Plankton dynamics under different climatic conditions in space and time

Abstract

1. Different components of the climate system have been shown to affect temporal dynamics in natural plankton communities on scales varying from days to years. The seasonal dynamics in temperate lake plankton communities, with emphasis on both physical and biological forcing factors, were captured in the 1980s in a conceptual framework, the Plankton Ecology Group (PEG) model.
2. Taking the PEG model as our starting point, we discuss anticipated changes in seasonal and long‐term plankton dynamics and extend this model to other climate regions, particularly polar and tropical latitudes. Based on our improved post‐PEG understanding of plankton dynamics, we also evaluate the role of microbial plankton, parasites and fish in governing plankton dynamics and distribution.
3. In polar lakes, there is usually just a single peak in plankton biomass in summer. Lengthening of the growing season under warmer conditions may lead to higher and more prolonged phytoplankton productivity. Climate‐induced increases in nutrient loading in these oligotrophic waters may contribute to higher phytoplankton biomass and subsequent higher zooplankton and fish productivity.
4. In temperate lakes, a seasonal pattern with two plankton biomass peaks – in spring and summer – can shift to one with a single but longer and larger biomass peak as nutrient loading increases, with associated higher populations of zooplanktivorous fish. Climate change will exacerbate these trends by increasing nutrient loading through increased internal nutrient inputs (due to warming) and increased catchment inputs (in the case of more precipitation).
5. In tropical systems, temporal variability in precipitation can be an important driver of the seasonal development of plankton. Increases in precipitation intensity may reset the seasonal dynamics of plankton communities and favour species adapted to highly variable environments. The existing intense predation by fish on larger zooplankters may increase further, resulting in a perennially low zooplankton biomass.
6. Bacteria were not included in the original PEG model. Seasonally, bacteria vary less than the phytoplankton but often follow its patterns, particularly in colder lakes. In warmer lakes, and with future warming, a greater influx of allochthonous carbon may obscure this pattern.
7. Our analyses indicate that the consequences of climate change for plankton dynamics are, to a large extent, system specific, depending on characteristics such as food‐web structure and nutrient loading. Indirect effects through nutrient loading may be more important than direct effects of temperature increase, especially for phytoplankton. However, with warming a general picture emerges of increases in bacterivory, greater cyanobacterial dominance and smaller‐bodied zooplankton that are more heavily impacted by fish predation.

Full text

Plankton dynamics under different climatic conditions in
space and time
LISETTE N. DE SENERPONT DOMIS*, JAMES J. ELSER
†
, ALENA S. GSELL*, VERA L. M. HUSZAR
‡
,
BAS W. IBELINGS*
,§
, ERIK JEPPESEN
–,
**
,††
, SARIAN KOSTEN
‡‡, § §
,WOLFM.MOOIJ*
,‡‡
,FABIO
ROLAND
––
, ULRICH SOMMER***, ELLEN VAN DONK*
, †††
, MONIKA WINDER***
, ‡‡‡
AND MIQUEL
LU
¨RLING*
,‡‡
*Department of Aquatic Ecology, NIOO-KNAW, Wageningen, The Netherlands
†
School of Life Sciences, Arizona State University, Tempe, AZ, U.S.A.
‡
Laborato
´rio de Ficologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s ⁄n, Sa
˜o Cristo
´va
˜o, Rio de Janeiro,
Brazil
§
Institut F.A. Forel, Universite
´de Geneve, Versoix, Switzerland
–
Department of Bioscience and the Arctic Centre, Aarhus University, Aarhus, Denmark
**Greenland Climate Research Centre (GCRC), Greenland Institute of Natural Resources, Nuuk, Greenland
††
Sino-Danish Education and Research Centre (SDC), Beijing, China
‡‡
Department of Aquatic Ecology and Water Quality Management, Wageningen University, Wageningen, The Netherlands
§§
Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB) Berlin ⁄Neuglobsow, Germany
––
Juiz de Fora Federal University, Juiz de Fora, MG, Brazil
***Leibniz-Institute of Marine Sciences at Kiel University (IFM-GEOMAR, Kiel, Germany
†††
Department of Ecology and Biodiversity, University of Utrecht, Utrecht, The Netherlands
‡‡‡
Systems Ecology, Stockholm University, Stockholm, Sweden
SUMMARY
1. Different components of the climate system have been shown to affect temporal dynamics in
natural plankton communities on scales varying from days to years. The seasonal dynamics in
temperate lake plankton communities, with emphasis on both physical and biological forcing factors,
were captured in the 1980s in a conceptual framework, the Plankton Ecology Group (PEG) model.
2. Taking the PEG model as our starting point, we discuss anticipated changes in seasonal and
long-term plankton dynamics and extend this model to other climate regions, particularly polar
and tropical latitudes. Based on our improved post-PEG understanding of plankton dynamics, we
also evaluate the role of microbial plankton, parasites and fish in governing plankton dynamics
and distribution.
3. In polar lakes, there is usually just a single peak in plankton biomass in summer. Lengthening of
the growing season under warmer conditions may lead to higher and more prolonged
phytoplankton productivity. Climate-induced increases in nutrient loading in these oligotrophic
waters may contribute to higher phytoplankton biomass and subsequent higher zooplankton and
fish productivity.
4. In temperate lakes, a seasonal pattern with two plankton biomass peaks – in spring and summer
– can shift to one with a single but longer and larger biomass peak as nutrient loading increases,
with associated higher populations of zooplanktivorous fish. Climate change will exacerbate these
trends by increasing nutrient loading through increased internal nutrient inputs (due to warming)
and increased catchment inputs (in the case of more precipitation).
5. In tropical systems, temporal variability in precipitation can be an important driver of the
seasonal development of plankton. Increases in precipitation intensity may reset the seasonal
dynamics of plankton communities and favour species adapted to highly variable environments.
Correspondence: Lisette N. De Senerpont Domis, Department of Aquatic Ecology, NIOO-KNAW, Droevendaalsesteeg 10, 6798 PB, Wageningen,
The Netherlands. E-mail: l.desenerpontdomis@nioo.knaw.nl
Freshwater Biology (2012) doi:10.1111/fwb.12053
2012 Blackwell Publishing Ltd 1

The existing intense predation by fish on larger zooplankters may increase further, resulting in a
perennially low zooplankton biomass.
6. Bacteria were not included in the original PEG model. Seasonally, bacteria vary less than the
phytoplankton but often follow its patterns, particularly in colder lakes. In warmer lakes, and with
future warming, a greater influx of allochthonous carbon may obscure this pattern.
7. Our analyses indicate that the consequences of climate change for plankton dynamics are, to a
large extent, system specific, depending on characteristics such as food-web structure and nutrient
loading. Indirect effects through nutrient loading may be more important than direct effects of
temperature increase, especially for phytoplankton. However, with warming a general picture
emerges of increases in bacterivory, greater cyanobacterial dominance and smaller-bodied
zooplankton that are more heavily impacted by fish predation.
Keywords: climate change, PEG model, phytoplankton, seasonal succession, zooplankton
Introduction
With our environment changing at an unprecedented rate,
an important challenge is to assess the impact of climate
change on the temporal plankton dynamics of lake
ecosystems (Christensen et al., 2007). Globally, tempera-
ture and precipitation have changed dramatically and are
predicted to change even more (Meehl et al., 2007). These
changes will affect other environmental conditions such
as nutrient loading and water column mixing. Tempera-
ture affects nearly all biological process rates, from
biochemical kinetics to species generation time, with
higher temperatures typically resulting in higher rates
until an optimum is reached, above which rate processes
usually decrease rapidly (Kingsolver, 2009). Various
components of the climate system have been shown to
relate to temporal dynamics of natural plankton commu-
nities on time scales varying from days (diel periodicity)
to years (seasonal periodicity). In a meta-analysis of
phytoplankton biomass time-series in temperate and
subtropical zones, Winder & Cloern (2010) observed a
unimodal pattern (i.e. spring bloom) prevailing at higher
latitudes following sinusoidal changes in irradiance and
temperature in temperate zones, whereas short-term
fluctuation in phytoplankton biomass was more common
at low latitudes. Periodicity in temperature at a daily scale
has been linked to vertical migration of both phytoplank-
ton and zooplankton in the subtropics (Becker, Cardoso &
Huszar, 2009), the tropics (Gliwicz, 1999) and to a lesser
degree in temperate regions (Gliwicz & Pijanowska, 1988).
