Carbon flows in natural plankton communities in the Anthropocene Anna de Kluijver

156 Pages·2012·2.39 MB·English

Carbon flows in natural plankton
communities in the Anthropocene
Anna de Kluijver
“Science is an imaginative adventure of the mind seeking truth in a world of mystery.”
Sir Cyril Herman Hinshelwood (1897-1967) English chemist. Nobel prize 1956.
Promotoren
Prof dr. J. J. Middelburg, Utrecht University, The Netherlands
Prof. dr. K. Soetaert, Royal Netherlands Institute for Sea Research, The Netherlands, and
Ghent University, Belgium
Thesis committee
Prof. dr. E. van Donk, Netherlands Institute of Ecology and Utrecht University, The Nether-
lands
Prof. dr. S. Schouten, Royal Netherlands Institute for Sea Research and Utrecht University,
The Netherlands
Prof. dr. J.A. Downing, Iowa State University, USA
Prof. dr. Z. Liu, Nanjing Institute of Geography and Limnology, China
Prof. dr. J.-P. Gattuso, Laboratoire d’Océanographie de Villefranche, France
ISBN: 978-90-3935-846-7
The research presented in this thesis has been primarily conducted in the department of
Ecosystem Studies of Royal Netherlands Institute for Sea Research in Yerseke (formerly
Center for Estuarine Marine Ecology, part of NIOO-KNAW) and was partly funded by
the Darwin center for Biogeosciences. Additional financial support was received from the
European Project on Ocean Acidification, Schure-Beijerinck-Popping fund and MesoAqua.
Cover and thesis design: HDK architecten bna bni bnsp, the Netherlands
Cover photographs courtesy of R. Wagner, Germany (cladoceran with green algae),
R. Hopcroft, USA (copepod).
Copyright © Anna de Kluijver, december 2012.
All rights reserved.
Carbon flows in natural plankton
communities in the Anthropocene
Koolstofstromen in natuurlijke plankton gemeenschappen in het
Anthropoceen
(met een samenvatting in het Nederlands)
Proefschrift
ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector
magnificus, prof.dr. G.J. van der Zwaan, ingevolge het besluit van het college voor promo-
ties in het openbaar te verdedigen op vrijdag 7 december 2012 des middags te 2.30 uur
door
Anna de Kluijver
geboren op 21 juli 1982 te Spijkenisse
Promotoren: Prof.dr J.J. Middelburg
Prof. dr. K. Soetaert
Contents
Chapter 1 2
General introduction
Chapter 2 16
Phytoplankton-bacteria coupling under elevated CO
2
levels: a stable isotope labeling study
Chapter 3 38
A 13C labeling study of carbon fluxes in Arctic plankton
communities under elevated CO levels
2
Chapter 4 64
Carbon isotope constraints on lake food-web interacti-
ons along a trophic gradient
Chapter 5 88
Cyanobacteria as a carbon source for zooplankton in
eutrophic Lake Taihu, China, measured by 13C labeling
and fatty acid biomarkers
Chapter 6 106
Macrophyte carbon subsidies to bacterioplankton and
zooplankton in a restored part of a shallow, eutrophic
lake in China
Chapter 7 120
References
Summary
Nederlandse Samenvatting
Publication list
Dankwoord - Acknowledgements
Photo: young volvox by Wim van Egmond
R
E
T
P
A
H
C
1
General Introduction
GENERAL INTRODUCTION
1.1 The Anthropocene
Human activities have a global impact on organisms and biogeochemical proces-
ses, causing changes in ecosystem functioning, biodiversity, and biogeochemical cycles.
Overexploitation of resources, loss and alterations of habitats, environmental pollution and
fossil-fuel burning, are examples of human activities, which have a severe impact on ecosy-
stems. The period and current times where humans alter the planet is called the recent age
of man or the “Anthropocene”.
Carbon cycle
One of the largest impacts of humans since the industrial revolution is alteration
of the global carbon (C) cycle. Carbon dioxide (CO) release, primarily due to burning of
2
fossil fuels, has increased atmospheric pCO with 30% to levels of ~390 ppmv compared
2
to ~280 ppmv in pre-industrial times (IPCC 2007). Changes in land use, like deforestation,
release CO and reduce the earth’s capacity for CO uptake. There is strong evidence that
2 2
the CO rise together with an increase in other greenhouse gases caused global warming of
2
~0.6°C since 1861 (IPCC 2007). Temperature is such an important driver in biotic (pro-
duction, metabolism) and abiotic (hydrology, ice melting) processes, that global warming
became a primary focus in research and environmental policy.
The oceans act as a strong sink for CO and have absorbed approximately one
2
third of the anthropogenic CO (Sabine et al. 2004). CO is soluble in (sea)water (CO[aq])
2 2 2
and reacts with water molecules to carbonic acid (HCO ), which dissociates to bicarbonate
2 3
(HCO -), and carbonate ions (CO-), while releasing protons (H+). The sum of CO species
3 3 2
are collectively referred to as dissolved inorganic carbon (DIC) and is dominated by bicar-
bonate (>90 %) at normal seawater pH. The increase in ocean surface CO[aq] increases
2
DIC and HCO - concentrations, but lowers CO2- concentrations and sea water pH, and
3 3
the latter lead to the name ocean acidification (Fig. 1.1). The average pH of the ocean has
already decreased by about 0.1 units compared to pre-industrial levels from 8.2 to 8.1 and a
further decrease of about 0.3-0.4 units is predicted for the year 2100, when CO emissions
2
continue at present rates (Caldeira and Wickett 2003) (Fig. 1.1).

