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To explore how environmental gradients shape the distribution of cyanophages and picocyanobacteria, we conducted high-resolution surveys in surface waters along five oceanic transects on three cruises covering thousands of kilometres in the North Pacific Ocean in the spring or early summer of 2015, 2016 and 2017 (Fig. 1a–c). These cruises, two of which were out-and-back, passed through distinct regimes from warm, saline and nutrient-poor waters of the North Pacific Subtropical Gyre to cooler, less saline and nutrient-rich waters of higher latitudes influenced by the subpolar gyre (Fig. 1d–i)27. The shift between the two gyres was marked by abrupt changes in trophic indicators such as particulate carbon concentrations (Fig. 1g) and a chlorophyll front (defined as the 0.2 mg m−3 chlorophyll contour28; Fig. 1a–c). As such, the inter-gyre transition zone, defined by salinity and temperature thresholds29 (Fig. 1d), was distinct from both the subtropical and subpolar gyre ecosystems28.Fig. 1: Gradients in environmental conditions across the North Pacific gyres.a–c, Transects of three cruises overlaid on monthly averaged satellite-derived sea-surface chlorophyll in March 2015 (a), April 2016 (b) and June 2017 (c). d, Temperature–salinity diagram showing the boundaries of the subtropical and subpolar gyres (black dashed lines) based on the salinity thresholds reported by Roden29. e–i, Temperature (e), salinity (f) as well as the levels of particulate carbon (g), phosphate (h) and nitrate + nitrite (i) as a function of latitude. The coloured dashed lines show the position of the 0.2 mg m−3 chlorophyll contour. For environmental variables plotted against temperature, see Supplementary Fig. 3.Full size imageUnexpected Prochlorococcus declineProchlorococcus concentrations in the oligotrophic waters of the subtropical gyre were 1.5–3.0 × 105 cells ml−1, comprising an average of approximately 29% of the total bacteria (Extended Data Fig. 1) and numerically dominating the phytoplankton community in all three cruises (Extended Data Fig. 2). Prochlorococcus abundance remained high in the southern region of the transition zone in 2015 and 2016, decreasing precipitously to less than 2,000 cells ml−1 north of the chlorophyll front, generally constituting 80% of cyanophages measured, with the remainder consisting of T7-like clade A and TIM5-like cyanophages (Fig. 3 and Extended Data Fig. 4). Cyanophage abundances correlated positively with total picocyanobacteria in the subtropical gyre (Pearson’s coefficient of multiple correlation (r) = 0.54, P = 0.02, n = 26; Fig. 2d), suggesting that cyanophages were limited by the availability of susceptible hosts in this region and were not regulating picocyanobacterial populations. On average, less than 1% of the cyanobacterial populations were infected (Fig. 4), with higher infection rates by T4-like cyanophages than T7-like cyanophages (Extended Data Figs. 5 and 6). These instantaneous measurements of infection were used to estimate the daily rates of mortality39 (Methods and Supplementary Discussion), which suggests that 0.5–6% of picocyanobacterial populations were lysed by viruses each day (Extended Data Fig. 7). This implicates other factors, such as grazing45, as the major causes of cyanobacterial mortality in the North Pacific Subtropical Gyre.Fig. 3: Cyanophage community composition across the North Pacific gyres.a–c, Cyanophage abundance for the March 2015 (a), April 2016 (b) and June 2017 (c) transects. Insets: T7-like clade A and TIM5-like cyanophage abundances on an expanded scale (similar to the main images, the units for the vertical axes are ×105 viruses ml−1). The grey shaded regions show the position of the virus hotspot. See Extended Data Fig. 4 for the confidence intervals and out-and-back reproducibility and Supplementary Fig. 4 for cyanophage lineages plotted against latitude.Full size imageFig. 4: Viral infection patterns of picocyanobacteria in the North Pacific Ocean.a–f, Viral infection levels (black) of Prochlorococcus (a,c,e) and Synechococcus (b,d,f) plotted against temperature for the March 2015 (a,b), April 2016 (c,d) and June 2017 (e,f) transects. Insets: infection levels on an expanded scale. The solid lines show infection (red), Prochlorococcus (green) and Synechococcus (pink) averaged and plotted for every 0.5 °C. The dashed lines and shaded regions show the position of the chlorophyll front and the virus hotspot, respectively. For plots by latitude and the upper and lower bounds of infection, see Extended Data Figs. 5 and 6.Full size imageWithin the transition zone we observed a steep latitudinal increase in the abundance of cyanophages for every transect, which we define as a cyanophage hotspot (Fig. 2c and Extended Data Figs. 2 and 4). The cyanophage abundances in this hotspot were between three- and tenfold greater than in the subtropical gyre (Fig. 2c). Notably, cyanophages were approximately 25% more abundant (an increase of approximately 5 × 105 viruses ml−1) in the hotspot on the 2017 cruise relative to the other two cruises, reaching a maximum of 2 × 106 viruses ml−1. The hotspot peaked at temperatures of 15–16 °C on all transects, regardless of the geographical location, season or the exact pattern of the Prochlorococcus and Synechococcus distributions (Fig. 2c). Notably, the numbers of T7-like clade B cyanophages increased sharply in the transition zone to become the most abundant lineage, whereas T4-like cyanophages increased more modestly (Fig. 3 and Extended Data Fig. 4). The