperatures (Fig. 3e–h, m–p) implying limited internal-wave cooling (IWC). Consistent warming across the water column was evident in 2019 and temperatures remained above the coral bleaching threshold for multiple days during early to late April (Table S1). By contrast, the 2016 MHW was characterized by temperatures remaining generally below the bleaching threshold and significant high-frequency variability indicative of IWC across depths, such that temperatures only exceed the predicted bleaching threshold for hours or less at a time (Fig. 3a–d, i–l; Table S1). The high-resolution temperature observations show that IWC was greatly reduced during 2019 (Fig. 3e–h). The power spectral density of observed temperatures, concentrated at semi-diurnal frequencies and consistent with internal-wave forcing at this location41, was significantly higher in 2016 and lower in 2019 than the average across years at 10 m depth (Fig. 4a; see inset). In deeper water at 20–40 m depths, temperature variance within the semi-diurnal frequency band increased relative to shallow depths and became more similar between the two events, such that at 40 m the semi-diurnal variability was equivalent in 2016 and 2019 (Fig. 4b–d; see insets). However, this similarity in temperature variance does not indicate an equivalent magnitude of IWC, since variability during 2019 (Fig. 3p) was around a warmer background temperature closer to the coral bleaching threshold. Extending the comparison of 2016 and 2019 to other recent local MHWs demonstrates two distinct types of events: greater IWC across reef depths during 2012, 2015, and 2016 MHWs, versus reduced IWC during the 2007, 2017 and 2019 MHWs (Fig. 5).Fig. 3: Contrasting reef-level temperature variations across depths on Moorea’s north shore during the 2016 and 2019 marine heatwaves.Panels on the left show the observed high-frequency water temperature variations (black lines, measured at 2-min intervals) during the hottest months (Apr–May) in a–d 2016 and e–h 2019 at a, e 10, b, f 20, c, g 30 and d, h 40 m depths. Right panels focus on relative variation during the heatwave peaks across the same depths: i–l* 06–12 Apr 2016 and m–p 11–17 Apr 2019. Non-internal-wave temperature variations are shown based on observed temperatures filtered to remove the high-frequency influence of internal waves (white lines). The satellite-derived sea-surface temperatures (SST; grey line) are shown for comparison to in situ temperatures. The horizontal dashed line shows the ‘bleaching threshold’ (maximum monthly mean + 1 °C) and the background shading provides a reference relative to temperatures above (red), equal (yellow) and below (blue) this threshold. The red dashed squares denote the axis limits in the right panels. *Note: 40 m logger during 2016 incorrectly recorded at 2-h interval.Full size imageFig. 4: Reduced semi-diurnal temperature variability during the summer of 2019 in shallower water on the north shore of Moorea.Power spectral density (PSD) plots (logarithmic scale) were computed within a 12-day window at a 10 m, b 20 m, c 30 m, and d 40 m water depths during the summer months (Dec–May) in 2016 (blue), 2019 (red), and 2004–2018 (black; excluding 2016 and 2019). Shading shows the 95% confidence intervals for each PSD. The tidal constituents (dotted lines) show variance consistent with semi-diurnal (M2) forcing across depths, with diurnal (K1) forcing in 10 m of water along with some variability consistent with the shallow water lunar overtide (M4). Insets show details of semi-diurnal differences at each depth.Full size imageFig. 5: Comparison of internal-wave cooling (IWC) across depths during recent surface marine heatwaves (MHWs) around Moorea.Based on average a daily temperature variance (in °C2) and b IWC ((overline{{{{{{rm{IWC}}}}}}}) in °C) during the six recent local MHWs (see Table S4 for dates) that can be grouped into: (1) high IWC events during 2012 (blue), 2015 (green) and 2016 (purple); and, (2) low IWC events that coincided with bleaching events in 2007 (red) and 2019 (orange), along with early 2017 (yellow). The daily variance and (overline{{{{{{rm{IWC}}}}}}}) during Dec–Apr across all years (2005–2019) is shown for reference (black dashed lines). Contours of c–f heat accumulation as degree heating days (DHD in °C days) and g–j degree cooling days due to internal waves (DCDIW in °C days) across depths are shown for 2007, 2012, 2016 and 2019. Due to data gaps in the in situ records, contours are not shown for the 2015 or 2017 events.Full size imageThe magnitude of temperature fluctuations produced by IWC, i.e., occurring at the semi-diurnal frequency, are of similar magnitude to long-term ocean warming and climate change threatening coral reefs globally. The average IWC ((overline{{{{{{rm{IWC}}}}}}})) during the high-IWC MHWs (2012, 2015 and 2016) was between 0.14 and 0.60 °C (Fig. 3a; Table S4) and comparable to the overall SST increase measured over tropical coral reefs during the last four decades (~0.65 °C18). As a result of the subsurface cooling caused by internal waves, the 2016 MHW, which was moderate at the surface (5.7 °C-days), was mild at 10 m ( More

