Philippa Kaur

The SYF outbreak that occurred in Brazil from 2016 onwards reached states in the southeast, northeast, and south. It became the most important outbreak in recent decades due to the large number of cases and deaths in humans and NHPs, reaching areas with high population densities and low vaccination coverage5,12,19,20. In SP, this process started in a region with high vaccination coverage and progressed to areas with low coverage and/or without vaccination recommendations, with high population densities11,12. The first region with these characteristics to be affected by the outbreak was Campinas12 and the period resulting from this advance was considered the first wave. In the second half of 2017, SYF advanced to the east, south, southeast, and northeast regions of SP, characterizing the second wave.Hill et al.4 analyzed only the SYF epizootics that occurred in SP between 2016 and 2018 and divided this process into three phases. Although this makes more sense for the epizootic disease analysis, considering the outbreak process in two waves made it possible to adequately capture the spatiotemporal process of SYF diffusion and to characterize it by contagion. Moreover, this characterization allowed a discussion on the relevance of the vaccine strategy adopted by SES-SP, especially during the second wave. The Ministry of Health, in view of the YF outbreak in areas without recommendation and/or low vaccination coverage, advocated the expansion of vaccination based on calculations of affected area/expanded area, with the municipality as smallest unit17. Until mid-2017, this strategy was an adequate response. However, it became demonstrably insufficient when the virus reached populous areas with low coverage and/or without a vaccination recommendation, both in SP12 and in other southeastern Brazilian states21.In SP, the advancement of YF within a period of less than six months from areas with high vaccination coverage to populous areas with low coverage or without vaccination recommendations triggered a public health crisis that generated panic in the population. At that time, there were insufficient time and vaccine doses to serve the entire population at risk21. Hence, SES-SP identified the priority vaccination areas based on the analysis of virus circulation in NHPs at forest fragments, which comprise functional ecological corridors for viral dispersion, and were therefore demarcated and used to select areas where populations were most exposed to YF risk. Instead of considering the entire municipal territory with the same risk level, the new strategy sought to identify priority intra-municipal areas for vaccination, considering the speed of dispersion16. Moreover, this strategy, plus the use of single doses1 and fractional doses22, allowed reasonable equation, in space–time, of the demand for vaccines in a large population contingent with an insufficient supply of the immunobiological product. It should be noted that this strategy had already been recommended by the WHO in outbreaks within the African continent in 2015/201621,23.Our results demonstrated that the YF virus dispersion in SP was caused by the outbreak process of territorial spread by contagion; therefore, the mosquito vectors and NHPs could act as a route of viral amplification and further transmission on epizootic waves. In this situation, there was a cadence in the spatiotemporal pattern of viral dispersion through contiguous and nearby areas. This also shows the appropriateness of the vaccination strategy adopted by SES-SP, which allowed the population to receive the vaccine at least two months before the establishment of on-site transmission risk15. A spatiotemporal process of sequential spreading was observed, wherein municipalities located at shorter distances from the areas with YF virus transmission were more likely to be affected first7,8. Although our analyses are limited by the fact that we used the municipality as a spatial study unit, this spreading pattern can also be observed at the intra-municipal level.The speed of the SYF dispersion that we obtained for the first and second waves, disregarding the RDSs of Registro and Itapeva, were similar to those reported by Hill et al.4. Through phytogeographic analysis of YF genomes in NHPs, they reported spreading speeds of around 1.0 km per day. Notably, they took into account epizootics that occurred in SP up to February 2018, and the occurrences of human cases and epizootics in the RDS of Registro and Itapeva were recorded from February 2018 onwards. The differences in the speed of viral dispersion between these two RDSs and the rest of SP during the second wave may be related to the greater vegetation cover and forest preservation of these areas, which can cause a dilution effect, as already demonstrated for other vectorborne diseases24. The spread of the SYF outbreak by contagion in most of SP, with a speed of approximately 1.0 km per day, opened a spatiotemporal window of opportunity for the vaccine to arrive before the virus15, avoiding or minimizing the occurrence of human cases and deaths. Since 2019, this outbreak has advanced to the southern region of the country and has reached the states of Paraná and Santa Catarina, and is still ongoing. This generated an emergency situation similar to that in SP, and the same vaccination strategy adopted in SP has been applied in this region16,18,20.Our findings (Fig. 2) showed important differences in human cases and epizootics that occurred in SP during the second wave, reflecting the degree to which municipalities