change in the cyanophage community structure was particularly pronounced in June 2017, when T7-like cyanophages were up to 2.3-fold more abundant than T4-like cyanophages (Fig. 3c). The switch in the relative abundance of T4-like and T7-like clade B cyanophages was diagnostic of the cyanophage hotspot compared with patterns in the subtropical and subpolar gyres.To begin assessing whether cyanophages negatively affected cyanobacterial populations in the hotspot, we tested the relationship between the abundance of cyanophages and total cyanobacteria. This showed a significant negative correlation between cyanophage and cyanobacterial abundances across all three cruises (Pearson’s r = −0.56, two-sided P = 0.0005, n = 34). This relationship was particularly distinct in 2017, when cyanobacteria were at their overall lowest abundances and cyanophages at their highest (Pearson’s r = −0.65, two-sided P = 0.004, n = 18). This suggests that viruses are one of the key regulators of picocyanobacteria in the region of the hotspot. However, no significant correlation was found across all regimes and all years (Pearson’s r = −0.008, two-sided P = 0.9, n = 87; Fig. 2d), indicating that factors other than viruses are likely to be more important in regulating the abundances of cyanobacteria in other regimes.Our single-cell infection measurements allowed us to directly evaluate active viral infection and its impact on picocyanobacteria in the transition zone. Viral infection spiked in this region each year with infection levels that were an average of two- to ninefold higher than those in the subtropical gyre (Fig. 4 and Extended Data Figs. 5,6 and 8). Infection peaked within the temperature range of 12–18 °C and was associated with a concomitant dip in Prochlorococcus abundances in all three cruises (Fig. 4 and Extended Data Fig. 5). These findings provide independent support for the strong negative correlation between cell and virus abundances (Fig. 2d) being the result of virus-induced mortality.Lineage-specific infection was also distinct in the transition zone relative to the subtropical gyre. Infection by T7-like clade B cyanophages generally increased to reach (2015 and 2016) or exceed (2017) those of T4-like cyanophages (Extended Data Figs. 5 and 6). In addition, the ratio of the abundances of T7-like clade B cyanophages to the number of cells they infected was 2.6-fold greater in the hotspot than the subtropics, whereas this ratio was similar in both regions for T4-like cyanophages. Together, these results indicate that, within the hotspot, the T4-like cyanophages displayed increased levels of infection, whereas the T7-like cyanophages displayed both increased levels of infection and produced more viruses per infection, suggesting that T7-like clade B cyanophages are better adapted to conditions in the transition zone (see below).Of the three cruises, the highest levels of viral infection were observed in June 2017, with up to 9.5% and 8.9% of Prochlorococcus and Synechococcus infected, respectively (Fig. 4e,f). This dramatic increase in infection mirrored the massive decline in Prochlorococcus abundances (Fig. 4e and Extended Data Fig. 5i). We estimate that viruses killed 10–30% of Prochlorococcus and Synechococcus cells daily at these high instantaneous levels of infection (Extended Data Fig. 6) based on the expected number of infection cycles cyanophages were able to complete at the light and temperature conditions in the transition zone (Methods and Supplementary Discussion). Given that Prochlorococcus is estimated to double every 2.8 ± 0.8 d at the low temperatures in this region12, we estimate that 21–51% of the population was infected and killed in the interval before cell division. Synechococcus is expected to have faster growth rates at these temperatures, doubling every 1.1 ± 0.2 d (refs. 12,46). Thus, we estimate that less of the Synechococcus population (9–31%) was killed before division.Under quasi-steady state conditions, abiotic controls on the growth rate of Prochlorococcus are balanced by mortality due to viral lysis, grazing and other mortality agents39,45,47. Based on the high levels of virus-mediated mortality, the parallel pattern between Prochlorococcus’ death and viral infection, and the negative correlation between cyanophage and picocyanobacterial abundances in the transition zone, we propose that enhanced viral infection in 2017 disrupted this balance, leading to the unexpected decline in Prochlorococcus populations. Grazing and other mortality agents not investigated here could also have contributed to additional mortality beyond the steady state, resulting in further losses of Prochlorococcus. In contrast to Prochlorococcus, Synechococcus maintained large populations despite high levels of infection (Fig. 4f), presumably due to their faster growth rates enabling them to maintain a positive net growth despite enhanced mortality. These findings suggest that virus-mediated mortality in 2017 was an important factor in limiting the geographic range of Prochlorococcus that resulted in a massive loss of habitat of approximately 550 km.Cyanophage abundances and infection levels dropped sharply in the higher-latitude waters north of the hotspot (Figs. 2c, 4 and Extended Data Figs. 1d,h and 2). The abundances of both T7-like clade B and T4-like cyanophages declined precipitously, yet T4-like cyanophages were the dominant cyanophage lineage (Fig. 3). T7-like clade A cyanophages generally increased locally at the northern border of the hotspot and became the dominant T7-like lineage