Field approachOur searches uncovered 301 papers reporting field studies. After screening the titles abstracts, and full texts, we kept 130 articles for the analysis (Supplementary Fig. 1), from which we obtained 1342 observations regarding 57 Cx. mosquito species from 28 countries and 135 localities (Fig. 1A). Of these 1342 observations, 733 (54.61%) were classified as high quality, (i.e., the number of individuals tested was specified) (Supplementary Tables 1 and 2). The best represented countries were the USA (64.7%, number of observations = 869), Italy (9.3%, n = 125), and Iran (2.9%, n = 39). Based on mosquito field surveillance and individuals testing positive, we concluded that JES is distributed mainly in the Nearctic, Palearctic and Oriental regions (Fig. 1A).Figure 1(A) Weighted Minimum Infection Rates and (B) Weighted Transmission Efficiency of mosquito populations for JES. High-quality data. The size of circles represents the magnitude of the estimates. Map was generated using R software version 4.1.2 with the packages mapdata, maps and tydiverse (https://www.r-project.org) and edited with Inkscape (https://inkscape.org/es/).Full size imageWest Nile virusWNV was detected mainly in the USA (76.5%, number of observations = 826), Italy (4.9%, n = 53) and Iran (3.6%, n = 39) (Fig. 1A). We also recorded 23 species (57%, 41 species) interacting with this virus (Supplementary Tables 1 and 3). Cx. quinquefasciatus became naturally infected in North America [Infection Frequency (IF) = 2.33] (Table 1). We recorded WNV interacting with Cx. tritaeniorhynchus in Asia (IF = 1.02), with Cx. pipiens in Europe (IF = 1.74) and with Cx. antennatus, Cx. neavei, Cx. perexiguus, Cx. perfuscus, Cx. poicilipes, Cx. quinquefasciatus and Cx. tritaeniorhynchus in Africa (IF = 1) (Supplementary Table 3).Table 1 Description of the variables.Full size tableThe highest infection rates were found in North America in Cx. restuans [Standardized minimum infection rate (SMIR) = 56.01], and in Africa and Europe in Cx. pipiens (SMIR = 20.45 and 29.25, respectively). No positive SMIR values were reported in Asian mosquitoes, and Oceanic mosquitoes were not sampled for this virus (Fig. 2A and Supplementary Table 3). The highest infection risk or potential was recorded in species from the USA, such as Cx. restuans (Infection Risk (IR) = 69.50), Cx. pipiens (IR = 55) and Cx. tarsalis (IR = 52.16) (Fig. 3A and Supplementary Table 3). Finally, WNV lineage 1 was detected in Algeria, Turkey, Portugal, Mexico, Tunisia, Iran, Spain and Italy, lineage 2 in Italy, Bulgaria, Greece and the Czech Republic, and lineage 5 in India (Supplementary Table 2).Figure 2(A) Box plots for the Weighted Minimum Infection Rates and (B) Weighted Transmission Efficiency Rates for JES. Boxes indicate 2nd and 3rd quartiles, vertical lines upper and lower quartiles, and horizontal lines the median. Points indicate outliers. The Y axis was transformed to Sqrt (Square root).Full size imageFigure 3JES (A) Infection Risk and (B) Transmission Risk by mosquito species.Full size imageJapanese encephalitis virusJEV was detected mainly in Taiwan (21.6%, n = 24), Korea (18%, n = 20) and Australia (15.3%, n = 17) (Fig. 1A). We found 23 mosquito species interacting with JEV: Cx. vishnui was the one most frequently found to be positive (IF = 1.20), followed by Cx. tritaeniorhynchus (IF = 1.17), Cx. pipiens and Cx. annulus (IF = 0.98) in Asia, while the most susceptible species in Oceania were Cx. sitiens and Cx. gelidus (IF = 0.71) (Supplementary Table 3).The highest SMIR values were recorded in Asia in Cx. rubithoracis (62.38), Cx. annulus (47.68) and Cx. tritaeniorhynchus (28.16) (Fig. 2A and Supplementary Table 3), and Cx. fuscocephala had the highest estimated natural IR (Fig. 3A, Supplementary Table 3). Three genotypes were recorded: genotype I (strain VNKT/479/2007, VNKT/486/2007, and JEV Ishikawa12), genotype III (Tibet-Culex-JEV1-5), and genotype V (K12YJ1174). These were isolated in China, Vietnam, and Japan (Genotype I), Italy, China (Genotype III), and Korea (Genotype V) (Supplementary Table 2).Usutu virusField studies on USUV have been conducted in Europe, Africa, and Asia, most of them in Italy (66.6%, n = 72), Czechoslovakia (11.1%, n = 12) and Slovakia (7.4%, n = 8) (Fig. 1A). Six species were reported to be susceptible to natural infection. Cx. perexiguus had the highest IF and SMIR (1.30) (Supplementary Table 3). In Africa, Cx. antennatus (IF = 1), and in Asia Cx. pipiens (IF = 1) were the most likely to be positive, while Cx. pipiens had the highest IR (5.19) (Fig. 3A, Supplementary Table 3). The recorded strains were USU181_09/USU090-10/USU173_09 (Italy) and