On a longer time scale, the typical sinusoidal annual
fluctuations of temperature in temperate regions have
been related to a multitude of seasonal planktonic events,
including the timing of peak biomass in phytoplankton
and zooplankton (Straile, 2000, 2002), emergence from
resting stages (Gyllstro
¨m & Hansson, 2004) or hatching
and growth of planktivorous fish (Mooij, De Senerpont
Domis & Hu
¨lsmann, 2008). Extreme weather events, such
as the 2003 and 2006 summer heat waves in central
Europe, promoted cyanobacterial blooms (Jo
¨hnk et al.,
2008) and shifts in phytoplankton (Wilhelm & Adrian,
2008) and zooplankton succession (Anneville et al., 2010).
Climate warming has also induced species-specific
changes in the seasonal timing of life-cycle events,
resulting in decoupling of trophic relationships (Winder
& Schindler, 2004a) and subsequent effects on food-web
functioning (De Senerpont Domis et al., 2007); however, in
the long term, the importance of such decoupling may be
mitigated through to adaptation and microevolution of
the plankton (Van Doorslaer et al., 2007).
The seasonal dynamics of lake plankton communities
just described have been partially captured in a concep-
tual framework, the Plankton Ecology Group (PEG)
model, published in one of the most highly cited papers
in plankton ecology (Sommer et al., 1986). The PEG model
has a special emphasis on both physical and biological
forcing factors and describes the seasonal succession of
phytoplankton and zooplankton in 24 sequential steps
based on the well-studied deep, peri-alpine Lake Con-
stance. PEG mainly covers deep stratified lakes and
strongly hinges on the assumption that plankton dynam-
ics during winter and spring are under abiotic control
(light, nutrients), whereas later in the year biotic interac-
tions (resource competition, herbivory, fish predation)
become dominant. The model identifies how basic pat-
terns in plankton seasonality depend on trophic state.
Under more eutrophic conditions, seasonal development
of phytoplankton biomass follows a bimodal or even
trimodal pattern, with a distinct spring clear-water phase
and a summer bloom of larger, less edible algae or
cyanobacteria. However, under more oligotrophic condi-
tions, both phyto- and zooplankton follow a unimodal
2L. N. De Senerpont Domis et al.
2012 Blackwell Publishing Ltd, Freshwater Biology, doi:10.1111/fwb.12053

pattern, with the spring bloom as the main event,
reflecting reduced availability of nutrients and increased
grazing impact on phytoplankton in summer. However,
since the PEG model appeared in 1986, this paradigm of
bottom-up versus top-down control has shifted (Brett &
Goldman, 1997) and the greater complexity of the aquatic
food web has been recognised, resulting in a perhaps
more nuanced view on plankton seasonality (Jeppesen
et al., 1997). Improved knowledge about winter conditions
and about shifts in response to recent climate change has
opened a debate about one of the basic assumptions
underlying the original PEG model: that is, that winter
effectively resets the plankton community (Jeppesen et al.,
2004; Blank et al., 2009; Hu
¨lsmann et al., 2012). Our
changed perspectives on aquatic food webs also involve
the inclusion of the microbial loop (Sanders, Caron &
Berninger, 1992), recognition of the potential impact of
parasites on plankton host populations (Wommack &
Colwell, 2000; Duffy et al., 2005; Kagami et al., 2007), as
well as acknowledgement of the effects of food quality on
trophic transfer efficiency and zooplankton dynamics
(Elser et al., 2000; Muller-Navarra et al., 2000).
Beyond the absence of such newly appreciated mech-
anisms, PEG also had limitations because the majority of
the lakes used to validate the PEG model were temperate
(with the exception of two subtropical lakes located in
South Africa) (Sommer et al., 1986). Traditionally, plank-
ton seasonality was assumed to be less prominent in low-
latitude than in high-latitude lakes due to the dampened
fluctuations in both irradiance and temperature in the
tropical zone (Gliwicz, 1999). However, the increasing
availability of data on temporal variability in (sub)tropical
systems shows that this assumption is not valid for
tropical lakes (<23 C latitude), as many of these are
sensitive to seasonal variations in hydrology due to
annual cycles of precipitation (de Domitrovic, 2003;
Loverde-Oliveira et al., 2009; Ndebele-Murisa, Musil &
Raitt, 2010); this seasonality occurs both directly through
flushing and indirectly through hydrological effects on
nutrient cycling by particle resuspension and run-off.
These latitudinal contrasts suggest that comparison of
seasonal patterns in plankton dynamics across different
regions may give us much-needed insight into the
coupling between climate and seasonality, which will be
helpful in predicting the possible effects of climate-change
scenarios. Here, we seek an overview of patterns in
plankton dynamics, highlighting those in different cli-
matic zones in the light of our improved, post-PEG,
understanding of plankton ecology. Rather than updating
the PEG model to the newest scientific insights (for this,
see Sommer et al., 2012), we will use the PEG approach as
a framework for synthesising available data on temporal
plankton dynamics in different climate zones. We empha-
sise that the degree of change in the different climate
components will result in the creation of new climate
regimes, rather than just warmer climates. In the light of
this, we discuss the role of bottom-up versus top-down
processes and trophic state in determining plankton
dynamics. In addition to phytoplankton and zooplankton,
we will discuss the role of the microbial food web,
parasites and fish in governing these seasonal events.
Projected changes in climate components
Temperature
Warming over land is expected to be greater than global
annual warming due to the smaller thermal inertia and
less available water for evaporative cooling on land. Thus,
climate warming will likely affect inland waters more
than oceans (Christensen et al., 2007). Based on modelling
output from Atmosphere-Ocean General Circulation
Models as well as data on recent changes in climate,
regional patterns in warming are emerging: most of the
Americas and all of Africa, Europe, the polar regions and
Northern and Central Asia are likely to warm more than
the global average. These projections suggest that the
warming will be least in South-East Asia, Australia and
New Zealand and southern South America (Christensen
et al., 2007).
Projected warming also differs by season: in the
northern part of Europe and North America, warming
will be largest in the winter, whereas in the southern areas
of North America and Europe warming will be largest in
summer (Christensen et al., 2007). In the polar regions,
warming in winter will be larger than in the summer as a
result of a reduction in sea ice and snow (Meehl et al.,
2007). This phenomenon will be more pronounced in the
Arctic, and consequently, snow and (sea) ice content will
continue to decrease. In most of Asia, warming in winter
will be more pronounced than in summer, but in South
America the projected seasonal differences in warming
may not be so distinct (Christensen et al., 2007).