in two samples between 38 and 39.2° N in 2017 (Fig. 3c and Extended Data Fig. 4). In contrast to all other cyanophages, the abundances of TIM5-like cyanophages increased in waters north of the hotspot (Fig. 3 and Extended Data Fig. 4d,i,m) but remained a minor component of the cyanophage community. No relationship was found between cyanophage and cyanobacterial abundances (Fig. 2d), and less than 1.5% of picocyanobacteria were infected by all cyanophage lineages in these waters (Fig. 4).The cyanophage hotspot in the transition zone is a ridge of high virus activity that separates the subtropical and subpolar gyres. The reproducibility of our observations, which were separated by days to weeks within each cruise (2016 and 2017) and by years among the three cruises (Extended Data Fig. 4), indicates that this virus hotspot is a recurrent feature at the boundary of these two major gyres in the North Pacific Ocean. This suggests that the hotspot forms due to the distinctive environment of the inter-gyre transition zone creating conditions that enhance infection of picocyanobacteria and proliferation of cyanophages. Prochlorococcus in the transition zone may be prone to stress due to being close to the limits of their temperature growth range5,6, which has the potential to increase susceptibility to viral infection. Alternatively, there may be temperature-dependent trade-offs between virus decay and production that lead to replication optima within a narrow temperature range48. Cyanophage infectivity has been observed to decay more slowly at colder temperatures49, which may allow for the accumulation of infective viruses, leading to increased infection. In addition, cyanophage infections may be more productive due to enhanced nutrient supply in the transition zone27 (Fig. 1h,i) relative to the subtropics, given that the cyanophages replicate in hosts with presumably greater intracellular nutrient quota and obtain more extracellular nutrients, both of which may increase progeny production9,10. The environmental factors influencing the production and removal of viruses probably vary in intensity at different times, leading to variability in cyanophage abundance and infection levels. Thus, the putative cyanophage replication optimum in the hotspot may reflect the combined effects of temperature and nutrient conditions that are intrinsically linked to the oceanographic forces that shape the transition zone itself.Changes in the cyanophage community structure over environmental gradients are likely to reflect differences in host range, infection properties and genomic potential to remodel host metabolism9. Our data, together with previous measurements in the North Pacific Subtropical Gyre38,39, indicate that the T4-like cyanophages are the lineage best adapted to the low-nutrient waters of the subtropics (Fig. 2d–f). As these waters are inhabited by hundreds of genomically diverse subpopulations of Prochlorococcus50, the broad host range of many T4-like cyanophages18,19,22,51 may be advantageous for finding a suitable host. T4-like cyanophages also have a large and diverse repertoire of host-derived genes21,51—such as nutrient acquisition, photosynthesis and carbon-metabolism genes—that augment host metabolism52 and may increase fitness in nutrient-poor conditions in the subtropics51. In contrast, T7-like clade A and B cyanophages seem to be better adapted to conditions in the transition zone (Fig. 3). T7-like cyanophages have narrow host ranges19,22,40, with smaller genomes and fewer genes to manipulate the host metabolism23, which may allow them to replicate and produce more progeny in regions with elevated nutrient concentrations relative to subtropical conditions. The maximal abundances of TIM5-like cyanophages were found in the most productive waters at the northern end of the transects where the cyanobacterial abundances were lowest and Synechococcus was the dominant picocyanobacterium. This may be partially due to the narrow host range of TIM5-like cyanophages and their specificity for Synechococcus40,44. Our findings of reproducible lineage-specific responses to changing ocean regimes indicate that cyanophage lineages occupy distinct ecological niches.Temperature and nutrient changes occurring in the transition zone are expected to result in shifts in picocyanobacterial diversity at the sub-genus level (Supplementary Discussion), which we speculate may affect community susceptibility to viral infection. One mechanism for this may be that the picocyanobacteria that thrive in the transition zone are intrinsically more susceptible to viral infection. Another scenario may be related to trade-offs associated with the evolution of resistance to viral infection. The horizontal advection of nutrient-rich waters to the transition zone28 may select for rapidly growing cells adapted for efficient resource utilization. Viral resistance in picocyanobacteria often incurs the cost of reduced growth rates53,54. Thus, competition for nutrients in this region may favour cells with faster growth rates but increased susceptibility to viral infection. Thus, it is probable that the cyanophage distributions do not always follow the cyanobacterial patterns (Extended Data Fig. 2) because of complex interactions between lineage-specific cyanophage traits, host community structure and environmental variables, which may vary seasonally or annually as a result of interannual variability in environmental conditions (see below).Despite consistent features in cyanophage distributions across the North Pacific Ocean, cyanophage