USU/Croatia/Zagreb-102/2018 (Italy).St. Louis encephalitis virusThe field studies on SLEV focused on North America (97.7%, n = 43) and Brazil (2.2%, n = 1). Three species were recorded interacting with this virus. Cx. erraticus had the highest IF (2.06), SMIR (2.06) and IR, followed by Cx. quinquefasciatus (North America) (IF = 0.73, SMIR = 1.97) (Fig. 2A, Supplementary Table 3).The highest estimated IR of JES was for Cx. pipiens (Europe), which can be naturally infected with WNV and USUV, followed by Cx. quinquefasciatus (North America), which can be infected with WNV and SLEV (Fig. 3A).Experimental approachExperimental studies were reported in 481 articles. After screening the titles, abstracts, and full texts, as well as opportunistic records, 95 articles remained for the analysis (Supplementary Fig. 2). From these we obtained 189 high quality observations of the TE of JES in 11 countries, 40 localities, and 21 species (Fig. 1B, Supplementary Table 1). The USA was the best represented country (54.4%, n = 103), followed by Germany (13.2%, n = 25) and Australia (12.6%, n = 24). There was, however, a notable lack of information on the vector competence of Cx. mosquitos for JES in many regions of the world, such as Central and South America, and Africa (Fig. 1B).The most common means of infection was oral (94.8%, 395 observations), while the rest were intrathoracic. Intrathoracic infection bypasses the midgut barrier so is not considered natural infection. We therefore carried out the subsequent analyses using only the data on oral infection (Supplementary Table 4).We used a generalised linear model (GLM) for the statistical analysis, which was conducted only on the WNV dataset (strain NY99), the only one with sufficient observations for the purpose (n = 63). We did not find a significant effect of viral titre, temperature, or days post infection on TE. However, more data with a wide range of values is necessary to confirm these observations. On the other hand, we found that the Extrinsic Incubation Period (as DPI) was shorter at higher temperatures (Fig. 4 and Supplementary Table 5).Figure 4Relationship between temperature and Days Post Infection for WNV strain NY99.Full size imageWest Nile virusMosquito populations from many locations on all continents have been studied for their vector competence for this virus, particularly in the USA (60.3% of observations, n = 96), Germany (15.7%, n = 25) and Australia (6.9%) (Fig. 1B). Our bibliographic research revealed 21 species of Cx. with the ability to transmit WNV under laboratory conditions (Supplementary Table 6). Cx. pipiens (North America) and Cx. tarsalis were the most frequently studied species and were the most efficient in transmitting the virus (Transmission Frequency (TF) = 2.33) (Table1). Cx. quinquefasciatus had the highest TF (1.70) in Africa, Cx. modestus in Europe (TF = 1.32), and Cx. annulirostris and Cx. quinquefasciatus in Oceania (TF = 1.48) (Supplementary Table 6).Concerning Standardized Transmission Rates (STE) estimates, Cx. quinquefasciatus had the highest values in the USA (STE = 1.63), Cx. pipiens in Europe (0.90), Cx. tritaeniorhynchus in Asia (1.8), Cx. neavei in Africa (0.17) and Cx. annulirostris in Oceania (2.45) (Fig. 2B, Supplementary Table 6). We found 20 different strains of WNV tested. The TE of the various WNV strains vary considerably, but lineage 1 was more efficient than lineage 2. There were also more studies on the lineage 1 strains (n = 11), which exhibited high variation (Fig. 5).Figure 5Box plots for WNV (A) lineages and (B) strains used to measure Weighted Transmission Rates.Full size imageJapanese encephalitis virusJEV has been studied mainly in mosquito populations from France (45%, n = 20) and Australia (34%, n = 15), but also the United Kingdom, India, Taiwan, New Zealand, and the USA (Fig. 1B). Six mosquito species are capable of transmitting JEV. Cx. pipiens (Europe) had the highest TF (1.85), while Cx. gelidus had high values of STE (1.73) (Fig. 3B and Supplementary Table 6).St. Louis encephalitis virusVector competence for SLEV has been studied in two countries: the USA (93.3%, n = 42) and Argentina (6.6%, n = 3), and 7 mosquito species have been investigated. Cx. nigripalpus was the most efficient in transmitting the virus (TF = 1.60), while Cx. pipiens had the highest STE (0.68) (Figs. 2B, 3B and Supplementary Table 6).Usutu virusStudies have also been conducted on the Usutu virus in mosquito populations in the USA (28.57%, n = 4), the United Kingdom (42.8%, n = 6) and Senegal (25%, n = 4), in particular on Cx. neavei, Cx. pipiens and Cx. quinquefasciatus (TF = 1). Cx. neavei also had the highest STE (0.79) (Fig. 3B).We found reports of JES transmission under laboratory conditions in 22 Cx. species, and natural infections in 32 species (55.1% of the total sample) in the field. Cx. pipiens complex (biotypes quinquefasciatus, pipiens, molestus