have adopted the vaccination strategy advocated by the SES-SP. If this is true, what happened in Mairiporã and Atibaia (37% of the total human cases between 2016 and 2019) could also have occurred in municipalities such as Jundiaí, Bragança Paulista, Itapecerica da Serra, Pinhalzinho, Louveira, and São Paulo. If the YF vaccination strategy had not been adapted for the emergency situation during the second wave, we could have had a worse outcome than that observed. These possible scenarios could be the subject of future studies.At the end of 2016 and 2017, the detection of YF epizootics in NHPs anticipated the notification of human cases by two and three months, respectively. This result is expected, since the seasonality observed among NHPs in Brazil differs from that observed in human cases. In primates, circulation is generally detected in September, whereas in humans, circulation is usually observed in December, with the detection of cases among non-immunized people and those exposed to the virus17,25. This also highlighted the importance of the NHP epizootic surveillance strategy, aimed at the early detection of the circulation of the YF virus while still in the enzootic cycle4,26. However, despite the heavy investment of SES-SP in making municipalities sensitive to detection of NHP mortality, the detection of epizootic diseases is still marked by a strong reporting bias26.One of the causes for the anticipation of epizootics in relation to human cases can be explained by seasonality of the precipitation in SP during the year. From the middle to the end of autumn, depending on the year, the total rain decreased and registered monthly values that were increasingly smaller. This becomes reversed in the beginning of spring, when an increase in the precipitated volume begins to be registered throughout SP27,28. To increase YF transmission, mosquito vectors need to be found in large quantities, and one of the determining factors for the proliferation of mosquitoes is the level of precipitation, as this allows the accumulation of water in reservoirs and the hollows of trees29.Another important factor is the rise in temperatures from the end of winter and the beginning of spring. Temperature increases accelerate the time for larval development of the vectors29 and reduces the extrinsic incubation period of the virus30. Precipitation and temperature directly influence the mosquito’s life cycle and viral replication31, hence their increase is an optimal scenario for the proliferation of YF vectors and for the increased occurrence of epizootic diseases in SP29. By contrast, the increase in the probability of detecting human SYF cases in December may be related to the greater degree of exposure among unvaccinated people due, among other issues, to tourism, and to the fact that this occurs simultaneously with the transmission of the YF virus sustained by NHPs.The occurrence of SYF outbreaks in regions with high population density and without adequate vaccine coverage represents a risk of YF reintroduction in urban areas. Even with the vaccination campaigns carried out so far, a large part of the Brazilian population has not yet been immunized5. UYF has been absent in Brazil since 1942, and in human cases that have occurred so far, there has been no epidemiological link with a possible urban cycle20 or involvement of its main urban vector, Ae. aegypti, in viral transmission3. However, this risk is increased by this vector’s presence in almost all Brazilian municipalities32. Another source of concern for the re-urbanization of YF in Brazil is the presence of Ae. albopictus. This mosquito reportedly transmits the YF virus in the laboratory setting and has already been found naturally infected by this virus in the city of Minas Gerais20,33. Present in both urban areas and the rural and forest areas of the country, this mosquito could be a link between the sylvatic and urban forms of the disease3,34. Efforts must be made to prevent the occurrence of UYF epidemics, as could constitute a major public health issue. Among the measures that can be adopted, the most urgent are investments in the production of vaccines, vaccination of the entire Brazilian population, and the development of effective measures to control Ae. aegypti1,21,35.This study has several limitations, such as the use of secondary surveillance data, which are subject to both notification and underreporting errors. Examples of these problems are the need to eliminate three municipalities from wave modeling and the NHP epizootic underreport. The unavailability of the exact probable site of infection for human cases and epizootics, as well as their occurrence dates, obliged us to consider the centroids of the municipalities and the months of the year. These limitations provide a partial view of the outbreak and did not allow us to investigate, for example, the characteristics of the places where the cases and epizootics occurred. Another limitation was that vaccination coverage was based only on vaccination data for children under 5 years of age.However, this study has strengths that contribute to its internal and external validity. Among them are the use of both information about sylvatic human cases, as well as epizootics, to investigate the outbreak process. Another strong point was the use of kriging geostatistics to assess the spread of SYF. This is a spatiotemporal process, and the use of kriging allowed us to consider the autocorrelation of the phenomenon in space–time and numerically represent it throughout the SP area. More