infection was higher (Fig. 4 and Extended Data Fig. 7), whereas Prochlorococcus abundances were consistently lower (Fig. 2a), across the June 2017 transects relative to the March 2015 and April 2016 transects. Seasonality and/or climate variability could explain this interannual variability, although the data currently available to assess this are sparse. Viral infection of picocyanobacteria in the subtropical gyre increased from early spring to summer, suggesting a potential seasonal pattern that may extend across the transect (Extended Data Fig. 9a). In addition, the June 2017 transect occurred during a neutral-to-negative El Niño phase with lower sea-surface temperatures relative to the 2015 and 2016 transects, which were in years of a record marine heatwave, followed by a strong El Niño55 (Extended Data Fig. 9b). In 2015 and 2016, the Prochlorococcus abundances were found to be higher than usual in the North Pacific Ocean in this (Fig. 2a) and other studies56,57. Irrespective of the underlying drivers for the observed interannual variability, we speculate that an ecosystem tipping point was reached in the hotspot under the prevailing conditions in June 2017, aided by the higher cyanophage abundances yet smaller Prochlorococcus population sizes. In this scenario, picocyanobacterial populations were subjected to high infection levels that resulted in an accumulation of cyanophages, initiating a stronger than usual positive-feedback loop between infection and virus production, and precipitating the unexpected Prochlorococcus decline. Continued observations in the North Pacific Ocean are needed to evaluate the potential link between seasonality and/or large-scale climate forcing as ultimate drivers affecting virus–host interactions.Predicting basin-scale virus dynamicsMeasurements of cyanobacterial and cyanophage abundances rely on discrete sample collection from shipboard oceanographic expeditions, which limits the geographical and seasonal extent of available data. Therefore, we developed a multiple regression model based on high-resolution satellite data of temperature and chlorophyll to predict cyanophage abundances, a key proxy of cyanobacterial infection (Pearson’s r = 0.61, two-sided P = 1.7 × 10−8, degrees of freedom = 68, n = 70). We used the model to estimate the geographical extent of the virus hotspot. The model accurately predicted the location of the hotspot and cyanophage abundances along a fourth transect in April 2019 (Supplementary Table 1), with the majority of observations falling within the 95% confidence intervals of the model predictions (Fig. 5a–c). Application of the model to the larger region predicted that the virus hotspot formed a boundary extending across the North Pacific Ocean, with lower cyanophage abundances on both sides (Fig. 5d,e and Supplementary Fig. 1). This boundary had the hallmarks of the hotspot with a core that was dominated by T7-like cyanophages and the flanking gyre regions dominated by T4-like cyanophages. Thus, this feature may be more appropriately termed a ‘hot-zone’ due to its substantial projected aerial extent. Assuming the infection levels observed in the hotspot in June 2017 were similar throughout the hot-zone, the potential habitat loss for Prochlorococcus would be about 3.2 × 106 km2, approximately half of the cumulative area loss of the Amazonian rainforest to date58.Fig. 5: Prediction of cyanophage abundances.a–c, Model-based predictions of cyanophage abundances corresponding to the empirically measured total (a), T4-like (b) and T7-like clade B (c) cyanophage abundances along a transect in the North Pacific in April 2019. The shaded regions show the 95% confidence interval for the model predictions. d,e, Predicted total cyanophages (d) and the ratio of T4-like/T7-like clade B cyanophages (e) in June 2017 in the North Pacific Ocean. The black lines indicate the cruise track. The grey areas represent regions with no values due to cloud cover or that were beyond the limits of the predictive model. The hotspot peak corresponds to yellow regions in d and red regions in e.Full size imageVirus hotspot biogeochemistryWith the ability to predict biogeographic patterns of cyanophages, we evaluated the potential biogeochemical implications of virus-mediated picocyanobacterial lysis and release of organic material in sustaining the bacterial community6,7,8,9. The aerial extent of the hot-zone (approximately 4 × 106 km2) is only 14% of the size of the subtropical gyre (2.9 × 107 km2), and yet the total virus-mediated organic matter released from picocyanobacteria in the hot-zone in June 2017 was estimated to be on par with that for the entire North Pacific Subtropical Gyre (Methods and Supplementary Discussion). We estimate that viral lysate released from picocyanobacteria in the subtropical gyre could sustain 4.4 ± 0.8% of the calculated bacterial carbon demand there (Extended Data Fig. 10). In contrast, viral lysate released in the transition zone could sustain an average of 21 ± 12% of the bacterial carbon demand, reaching 33% in some regions (Extended Data Fig. 10), assuming that the bacterial assimilation and growth efficiencies were similar between the subtropical gyre and the hotspot. Thus, local generation of cyanobacterial viral lysate in the transition zone is likely to be an important source of carbon for the heterotrophic bacterial community that can rapidly utilize large molecular weight dissolved organic matter59 and may have contributed to the increase in their abundances south of the chlorophyll front in 2017 (Extended Data Fig. 1a,e). More