and pallens) was the most common vector accounting for 36.9% (n = 660) of the experimental observations and 25.7% (n = 1342) of the field observations. With both approaches, WNV was the most common flavivirus, accounting for 80.4% of the field observations and 86.7% of the experimental data (Fig. 1A,B). Only WNV, therefore, had enough observations to make comparison between the experimental and field data possible. We were able to compare 16 mosquito species and found a high positive correlation between TF and IF (R = 0.57, p = 0.02) (Fig. 7).In summary, we found that the species with the highest infection-transmission risk (IRT) for WNV was Cx. restuans, for USUV it was Cx. pipiens (Europe), for SLEV Cx. quinquefasciatus (North America), and for JEV Cx. gelidus (Oceania) (Fig. 6 and Supplementary Tables 2 and 6).Figure 6JES infection-transmission risk by continent and flavivirus.Full size image More

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Identification of windthrow eventsLandsat images from January 1st 2018 to December 31st 2019 were filtered on 20% or less of cloud coverage, and only the least cloudy image at each location was selected to make an image composite covering the entire Amazon region. In total, 395 least cloudy Landsat 8 images within the Amazon boundary during 2018–2019 were selected and displayed in false color (red: shortwave infrared band, green: near-infrared band, blue: red band) on Google Earth Engine for windthrow events identification (Supplementary Fig. 6). Hollow regions on Supplementary Fig. 6 (2.8% of the total area of the Amazon region) indicated that no clear images with 1 year before the identification were displayed in bright green colors (due to reflectance in near-infrared band from the pioneer species). “Old” windthrows account for ~80% of total identified windthrows, and they were verified using historical Landsat images that can go as far as 1984 (when Landsat 5 was launched). “Old” windthrows were validated once they were found with clear shape and more distinguish color on the historical Landsat images (Supplementary Fig. 7c). 10–15% of “old” windthrows without fan-shape were eliminated from this study because it was hard to identify if they were windthrows or other types of forest disturbance. The minimum size of windthrows identified in this study was 25,000 m2. This process generated the location and rough size of 1012 visible (both “old” and “new”) windthrow scars with fan-shaped patch, scattered small disturbance pixels tails, and an area of over 25,000 m2 (Supplementary Fig. 8). Based on a gap-size probability distribution function that simulates the entire disturbance gradient from all sizes of windthrows19, the proportion of total tree mortality represented by large windthrows ( >25,000 m2) identified in this study is 0.5–1.1%.Among 1012 visual identified windthrows, the occurrence year of 125 windthrows were identified using Landsat 5,7,8, MODIS, and TRMM dataset (Supplementary Table 2), and 38 windthrows from these 125 windthrows had clear remote sensing evidence to validate their occurring date (Supplementary Table 3). It is difficult to get the accurate year and date of occurrence of all identified windthrows. Previous studies showed that windthrows in the northwestern Amazon took ~20 years to recover to 90% of “pre-disturbance” biomass from all damage classes while forests in the central Amazon took ~40 years to recover40. The biomass recovery depends on the windthrow severity and time since disturbance33. Based on the recovery time (20–40 years) and the time of windthrow identification (2018–2019), we estimated that these 1012 windthrows most likely occurred within 30 years (between 1990 and 2019), and the estimated occurrence period was validated using the range of the occurrence year (1986–2019) of 125 windthrow cases.Windthrow density dataThe windthrow density shown in Fig. 1b was generated using 1012 windthrow points in QGIS45. We created a 2.5° by 2.5° grid map, and the windthrow density was calculated by counting the number of windthrows in each grid. These values were then converted to a density with units of counts of windthrows per 10,000 km2. We chose 2.5 degrees to aggregate the data to make sure that over 50% of grids have at least 1 windthrow event while still preserving the spatial distribution of mean afternoon CAPE over the Amazon. The contour lines displayed in Fig. 1c were generated using the “Contour” function on the windthrow density map in QGIS.Meteorological dataTo derive the correlation between windthrow density and meteorological variables, we used ERA 5 global reanalysis hourly CAPE on single levels from 1979 to present at 0.25° × 0.25° resolution provided by the European Center for Medium-Range Weather Forecasts. ERA 5 CAPE was computed by considering parcels of air departing at different pressure levels below the 35 kPa level, with maximum–unstable