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CORRESPONDENCE
10 August 2021

Iran: drought must top new government’s agenda

Jamshid Parchizadeh

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Jerrold L. Belant

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Jamshid Parchizadeh

Global Wildlife Conservation Center, State University of New York College of Environmental Science and Forestry, Syracuse, New York, USA.

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Jerrold L. Belant

Global Wildlife Conservation Center, State University of New York College of Environmental Science and Forestry, Syracuse, New York, USA.

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We urge Iran’s incoming government to give priority to resolving the country’s worst drought in 50 years (see go.nature.com/2wkwyqn). In our view, the government needs to consult with international as well as domestic water experts to prevent the imposition of flawed agendas. It should also revise earlier policies that have contributed to the crisis.Outgoing president Hassan Rouhani blamed the drought on a 52% reduction in rainfall since last year. However, unregulated aquifer depletion and mismanagement of water resources by the authorities (see, for example, go.nature.com/3cce7or) have contributed.The drought and its associated dust haze is also severely affecting ecosystems in and around Iran (see go.nature.com/3jhauvc and http://pana.ir/news/1178597).

Nature 596, 189 (2021)
doi: https://doi.org/10.1038/d41586-021-02189-z

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The authors declare no competing interests.

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The data collection protocol is described in Sánchez et al.19 and followed Reporting Standards for Systematic Evidence Syntheses (ROSES) guidelines20. Philibert et al.21, also proposed eight criteria for conducting high quality meta-analysis, which overlap to some extent with ROSES guidelines. Our methods fulfil the Philibert et al. requirement to use a repeatable procedure for paper selection, provide a list of references, and ensure availability of the dataset, while other quality criteria are only relevant at the meta-analysis stage.Search processThe literature search was conducted on 29 November 2019 and updated on 5 January 2021, and aimed to identify relevant English language articles published in peer-reviewed literature. We searched in titles, abstracts and keyword lists of literature in the Scopus and Web of Science databases, using the following search string (formatted for Scopus; see Dataset 1 for the equivalent string formatted for Web of Science): TITLE-ABS-KEY (“agricultur*” AND “biodiversity”) AND TITLE-ABS-KEY (“agro?ecology” OR “agro?biodivers*” OR “agroforestry” OR “border plant*” OR “riparian buffer” OR “woodlot” OR “hedgerow” OR “cover crop*” OR “crop rotation” OR “crop divers*” OR “inter?crop*” OR “mixed crop*” OR “cultivar mixture” OR “plant divers*” OR “polyculture” OR “tree divers*” OR “variet* diversity” OR “fallow” OR “field margin*” OR “grass strip*” OR “*flower strip*” OR “insect* strip” OR “conservation strip” OR “vegetation strip” OR “catch crop” OR “inter?crop*” OR “crop variety” OR “crop sequenc*” OR “mixed farming” OR “land sparing” OR “landscape heterogeneity” OR “heterogeneous landscape” OR “landscape diversi*” OR “divers* landscape” OR “homogeneous landscape” OR “landscape homogeneity” OR “landscape complexity” OR “simplif* landscape” OR “complex landscape” OR “multi?function* landscape” OR “integrated crop-livestock” OR “integrated crop-forest” OR “land sharing”) AND TITLE-ABS-KEY (“ richness” OR “ abundance” OR “species diversity” OR “functional diversity” OR “index”) AND TITLE-ABS-KEY (“crop yield” OR “crop production”) AND (LIMIT-TO (LANGUAGE, “English”)). We extracted the primary studies included in all relevant meta-analyses identified from the database search. In addition, we included a small number of peer-reviewed articles known to scientists consulted through the Sustainable Foods project and which were not retrieved by the search string or from previous meta-analyses. In total, 1590 articles with the potential to be included in the meta-analysis were identified (Fig. 1).Article screeningAll identified articles were screened at full-text level. We used the PICOC (Population, Intervention, Comparator, Outcomes, Context) framework to define the inclusion-exclusion criteria as described in Sánchez et al.19. These criteria required that, to be included: (i) the article presents a quantitative comparison of a diversified farming system (Intervention) compared to either a relatively simplified farming system (first Comparator) or to natural habitat (second Comparator), ii) the article reports quantitative outcomes for any terrestrial organism that is non-domesticated (Population), iii) the article provides the mean or median, variance and sample size for biodiversity outcomes, and outcome measures in comparator and intervention sites were collected using comparable sampling approaches (Outcome), iv) results are from primary field studies and not from experiments conducted in greenhouses or laboratories (Context).Diversified farming systems were defined as agricultural plots where: i) more than one plant species or variety is cultivated at multiple temporal and/or spatial scales, such as crop rotations, intercropping or agroforestry, or ii) semi-natural habitat such as hedgerows and flower strips is embedded into the system, or iii) crop production is integrated with livestock or fish production, such as aquaculture or integrated crop-livestock systems. Simplified farming systems were agricultural plots with less diversity than in eligible interventions, i.e., plots with relatively fewer plant species or varieties (usually monocultures), less semi-natural habitat embedded, or no mixed crop-animal production. Where natural habitat was used as a comparator, this was defined as habitat that is not actively used for human activities, such as primary and secondary forests, wetlands, unmanaged grasslands and shrublands.Suitable outcome metrics for biodiversity included any comparable quantified measure, such as richness, abundance, or Shannon’s diversity index. While studies only needed to report biodiversity outcomes to be considered for inclusion, we recorded harvested yield in all cases where this was reported and met our inclusion criteria. For yield outcomes to be included, the article must have provided means or medians, variance and sample sizes, and outcome measures at intervention and comparator sites must have been collected using comparable sampling approaches. Suitable outcome metrics for yields included the land equivalent ratio, weight of harvested produce per unit land area, or counts of harvested produce per standardized unit (e.g. grape bunch per plant, apples per branch). For comparisons comparing intercropped or agroforestry systems against simplified farming systems, the land equivalent ratio was prioritized as the outcome metric while other metrics were used only when the land equivalent ratio could not be calculated.In total, 237 (14.9%) of retrieved articles met our inclusion criteria (Fig. 1).Data extractionFrom each article that met our inclusion criteria, we extracted qualitative data on: the literature source (e.g. authors, publication year, title); crop type (common name, scientific name); agricultural system (e.g. intercropping, monoculture, agroforestry, integrated crop-livestock system, crop rotation, set aside); non-domesticated taxa sampled (common and scientific names); functional group of the non-domesticated taxa, if specified (e.g. pest, decomposer, predator); biodiversity outcome metric (e.g. species richness, abundance, Shannon’s diversity index); yield metric (e.g. kilogram per hectare, grams per plant, land equivalent ratio); sampling method used (e.g. transect, trap); pesticide use (yes or no, and kg/ha); fertilizer use (yes or no, and chemical fertiliser use yes or no); soil management (e.g. tillage, no tillage, slash and burn); landscape characteristics (e.g. % agricultural land use, climate); and study location (local name, country and geographic coordinates). Following initial data-entry, we classified several variables into categories to facilitate data exploration and analysis. This included categorizing crops by the Food and Agriculture Organisation of the United Nations commodity group, woodiness (e.g. tree, shrub, herb), and growth cycle (perennial, annual), and documenting the phylum, class, order and functional group of each non-domesticated taxon.We extracted quantitative data on: biodiversity outcome means or medians, variance and sample size; yield means or median, variance and sample size; farm size, if specified; length of time that the land has been in its current state, and; sampling duration (in days, from start to finish). Data on biodiversity outcomes and yield were extracted from figures using GetData Graph Digitizer 2.26 or WebPlotDigitizer v4.2. Where outcome values or units in an article were unclear or not provided, the corresponding author was contacted by email to request this information. If the author did not respond, the data entry was removed. We provide a dictionary of how the extracted data were recorded and coded in Dataset 2.Data were organized using R-4.0.0 (R-Core Team, 2013) such that each row contained a pair of biodiversity outcomes and, where provided, a pair of yield outcomes, for a single comparator-intervention pair. In total, 237 studies containing 4076 comparisons of biodiversity outcomes and 1214 comparisons of yield outcomes were retained for analysis (Fig. 1). More