The generation of this map of the world’s mountains consisted of five steps (Fig. 1): (i) the identification and hierarchisation of named mountain ranges and the recording of range-specific information; (ii) the manual digitization of the ranges’ general shape; (iii) the definition of mountainous terrain (and the inventory’s outer borders) using a DEM-based algorithm; (iv) the automatic refinement of the digitized and named ranges’ inner borders; and (v) the preparation of the final layers. The resulting products consist of a refined mountain definition (GMBA Definition v2.0), two versions of the inventory (GMBA Inventory v2.0_standard & GMBA Inventory v2.0_broad), and a set of tools to work with the inventories.Step i: Identification and hierarchisation of mountain rangesIn a first step, we identified mountain ranges worldwide. To do so we adopted the mountain ranges identified in the GMBA Inventory v1.410,14 and searched existing resources in any languages for other named ranges not yet included. The ranges added could either be adjacent to, included in (child range or subrange) or including (parent range or mountain system) mountain ranges of the GMBA Inventory v1.4. The resources used for our searches included world atlases (e.g. The Times Comprehensive Atlas of the World19, Knaurs grosser Weltatlas20, Pergamon World Atlas21); topographic maps (e.g. http://legacy.lib.utexas.edu/maps/imw/, http://legacy.lib.utexas.edu/maps/onc/, https://maps.lib.utexas.edu/maps/tpc/, www.topomap.co.nz, https://norgeskart.no, www.ign.es/iberpix/visor/); encyclopaedias (www.wikipedia.org; www.britannica.com); online gazetteers and reference sites (e.g. www.wikidata.org, www.geonames.org (GeoNames), www.mindat.org); mountain classification systems (e.g. the International Standardized Mountain Subdivision of the Alps or SOIUSA for the Alps22, Alpenvereinseinteilung der Ostalpen23, Classification of the Himalaya24, www.peakbagger.com/rangindx.aspx (PEMRACS), www.carpathian-research-network.eu/ogulist, http://www.sopsr.sk/symfony-bioregio/lkpcarporog, www.dinarskogorje.com, https://bivouac.com/, https://climbnz.org.nz/); and national or regional landscape, geomorphological, or physiographic maps and publications4,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42. The full list of the consulted sources and references is available on GitHub at https://www.github.com/GMBA-biodiversity/Inventory (GMBA Mountain Inventory v2.0 References.pdf).All identified mountain ranges were recorded in a Microsoft Access relational database (“Mountain database”, see below) and given a name, a unique 5-digit identifier (GMBA_V2_ID), and the corresponding Wikidata unique resource identifier (URI), when available. This URI gives access to a range’s name as well as to its Wikipedia page URL in all available languages and lists other identifiers for given mountain ranges in a variety of other repositories such as GeoNames or PEMRACS. The primary mountain range names were based on the resources used for range identification and were preferably recorded in English. Names used nationally, locally, as well as/or by indigenous people and local communities were extracted from Wikidata and recorded in a separate attribute field.In the process of cataloguing, we attributed a parent range to each of the mapped mountain ranges. Information about parent ranges is included in PEMRACS, often also in Wikidata as a property that can be extracted though a SPARQL query, in the corresponding Wikipedia pages description, and in regional hierarchical mountain classifications that exist for the European Alps (SOIUSA), the Carpathians, and the Dinaric Alps. When no such information was available, we relied on other sources of information that we found either using a general web search (leading to specific papers, reports, or web pages on mountain ranges) or by consulting (online) topographical maps and atlases at different scales. The information about parent ranges was used to construct a hierarchy of up to 10 levels using a recursive SQL query (see Step v). The result of this step was a relational database with a hierarchy of mountain systems and (sub-) ranges (Fig. 1, “Mountain database”).Step ii: Digitization of the mountain rangesIn a second step, we digitized all identified ‘childless’ mountain ranges (i.e. smallest mapping units, called ‘Basic’ as opposed to ‘Aggregated’ in the database) in one vector GIS layer. To do so, we used the Google Maps Terrain layers (Google, n.d.) as background and the WHYMAP named rivers layer42 as spatial reference since descriptions of mountain range areal extension is often given with reference to major rivers. The digitization, which was done in QGIS43 using the WGS 84 / Pseudo-Mercator (EPSG 3857) coordinate reference system, consisted in the drawing of shapes (polygons) that roughly followed the core area of each mountain range. In general, the approximate shape and extent of the mountain ranges we digitized could be distinguished based on the terrain structure as represented by the shaded relief background that corresponded to the placement and orientation of the range’s name label on a topographical map, atlas or other resource. As the exact placement and orientation of mountain range labels in each specific source can be influenced by cartographic considerations (e.g. avoiding overlaps with other features), the final approximation of the mountain range was obtained by consulting a variety of sources for each mountain range. Occasionally, the mountain terrain’s geomorphological characteristics