algorithm under a pseudo-adiabatic assumption46. Afternoon mean CAPE map was calculated as the average of hourly CAPE data from 17:00–23:00 UTC (13:00–19:00 local time in Amazon) over all the months between 1990 and 2019. We chose to average CAPE over 30 years because these windthrow events occurred in these 30 years and calculating the average can help capture the overall spatial pattern of CAPE and minimize the influence of interannual climate variability on windthrow events.To project future windthrow density in the Amazon for the end of the 21st century, we analyzed meteorological output from 10 ESMs that participated in CMIP6 (https://www.wcrp-climate.org/wgcm-cmip/wgcm-cmip6). The models used in this research were listed in Supplementary Table 1. We extracted daily surface temperature (tas), specific humidity (huss), surface pressure (ps), temperature (ta) from these models to calculate daily nondilute, near-surface-based, adiabatic CAPE. CMIP6 CAPE was calculated by considering the buoyancy of a near-surface parcel lifted adiabatically to a series of discrete pressure levels (100 kPa to 10 kPa in increments of 10 kPa). CMIP6 CAPE is calculated as follows:$${CAPE}=mathop{sum }limits_{i=1}^{10}{{{{{rm{d}}}}}}p{{{{{rm{H}}}}}}({b}_{i}){b}_{i}$$
(1)
Where ({{{{{rm{d}}}}}}p) = 10 kPa, H is the Heaviside unit step function, and ({b}_{i}=frac{1}{{rho }_{i}}-frac{1}{{rho }_{e,i}}), with ({rho }_{i}) being the parcel density at pressure level i and ({rho }_{e,i}) being the environmental density at pressure level i.The future projections in our analysis were based on SSP585, a high-emission scenario with high radiative forcing by the end of the century. We calculated mean daily CAPE over 1990–2015 as current CMIP6 CAPE and mean daily CAPE over 2070–2099 as future CMIP6 CAPE. Since different approaches were used to calculate ERA 5 CAPE and CMIP6 CAPE47, the absolute CAPE values of the two datasets are not comparable. Therefore, for each ESM model, we scaled future CMIP6 CAPE by multiplying, grid-wise, the delta CAPE generated from an individual model in CMIP6 with the ERA 5 current mean afternoon CAPE (Fig. 1c) as follows:$${delta},{CAPE}=(CAPE_{CMIP6_{,future}},-CAPE_{CMIP6_current})/CAPE_{CMIP6_current}$$
(2)
$$CAP{E}_{scaled_CMIP6_,future}=(1+delta,CAPE)times CAP{E}_{ERA5}{_}_{current}$$
(3)
The delta CAPE indicated the projected increase in CAPE from 1990–2015 to the end of the 21st century. In this way, a scaled CMIP6 future CAPE map was generated for each model, and an ensemble-mean scaled CMIP6 CAPE map over 10 ESM models can be found in Supplementary Fig. 5b. The scaled CMIP6 future CAPE values were within plausible range compared to the ERA 5 current mean afternoon CAPE values, and both current and future CAPE maps were used to produce the increase in area with high CAPE values ( >1023 J kg−1) in Table 1. However, it is worth noting that the scaling with relative changes in delta CAPE (%) is more sensitive to CMIP historical baseline conditions than absolute changes of CAPE (J kg−1), which will likely introduce a larger scaled spread (min/max CAPE changes).The increase in area with storm-favorable environments was calculated as follows:$$Increase=(are{a}_{future}-area_{current})/are{a}_{current}$$
(4)
Where areacurrent is the area of CAPE  > 1023 J kg−1 for current ERA 5 CAPE, and areafuture is the area of CAPE  > 1023 J kg−1 for the scaled CMIP6 future CAPE.A model of windthrow densityWe developed a model based on the relationship between satellite-derived windthrow density and mean afternoon CAPE from the ERA 5 reanalysis over 1990–2019. The non-parametric model provides a look-up table of windthrow density as a function of CAPE within the range of observations. Counts of observed windthrow events and Amazon’s area were separately binned by CAPE using the same bins, producing two histograms of CAPE. The ratio of the former to the latter gives the density of windthrow events (windthrow events per area) as a function of CAPE. To avoid noise at the tails of the histograms, the six CAPE bins were chosen such that each bin would have about the same number of windthrow events (either 168 or 169). The total number of windthrow events is given by the sum over bins of the product of windthrow density and area. The minimum and maximum of current ERA 5 mean afternoon CAPE was 42 and 1549. The minimum CAPE value of the first bin was extended to 0 and the maximum CAPE value of the last bin was extended to infinity under the assumption that the windthrow density is similar for neighboring values. Based on the windthrow density and CAPE relationship used in the model, it is the increase in the area with high CAPE that then leads to an increase in the number of windthrow events.It is worth noting that the future windthrow density produced by models may be underestimated because the windthrow observations within regions with high CAPE were incomplete