Beyond these model projections, data records can also
be examined to assess the patterns of climatic change. In
most regions of the world, long-term records have shown
a decrease in the number of very cold days and nights and
an increase in the number of very hot days and nights
(Trenberth et al., 2007); this trend will most likely con-
tinue. Indeed, global climate projections indicate that heat
waves will be more intense, more frequent and longer
lasting (Meehl et al., 2007). Likewise, the frost-free season
Plankton dynamics under different climatic conditions 3
2012 Blackwell Publishing Ltd, Freshwater Biology, doi:10.1111/fwb.12053

has increased in length at mid- and high latitudes in both
hemispheres during the past several decades; this trans-
lates to shorter duration of ice cover in lakes. In the next
hundred years, the number of frost days will continue to
decrease (Meehl et al., 2007). On a global scale, the diurnal
temperature range will decrease, as daily minimum
temperatures are projected to increase faster than daily
maximum temperatures (Meehl et al., 2007). While regio-
nal information is too sparse to make global statements on
temperature variability, most model projections agree that
projected temperature variability will be lower in winter
in most of Europe, whereas in summer both interannual
and daily temperature variability are predicted to increase
(Christensen et al., 2007).
Precipitation
Precipitation has shown a significant upward trend over
the past few decades as a consequence of a warming-
driven increase in the water-holding capacity of the
atmosphere. This increase has affected mainly regions
that are already receiving a considerable amount of
precipitation, for example eastern parts of North and
South America, northern Europe and northern and central
Asia (Trenberth et al., 2007). In contrast, during the last
century, historically low precipitation areas, such as the
Mediterranean, southern Africa and Asia and the Sahel,
have experienced decreased precipitation. Due to the
temperature rise over the recent decades, more precipita-
tion has fallen as rain rather than snow in mid- and high-
latitude regions. All these trends are predicted to continue
under current climate model projections (Christensen
et al., 2007). In addition, it is very likely that precipitation
will increase in areas with monsoon regimes, such as
tropical parts of Asia and South America (Meehl et al.,
2007).
How precipitation intensity will change at local and
regional scales is to a large extent governed by changes in
atmospheric circulation patterns such as the El Nin
˜o
Southern Oscillation and the North Atlantic Oscillation. In
areas predicted to experience increases in mean precipi-
tation, such as some tropical and high-latitude areas, the
intensity of precipitation events will grow. This projection
also holds true for areas that are expected to experience a
decrease in mean precipitation, such as large parts of the
subtropics, but the interval between subsequent rainfall
events will be longer (Meehl et al., 2007). In these areas,
this precipitation variability translates not only to a higher
incidence of flooding but also to extended drought. In
Asia in particular (Christensen et al., 2007), tropical storms
and hurricanes are likely to become more intense,
producing stronger peak winds and increased rainfall
over some areas due to warming sea surface temperatures
that can energise these storms.
Climate-induced changes in physical characteristics
of lakes and biogeochemical cycling
Stratification
Thermal stratification has long been accepted as a prime
environmental variable steering plankton succession in
deep lakes (Sommer, 1985). There is increasing evidence
that a warmer climate will result in earlier, stronger and
longer stratification (DeStasio et al., 1996; Peeters et al.,
2002). This might even lead, for some lakes at least, to a
scenario in which dimictic lakes become warm monomic-
tic lakes (Gerten & Adrian, 2002) and monomictic ones
become oligomictic.
While such shifts in stratification are relevant mostly to
deeper lakes that can establish stable thermal gradients, in
shallow waters (typically waterbodies with average
depths <2 m) higher temperatures and an increase in
solar energy input can also lead to stronger (micro)strat-
ification, strengthening of water column stability and
resistance to complete mixing. In warm shallow waters,
even small differences in water temperature between
upper and lower water layers can result in the water
column becoming stably stratified (Huszar & Reynolds,
1997). In tropical lakes, superficial stratification occurs
during the daytime followed by nocturnal mixing, a
process that is sometimes called atelomixis. In deeper
tropical lakes, this diurnal stratification may result in a
situation where the hypolimnion stays intact, whereas the
epilimnion splits up in multiple isolated layers, each with
its own physical and chemical properties (Lewis, 1973;
Barbosa & Padisa
´k, 2002). Particularly during warmer
episodes, this pattern of alternating periods of stabilisa-
tion and mixing, operating at the diel scale, has been
observed in temperate lakes as well (Riley & Prepas, 1984;
Kallio, 1994). Reduced convectional cooling during the
night under future, warmer conditions will render this
type of microstratification more stable, especially in small,
wind-sheltered lakes (Hanson et al., 2008). Since micros-
tratification can have important implications for lake
metabolism with net ecosystem production being signif-
icantly higher on days with microstratification (Coloso,
Cole & Pace, 2010), future climate change could signifi-
cantly alter ecosystem dynamics in lakes that are subject
to such microstratification. Under future climate change,
oxygen depletion of the hypolimnion is likely to be
aggravated by the projected longer period of summer
4L. N. De Senerpont Domis et al.
2012 Blackwell Publishing Ltd, Freshwater Biology, doi:10.1111/fwb.12053

stratification. As a result, earlier and longer phosphorus
release from anoxic sediments is expected (Jankowski
et al., 2006). In shallower lakes, this hypolimnetic nutrient
accumulation might fuel phytoplankton blooms, espe-
cially when periods of stability come to an end by an
increased number of mixing events that introduce nutri-
ent pulses (Wilhelm & Adrian, 2008).
Besides an earlier onset of stratification due to climate
change, changes in the depth of the mixed layer are also
expected in temperate waters (Hondzo & Stefan, 1993).
The direction of change will depend on the interplay
between lake morphometry, transparency and radiative
balance (Magnuson et al., 1997). For example, wind-
exposed lakes in regions experiencing an increase in wind
velocity (a likely scenario for some coastal regions in the
temperate zone) will probably see a deepening of the
thermocline during the summer months (Hondzo &
Stefan, 1991). As a result of this, regeneration of nutrients
within the epilimnion should increase as particles would
be retained longer (Fee et al., 1994). In contrast, warming
will probably result in a shallower epilimnion during
summer stratification in smaller lakes with their short
fetch (Hondzo & Stefan, 1993). For lakes with heat carry-
over during the winter from 1 year to the next (e.g. lakes
that are not strictly dimictic), warmer winter temperatures
may result in hypolimnetic warming (Peeters et al., 2002;
Livingstone, 2003; Straile et al., 2010). This deep-water
warming might not only enhance the solubilisation of
accumulated phosphorus from the sediments but also the
mineralisation of hypolimnetic organic matter. This
would increase the likelihood of anoxia (Gudasz et al.,
2010). Conversely, in strictly dimictic lakes, earlier and
more rapid onset of stratification may shield deeper water
from warming, resulting in colder hypolimnetic temper-
atures (Hondzo & Stefan, 1993).
Increases in precipitation may also disrupt stratification
for many aquatic systems due to washout. For example,
extreme events of precipitation are projected for the entire
east coast of South America (Marengo et al., 2009); as a
consequence, thermal stratification in small- and medium-
sized reservoirs in this region is likely to be disrupted due
to the effects of hydrological flushing on thermal condi-
tions (Bouvy et al., 2003).
Changes in nutrient cycling and hydrology
Ongoing global climate change will likely intensify the
hydrological cycle, consistent with ongoing global
increases in evaporation and thus precipitation (Hunting-
ton, 2006) (Fig. 1). However, the hydrological response to
climate change of drainage basins strongly depends on
latitude. Whereas increased run-off is predicted for the
Arctic, mid-latitude humid and some tropical regions,
decreased run-off is predicted for semi-arid and arid
regions (Solomon et al., 2007; Praskievicz & Chang, 2009).
In the northern temperate zone, the expected climate
change will most probably boost the nitrogen (N) and
phosphorus (P) load to lakes, predominantly in winter due
to higher winter rainfall (Jeppesen et al., 2009). As erosion
is generally a major contributor of P to lakes, increased
surface flow will result in increased P loading (Praskievicz
& Chang, 2009). Climate change–induced land-use shifts
may modulate or further strengthen the loss of nutrients,
depending on the scenario (Jeppesen et al., 2009).
