The vertical distribution of phytoplankton in stratified water columns

Abstract

What determines the vertical distribution of phytoplankton in different aquatic environments remains an open question. To address this question, we develop a model to explore how phytoplankton respond through growth and movement to opposing resource gradients and different mixing conditions. We assume stratification creates a well-mixed surface layer on top of a poorly mixed deep layer and nutrients are supplied from multiple depth-dependent sources. Intraspecific competition leads to a unique strategic equilibrium for phytoplankton, which allows us to classify the distinct vertical distributions that can exist. Biomass can occur as a benthic layer (BL), a deep chlorophyll maximum (DCM), or in the mixed layer (ML), or as a combination of BL+ML or DCM+ML. The ML biomass can be limited by nutrients, light, or both. We predict how the vertical distribution, relative resource limitation, and biomass of phytoplankton will change across environmental gradients. We parameterized our model to represent potentially light and phosphorus limited freshwater lakes, but the model is applicable to a broad range of vertically stratified systems. Increasing nutrient input from the sediments or to the mixed layer increases light limitation, shifts phytoplankton towards the surface, and increases total biomass. Increasing background light attenuation increases light limitation, shifts the phytoplankton towards the surface, and generally decreases total biomass. Increasing mixed layer depth increases, decreases, or has no effect on light limitation and total biomass. Our model is able to replicate the diverse vertical distributions observed in nature and explain what underlying mechanisms drive these distributions.

Introduction

The aquatic environment of phytoplankton creates an opportune situation to study the feedbacks between resource gradients, behavioral movement, population dynamics, and passive dispersal. The major axis of spatial heterogeneity for phytoplankton is the vertical dimension. The vertical distribution of phytoplankton affects primary production as well as energy transfer to higher trophic levels (Leibold, 1990, Williamson et al., 1996, Lampert et al., 2003). Therefore, there is an immediate need to understand the fundamental principles that govern the vertical distribution of phytoplankton, ecologically important organisms that contribute roughly half of global net primary productivity (NPP) (Field et al., 1998) and continue to be affected by climate change (Hays et al., 2005).

A dizzying diversity of phytoplankton vertical distributions have been observed (see Fig. 1 for a few examples). Physical stratification breaks the water column into distinct strata resulting in non-uniform mixing, often with a well-mixed surface layer on top of a poorly mixed deep layer (Wetzel, 1975, Wüest et al., 2000). Phytoplankton may be found in high abundance in the mixed layer, in the deep layer, directly on the bottom, or in some combination of these layers. What determines their vertical distribution in stratified water columns? Light is in greatest supply at the top of the mixed layer and phytoplankton are hypothesized to exist there when there is adequate nutrient supply (Reynolds, 1984, Paerl, 1988). Frequently, phytoplankton form a peak in abundance known as a deep chlorophyll maximum, or DCM, in the deep layer. Low turbulence and sufficient light penetration have been hypothesized as necessary for a DCM to persist (Fee, 1976) and the light and nutrient gradients control the depth of the peak (Fee, 1976, Klausmeier and Litchman, 2001). Under low nutrient concentrations and if sufficient light penetrates to the bottom, algae may form a benthic layer on the sediments and access nutrients diffusing through the sediment pore water before it enters the water column (Sand-Jensen and Borum, 1991).

In a well-mixed water column, phytoplankton and nutrients are homogenized throughout the water column; however, a light gradient is inevitable. As a consequence, phytoplankton experience varying local light levels and therefore varying growth rates. The light level at the bottom of the water column, I_out, predicts the outcome of competition for light (Huisman and Weissing, 1994, Huisman and Weissing, 1995) in a way similar to R⁎ for nutrients (Tilman, 1982). In contrast, in a poorly mixed water column, motile phytoplankton can be thought of as playing a competitive game in opposing essential resource gradients. A shallower position allows a cell to shade those below it but a deeper position allows it to intercept nutrients mixing up from below. Eventually, through movement and/or growth, phytoplankton will aggregate at their evolutionarily stable strategy (ESS) depth z*, which is the depth of equal limitation by nutrients and light and prevents growth elsewhere in the water column (Klausmeier and Litchman, 2001). These studies are applicable to the two extremes of whole water columns, one of well-mixed and one of poorly mixed.

Many bodies of water stratify. Several models have considered stratified water columns, ranging from complex simulation models particular to specific ecosystems (Lucas et al., 1998, Fennel and Boss, 2003, Peeters et al., 2007, Ross and Sharples, 2007) to simpler models aimed at general understanding. Condie and Bormans (1997) and Hodges and Rudnick (2004) included sinking but neglect the feedback of phytoplankton on light. Huisman and Sommeijer, 2002b, Huisman and Sommeijer, 2002a incorporate the feedback of phytoplankton on light, but omit nutrients and assume no mixing in the hypolimnion. Yoshiyama and Nakajima (2002), Yoshiyama et al. (2009), and Ryabov et al. (2010) do not include nutrient loading to the mixed layer. Our study systematically explores the different vertical distributions of phytoplankton that can arise from intraspecific competition for nutrients and light in a stratified water column.

In this paper, we build on previous work by considering a stratified water column with a well-mixed surface layer on top of a poorly mixed deep layer, a combination of approaches by Huisman and Weissing, 1994, Huisman and Weissing, 1995 and Klausmeier and Litchman (2001). We relax the assumption of an infinitely thin layer (Klausmeier and Litchman, 2001) to a mixed layer of finite depth and show what resources limit growth at different depths within the layer. Furthermore, we consider multiple nutrient inputs, including input directly to the mixed layer, expanding on Diehl (2002). Current models for poorly mixed water columns consider only nutrient supply from below (Klausmeier and Litchman, 2001, Huisman et al., 2006, Beckmann and Hense, 2007). We enumerate the possible equilibrium algal vertical strategies and show under what conditions each should occur.