due to high cloud coverage. Moreover, the non-parametric model makes the conservative assumption that the windthrow density does not increase at higher, as-yet unobserved values of mean afternoon CAPE.Future projections of windthrow densityWe combined the non-parametric relationship (Fig. 2a) with the future CAPE map generated from the ten CMIP6 ESMs (adjusted by ERA 5 mean CAPE values) to estimate the changes in windthrow density at the end of the 21st century. We estimated uncertainties for windthrow density projections by combining information about model-to-model differences. The analysis yielded a set of 10 estimates. The overall windthrow density increase and uncertainty were estimated using the mean increase and one standard deviation from the ensemble of the 10 models. More

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Systematic paleontologySauropterygia Owen, 186038.Eosauropterygia Rieppel, 199439.Pachypleurosauroidea Huene, 195640.Pachypleurosauridae Nopcsa, 192841.Luopingosaurus imparilis gen. et sp. nov.EtymologyThe genus name refers to the Luoping County, at which the fossil site is located. Species epithet imparilis (Latin) means peculiar and unusual.HolotypeA ventrally exposed skeleton with a posterior part of the caudal missing, IVPP V19049.Locality and horizonLuoping, Yunnan, China; Second (Upper) Member of Guanling Formation, Pelsonian (~ 244 Ma), Anisian, Middle Triassic37.DiagnosisA pachypleurosaurid distinguishable from other members of this family by the following combination of features (those unique among pachypleurosaurids identified with an asterisk): snout (preorbital portion) long and anteriorly pointed, 55.0% of skull length (*); orbital length about one quarter of skull length; internal naris retracted, without contribution from premaxilla; nasal ending at level of anterior margin of prefrontal; dentary length 71.7% of mandibular length; hyoid length 9.7% of mandibular length; presence of entepicondylar foramen in humerus; 21 cervical and 27 dorsal vertebrae (*); distinct expansions of distal heads of posterior two sacral ribs; six pairs of caudal ribs; phalangeal formula 2–3-5–5-3 for manus and 2–3-4–6-4 for pes (*); Metatarsal I short and stout with expanded proximal end, 56.4% of Metatarsal V in length (*); and Metatarsal IV being longest phalange in pes.Comparative descriptionThe holotype and only currently known specimen of Luopingosaurus has a preserved length of 46.2 cm from the rostral tip to the 30th caudal vertebra (for measurements, see Table 1). The estimated total length of the body may have reached 64 cm, assuming similar tail proportions of pachypleurosaurids. As such, Luopingosaurus is longer than most of other pachypleurosauroids that are small-sized with a maximum total length rarely exceeding 50 cm4,9,10,11,12,14,15,16,18,23,25, although some pachypleurosaurids are notably larger (e.g., 88 cm in Diandongosaurus cf. acutidentatus22, ~ 120 cm in Neusticosaurus edwardsii8, and ~ 130 cm in Wumengosaurus delicatomandibularis13).Table 1 Measurements (in mm) of the holotype (IVPP V19049) of Luopingosaurus imparilis gen. et sp. nov. R, right.Full size tableThe pre-orbital portion, distinctly longer than the postorbital region, measures 55% of the total skull length (the premaxillary symphysis to the occipital condyle) and 51% of the mandibular length. The paired premaxillae form most of the snout anterior to the naris with a pointed anterior tip, similar to the conditions in Wumengosaurus13,30 and Honghesaurus23. By contrast, other pachypleurosauroids uniformly have a blunt rostrum4,6,7,8,9,10,11,12,14,15,16,18,22,25. The premaxilla bears a long posteromedial process inserting between the anterior parts of the elongate nasals (Fig. 3). The premaxillary teeth are homodont with a tall peduncle and a short, conical crown, but the tooth number is hard to estimate because of occlusion of jaws. The posterior parts of nasals contact each other medially, and posteriorly, they contact the frontals in an interdigitating suture at the level of the anterior margin of the prefrontal. In Honghesaurus23, Wumengosaurus30, Neusticosaurus8 and Serpianosaurus9, the even longer nasal extends posteriorly beyond this level and ends at the anterior portion of the orbit.Figure 3Skull and mandible of Luopingosaurus imparilis gen. et sp. nov., IVPP V19049. Head before (a) and after (b) dusted with ammonium chloride. (c), Line- drawing. (d, e), two computed laminography scanning slices. (f), reconstruction in ventral view. ac, acetabulum; an, angular; ar, articular; ax, axis; c, cervical vertebra; den, dentary; eo, exoccipital; f, frontal; hy, hyoid; in, internal naris; j, jugal; m, maxilla; n, nasal; p, parietal; par, prearticular; pof, postfrontal; prf, prefrontal; pt, pterygoid; q, quadrate; qj, quadratojugal; sa, surangular; sp, splenial; sq, squamosal; stf, supratemporal fossa; v, vomer.Full size imageThe orbit is