Eutrophication
Also other elemental cycles, such as those of phosphorus (P) and nitrogen (N), are
altered by human activities. Especially the intensification of agriculture, but also increases
in industrial and urban wastewater production have dramatically increased the loading of N
and P in aquatic systems. Atmospheric deposition of the increased nitrogen concentrations
in the atmosphere, due to agriculture and fossil-fuel burning, additionally adds nutrients to
aquatic systems. The anthropogenic nutrient loading led to eutrophication, one of the most
severe and pertinent environmental problems, causing degradation of aquatic ecosystems
and deteriorating water quality. Increased nutrients stimulate phytoplankton productivity,
resulting in recurring harmful algae blooms. Due to the high primary production, the
water transparency decreases and sedimentation increases. The consequent degradation of
sedimented matter consumes oxygen and causes anoxia in the bottom waters, creating dead
zones and massive fish kills (reviewed by Carpenter et al. 1998). Cyanobacteria are the
most notorious bloom formers by their abilities to form surface scum and to produce toxic
compounds (reviewed in Paerl et al. 2001). The reduced transparency induced by these
organisms leads to disappearance of macrophytes (aquatic plants).
4
CHAPTER 1
Fig. 1.1. Predicted changes in the surface seawater chemistry in response to changes in atmospheric pCO
2
assuming the “business as usual” scenario. Figure taken from Rost et al. 2008.
In the past decades, many shallow lakes shifted from a clear water, macrophyte dominated
state to a turbid, algal dominated state, often dominated by toxic cyanobacteria
(Scheffer et al. 1993).
Especially lakes are sentinels for anthropogenic disturbances, where global war-
ming, eutrophication, and land-use changes act in conjunction (Williamson et al. 2008). En-
vironmental problems often reinforce each other’s effect. For example, global warming is
expected to reinforce eutrophication effects, including an increase in cyanobacteria blooms
(Paerl and Huisman 2008) and to aggravate anoxia, due to increased water-column strati-
fication. Increased erosion and sediment input due changes in land use, amplify terrestrial
nutrient loading and enhances eutrophication effects.
1.2 Plankton community structure and the microbial food web
Environmental problems such as ocean acidification and eutrophication affect
the base of aquatic food webs: the structure and functioning of plankton communities. A
food web represents an ecological network of feeding interactions, where organisms can be
lumped into functional groups (i.e. producers, consumers) that perform at different trophic
levels (the position in the food chain). The base of aquatic food webs is formed by phyto-
plankton, the primary producers, which convert inorganic carbon (CO ) and nutrients into
2
organic matter (OM) during primary production.
GENERAL INTRODUCTION
Marine phytoplankton accounts for roughly half of the global primary production, despite
their low biomass (Field et al. 1998). In a classical view of the aquatic food web, the phyto-
plankton produced particulate organic matter (POM) is grazed by zooplankton, which can
be subsequently consumed by higher trophic levels, called the herbivorous food web.
Microbial food web
About 10-15 % of phytoplankton primary production is released as dissolved
organic matter (DOM), a mechanism of phytoplankton to release the surplus of carbon-rich
photosynthates (Fogg 1983, Baines and Pace 1991) over nutrients. The exudated DOM is
a high-quality substrate for growth of heterotrophic bacteria, which are key players in the
recycling of organic matter and nutrients in aquatic food webs (Azam et al. 1983). Hete-
rotrophic bacteria (hereafter denoted by bacteria) dominate pelagic (water-column) food
webs in terms of respiration and secondary production and it is estimated that 30-60% of
phytoplankton primary production is finally processed by bacteria (Cole et al. 1988, Del
Giorgo et al. 1997). Bacterial production forms the base of the microbial loop, which starts
with the consumption of DOM by bacteria that are in turn grazed upon by small, unicel-
lular organisms, named protozoans. Protozoans can be grazed by (metazoan, multicellular)
zooplankton, which links the microbial loop with the classical food web (Fig. 1.2).
Fig. 1.2. Schematic diagram of carbon flows between different components of planktonic food webs. Modified
after J.P. Torréton, IRD.
The importance of phytoplankton derived DOM as substrate for bacteria has been demon-
strated amongst others, through the existence of robust, general relationships between the
abundance and production of bacteria and phytoplankton (Cole et al. 1988).
6