In warm temperate and arid climates, the projected
reduction in precipitation and the higher evaporation will
lead to a severe drop in run-off. Whereas diffuse loadings
may consequently decrease, concentrations of nutrients in
inflows may increase (Jeppesen et al., 2009, 2011). Fur-
thermore, enhanced evaporation and water extraction for
irrigation in warm regions will aggravate salinisation
(Jeppesen et al., 2009, 2011). The resulting lower water
levels and increased lake residence times could promote
the internal release of nutrients and dominance of cyano-
bacteria and chlorophytes (Beklioglu et al., 2007). On the
other hand, in a drier climate, lakes might also completely
disappear (Schindler, 2009), a possibility exacerbated by
likely compensatory increases in water extraction for
irrigation (Jeppesen et al., 2011). A modelling exercise
based on projected local run-off indicated that, while the
overall distribution of lakes will change regionally, total
global lake area will not be altered by 2050 (Tranvik et al.,
2009). Nonetheless, a significant reduction in total lake
area is expected in North America, Western Europe, the
Mediterranean, Russia and Australia (Tranvik et al., 2009).
Higher
temperature
Precipitaon/
snow melt
+
Ice cover
–
+
Run-o
+
+
Stracaon
Evaporaon
Respiraon/
decomposion
+
+
Anoxia/P-
release
+
++C
Denitricaon
N
P
–
+
+
+
Fig. 1 Schematic overview of the effect of temperature on physical
and chemical processes influencing nutrient cycling of phosphorus
(P), carbon (C) and nitrogen (N).
Plankton dynamics under different climatic conditions 5
2012 Blackwell Publishing Ltd, Freshwater Biology, doi:10.1111/fwb.12053

Global change scenarios predict that atmospheric CO
2
concentrations will rise to 750 ppm by the year 2100
(Solomon et al., 2007). Increased atmospheric CO
2
con-
centrations may affect the inorganic carbon chemistry of
freshwater ecosystems and themselves alter elemental
composition and species interactions in freshwater phy-
toplankton communities. Many studies have reported an
increase in phytoplankton productivity under increased
atmospheric CO
2
(Hein & Sand-Jensen, 1997; Ibelings &
Maberly, 1998; Schippers, Lurling & Scheffer, 2004).
Furthermore, the species composition of phytoplankton
may also change substantially (Verschoor et al., 2012),
depending on the magnitude of change in CO
2
(Low-
De
´carie, Fussmann & Bell, 2011).
The effects of climate on water quality are clearly
complex, since warming and different temperature-
related drivers influence interacting physical, biogeo-
chemical and biological processes (Kosten, 2010).
Nonetheless, the projected increase in overall lake nutri-
ent levels has been identified as an important contributor
to predicted deterioration of lake water quality under
future climate scenarios (Genkai-Kato & Carpenter, 2005;
Bicudo et al., 2007).
Climate-induced patterns in plankton dynamics
Phytoplankton
With anticipated changes in length of growing season and
nutrient loading, we expect that the seasonality of phy-
toplankton will be altered with warming. However, such
changes will likely vary in different regions and latitudes.
Polar lakes and ponds. In polar lakes and ponds, maximum
productivity during the warmer summer months results
in a single biomass peak. Extended periods of snow and
ice cover strongly hamper photosynthesis, favouring
dominance of mixotrophic species that are able to actively
survive cold and dark periods, such as Dinobyron,Chrys-
ochromulina and Ochromonas (Laybourn-Parry, 2002;
Laybourn-Parry & Marshall, 2003). With warming, an
earlier onset and longer duration of the growth period
may result in higher biomass. Several studies have shown
that climate warming, that is, change in ice cover and ⁄or
enhanced thermal stratification, is a prime determinant of
recent changes in diatom assemblages in arctic lakes
(Smol, 2005; Keatley, Douglas & Smol, 2008; Ruhland,
Paterson & Smol, 2008). More specifically, a pronounced
increase in the abundance of planktonic diatoms such as
Cyclotella has been noted at the expense of benthic species
of Fragilaria and Achnantes, and tychoplanktonic genera
such as Aulacoseira (Smol, 2005; Keatley et al., 2008;
Ruhland et al., 2008). Phytoplankton growth in arctic
lakes often shows concurrent N and P limitation; thus,
phytoplankton productivity should increase in response
to changes in climate that increase nutrient loading, such
as increased landslides, erosion and thawing of the
permafrost (Levine & Whalen, 2001). Enhanced temper-
atures may also significantly boost nutrient acquisition
and phytoplankton biomass accumulation in arctic lakes
(Ogbebo et al., 2009).
Temperate lakes. In most temperate lakes, ample nutrient
and light availability towards the end of winter triggers an
initial spring bloom of small- to medium-sized algae (e.g.
centric and pennate diatoms and cryptophyceae). In
shallow lakes, this initial bloom of small algae is soon
replaced by large pennate diatoms, such as Asterionella,
and in summer by green algae and ⁄or cyanobacteria
(Sommer et al., 1986; Reynolds, 1989). Heavy grazing by
zooplankton may strongly reduce phytoplankton biomass
(the ‘clear-water phase’). However, whether a clear-water
phase actually occurs in temperate lakes depends on fish
predation (Carpenter et al., 2008); indeed, no clear-water
phase occurs in hypertrophic shallow lakes with high fish
predation (Jeppesen et al., 1997).
How might climate change alter these typical dynam-
ics? As in polar lakes and ponds, extension of the growing
season can lead to larger phytoplankton biomass, as
indicated by a correlative study of Weyhenmeyer, Peter &
Willen (2012) on variations in the length of the ice-free
season and phytoplankton species richness and biomass
patterns over a latitudinal gradient. Their results suggest
that this shift in biomass corresponds to a shift in nutrient
conditions. In a cross-lake comparison of shifts in phyto-
plankton phenology over 58 years, Feuchtmayr et al.
(2012) found that locally variable phosphate levels had a
more consistent effect on phenology than temperature.
As a consequence of changes in thermal stratification in
warming climates, the spring phytoplankton bloom is
likely to start earlier, as is the case in arctic lakes (Muller-
Navarra, Guss & Von Storch, 1997; Winder & Schindler,
2004b; Christoffersen et al., 2008). This would then be
followed by an earlier zooplankton peak and clear-water
phase or by a decoupling of trophic interactions in which
zooplankton is no longer able to make optimal use of its
food source (Edwards & Richardson, 2004; Winder &
Schindler, 2004a; De Senerpont Domis et al., 2007). At
present, it is not clear how frequently trophic uncoupling
will occur, as we have insufficient understanding of the
consequences of an earlier spring bloom for later stages of
the seasonal plankton succession. Furthermore, changes
6L. N. De Senerpont Domis et al.
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in (fish) predation need to be taken into account. For
example, the study by Wagner et al. (2012) on warming-
induced changes in trophic coupling between the key
herbivore Daphnia and both a vertebrate and invertebrate
predator underlines the importance of a mechanistic
understanding of temperature-driven changes in trophic
interactions.
The extended period of thermal stratification under
climate warming seems to open a window for prolonged
summer blooms of cyanobacteria or large dinoflagellates
and also for invasive species (Blenckner et al., 2007; Paerl
& Huisman, 2008; Masclaux et al., 2009). In a more stable
water column, positively buoyant cyanobacteria will more
easily disengage from turbulent mixing and use their
buoyancy-controlled vertical migration to position them-
selves in the water column nearer to the surface (Ibelings,
Mur & Walsby, 1991), promoting their dominance (Jo
¨hnk
et al., 2008). Consistent with this scenario, Blenckner et al.