oval and large, measuring 24.8% of the skull length (Fig. 3). The lateral margin of the frontal contacts the prefrontal anteriorly and the postfrontal posteriorly, and defines most of the medial border of the orbit. The L-shaped jugal, together with the posterolateral process of the maxilla, forms the lateral border of the orbit. No distinct lacrimal is discernable; the bone is probably absent as in other sauropterygians. The postfrontal contacts the dorsal process of the triradiate postorbital ventrally, and both bones define the posterior border of the orbit. Additionally, the posterior process of the postorbital contacts the anterior process of the squamosal, forming the bar between the supratemporal fossa and the ventrally open infratemporal fenestra. The jugal extends beyond the ventral margin of the postorbital and also contacts the anterior process of the squamosal, resembling the conditions in Wumengosaurus30, Honghesaurus23 and Diandongosaurus15. This contact is absent in other pachypleurosauroids4,6,7,8,9,10,11,12.A pair of vomers and pterygoids and a right palatine are discernable in the palate (Fig. 3a–c). The vomer is elongate and slender, extending anteriorly well beyond the nasal. The internal naris, partly covered by the detached splenial, is longitudinally retracted, corresponding to a retracted external naris (Fig. 3d–f). The medial margin of the naris is defined by the nasal, without contribution from the premaxilla. A retracted naris is otherwise present in Wumengosaurus13,30, Qianxisaurus16 and Honghesaurus23. Similar to the condition in Honghesaurus23, the retracted naris of Luopingosaurus is relatively short, having a longitudinal diameter distinctly less than half of the longitudinal diameter of the orbit. By contrast, other pachypleurosauroids4,6,7,8,9,10,11,12,25 generally have an oval-shaped naris. The elongate palatine has a slightly convex medial margin suturing with the pterygoid. Because of the coverage of the detached splenial, the lateral portion of the palatine is unexposed, and it is hard to know whether an ectopterygoid is present or not. The pterygoid is the largest and longest element of the palate, measuring 55.2% of the mandibular length. It has an anterior projection that contacts the vomer anteromedially, and does not participate in the margin of the internal naris. At the level of the posterior orbital margin, the pterygoid has a triangular lateral extension, which was termed as the ectopterygoid process of the pterygoid in Neusticosaurus8. The pterygoid extends back to the occipital condyle, and covers the basicranium and parietals in ventral view. Additionally, the bone has a broad posterolateral process that is set off from the palatal surface by a distinct ridge, resembling the conditions in Serpianosaurus9 and Neusticosaurus8. Posteriorly, the basioccipital is exposed in ventral view, showing the area for attachment to the right exoccipital.The left quadrate is exposed in lateral view with its dorsal process extending underneath the base of the descending process of the squamosal. The posterior margin of the quadrate is excavated, as in many other pachypleurosaurids (e.g., Serpianosaurus9 and Honghesaurus23). The quadratojugal is narrow and splint-like, flanking the anterior margin of the quadrate. A pair of hyoids are ossified. They are rod-like, slightly expanded at both ends. The dentary is wedge-shaped, being 71.7% of the mandibular length. Laterally, it bears a longitudinal series of pores and grooves parallel to the oral margin of the bone (Fig. 3a). The elongate angular tapers at both ends, contacting the dentary anterodorsally and the surangular dorsally in ventral view. The surangular, slightly shorter than the angular, contacts the articular posterodorsally, with a pointed anterior tip wedging into the notched posterior margin of the dentary. The retroarticular process of the articular is very short with a rounded posterior margin. Medially, the splenial and prearticular form most of the inner wall of the mandible. The splenial tapers at both ends and enters the mandibular symphysis anteriorly, having a length similar to the dentary. The relatively slender prearticular contacts the splenial anterodorsally, extends posteriorly and abuts the articular dorsally, measuring 41.1% of the mandibular length.The whole series of 21 cervical vertebrae (including the atlas-axis complex) is well exposed ventrally. The atlas centrum is oval, much smaller than the axis centrum (Fig. 3c). From the axis, the cervical vertebrae increase gradually in size toward the trunk vertebrae posteriorly. The bicephalous cervical ribs have typical free anterior and posterior processes as in other pachypleurosauroids8,9. The trunk is relatively long, including 27 dorsal vertebrae. The posterior dorsal ribs show certain pachyostosis (Fig. S1). Each gastralium consists of five elements (a short and more massive median