Habitat typesThe sampled stations were classified into 5 habitat types (Fig. 1a,b) as described by Weber et al.35: young plume core (YPC), old plume core (OPC), west plume margin (WPM), east plume margin (EPM) and oceanic seawater (OSW). Each habitat was characterized by a unique combination of sea surface salinity, sea surface temperature, nitrate availability index, mixed layer depth and chlorophyll maximum depth35. Geographically, the different habitats were unevenly distributed along the transect (Fig. 1c), illustrating the dynamic and patchy nature of the ARP. At each station, the temperature and salinity profiles confirmed the stratification of the water column. Maximum Brunt–Väisälä buoyancy frequency was high (3–15 × 10–3 s−1) and close to the surface in the plume core (YPC and OPC), restricting turbulent mixing between the plume waters and the underlying ocean waters. The plume margin stations (WPM and EPM) showed deeper and more muted (1–2 × 10–3 s−1) maximum buoyancy frequency peaks while OSW stations exhibited turbulent mixing from the surface to ~ 100 m (Supplementary Fig. S1). Fluorescence profiles provided guidance to sample within the chlorophyll maximum (Supplementary Fig. S1). In the plume core, the chlorophyll peak was located above the halocline. At plume margin stations, multiple chlorophyll maxima were detected at the halocline or just below, while the oceanic seawater stations did not have haloclines, and chlorophyll peaks were far below the surface (deeper than 50 m). Surface samples from the core plume stations corresponded to high temperature-low salinity waters, with low density. These plume waters mixed with coastal waters at the surface of plume margin stations, but this was not the case at OSW stations (Supplementary Fig. S2).Figure 1Location of the study (A), distribution of sampling stations (B) and identification of the habitat types using a principal component analysis (C) and Ward’s hierarchical cluster analysis (D). The map in B shows the monthly composite surface chlorophyll concentration for May 2018 from satellite observations Reprocessed L4 (ESA-CCI: OCEANCOLOUR_GLO_CHL_L4_REP_OBSERVATIONS_009_093) downloaded from Copernicus Marine Service (https://resources.marine.copernicus.eu). The map was created using the NASA SeaDAS 7.5.3 software with land and exclusive economic zones boundaries (yellow lines) added with gmt v5.4.5 software. Note that all stations from EN614 were used to establish habitat types, but only the 10 stations highlighted in bold and shown on the map were used in this study. SSS, sea surface salinity; SST, sea surface temperature; NAI, nitrogen availability index; MLD, mixed layer depth; ChlMD, chlorophyll maximum depth.Full size imageSmall-sized pigmented eukaryote populations, size, abundance and biomass:Overall, the small pigmented eukaryote communities were composed of a variable combination of 3 to 4 populations per sample, with a total of 6 different populations (named P1, P2, P3, P4, P5 and P6) among all samples, identified by flow cytometry according to cell size range and pigment content (Fig. 2). Based on relative estimates from flow cytometry calibrations using beads of known sizes, most populations belonged to the picoplankton (≤ 2–3 µm). Cells in P1 were approx. 0.8 µm. P2 was a very diverse cluster resulting in a size range from ≤ 0.8 to 5 µm, with a majority of cells clustered around 2 µm, while P3 and P6 were characterized by cells of 0.8–2 µm and P4 by cells of 2–3.5 µm. Cells identified within P5 were larger, ranging from 3.5 to  > 5 µm, therefore encompassing small-sized members of the nanoplankton (3–20 µm). Studies that provide size calibrations for sorted picoeukaryote populations are rare37, making direct comparisons unreliable.Figure 2Example of a cytogram illustrating the gates used for small pigmented eukaryote population counts and sorting. Populations were first discriminated based on their position in the chlorophyll vs forward scatter cytogram (A, all events represented) and then redefined in the chlorophyll vs phycoerythrine (PE) autofluorescence cytogram (B, only events gated in A represented). In the later, we avoided Synechococcus overlapping with small pigmented eukaryote populations in A and cells exhibiting high PE fluorescence among the populations from cytogram B. Note that all 6 populations were never found present in the same sample. In particular, the sample represented here (S003 surface) did not contain P1 or P6, but the gates are represented nonetheless in panel A to provide an illustration for these populations. Note that the gating had to be adjusted between samples but the relative positions stayed similar to those illustrated here. The positions of standard size-calibrated non-fluorescent beads (dashed lines) along the x-axis were used to determine the size range of each gated population in cytogram A. Red ellipses mark the position of yellow-green reference beads of 1 and 2 µm (1-YG and 2-YG, respectively) used to maintain instrument alignment, although the bead clusters are not apparent in the sample since they were run separately (for details see “Methods”).Full size imageThe different small pigmented eukaryote populations had variable cell abundances relative to each other and varied with sampling location (Table 1). Surface communities were either dominated by population P3 (57–74% of small pigmented eukaryote abundance, hereafter counts) in the WPM (S003, S031 cast 03 (henceforth S031_03), and S031 cast 11 (henceforth S031_11)) as well as one station from EPM (S022) and one from OSW (S020), or by P2 (52–66% of counts) at the OPC (S024) and stations of the EPM (S025) and OSW (S027). All stations had lower abundances of P4 (5.7–32% of counts), and only four stations (S003, S020, S022, S031_11) also presented a small P5 population (3.1–6.3% of counts). The small pigmented eukaryote communities collected from chlorophyll maxima were all dominated by P2 (69–94% of counts) and accompanied by much less abundant P3 (5.6–23% of counts), except for station S022 whose chlorophyll maximum small