(2007) showed that cyanobacteria responded positively to
positive NAO years, increasing their abundance in
response to both higher temperatures (on the basis of a
supposedly superior Q
10
of cyanobacteria, but see Lu
¨rling
et al., 2012) and enhanced stratification, benefitting from
efficient buoyancy (Ibelings et al., 1991). Also in support of
such shifts is a regression analysis on data from numerous
Danish lakes (Jeppesen et al., 2009). This study found that
dominance of cyanobacteria and dinophytes increased
with warming, while the contribution of green algae and
diatoms decreased. Finally, the earlier seasonal increase in
water temperature under climate warming permits earlier
germination from cyanobacterial resting stages, poten-
tially promoting the spread of invasive cyanobacteria such
as Cylindrospermopsis raciborskii in the temperate zone
(Wiedner et al., 2007).
In historically low precipitation areas, such as the
Mediterranean, anticipated decreases in precipitation will
lead to longer water residence times. Romo et al. (2012)
found that, during dry years in the large shallow Lake
Albufera, stagnant water columns as well as long resi-
dence time led not only to higher total cyanobacterial
biomass but also to increased amounts of cyanotoxins.
Segura et al. (2012) used a mechanistic model based on
morphology-based functional groups to confirm these
observations, showing that, compared to other functional
groups, the competitive ability of large cyanobacteria with
gas vesicles was highest under low flushing rates.
In temperate floodplain areas prone to inundation
(Roozen et al., 2008), the projected intensification of annual
precipitation may reset the seasonal dynamics of plankton
communities. Timing of inundation seems to play an
important role: spring inundation synchronised plankton
dynamics in different waterbodies in a floodplain, while
winter inundation did not have the same effect (Roozen
et al., 2008). Through increases in run-off, increased
precipitation can lead to higher external nutrient loading
(Rip et al. 2007), boosting phytoplankton growth. Extreme
rainfall events cause even higher run-off during winter
periods when catchment vegetation lacks foliage (Ander-
sen et al. 2006).
In eutrophic shallow lakes in the temperate zone, higher
temperatures in winter and spring will enhance the
internal loading of P (Jensen & Andersen, 1992; Sønderg-
aard, Jensen & Jeppesen, 2003), which in turn will
reinforce a warming-induced stimulation of phytoplank-
ton in spring and autumn (E. Jeppesen, unpublished
data). Higher temperature can also boost summertime
internal loading in shallow lakes (Jensen & Andersen,
1992; Søndergaard et al., 2003) and thus potentially lead to
higher phytoplankton biomass (Jeppesen et al., 2009).
Tropical lakes. A comparison of phytoplankton dynamics
in tropical lakes spanning three continents (Melack, 1979)
suggests that in most tropical lakes, seasonality is usually
dominated by either hydrological (water input and
output) or hydrographical features (water column strat-
ification and mixing), both of which are also related to
climate (Talling, 1986). In addition, both Melack (1979)
and Gliwicz (1999) have suggested that the diel cycles of
physical, chemical and biological processes in tropical
productive lakes can have a much stronger periodicity
than the seasonal cycle. Seasonal fluctuations in plankton
biomass and species composition are also strongly gov-
erned by the hydrological and hydrographical cycle in
tropical floodplain lakes, such as in the Amazon region
(equatorial latitudes) or in the Pantanal wetlands (Huszar
& Reynolds, 1997; Bozelli & Garrido, 2000; Loverde-
Oliveira et al., 2009).
High flushing rates during high water and low flushing
rates during low water favour species better adapted to
those conditions and also influence the structure, metab-
olism and productivity of communities. The pattern of
hydrographical variability is driven by seasonal differ-
ences in the distribution of local precipitation and
precipitation in the headwaters and, in case of Amazonian
floodplain lakes, also by seasonality in the glacial melting
in Andean regions (Junk et al., 2006). Phytoplankton
seasonal patterns in floodplain lakes at intermediate
subtropical latitudes (such as in the Parana
´River basin
in South America, 31S, where there is a considerable
variability in temperature and irradiance) are also
explained by interactions between hydrology and clima-
tology (de Emiliani, 1997). Precipitation is also an
Plankton dynamics under different climatic conditions 7
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important driver of plankton communities in other
regions. For example, rain events disrupt the long-stand-
ing cyanobacterial dominance in man-made lakes in semi-
arid regions (8S), leading to decreases in biomass and
changes in species composition (Bouvy et al., 2003). With
anticipated higher precipitation intensities in these sys-
tems, higher flushing rates may result in a stronger reset
of the biomass build-up as well as a community domi-
nated by species more closely adapted to variable envi-
ronments.
Mesozooplankton
As with phytoplankton, zooplankton have characteristic
seasonal cycles that are strongly linked to the seasonality
of temperature (arctic and temperate regions), hydrology
(tropical regions), food availability and predation pres-
sure. Variation in these factors can modify the population
fluctuations in these organisms. Indeed, the interplay
between seasonal increases in temperature, resource
availability and predation pressure results in the typical
unimodal and bimodal patterns in zooplankton seasonal-
ity often observed in temperate lakes (Jeppesen et al.,
1997; Angilletta, Huey & Frazier, 2010), whereas a
combination of year-round strong predation pressure
and hydrological forcing seems to govern zooplankton
seasonality in warmer lakes (Havens et al., 2009).
Zooplankton population growth shows strong coher-
ence with seasonal temperature fluctuations as evidenced
by latitudinal gradients (Gillooly & Dodson, 2000; Straile,
2002) and seasonal timing or phenologies (Adrian, Wil-
helm & Gerten, 2006): peaks in biomass typically occur
earlier with warmer temperatures. Given sufficient re-
sources, an increase in temperature within the tolerance
range of a species accelerates growth, developmental and
reproductive rates. For zooplankton, changes in phenol-
ogy and life-history strategies, increased turnover rates,
increased number of generations per year and greater
population instability can be anticipated with climate
warming (Drake, 2005). In addition, seasonality is gov-
erned to a large extent by the structure of the predator
communities (fish and macroinvertebrates); this impact of
predation seems to be stronger in warmer climates than in
colder climates (Meerhoff et al., 2007).
Polar lakes and ponds. In polar lakes and ponds, the short
duration of the growing season and the absence of strong
predation typically result in a unimodal pattern of
zooplankton biomass over time, regardless of trophic
state. Here, the lack of food, but not the cold temperature,
seems to be dominant in driving zooplankton dynamics
(Van Geest et al., 2007); therefore, increased food avail-
ability under warmer conditions, rather than the direct
effect of warmer temperatures on vital rates, is likely to
result in higher zooplankton productivity. Whether this
higher zooplankton productivity translates into higher
annual biomass will likely depend on the predation
pressure. For example, arctic lakes that contained fish
did not support significant populations of Daphnia
middendorffiana, although growth and survivorships
experiments indicated that this species could do well in
these environments (Yurista & O’Brien, 2001). Low den-
sity of large-bodied zooplankton is also characteristic for
lakes in Greenland hosting fish, while they are abundant
in fishless lakes (Lauridsen et al., 1999; Davidson et al.,
2011). Studies of Greenlandic lakes have further shown
that warming may result in fish colonisation of lakes
when enhanced precipitation as rain enhances connectiv-
ity to the sea, and consequently, large-bodied zooplankton
are lost (Bennike et al., 2008).
Temperate lakes. In temperate lakes, the annual cycles in
zooplankton biomass and grazing pressure on phyto-
plankton represent a bimodal pattern with high grazing
pressure in spring and autumn in oligo-mesotrophic
lakes. In contrast, a unimodal pattern with relatively low
grazing pressure prevails throughout the year in hype-
reutrophic lakes (Jeppesen et al., 1997). This difference in
modality has been attributed to a shift from mid-summer
high fish predation [particularly by young-of the-year
(YOY) fish] creating bimodality in oligo-mesotrophic lakes
to high predation by planktivorous fish of all size classes
throughout the year in hypertrophic lakes (Jeppesen et al.,
1997).