strongly hampered the accuracy of our visual identification of mountain subranges within larger systems. This was particularly the case in old, eroded massifs such as the Brazilian Highlands or the highlands of Madagascar, where individual mountain ranges are not separated by deep well-defined valleys and have a very complex topography. In these cases, we referred to available topographical descriptions of range extent and to the river layer (see above). Other complex regions included Borneo and the Angolan Highlands, whereas subranges in mountain systems such as the European Alps, the Himalayas, and the North American Cordillera were comparatively easy to map. Moreover, the density of currently available mountain toponymical information varied quite strongly between regions. Accordingly, regional variation in the size of the smallest mountain range map units can be considerable. The result of this step was a (manually) digitized vector layer of named mountain ranges shapes (Fig. 1, “Manual mountain shapes”).Step iii: Definition of mountainous terrainIn a third step, we defined mountainous terrain (GMBA Definition v2.0). To distinguish mountainous from non-mountainous terrain, we developed a simple algorithm which we implemented in ArcMap 10.7.144. This algorithm is based on ruggedness (defined as highest minus lowest elevation in meter) within eight circular neighbourhood analysis windows (NAWs) of different sizes (from 1 pixel (≈ 250 m) to 20 (≈ 5 km) around each point, Fig. 2c) combined with empirically derived thresholds for each NAW (Fig. 2). The decision to use multiple NAW sizes was made because calculating ruggedness based on only a small or a large NAW comes at the risk of identifying the many local irregularities typically occurring in flat or rolling terrain as mountainous or of including extensive flat ‘skirts’ through the smoothing and generalization of large NAWs3. Accordingly, our approach ensures that any point in the landscape classified as mountainous showed some level of ruggedness not only at one but across scales. This also resulted in a smooth and homogeneous delineation of mountainous terrain, very suitable for our mapping purpose.Fig. 2Elevation range thresholds for the eight neighbourhood analysis windows (NAW) and their contribution to calculations of the GMBA Definition v2.0. (a) distribution of elevation range values (ruggedness) for NAWs (numbered I to VIII) in mountain regions as defined by the geometric intersection of K1, K2 and K3. (b): plot of the minimum elevation range versus the area of the NAW (n = 920). (c) NAWs and their corresponding threshold values. (d) percent overlap between GMBA Definition v2.0 (intersection of eight NAW-threshold pairs) and area defined by each individual NAW-threshold pair. (e) percent eliminated by each NAW-threshold pair (I to VIII) from the mountain area defined by the other 7 NAW-threshold combinations. Highlighted bars in the two graphs represent the combination of three NAW-threshold pairs that results in the highest overlap with the GMBA Definition v2.0.Full size imageWe used the median value of the 7.5 arc second GMTED2010 DEM45 as our source map. To reduce the latitudinal distortion of the raster, and thus the shape and area of the NAWs, we divided the global DEM into three raster layers corresponding to three latitudinal zones (84° N to 30° N, 30° N to 30° S and 30° S to 56° S) excluding ice-covered Antarctica and projected the two high latitude zones to Lambert Azimuthal Equal Area and the equatorial zone to WGS 1984 Cylindrical Equal Area. We used these reprojected DEM layers to produce eight ruggedness layers, each using one of the eight NAWs.To determine the threshold values of our algorithm, we selected 1000 random points within the area defined by the geometric intersection (Fig. 1b) of the three commonly applied mountain definitions, i.e. the definitions by UNEP-WCMC46, GMBA15, and USGS3. These layers (referred to as K1, K2, and K3, respectively by Sayre and co-authors12) were obtained from the Global Mountain Explorer47. We eliminated 80 clearly misclassified points (i.e., points that fell within lakes, oceans, or clearly flat areas according to the shaded relief map we used as a background) and used the remaining 920 to sample the eight ruggedness layers. For each of the 8 layers, we retained the lowest of the 920 ruggedness values as the threshold for the layer’s specific NAW (Fig. 2c). The eight threshold values were then used to reclassify each of the eight layers by attributing the value 1 to all cells with a ruggedness value higher than or equal to the corresponding threshold and the value 0 to all other cells. Finally, we performed a geometric intersection (see Fig. 1b) of the eight reclassified layers to derive the new mountain definition.After these calculations, we reprojected the three raster layers to WGS84 and combined them through mosaic to new raster. To eliminate isolated cells and jagged borders, we then generalized the resulting raster map by passing a majority filter (3 × 3 pixels, majority threshold) three times. This layer corresponds to the GMBA Definition v2.0.The resulting mountain definition (GMBA Definition v2.0) distinguishes itself from previous ones because of the empirically derived thresholds method used to develop it and the use of eight NAWs. In line with the previous GMBA definition, it relies entirely on the ruggedness values within NAWs. The GMBA Definition v2.0 was used to determine the outer delineation of this inventory’s mountainous terrain. As expected, it includes neither the wide ‘skirts’ of flat or undulating land around mountain ranges nor the topographical irregularities that are both typically included when other approaches are applied. It also successfully excludes extensive areas of rolling non-mountainous terrain such as the 52,000 km2 Badain Jaran Desert sand dunes in China. However, this mountain definition is conservative and only includes the highest, most rugged cores of low mountain systems, as for example in the Central Uplands of Germany, and therefore excludes some lower hill areas still considered by some as mountains.As a further step towards generalization, we considered that small ( More