pigmented eukaryote community was dominated by P3 (93% of counts). All chlorophyll maximum communities were characterized by a low contribution of P4 (0.6–6.2% of counts). The small pigmented eukaryote community collected from 40 m at S017 was characterized by the presence of population P6 (16% of counts), absent from the other stations. P1 was only present at the chlorophyll maximum of the OPC station (11% of counts). However, the amount of DNA extracted from P1 was too small to allow for sequencing of the 18S rDNA and it is therefore not part of the subsequent analyses.Table 1 Cell counts per population, as the proportion of the summed total cell density for all 6 gated populations. CM, chlorophyll maximum.Full size tableAt the surface, small pigmented eukaryotes contributed on average 1.3 ± 0.4% of the total small phytoplankton abundance (Supplementary Table S1), indicating that picocyanobacteria dominated all stations. Synechococcus dominated cell abundances at most stations (57–97%), except in the OSW (S020, S027) where Prochlorococcus dominated (92–97%). These results reflect the established paradigm that the eukaryotic component of small phytoplankton communities is less abundant than the prokaryotic component10,16,37. Nonetheless, in terms of biomass, small pigmented eukaryote dominated the small phytoplankton in all surface samples (11–44 × 103 µg C/m3; 47–71%), representing a biomass greater than or equal to the picocyanobacteria (Supplementary Table S2). The horizontal shift in surface nutrient concentrations among habitats was too modest to affect the relative contribution of small pigmented eukaryote to total small phytoplankton abundances, contrary to reports for much larger spatial scales involving greater differences in nutrient concentrations, ranging from coastal systems to the open ocean10,16. Small photosynthetic eukaryote abundance and biomass were not significantly correlated to nutrient concentrations, salinity or temperature (Spearman rho  0.05).At the chlorophyll maxima and in deeper waters, despite a consistent predominance of Prochlorococcus, small pigmented eukaryotes generally contributed more to the total small phytoplankton abundance than at the surface, similar to previous reports from the Indian Ocean7 and the south Pacific Ocean8,9. These samples showed decreased absolute abundances of ≤ 5 µm phytoplankton (Supplementary Table S1), with the plume core stations (S017, S024) exhibiting the lowest overall absolute abundances (8.2–32 × 103 cells/mL). This decrease in absolute numbers of the picocyanobacteria, concomitant with increased small pigmented eukaryote relative abundances (6–18%), indicated that eukaryotes fared better than the picocyanobacteria in the low light conditions of waters shaded by the plume. Dominance of the small phytoplankton biomass by small eukaryotes (5.9–50 µg C/m3; 53–95% of the total biomass), representing more than twice the picocyanobacterial biomass at the chlorophyll maxima and deeper water, is reminiscent of reports that small pigmented eukaryotes can contribute significantly to primary production in coastal regions12. Although this contrasts with findings from open oceans where Prochlorococcus dominates small phytoplankton biomass11,37, small pigmented eukaryotes were found to be similarly biomass-dominant and contributing up to a third of total primary production in surface seawater of the western subtropical North Atlantic under phosphorus depletion13.Taxonomic composition of small pigmented eukaryote populationsHigh-throughput sequencing of the small ribosomal subunit gene provided insights into the taxonomic composition of resident (live, inactive and recently dead) small pigmented eukaryote populations. A total of 234 operational taxonomic units (OTUs) were obtained, covering the full diversity of the populations in each sample (Supplementary Fig. S3) and after removal of metazoan OTUs and OTUs  1,000 OTUs38,39,40,41,42, the low OTU richness is a reminder that our cell sorting protocol allowed the focused targeting of small pigmented eukaryote populations. The low OTU counts (3–42) for each population (Table 2) further reflect the accuracy of the sorting method and the near taxonomic purity of some of the sorted populations.Table 2 Operational taxonomic units (OTUs) counts per population. CM, chlorophyll maximum.Full size tableMajor OTUs, constituting at least 20% of the total reads per population for at least one sample, represented 29 out of the 201 OTUs (Fig. 3; Supplementary Table S1). The most frequent OTU was a Chloropicophyceae (Chlorophyta), averaging 19.55% of total reads/sample. The second most frequent Chlorophyta OTU belonged to prasinophyte clade IX with an average of 4.36% of the total reads/sample. The Ochrophyta were represented by two Marine Ochrophyta clade 5 (MOCH-5) OTUs and five Bacillariophyceae OTUs ranging on average from 5.5 to 2.1%, and 5.3 to 1.6% of total reads per sample, respectively. Only one major OTU was associated with the prymnesiophytes, classified within the order Isochrysidales, representing 1.3% of the total reads/sample (Fig. 3). The rest of the major OTUs had lower average abundances throughout the samples ( 8 µm cells from our sorted populations. Furthermore, the consistently low abundance or absence of P5 throughout our samples suggests that this Isochrysidales OTU5 (Noelaerhabdaceae) did not dominate the small pigmented eukaryote communities of the ARP in the spring.Distinguishing the small pigmented eukaryote community composition between habitat typesA UniFrac unweighted paired group method with arithmetic mean analysis revealed stronger clustering among populations than among stations or depths, suggesting a consistency in the phylogenetic composition of the sorted populations (Supplementary Fig. S4). The only exceptions were S031_03 chlorophyll maximum and S031_11 surface samples for which the three populations clustered distinctly from the rest. A canonical correspondence analysis based on assemblages of major OTUs separated populations P2 and P4 of the OPC surface and subsurface and