However, the pattern in seasonality (i.e. unimodal
versus bimodal) might not be directly regulated by
temperature, but rather by top-down regulation. Lake
comparisons by Straile (2002) suggest that the timing of
the zooplankton peak(s) seems to be influenced by
temperature: increases in temperature advance the timing
of peak zooplankton abundance. The effect of temperature
on zooplankton phenology might also be modified by
trophic state as suggested by the large differences
observed in the response of two peri-alpine lakes to heat
waves (Anneville et al., 2010). These data showed that,
during the heat waves, zooplankton in oligotrophic Lake
Annecy followed the usually observed succession from
herbivorous zooplankton to carnivorous zooplankton,
whereas dominance of herbivorous zooplankton was
maintained throughout the summer in meso-eutrophic
Lake Geneva. Further evidence comes from a fish-free
mesocosm experiment in the U.K. (Feuchtmayr et al.,
8L. N. De Senerpont Domis et al.
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2010). The experiment tested the combined effects of
warming (4 C above ambient) and increased nutrient
loading on plankton communities and found warming to
advance zooplankton phenology. However, this advance
could be dampened in systems with high nutrient
concentrations. The experiment revealed high peak zoo-
plankton abundances with warming at high nutrient
loadings; these high abundances induced a clear-water
phase due to heavy zooplankton grazing, despite high
nutrient concentrations.
The synchronisation of key zooplankton life stages with
resource availability plays an important role in governing
seasonality, particularly in temperate regions where
quantity and quality of phytoplankton are highly variable
on a seasonal basis (Sommer et al., 1986; Cushing, 1990; De
Senerpont Domis et al., 2007). As a result, climate warm-
ing may indirectly affect population dynamics and life
histories of zooplankton in temperate regions through its
effect on the seasonality of resource availability and other
components of the ecosystem, such as the duration of the
growing season (Ottersen et al., 2001; Stenseth et al., 2004).
These modifications in the environment are especially
likely to affect life-cycle responses in longer-lived species
such as copepods (Chen & Folt, 1996; Drake, 2005), but the
effects may be quite complex (Adrian et al., 2006; Winder
et al., 2009). For example, shifts in the number of gener-
ations (voltinism) were observed for copepod species
concurrent with warming and lengthening of the growing
period (Adrian et al., 2006; Winder et al., 2009), as
predicted by generic population dynamics models (Drake,
2005). Shifts in voltinism are important from an ecological
and evolutionary perspective because an additional gen-
eration per unit time may strongly accelerate population
growth or adaptation.
Tropical lakes. In low-latitude lakes, zooplankton dynam-
ics seem to be characterised by an almost perennial but
low biomass (Havens et al., 2009). Meerhoff et al. (2007)
argue that this observed difference in seasonality in low-
latitude lakes versus high-latitude lakes for cladocerans
(Gillooly & Dodson, 2000) cannot be primarily ascribed to
direct temperature effects on zooplankton performance.
Instead, it more likely reflects temperature-mediated
shifts in the community preying on zooplankton. Indeed,
fishes in tropical lakes likely exert a stronger predation
pressure on large zooplankton due to enhanced repro-
duction rates, early reproduction and a high degree of
omnivory. This leads to cascading effects promoting water
turbidity (van Leeuwen et al., 2007; Meerhoff et al., 2007;
Jeppesen et al., 2010). The experiments of Lacerot et al.
(2012) support the view that the small-bodied cladocerans
generally present in (sub)tropical lakes have limited
abilities to exert top-down control of the phytoplankton
biomass. Consistent with this, Iglesias et al. (2011) showed
that large zooplankton dominated in a subtropical lake
after a fish kill and also appeared in fish-free enclosures
open to the sediment but were missing in similar
enclosures with fish. They also found resting eggs of
Daphnia in the surface sediment of many subtropical
Uruguayan lakes even when Daphnia were missing in
contemporary samples, demonstrating that Daphnia
potentially are capable of developing populations but
are kept low by high fish predation. In addition, unlike in
higher-latitude lakes, submerged macrophytes in low-
latitude lakes do not seem to offer zooplankton refuge
from predation due to abundant littoral predators, as
indicated by weak diel horizontal migration (Meerhoff
et al., 2007). Furthermore, the impact of a cold-water
refuge from predation by planktivorous fish is larger in
temperate lakes than in tropical and arctic lakes, in which
temperature differences between stratified water layers
are smaller. Regression analysis of Danish lakes also
indicates a reduction in both the abundance and the size
of zooplankton and an increase in proportion of small fish
with increasing temperature, which is consistent with a
view that the low-latitude dominance of small zooplank-
ton species cannot be attributed to biogeographical or
evolutionary issues (Jeppesen et al., 2009, 2010).
Microbial plankton
Climate-induced increases in carbon and nutrient loading
(see above) might have consequences for the relative
roles of bacteria and bacterivores in the aquatic food web,
especially in oligotrophic systems. Based on cross-system
observations, Cotner & Biddanda (2002) argued that, in
eutrophic systems, phytoplankton and phagotrophic
heterotrophs (i.e. most ciliates and flagellates, rotifers
and mesozooplankton) are favoured over bacteria due to
both the high overall inorganic nutrient availabilities and
the dominance of inorganic nutrients relative to dis-
solved nutrients in organic form. Support for the role of
climate-induced changes in the nutrient loading rather
than climate warming itself comes from a mesocosm
study that manipulated nutrient levels along with tem-
perature in the simulation of shallow-lake warming
towards the end of this century. The data showed that
the abundances of picoalgae, bacteria and heterotrophic
nanoflagellates were far more affected by the nutrient
state than by temperature and that the temperature effect
was highest at the low nutrient level (Christoffersen et al.,
2006).
Plankton dynamics under different climatic conditions 9
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Polar lakes and ponds. The truncated food webs of these
extreme habitats are often dominated by the microbial
loop (Laybourn-Parry, 1997; Laybourn-Parry & Marshall,
2003). In these oligotrophic systems, large input of labile
allochthonous dissolved organic matter with snowmelt
water can result in high bacterial productivity in early
spring. In the ultra-oligotrophic arctic Lake Toolik,
seasonal changes in the source of organic matter (allo-
chthonous versus autochthonous) were related to shifts in
bacterial community composition (Crump et al., 2003).
Typically, the low productivity of these lakes cannot
sustain high microzooplankton biomass, so the higher
levels of the microbial food web cannot control flagellates
and bacteria (Hobbie, Bahr & Rublee, 1999). Mixotrophy
can provide a survival mechanism to survive the cold,
dark winter months (Laybourn-Parry, 2002). Mixotrophic
and heterotrophic flagellates typically peak in abundance
during winter and early spring, whereas rotifers and
ciliates are the dominant bacterivores in late spring to
early summer (Rautio, Mariash & Forsstrom, 2011). With
the anticipated changes in nutrient loading and temper-
ature in these systems, most likely a shift will occur from
bottom-up control of the bacterioplankton to top-down
control of the bacterioplankton. In a long-term study on
the effects of warming and nutrients, O
¨zen et al. (2012)
found the bacteria ⁄phytoplankton ratio to be lowest in
nutrient-rich warm mesocosms, which had the highest
heterotrophic nanoflagellate ⁄bacteria ratio as well as the
highest rotifer ⁄bacteria ratio. Their results suggest stron-
ger grazer control of bacterioplankton under warmer,
more nutrient-rich conditions.