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Study origin and designThe MeadoWatch project (MW) is a project run collaboratively between the University of Washington (UW) and the United States National Park Service to monitor the phenology of alpine and subalpine wildflower species across large elevational gradients in Mount Rainier National Park (Fig. 2). MW was established in 2013 with the goal of understanding long-term effects of climate change on Mount Rainier National Park wildflower communities using community-science approaches. The first MW transect was established along Reflection Lakes, Skyline, and Paradise Glacier trail system in 2013 (9–11 plots). In 2015, MW expanded to include a second transect (15–17 plots) along the Glacier Basin trail (Fig. 1a). The MW transects span around 5 km each, over a 400 m altitudinal gradient (Reflection Lakes: 1490m–1889m a.s.l.; Glacier Basin: 1460m–1831m a.s.l.)Fig. 2Alpine meadows, plot extension, and target species. (a) Species-rich alpine meadow in Mount Rainier National Park (Mount Tahoma), showing many of the target species in the foreground. (b) MW volunteer coordinator Anna Wilson at a plot, indicating the arm span that defines the plot area (personal likeness used with confirmed consent). (c) Species composition and proportion of reports per species in each of the transects; species common to both trails are highlighted with striped shadowing. Photographs: A. John (a), L. Felker (b).Full size imagePlots are located along the side of each trail, marked with a colored survey marker. The area of each plot is defined by the arm-span of volunteers when they position themselves over the plot marker looking away from the trail (Fig. 2b). While less accurate than marking the corners of plots, this approach was used to avoid establishing permanent structures in wilderness areas within the National Park. The surveyed area in each plot is, on average, 1.25 m2. Each plot is also equipped with temperature sensors (HOBO Pendant Logger, Onset Computer Corp.) buried approximately 4 cm below the ground. Sensors are placed at the start of each fall season and removed at the beginning of each summer season for data downloading. The HOBO sensors provide an estimate for the date of snow disappearance and in-situ temperature at 3 hours intervals. Once plots are covered in snow, soil temperatures remain at 0 °C and show no diurnal variation, so that daily changes in temperatures above 1 °C can be used to determine the earliest date without snow cover20. We use these approaches to provide dates of snow appearance and disappearance, snow cover duration, and minimum soil temperatures for each year and plot. Occasionally, temperature data during the snow disappearing window were lost due to sensor failure or loss of sensors (which occurs because plots are not permanently marked and/or well-meaning visitors remove sensors). This, and the lack of temperature sensors in the first year of the project, resulted in approx. 20% of cases of missing data. In those cases, we used a data imputation method to estimate the missing values based on data from nearby plots and a parallel temperature data collection with 890 total observations. These estimates were highly reliable in filling the data gaps (see Appendix C in16 for further details).Focal speciesWe originally targeted 16 native wildflower species along each transect, which were chosen based on their abundance, ease of identification, and presence in the plot. Four of those target species were present on both transects. In 2016 we replaced one species with a different one (see further information below), making for a total of 17 species monitored (Fig. 2c). The focal species are: American bistort* (Polygonum bistortoides), avalanche lily (Erythronium montanum), bracted lousewort* (Pedicularis bracteosa), broadleaf arnica (Arnica latifolia), cascade aster (Aster ledophyllus; synonym Eucephalus ledophyllus), glacier lily (Erythronium grandiflorum), Gray’s lovage (Ligusticum grayi), magenta paintbrush (Castilleja parviflora), mountain daisy (Erigenon peregrinus; synonym Erigeron glacialis), northern microseris (Microseris alpestris; synonym Nothocalais alpestris), scarlet paintbrush (Castilleja miniata), sharptooth angelica (Angelica arguta), sitka valerian* (Valeriana sitchensis), subalpine lupine* (Lupinus arcticus; synonym Lupinus latifolius var. subalpinus), tall bluebell (Mertensia paniculata), Canby’s licorice-root (Ligusticum canbyi), and western anemone (Anemone occidentalis). Asterisks denote species monitored along both trails.Due to challenges in species identification, we dropped Canby’s licorice-root (Ligusticum canbyi) as a target species in 2016. Consequently, Ligusticum canbyi has limited replication in the database (Fig. 2c). While we included the phenological records of this species for the sake of completeness, we recommend focusing on the other 16 species, which