microorganisms
Article
Grazing Induced Shifts in Phytoplankton Cell Size Explain the
Community Response to Nutrient Supply
Evangelia Charalampous *
,†
, Birte Matthiessen and Ulrich Sommer
Citation: Charalampous, E.;
Matthiessen, B.; Sommer, U. Grazing
Induced Shifts in Phytoplankton Cell
Size Explain the Community
Response to Nutrient Supply.
Microorganisms 2021, 9, 2440. https://
doi.org/10.3390/microorganisms9122440
Academic Editors: Silvia Pulina and
Cecilia Teodora Satta
Received: 26 October 2021
Accepted: 22 November 2021
Published: 26 November 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
GEOMAR, Helmholz Center for Ocean Research, 24148 Kiel, Germany; bmatthiessen@geomar.de (B.M.);
usommer@geomar.de (U.S.)
* Correspondence: evangelia.charalampous@lnu.se
† Current address: Centre for Ecology and Evolution in Microbial Model Systems (EEMiS), Linnaeus University,
39231 Kalmar, Sweden.
Abstract: Phytoplankton cell size is important for a multitude of functional traits such as growth
rates, storage capabilities, and resistance to grazing. Because these response traits are correlated,
selective effects on mean community cell size of one environmental factor should impact the ability
of phytoplankton to cope with other factors. Here, we experimentally apply expectations on the
functional importance of phytoplankton cell size to the community level. We used a natural marine
plankton community, and first altered the community’s cell size structure by exposing it to six
different grazer densities. The size-shifted communities were then treated with a saturated nutrient
pulse to test how the changes in community size structure influenced the mean community growth
rate in the short-term (day 1–3) and nutrient storage capacity in the postbloom phase. Copepod
grazing reduced the medium-sized phytoplankton and increased the share of the smallest (<10 μm
3
)
and the largest (>100,000 μm
3
). Communities composed of on average small cells grew faster in
response to the nutrient pulse, and thus confirmed the previously suggested growth advantage
of small cells for the community level. In contrast, larger phytoplankton showed better storage
capabilities, reflected in a slower post-bloom decline of communities that were on average composed
of larger cells. Our findings underline that the easily measurable mean cell size of a taxonomically
complex phytoplankton community can be used as an indicator trait to predict phytoplankton
responses to sequential environmental changes.
Keywords: phytoplankton; cell size; copepod grazing; nutrients
1. Introduction
Phytoplankton community structure is currently changing due to anthropogenic
global change with consequences for the structure and functioning of the associated pelagic
food webs [1–4]. Trait-based approaches are believed to be a key tool to understand
the causes and consequences of phytoplankton change. While they simplify the vast
taxonomic complexity, trait-based approaches also provide a way to explain phytoplankton
community property changes because phytoplankton traits are functionally relevant. As a
way of complexity reduction Litchman and Klausmeier [5] proposed the identification of a
few “master” traits based on correlations among traits. Among these, cell size is a strong
candidate that can be easily measured. Linear measures of cell size in phytoplankton spans
four to five orders of magnitude; cell diameters range from less than a micrometer up to
several millimeters [6]. Size affects several other traits that are either related to nutrients
and growth, or to loss factors [5,7]. Across studies, cell size correlates negatively with
growth rate [6,8–12] and the ability to take up nutrients at low concentrations [13,14]. It
correlates positively with the abilities to rapidly take-up replete nutrients provided in a
pulsed way, and to store nutrients [12,13,15,16], which means that slower growing larger
cells can preserve the gained biomass for longer compared to smaller cells. In particular,
the relationship between cell size and growth-related traits was extensively examined
Microorganisms 2021, 9, 2440. https://doi.org/10.3390/microorganisms9122440 https://www.mdpi.com/journal/microorganisms