Temperate lakes. While bacterial production and abun-
dance in most temperate systems show a more dampened
seasonal variation than phytoplankton and zooplankton,
overall abundances are lowest in winter and highest in
summer (Sanders et al., 1989, 1992; Christoffersen et al.,
2006). Furthermore, bacteria sometimes exhibit a time lag
in their response to changes in chlorophyll abiomass,
which is usually highest in later winter–early spring and
decreases over the summer (with the exception of the
above-mentioned summer nuisance algal blooms). The
correlation between phytoplankton and bacterioplankton
biomass seems to be predominantly strong and positive in
temperate systems (unless the grazing pressure by zoo-
plankton on phytoplankton is high, Jeppesen et al., 1997;
Ju
¨rgens & Jeppesen, 2000). As in polar systems, warmer
and more nutrient-rich conditions could potentially lead
to stronger grazer control of the bacterioplankton with
consequently lower bacteria ⁄phytoplankton ratios (O
¨zen
et al., 2012).
Tropical lakes. In contrast to colder lakes, the correlation
between phytoplankton biomass and bacterial biomass
appears to be much weaker in (sub)tropical lakes (Roland
et al., 2010). Bacterial abundance in deep tropical African
Lake Kivu and Lake Tanganyika was constant throughout
the year, whereas chlorophyll awas strongly seasonal
with the alternation of dry and wet seasons (Sarmento
et al., 2008). This difference may reflect a larger influence
of terrestrial, allochthonous carbon subsidies in tropical
lakes due to impacts of flooding or it may reflect higher
abundances of small heterotrophs such as flagellates and
ciliates due to the absence of large-bodied zooplankton
(Roland et al., 2010).
A comparison of ciliate dynamics in 20 subtropical
lakes with varying trophic states found that seasonal
patterns were modified by trophic state: oligotrophic and
mesotrophic systems had ciliate biomass peaks in fall,
whereas eutrophic and hypertrophic systems showed
biomass maxima during summer (Beaver & Crisman,
1990). Compared to their high-latitude counterparts, low-
and mid-latitude lakes often maintain a higher abundance
of smaller zooplankton, including rotifers, ciliates and
nanoflagellates, resulting in a higher degree of bacterivory
(Crisman & Beaver, 1990; Jeppesen et al., 2007). This
higher productivity may be because higher temperatures
and the longer growing season allow sustained produc-
tivity or because of higher fish predation on large-bodied
zooplankton (Roland et al., 2010; Havens & Beaver, 2011).
Parasites
Parasites (including viruses and fungi) are often missing
links in (aquatic) food webs (Lafferty et al., 2008) and can,
for instance through parasitising otherwise inedible large
phytoplankton, unlock nutrients that would otherwise be
unavailable for grazers (Kagami, Helmsing & van Donk,
2011). As the abundance of parasites is hard to quantify,
their occurrence is often underestimated (Lefe
`vre et al.,
2008). Parasitism is argued to be a more common life
strategy than traditional predation (Lafferty et al., 2008),
and parasites are suggested to exert a comparable or even
stronger influence on the wax and wane of their (plank-
tonic) host than other consumers (Gerla et al., 2012).
Compelling evidence from humans and wildlife shows
that seasonal variation in temperature, precipitation and
sunlight can cause changes in parasite abundance through
determining seasonality in host abundance and host
immunity to infection (Altizer et al., 2006). The projected
climate change–induced prolongation of the growing
season for parasites may increase the potential for
faster generation cycles and year-round transmission
10 L. N. De Senerpont Domis et al.
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(Marcogliese, 2001); however, such year-round transmis-
sion does not necessarily result in higher overall parasite
abundances. Effects of increasing temperature on host–
parasite interactions may generally cause faster parasite
population growth and earlier maturation but also
increased mortality of transmission stages (Marcogliese,
2001). Differential responses to temperature change of
host and parasite may lead to a mismatch in life-cycle time
between hosts and parasites (Lafferty, 2009) and to
asynchrony between hosts and parasite phenology, dis-
tribution and abundances in a changing climate (Marco-
gliese, 2001; Parmesan, 2006).
Polar lakes and ponds. While only few studies are available
on seasonality of parasites in these extreme habitats,
existing data reveal the importance of the viral loop for
the carbon cycle in polar lakes and ponds (Laybourn-
Parry, Hofer & Sommaruga, 2001). The viral loop makes
particulate organic carbon and nutrients available again
for the production of new bacterial populations through
virus-induced lysis of bacteria (see Sawstrom et al., 2007).
In polar lakes and ponds, viruses seem to be particularly
important during the winter months as more than 60%of
the carbon supplied to the DOC pool originates from viral
lysis, even though bacterial abundance is lowest in winter.
In contrast, during the summer months, <20%of DOC
originates from viral lysis; grazers likely play a bigger role
(Sawstrom et al., 2007). As mentioned in the previous
section, the role of these bacterivores might even become
larger with warmer temperatures.
Temperate lakes. Seasonality in the occurrences and impacts
of microparasites on host populations and nutrient cycling
is well documented: viruses have population maxima in
late summer to autumn and minima in winter (Wommack
& Colwell, 2000). This pattern is likely to be a density-
dependent response to summer increases in phytoplank-
ton and bacterioplankton populations, with increases in
chlorophyll aand bacterial populations preceding
increases in viral populations (Wommack & Colwell,
2000). Parasitic fungi, such as chytrids, can also be an
important factor in controlling plankton seasonal succes-
sion in temperate lakes (Van Donk & Ringelberg, 1983;
Kagami et al., 2007). Many chytrids show a distinct
seasonality with maxima in late winter ⁄early spring (Van
Donk & Ringelberg, 1983; Johnson et al., 2006) that reach
densities sufficient to regulate and even terminate peaks in
the planktonic host abundance. Such strong seasonal
patterns may be brought about by the seasonality of the
host populations, but parasites also directly respond to
external environmental conditions (Gsell et al., 2012). This
is illustrated in the diatom host – chytrid parasite system of
Asterionella formosa – Zygorhizidium planktonicum where
warmer temperatures result in a constant infection of the
host population, preventing the build-up of host blooms
(Ibelings et al., 2011). In the Daphnia–Metschnikow-
ia–bluegill system (Hall et al., 2006), warmer temperatures
need not lead to higher prevalence, as higher temperature
allows stronger predation on infected Daphnia by bluegill
sunfish.
Tropical lakes. Few studies have examined the effects of
climate on plankton–parasite dynamics in tropical lakes,
but most studies to date support the expected picture of
host density-dependent parasite dynamics. In an Amazo-
nian floodplain lake, close coupling of viral and bacterial
abundances as well as a low virus ⁄bacterium ratio
suggests that viral abundance in this system tends to be
driven by the reduction of hosts for viral infection (Barros
et al., 2010). Overall, the authors argued that, while
viruses are strongly controlled by host abundances in
this system, bacteria are regulated both by predation
losses and by physical processes associated with turbidity,
which affects the underwater light distribution and
dissolved organic carbon availability (Barros et al., 2010).
In another example, the bacterium that induces cholera,
Vibrio cholerae, is associated with warm conditions and
with high abundances of chitinous plankton such as
copepods and cladocerans (Huq et al., 1983). Indeed, its
abundance has been observed to follow copepod seasonal
populations, which in turn again follow their prey
populations (Colwell, 1996).
Synthesis and implications
Our climate is changing; however, the (projected) rate and
impact of this change depends on region and season.
Areas exposed to a strong sinusoidal annual cycle in tem-
perature (temperate and polar regions) will be exposed to
stronger relative increases in temperature. In these higher-
latitude areas, the anticipated warming will extend the
growing season (Fig. 2, upper left and right). Higher run-
off in summer (polar regions) and winter (temperate
regions) will most likely increase the overall external
loading of nutrients; furthermore, in shallow systems,
warmer temperatures may also increase internal nutrient
loading. The projected higher incidence of heat waves in
temperate systems will intensify thermal stratification.
