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Fig. 1 Global patterns of monthly phytoplankton species richness and species turnover.

Global pattern of phytoplankton diversity driven by temperature and environmental variability

Abstract - Despite their importance to ocean productivity, global patterns of marine phytoplankton diversity remain poorly characterized. Although temperature is considered a key driver of general marine biodiversity, its specific role in phytoplankton diversity has remained unclear.

Abstract (continued) - We determined monthly phytoplankton species richness by using niche modeling and >540,000 global phytoplankton observations to predict biogeographic patterns of 536 phytoplankton species. Consistent with metabolic theory, phytoplankton richness in the tropics is about three times that in higher latitudes, with temperature being the most important driver. However, below 19°C, richness is lower than expected, with ~8°– 14°C waters (~35° to 60° latitude) showing the greatest divergence from theoretical predictions. Regions of reduced richness are characterized by maximal species turnover and environmental variability, suggesting that the latter reduces species richness directly, or through enhancing competitive exclusion. The nonmonotonic relationship between phytoplankton richness and temperature suggests unanticipated complexity in responses of marine biodiversity to ocean warming.

INTRODUCTION

Marine phytoplankton dominate primary production across ~70% of Earth’s surface (1), play a pivotal role in channeling energy and matter up the food chain, and control ocean carbon sequestration (2). The diversity of phytoplankton species in open waters has intrigued ecologists for at least half a century (3), but the global pattern of this diversity and its underlying drivers have been unclear (4, 5). This is a critical gap in our understanding of the oceans since the richness of phytoplankton species, a key element of their diversity, may enhance resource use efficiency (6), and thus primary production, as often seen in terrestrial systems (7). For those oceanic taxa that have been investigated, including foraminifera, fish, and invertebrates, species richness tends to peak at low to mid-latitudes and to decline sharply toward the poles (811). This decline is consistent with the metabolic theory of ecology (12, 13); i.e., the hypothesis that temperature exerts a key control on metabolic rates and thus promotes speciation and increased species richness in warm tropical areas through time (14). However, a recent large-scale study on marine phytoplankton richness is at odds with the prediction by metabolic theory (4), and latitudinal richness gradients identified for individual phytoplankton groups have taken various shapes (5, 1517). Observed discrepancies may originate from other factors such as resource competition (17, 18), differences in body size (15, 19), or undersampling of richness (20). Empirical tests of the competing theories explaining global diversity patterns have so far been impeded by the paucity of in situ observations and the lack of systematic sampling schemes for open-ocean phytoplankton (21).

Here, we overcome these limitations and provide the first analysis of marine phytoplankton species richness and its ecological drivers at the global scale, using 1,056,363 presence observations of 1300 species compiled from multiple sources as the basis for our analysis. These data span all major taxa, ocean basins, latitudes, and most seasons (fig. S1). To address the strong spatial and seasonal bias in sampling effort, we analyze the subset of data of species with at least 24 presences (553 species and 699,387 observations) using species distribution models (SDMs), which have been set up specifically to account for uneven sampling and fit each species’ ecological niche as a function of multiple environmental predictors. Our statistical approach thus aims at filtering out spurious patterns in the raw data while integrating all observational evidence. We successfully build probabilistic SDMs (fig. S2) for 536 species using generalized additive models (GAM) and use generalized linear models (GLM) and random forest models (RF) to assess the robustness of our findings. We project the species’ niches to the global ocean at a 1° resolution and at monthly scales and diagnose richness from the overlap of species’ presence-absence projections. Since the diversity of short-lived phytoplankton may change over the course of each year, we project species richness for each month and map its annual mean state, as well as monthly species turnover (see Materials and Methods).

RESULTS AND DISCUSSION

Our diagnosed annual mean of monthly phytoplankton richness varies strongly with latitude, while longitudinal differences are comparably small (Fig. 1A). Phytoplankton richness is highest and least variable throughout the year in the inner tropics (<5°N and S; Fig. 3A), reaching more than 240 species on average. Richness hotspots, where roughly half of the total species analyzed occur simultaneously, are found in the central Indian, the equatorial and west Pacific, and the Indo-Australian Archipelago (Fig. 1A). Thus, hotspots of phytoplankton richness tend to be more tropical than those of foraminifera and other oceanic taxa (8, 9). Analyzed by latitude, richness declines steeply poleward of 30° (Fig. 1C), reaches its minima (~50 species) and associated inflexion points at mid-latitudes (~45° to 65°N and ~45°S), and increases slightly toward the poles. This latitudinal pattern is composed of species with notable wide thermal ranges (15.8° ± 6.8°C, mean ± SD; Fig. 2B) and broad geographic distributions (Fig. 2C), with more than 60% of high-latitude species (>70°N and S) recorded close to the equator as well (table S1). The latitudinal ranges of most species (n > 400) tend to be aggregated between 30°N and 30°S, with relatively few specialist species populating the extratropics (Fig. 2C).

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