all four populations of S031_11 surface from the rest of the samples (Fig. 6a). The low abundance OTU composition of the surface and subsurface OPC populations and the deep YPC sample were distinct from the rest of the samples, the latter being strongly driven by salinity (Fig. 6b). The environmental variables used in the canonical correspondence analysis explain a sizable portion of the variability (33–50%), although it seems that an important driver of community composition was unaccounted for.Figure 6Canonical correspondence analysis with A major OTUs, and B low abundance OTUs.Full size imageThe YPC populations had low OTU richness (Table 2), and most of their major OTUs were shared with other stations, namely the Chloropicophyceae OTU192 and OTU165, detected in all 4 populations (16–86% of total reads/population). Notably, this sample was only distinguished from the rest by its low abundance OTU composition (Fig. 6b). Of the 15 low-abundance OTUs among the 4 populations detected, a few were shared with other samples, but only one or two at a time (Supplementary Table S3). The OPC surface was also characterized by a low OTU richness (Table 2), each population dominated by one or two major OTUs (Fig. 5). P2 was dominated by Bacillariophyta Nitzschia (OTU86), also found at other stations in lower abundance, and by a Syndiniales GrpI OTU108 unique to this station. P3 was composed of the ubiquitous Chloropicophyceae OTU192, classified as Chloropicon, and two MOCH-5 OTUs, which were also found in P4. The chlorophyll maximum sample was composed of a very similar small pigmented eukaryote community, albeit with a larger proportion of low abundance OTUs in P2. Interestingly, P3 at both surface and chlorophyll maximum was distinguished from other samples by the low abundance OTUs that accompanied the dominant Chloropicophyceae OTUs (Fig. 6b). The small pigmented eukaryote community of the sample below the chlorophyll maximum was characterized by an abundant P3 dominated by Chloropicon OTU192, accompanied by the Pelagophyceae Pelagomonas OTU232, which was also detected at S025 (EPM) and S027 (OSW). This sample collected below the halocline was distinct from the upper water column and more similar to the margin and oceanic samples. Such a pattern is consistent with the plume overriding the surrounding margin or oceanic waters and submerging the endemic communities that were there previously at the surface.In contrast to our first hypothesis regarding small pigmented eukaryote variability across the horizontal gradients of the ARP, the composition of small pigmented eukaryote communities was stable among the different habitat types. This is attributable to a combination of variability in OTU composition among samples from the same habitats and similarity of the small pigmented eukaryote assemblages between stations of different habitats. Indeed, the populations exhibited no significant differences between average UniFrac distances among habitats, stations of the same habitats and depths of the same stations (ANOVA, p  > 0.164 for P2, p  > 0.251 for P3 and p  > 0.735 for P4). The lack of statistical differences, particularly among the plume margins and oceanic waters, are indicative of the dynamic nature of large river plumes, such as reported for the Columbia River67. The meandering of the ARP creates a very dynamic system with a variable influence on local oligotrophic ocean waters68,69. It is possible that each station is too unique to establish a consensus small pigmented eukaryote community structure per habitat type, while abundant populations are shared between stations of different habitats limiting the detectable distinctions between the assemblages. For instance, the dominant Nitzschia OTU86 was shared between the OPC, one of the WPM stations and one of the EPM stations. Similarly, Chloropicon OTU192 dominated P3 at all stations, except in the surface waters of one WPM station (S031_11) and one OSW station (S027). Furthermore, our use of DNA as template for the taxonomic survey might have masked changes in the active communities among different habitats that would have been more apparent with RNA templates.The progressive mixing of oceanic waters into the plume is likely to exchange small pigmented eukaryote communities between the adjacent environments. This hydrodynamic phenomenon would allow the unrestrained dispersal of small pigmented eukaryotes between habitats, resulting in the observed similarities between the plume and surrounding ocean surface waters. In the dynamic environment of the ARP margins, the similarity between communities of different habitats is a function of time since the onset of the mixing event that exposed oceanic and plume small pigmented eukaryote communities to adjacent environments. Time-since-mixing might be the environmental parameter unaccounted for in our dataset that would explain the intra-habitat variability in major OTU composition, incidentally, obscuring the differences between habitats.Contrary to picocyanobacteria, which mostly use recycled, reduced forms of nitrogen (ammonium and urea), small pigmented eukaryotes rely more on nitrate70,71, making them more sensitive to the low nitrate concentrations in and around the ARP. While the uniformity of small pigmented eukaryote biomass between the oligotrophic ocean waters and the plume margins is likely the product of low nutrient concentrations in both environments, the variability of the OTU composition might be explained by a variable nitrate metabolism among small pigmented eukaryote taxa70. Alternatively, mixotrophy, the combination of photosynthesis and bacterivory common among small pigmented eukaryotes13,72,73,74, might confer a generalist advantage relative to picocyanobacteria by allowing maintenance of activity and abundance in rapidly varying habitats.Corroborating our second hypothesis that the small pigmented eukaryote diversity should vary with depth within the euphotic layer, the small pigmented eukaryote diversity and abundance varied vertically, with higher cell counts at the chlorophyll maximum. The