are both better represented (in terms of data coverage) and are free of any potential misidentification issues.For additional information on the species, methods, identification cues, and image resources see: http://www.meadowatch.org, https://www.youtube.com/channel/UCGBFTKxf8FIWswMDxBavpuQ, and the appendices therein16.Data collection and volunteer trainingDuring the summer months, MW volunteers and scientists collect reproductive phenology data with a frequency between 3 and 9 trail reports per week. Each report records the presence or absence of 4 phenophases for each target species present in each of the plots. The phenophases are ‘budding’, ‘flowering’, ‘ripening fruit’, and ‘releasing seed’. Phenophases were defined as follows:BuddingThe beginning growth of the flower which has not yet opened. A plant is considered budding if buds are present, but the stamen and pistils are not yet visible and available to pollinators.FloweringThe generally “showy” part of the plant that holds the reproductive parts (stamens and pistils). A plant is considered flowering when at least one flower is open, and the stamens and pistils are visible and available for pollination and reproduction.Ripening fruitThe fruit develops from the female part of the flower following successful pollination. In the target species, fruits can take many forms, from hard, fleshy capsules, juicy berries, to a feathery tuft on the end of a seed. A plant is in the ripening fruit stage when reproductive parts on at least one reproductive stalk are non-functional and the formation of the fruit part is clearly ongoing (visible), but seeds are not yet fully mature and not yet being dispersed.Releasing seedAfter the fruit ripens, seeds are released to be dispersed by gravity, wind, or animals. A plant is considered in the releasing seed stage if seeds are actively being released on at least one reproductive stalk (but there are still seeds present).A full description, including illustrations for each species’ phenophase and identification cues is available in http://www.meadowatch.org/volunteer-resources.html, as well as in Annex 1 – Supplementary Documentation. Multiple phenophases can be present simultaneously, depending on the species, and are noted independently. Additionally, volunteers are also asked to record the presence of snow (‘snow covered plot’, ‘partially covered plot’, or ‘snow-free plot’), and, since 2017, the presence of damage by herbivory (‘presence of browsed stems’) on each plot.In years not impacted by the SARS-Cov-2 pandemic MW volunteers attend an in-person 3-hour botanical and phenological training session taught by UW scientists at the beginning of each sampling season. Volunteers were also provided with detailed species-identification guides, including an extensive description of sampling methods and location of the plots. The trainings for the 2020 and 2021 seasons were held virtually via a series of online training videos. In these years, volunteers took a quiz on wildflower phenology, plant identification and data collection methods after viewing these videos and were required to ‘pass’ a certain threshold to volunteer (unlimited attempts were allowed). During these virtual trainings, volunteers were provided with digital copies of the species identification guides, with many returning volunteers using printed guides they had kept from previous years.At the end of their phenological hike, volunteers submit their data sheets either by depositing them in lockboxes located within the park, or by scanning and emailing them directly to mwatch@uw.edu. Data are then entered manually and stored in the UW repositories after being checked for consistency at the end of each sampling season.The parallel data collection by members of UW’s Hille Ris Lambers group (including PI, postdoctoral researchers, graduate students, and trained interns) acted as the following: (i) a quality-control, i.e., allowing us to compare the consistency in phenology assessments between volunteers and scientists, and (ii) a way to increase the temporal resolution and scale of the data, e.g., by reducing early season gaps and ‘weekend bias’17. This parallel expert sampling was carried out around once a week between 2013 and 2020, showing great consistency between the two groups. For detailed comparisons between volunteers and scientists’ assessments see the data validation section (as well as Appendix E in16).Processed dataIn addition to the raw phenological data, we also provide here parameters to construct the year, species, and plot-specific flowering phenology based on the timing of snow disappearance (as in16). Models describe unimodal probability distributions that were fitted with maximum likelihood models to binomial flowering data from each species, year, and plot. These curves have been used to estimate peak flowering dates and diversity and link them to reported visitor experiences16. Here, we provide the 3 parameters defining the unimodal curve of flowering probability per species i, plot j and year k: the duration of flowering (𝛿ijk), the maximum probability of flowering (𝜇ijk), and peak flowering (in DOY – ρijk); following the equations described in16 and https://github.com/ajijohn/MeadoWatch).The parameters of these probability distribution curves are ready-to-use values that can be broadly and easily used to estimate floral compositional change over past seasons due to changing environmental conditions—for example, to inform plant-pollinator interaction networks if combined with pollinator behavioral data (e.g.21). More