Macroecological patterns of planktonic unicellular eukaryotes richness in the Southeast Pacific Ocean

Abstract

In recent years, studies focusing on microbial biogeography have been developed, but macroecological processes in marine microorganisms remain unclear, especially in seemingly continuous environments such as the Southeast Pacific Ocean (SPO), where information on microbial distribution patterns is limited, and they may vary depending on the habitat and lifestyle. We used unicellular planktonic eukaryotes as model organisms to determine their biogeographic patterns in the SPO, identify the underlying ecological and historical-evolutionary processes and compare with other microorganism groups. Our analyses were based on the Niche Theory to model species diversity distribution using large open-access ecological and physical-biogeochemical databases based on Bayesian approaches, an integrated nested Laplace approximation (INLA), and Generalized Additive Models (GAM). As a result, two richness hotspots were observed, which are associated with coastal and offshore regions in the central southern areas of SPO. The richness hotspots were associated mainly with nutrients (N/Si ratio) and Mixed Layer Depth (MLD), which could be explained by highly productive upwelling events in the SPO. In contrast, the negative correlation of predicted richness with low pH is strongly related to the effect of calcareous shells (tests), as lower pH levels hinder the formation and stability of calcium carbonate shells in protists like foraminifera and radiolaria, thereby affecting overall unicellular planktonic eukaryote diversity. Our results support the role of ecological processes related to productivity, energy dynamics, and ecological limits in shaping broad-scale diversity patterns of unicellular planktonic eukaryotes in the SPO. The results show colonization and extinction dynamics through species replacement (i.e. High Turnover) along the Chilean and Equatorial coasts associated mainly with the Hotspots of their biodiversity, but also a gradual species loss (i.e. High Nestedness) along the Peruvian Coast associated mainly with the Coldspots of their biodiversity; highlighting how local environmental fluctuations can shape these planktonic microorganisms' behavior, ecology and distribution. The distribution patterns of planktonic unicellular eukaryotes show little evidence of the effects of historical and evolutionary processes. This is because the high dispersal capacity of planktonic microbes probably dilutes the influence of these processes in environments lacking clear barriers to species dispersal. Additionally, the effect of historical events could be highlighted in specific taxonomic groups at the kingdom, phylum level or habitat type and addressing gaps about latitudinal richness in the SPO. This provides insight into the spatial distribution of marine microbes and contributes to conservation efforts, as these organisms are an essential foundation of the upper levels of the food web.

Keywords: Biogeographic patterns; Humboldt Current System; Latitudinal gradient; Planktonic microorganisms; Protists; Species diversity distribution.

Fig. 1

A map of the study area with the Humboldt Large Marine Ecosystem is shown as a hatched fill area.

Fig. 2

Taxonomic composition of phyla of planktonic unicellular eukaryotes of Southeast Pacific Ocean.

Fig. 3

Percentage contribution of species or genera of planktonic unicellular eukaryotes from the Southeast Pacific Ocean.

Fig. 4

Examples of widely distributed planktonic unicellular eukaryotes in the Southeast Pacific Ocean. Phylum Foraminifera: (a) Neogloboquadrina dutertrei, (b) Neogloboquadrina incompta, (c) Orbulina universa and (d). Phylum Radiozoa: Carposphaera sp. *The white bar indicates a size scale of 1 mm.

Fig. 5

Survey of planktonic unicellular eukaryotes richness of the Southeast Pacific Ocean. (a). Observed Richness, and (b) Getis-ord analysis.

Fig. 6

Spatial patterns of Beta diversity of the planktonic unicellular eukaryote’s richness in the Southeast Pacific Ocean. Where: (a) Turnover, showing spatial variation in species replacement across latitudinal gradients; and (b) Nestedness, highlighting the contribution of species loss to patterns of richness.

Fig. 7

Survey of unicellular eukaryote richness and environmental variables used as predictors in Species Distribution Models (SDMs) along latitudinal gradients in the coastal region of the Southeast Pacific Ocean. (a). Observed vs. Predicted Richness, (b). Mixed Layer Depth (MLD), (c) pH, and (d) N/Si Ratio and Upwelling Index (m²/s).

Fig. 8

Maps showing (a) the mean posterior distribution of the spatial random effect of the INLA model, (b) the mean posterior predictive probability of planktonic unicellular eukaryotes richness of coastal regions in the Southeast Pacific Ocean, and (c) the Pearson correlation between the observed species richness and the model predicted species richness.

Fig. 9

Taxonomic distinctiveness obtained for planktonic unicellular eukaryotes of the Southeast Pacific Ocean. The dotted lines indicate the upper and lower limits of the null model.