taxonomic composition of chlorophyll maximum communities differed from those at the surface with populations characterized by high abundances of OTUs associated with Bacillariophecae, Pelagophyceae, radiolarians or Dinophyceae. The presence of Dinophyceae or Pelagophyceae OTUs at the chlorophyll maxima of plume stations (OPC, WPM and EPM), which were absent from surface waters, reflects the strong stratification at plume-influenced stations, reducing mixing between the surface and the bottom of the euphotic zone, the latter of which can be strongly influenced by oceanic waters. In particular at these stations (S024, S031 and S022), the chlorophyll maximum samples were collected below the halocline depth. Hence, these Dinophyceae and Pelagophyceae OTUs, uniquely shared with one of the oceanic stations, suggest that water masses under the plume-influenced surface might correspond to the oceanic water masses at the OSW stations.Station S031, a time-series station, showed a variation in major OTU assemblages between the cast conducted at 3 pm on May 26th (S031_03) and another cast carried out at 11am on May 27th (S031_11). Within this 19-h interval, in which environmental conditions remained consistent with the habitat type (Fig. 1), the OTU composition underwent a shift (Figs. 5, 6a). The relative cell abundances of each population remained similar, except for a P5 population appearing in samples from the second time point (Fig. 5). At the surface, the shift was characterized by the replacement of all OTUs from S031_03 with major OTUs assigned to Syndiniales in S031_11. The only common OTU, MAST-3A (OTU115), had low abundances (0.4–3.7%) in S031_03 and reached 14–24% in the S031_11 populations (Supplementary Table S3). Interestingly, the major Syndiniales OTUs in S031_11 were unique to this station, and different from the Syndiniales OTUs detected in the OPC and EPM stations (Fig. 5). This unexpected abundance in unpigmented Syndiniales OTUs in S031_11 might be due to the presence of dinospores in transitory free-living form, attached to or inside alveolate hosts or predators75,76. The large proportion of low abundance OTUs, which represented 70% of total reads in P3, were related to Syndiniales, ciliates and dinoflagellates (Supplementary Material SM2).Changes were also observed at the chlorophyll maximum where the unique radiolarian Collophidium OTU that dominated S031_03 disappeared in S031_11. This abundance of sequences related to the Radiolaria, large heterotrophic protozoa (≥ 100 µm), was unexpected among our targeted populations sorted by size and chlorophyll content. However, radiolarian sequences have been found among small size fractions before77,78, particularly at depth79,80 where they are suspected to descend and release small flagellate gametes called swarmers81. Hence, if attached to exopolymer-producing pigmented cells such as in the late stages of a phytoplankton bloom82, these swarmers could have been indiscriminately sorted into the three populations. In addition, three dinoflagellate OTUs appeared in P2 and P4 in cast S031_11, of which one was only found in the deep YPC, and one was shared with the chlorophyll maximum of S022 (EPM) and the surface of S027 (OSW).The radical shift in small pigmented eukaryote community composition between the two casts from station S031 reflects the dynamic nature of the ARP ecosystem and the multiple scales of heterogeneity within this system that is unlikely to be uncovered without the multiple approaches used in this study. It is unlikely that this interval of 19 h was sufficient for the resident small pigmented eukaryote community to change so radically as to completely replace the original taxa, as taxonomic turnover on daily time scales is usually very limited83,84. The salinity profiles indicated a stronger stratification at the time of cast 11, with a deeper mixing depth (22 m) compared to cast 03 (16 m), reflected in the chlorophyll profiles showing more homogenous concentrations in the top 22 m of cast 11 (Supplementary Fig. S1). In addition, the chlorophyll maximum peak sampled at 27 m was much smaller in cast 11 compared to cast 03, with a stronger secondary peak at 39 m. Satellite observations show the river plume defined as high surface chlorophyll, spreading north and eastward between the 25th and 29th of May (Supplementary Fig. S9—higher chlorophyll concentrations north of 17°N), suggesting a plume that was advecting past the ship during this time. This likely caused the deepening of the mixing depth, forcing the surface small pigmented eukaryote community northwards and the chlorophyll maximum community deeper below the mixing depth, effectively displacing the communities identified during cast 03.As a first study of the small pigmented eukaryotes and their response to the environmental habitats of the ARP, this work provides new insights into the detailed 18S rDNA-based taxonomy of an underexplored fraction of the phytoplankton. Our results illustrate that FACS is a reliable tool to enrich targeted taxonomic groups, such as Bacillariophyta, Chlorophyta and MOCH-5. The small pigmented eukaryote taxonomic composition was influenced by the ARP only at the plume core (OPC) where surface assemblages showed a strong dissimilarity with other stations, which were otherwise similar despite belonging to different habitat types. This result stands in apparent contrast to the drastic succession in community composition of the microphytoplankton driven by the nutrient gradients in the ARP1,3,4,6. The surprisingly limited influence of the ARP on surface small pigmented eukaryote communities warrants further inquiry. Sampling at different times of the year and using 18S rRNA as template for sequencing might reveal small pigmented eukaryotes to be more reactive to the habitat types earlier in the season, at the beginning of the massive discharge period from the Amazon River, or at the end of the summer when the ARP is entrained toward the east by the north equatorial countercurrent. More

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