element and two slender rods in line towards each side; Figs. 3, 4a, b, S1), similar to the conditions in most of other pachypleurosauroids9,11,18,25 (except Neusticosaurus8). Three sacral ribs are clearly revealed by X-ray computed microtomography (Fig. 4c–f). They are relatively short and stout, with the posterior twos bearing a distinct expansion on their distal heads. The distal expansion of the sacral rib is also present in Keichousaurus11, Prosantosaurus25, Qianxisaurus16 and Wumengosaurus13, but it is not pronounced in other pachypleurosauroids4,6,7,8,9,10. The caudal ribs are relatively few, six pairs in number. Additionally, several chevron bones are visible in the proximal caudal region, and they are gradually reduced in length posteriorly (Fig. 4d).Figure 4Girdles, limbs and vertebrae of Luopingosaurus imparilis gen. et sp. nov., IVPP V19049. Photo (a) and line-drawing (b) of pectoral girdle, forelimbs and anterior dorsal vertebrae. Photo (c), line-drawing (d) and two computed laminography scanning slices (e, f) of pelvic girdle, hind limbs and posterior vertebrae. as, astragalus; ca, caudal vertebra; cal, calcaneum; car, caudal rib; co, coracoid; d, dorsal vertebra; dltp, deltopectoral crest; enf, entepicondylar foramen; fe, femur; fi, fibula; h, humerus; il, ilium; int, intermedium; is, ischium; mc, metacarpal; mt, metatarsal; pu, pubis; s, sacral vertebra; sc, scapula; sr, sacral rib; ti, tibia; ul, ulna; uln, ulnare.Full size imageThe paired clavicles and the median interclavicle form a transverse bar at the 20th cervical vertebrae (Fig. 4a, b). The blade-like clavicle tapers posterolaterally with its distal projection overlapped by the scapula in ventral view. The left clavicle contacts the right one anterodorsally to the interclavicle. The interclavicle tapers laterally to a point at each end. The anterior margin of the interclavicle is convex and its posterior margin is slightly concave without a midline projection (contra the condition in Anarosaurus42). The scapula consists of a broad ventral portion and a relatively narrow and elongate dorsal wing that varies little through its length. The coracoid is hourglass-shaped with a slightly concave posterolateral margin and a conspicuously concave anteromedial margin. The medial margin is straight, along which the coracoids would articulate each other in the midline. The humerus is constricted at the middle portion with a nearly straight preaxial margin and a concave postaxial margin. A slit in the expanded distal portion of this bone indicates the possible presence of an entepicondylar foramen (Fig. 4a, b). The radius, slightly longer than the ulna, is more expanded proximally than distally. The ulna is straight with a slightly constricted shaft. In each forelimb, there is two nearly rounded carpals, ulnare and intermedium; the former is half the width of the latter. Five metacarpals are rod-like, slightly expanded at both ends. Among them, Metacarpal I is the shortest, 48% of the length of Metacarpal II. Metacarpal III is slightly shorter than Metacarpal IV, which is the longest. Metacarpal V is 71% of the length of Metacarpal IV. The phalangeal formula is 2–3–5–5–3 for the manus, indicating presence of hyperphalangy in Luopingosaurus (see Discussion below).In the pelvic girdle, the ilia, pubes and ischia are well exposed (Fig. 4c–f). The ilium is nearly triangular with a relatively long and tapering posterior process. The plate-like pubis is well constricted at its middle portion, with the medial portion nearly equal to the lateral portion. The obturator foramen is slit-like, located at the posterolateral corner of this bone (Fig. 4e). The ischium is also plate-like, having a relatively narrow lateral portion and an expanded medial portion that is notably longer than the medial portion of the pubis. The posterolateral ischial margin is highly concave. The posterior pubic margin and anterior ischial margin are moderately concave, and both together would enclose the thyroid fenestra. The femur is slightly longer than the humerus, with a constricted shaft and equally expanded ends (Fig. 4d). No internal trochanter is developed. The tibia is nearly equal to the fibula in length; the former is straight and thicker than the slightly curved latter. Two ossified tarsals, calcaneum and astragalus, are nearly rounded; the latter is significantly larger than the former. As in Honghesaurus23, the astragalus lacks a proximal concavity. The right metatarsals are well-preserved. Metatarsal I is the shortest and stoutest phalange with an expanded proximal end, and Metatarsal IV is the longest. Metatarsal II is nearly twice the length of Metatarsal I. Metatarsal III is slightly shorter than Metatarsal IV, and Metatarsal V is 76% of the length of Metatarsal IV. The phalangeal count is 2–3–4–6–4, which is complete judging from the appearance of the distal phalanges in the right pes (Fig. 4c). More