In subtropical systems (Fig. 2, lower right), drier sum-
mers will increase water residence times and increased
evapotranspiration will result in more saline waters
(Beklioglu et al., 2007). The intensification of precipitation
Plankton dynamics under different climatic conditions 11
2012 Blackwell Publishing Ltd, Freshwater Biology, doi:10.1111/fwb.12053

events will have stronger consequences for hydrology-
driven systems, characteristic of some tropical areas
(Fig. 2, lower left). In these systems, increased incidence
of flooding events will lead to elevated washout.
Our comparison of plankton dynamics under different
climatic conditions suggests that the consequences of
these changing climates for plankton dynamics are to a
large extent system specific and depend on characteris-
tics such as food-web topology, trophic state, lake
morphometry and catchment area. Some of these char-
acteristics show a strong relationship with geographical
location and latitude, thus obscuring or even confound-
ing our comparison. Other non-climate-related factors,
such as day length, covary with latitude and have a
strong effect on both phytoplankton and zooplankton.
This further complicates prediction of climate-related
forcing of plankton dynamics. Stochasticity in species
composition adds another complicating factor in predict-
ing plankton succession, although time-series analyses
such as those of Bauer, Sommer & Gaedke, (2012)
suggest that internal feedback mechanisms will make
spring development of plankton succession in temperate
systems more predictable.
We took the conceptual PEG model (Sommer et al.,
1986) as a starting point for framing our review. A recent
update of the PEG model with the newest scientific
insights (Sommer et al., 2012) gives a more nuanced view
of plankton succession, although the core patterns of the
original PEG model still hold. Seasonality of bacteria
seems to be more muted than phyto- or zooplankton, but
a significant correlation exists between microbial and
phytoplankton dynamics, especially in colder lakes. In
warmer lakes, and with future warming, a greater influx
of allochthonous carbon may obscure the association
between phytoplankton and bacteria. Existing data show
that parasites can strongly control plankton succession,
Fig. 2 Increased temperature as an important climate stressor leading to higher evapotranspiration in all climate regions (polar to tropics), more
precipitation in all regions except subtropical areas and, consequently, more run-off except in the subtropical areas where evapoconcentration
leads to salinisation (lower left panel). Expected effects in polar regions are shorter ice cover, thawing of permafrost, fewer glaciers, but more
melt water, summer run-off, a longer growing season, potentially more nutrient release from sediments and more resident water birds (upper
left panel); in temperate waters, intensified stratification is expected, more summer heat waves and heavy summer storms (upper right panel),
while more storms are also expected in the tropics (lower right panel).
12 L. N. De Senerpont Domis et al.
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but limitation of available data constrains our potential to
generalise.
Despite the difficulties that complicating factors present
for predicting plankton dynamics under different climatic
conditions, some general patterns based on lake experi-
ments, mesocosm experiments and field observations
emerge (Fig. 3). Importantly, the patterns depicted in
Fig. 3 are stylised and need to be further elaborated. In
general, we propose that the indirect consequences of
warmer climates will exceed the direct effects of warmer
temperatures on vital rates.
In polar systems, warming-induced lengthening of the
growing season may lead to higher and prolonged
phytoplankton productivity (Fig. 3, upper panel). In
addition, increased nutrient input in these predominantly
oligotrophic waters will lead to higher phytoplankton
biomass. For systems without high predation pressure on
zooplankton, this higher algal food availability will result
in higher zooplankton productivity and abundance
(Fig. 3, upper panel).
In temperate systems, the response of the plankton to
climate change is seen to depend strongly on the trophic
state of the system (Fig. 3, middle panel), with two biomass
peaks – in spring and summer – in oligotrophic systems,
but a lengthier and larger biomass peak in more eutrophic
systems. With anticipated increases in external loading
(precipitation) and internal loading (warming) of nutrients,
a shift from two biomass peaks to a single biomass peak
with associated higher populations of zooplanktivorous
fish seems more likely in the temperate region. Increased
water column stability and nutrient loading with climate
change may likely intensify the frequency and duration of
nuisance phytoplankton blooms in temperate lakes;
whether trophic uncoupling will occur is likely to be lake
system specific (Wagner et al., 2012).
In warmer low-latitude systems, high grazing pressure
by fish on large-bodied zooplankton may shift the
zooplankton community towards small-bodied zooplank-
ton, such as rotifers, ciliates and small cladocerans. In
areas with projected decreases in precipitation, such as the
Mediterranean lakes, decreases in flushing rates may
increase the dominance of cyanobacteria (Romo et al.,
2012; Segura et al., 2012). We propose that climate pres-
sures on these semi-arid to arid shallow systems are likely
strong (salinisation, increased nutrient loading, high
water residence times), and the need for more data on
these understudied systems is therefore urgent. In tropical
systems where temporal variability in precipitation inten-
Fig. 3 Generalised seasonal development of current (blue area) and future (red solid line) phytoplankton biomass in polar lakes (upper panel),
temperate lakes of different trophic states (middle panel) and tropical systems (lower panel). The generalised expected zooplankton biomass in
current and future climate scenarios is indicated by dark blue and brown dotted lines.
Plankton dynamics under different climatic conditions 13
2012 Blackwell Publishing Ltd, Freshwater Biology, doi:10.1111/fwb.12053

sity is an important driver in plankton dynamics, we
suggest that the anticipated increases in precipitation
intensity will result in resetting the seasonal dynamics of
plankton communities, selecting for species adapted to
highly variable environments (Fig. 3, lower panel). In
these systems, the existing intense predation by fish on
large-bodied zooplankton may increase further, resulting
in a perennially low zooplankton biomass.
Our review aimed at outlining some general predictions
on plankton dynamics under different climatic conditions
now and in the future. With warming, a general picture
emerges of increases in bacterivory, greater cyanobacterial
dominance and smaller-bodied zooplankton that is more
heavily impacted by fish predation. Our picture reflects
gross biomass changes in trophic groups; however, spe-
cies-specific differences in response to anticipated climate
changes could have a strong impact on aquatic food webs
in which a key role is reserved to single species. Typically,
freshwater food webs are characterised by a high degree of
redundancy and trophic generalism, indicating a high
degree of functional similarity among species, with a small
proportion of species exerting disproportionally strong
effects on lake ecosystem functioning (Woodward, 2009).
In these cases, differential responses to the anticipated
changes in climate between species might weaken or
intensify the match between trophic groups. Sublethal
warming of ectotherm herbivores, for instance zooplank-
ton, can potentially strengthen top-down control, resulting
in a more intense match (O’Connor, 2009), although
enhanced top-down control by fish and higher degree of
fish omnivory (Gonza
´lez-Bergonzoni et al., 2012) may alter
such relationships. Importantly, indirect effects of climate
change, for example, through increases in nutrient loading
and changes in stratification pattern may be more impor-
tant than the direct effects of temperature on vital rates,
especially for phytoplankton.
Acknowledgments
LdSD was supported by grant 817.01.007 from The Neth-
erlands Organization for Scientific Research (NWO). EJ
was supported by the EU-WISER and EU-REFRESH
projects, CLEAR (a Villum Kann Rasmussen Centre of
Excellence Project), CRES and The Research Council for
Nature and Universe (272-08-0406). We want to thank the
participants of the KNAW-colloquium ‘Plankton predict-
ability in an unpredictable world’ in Amsterdam, 2010, for
the fruitful discussions which in part led to the present
paper. This is publication 5360 of the Netherlands Insti-
tute of Ecology (NIOO-KNAW).
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