Responses of cyanobacteria to herbivorous zooplanktonacross predator regimes: who mows the bloom?

PABLO URRUTIA-CORDERO* ,† , MATTIAS K. EKVALL* AND LARS-ANDERS HANSSON*

*Department of Biology, Lund University, Lund, Sweden†Center for Environmental and Climate Research, Lund University, Lund, Sweden

SUMMARY

1. The massive growth of large, toxic cyanobacteria in eutrophic waters has traditionally been

explained by their evolution of defences to herbivorous zooplankton. These conclusions come mostly

from studies using the large-bodied cladoceran Daphnia as a grazer model. In contrast, very little is

known about the effects of other zooplankters such as copepods and small cladocerans that, unlike

Daphnia, often coexist with cyanobacterial blooms and under high levels of fish predation.

2. We performed a series of grazing experiments during a cyanobacterial bloom in a eutrophic lake,

subject to decreasing predation on zooplankton (removal of cyprinid fish). We also used long-term

observational data to analyse the response of cyanobacteria to changes in abundance, body size and

biomass of the naturally, coexisting zooplankton community across different predator regimes.

3. A natural grazer community, dominated by selective herbivores like calanoid and cyclopoid cope-

pods, positively affected cyanobacterial growth in early summer at low cyanobacterial densities.

However, cyclopoid copepods and small cladocerans suppressed the growth of Anabaena, Microcystis

and Planktothrix species under bloom conditions in late summer, with the exception of the highly

toxic Microcystis botrys.

4. Long-term observational data support the results from the grazing experiments regarding the

potential capacity of the natural zooplankton community to suppress cyanobacterial growth, espe-

cially of the dominant taxon Microcystis (including the most toxic species, M. botrys). In particular,

these results suggest that direct grazing may contribute significantly to the observed 72% decrease in

Microcystis biomass through a 111% increase in abundance of cyclopoid copepods, and an 18%

increase in body size of cyclopoid copepods and a 31% increase in body size of the generalist feeder

Daphnia, during the biomanipulation.

5. Together, these results suggest that, within the complex interactions brought about by trophic cas-

cades, direct grazing by the coexisting zooplankton community is a strong driver regulating cyano-

bacterial growth in eutrophic lakes and that this can display contrasting effects, both seasonally and

under different levels of fish predation. Importantly, we show that herbivory may be enhanced along

a gradient of decreasing fish predation by the combined action of copepods (selective herbivores)

and Daphnia (generalist herbivores).

Keywords: copepods, cyanobacteria, herbivory, predation, zooplankton

Introduction

Massive proliferations or ‘blooms’ of potentially toxic

cyanobacteria are common in eutrophic waterbodies and

have been associated with the evolution by these cyano-

bacteria of defences against herbivorous zooplankton

(Hansson et al., 2007a, 2013; Chislock et al., 2013a). The

large size and specific morphology (single cells aggre-

gated in filaments or colonies) of cyanobacteria may

provide resistance against herbivorous zooplankton

(Wilson, Sarnelle & Tillmanns, 2006). In addition, cyano-

bacteria may also produce toxic metabolites and possess

Correspondence: Pablo Urrutia-Cordero, Department of Biology, Lund University, Ecology building, SE-223 62 Lund, Sweden.

E-mail: pablo.urrutia_cordero@biol.lu.se

960 © 2015 John Wiley & Sons Ltd

Freshwater Biology (2015) 60, 960–972 doi:10.1111/fwb.12555

low nutritional values reducing the growth and fitness

of herbivore communities (Brett & Muller-Navarra, 1997;

Hansson et al., 2007a; Urrutia-Cordero et al., 2013).

The understanding of zooplankton–cyanobacteria

interactions has mainly been obtained from laboratory

and field studies with the generalist cladoceran grazer

Daphnia (Wilson et al., 2006; Chislock et al., 2013a; Ger,

Hansson & L€urling, 2014). However, fish predation on

zooplankton is generally intense in eutrophic waters and

smaller-bodied zooplankton, such as copepods and

small cladocerans, tend to dominate plankton communi-

ties in these ecosystems (Jeppesen et al., 2000). Of spe-

cific interest is the impact of selective herbivores like

copepods, which have shown contrasting effects on

cyanobacterial growth depending on cyanobacterial tox-

icity or presence of alternative food in laboratory sys-

tems (Kurmayer & Juttner, 1999; Ger et al., 2010; Ger,

Panosso & Lurling, 2011), but for which evidence under

natural conditions is still lacking (Ger, Hansson &

L€urling, 2014). Therefore, focusing solely on Daphnia is

an over-generalisation that ignores the most common

zooplankton–cyanobacteria interactions and hinders pre-

dictions about bloom dynamics in natural environments

(Ger, Hansson & L€urling, 2014).

There is mounting evidence that increased herbivore

pressure on cyanobacteria, via changes in zooplankton

community structure (abundance or size spectrum), can

be achieved through alterations at higher trophic levels,

by the deliberate removal of planktivorous fish, enhance-

ment of piscivorous communities or natural massive

‘fish kills’ (Shapiro, Lamarra & Lynch, 1975; Hansson

et al., 1998). The effects of such trophic cascades seem to

depend greatly on the recovery of large-bodied Daphnia,

which have higher grazing rates and feed on a wider

size range of algae than smaller-bodied zooplankters

(Burns, 1968; Lacerot et al., 2013). However, still very lit-

tle is known about the potential impact of top-down

forces on phytoplankton communities through control of

different herbivore traits of other zooplankton communi-

ties that typically coexist with cyanobacterial blooms

(Hansson et al., 1998; Ger, Hansson & L€urling, 2014).

Similarly, only few studies have focused on sufficiently

extensive periods to assess zooplankton–cyanobacteria

interactions throughout the entire duration of cyanobac-

terial blooms (Ger, Hansson & L€urling, 2014).

We performed a series of grazing experiments to

quantify the seasonal response of cyanobacteria to graz-

ing by the naturally occurring herbivore community in a

eutrophic lake, subject to long-term fish removal (bioma-

nipulation). These experimental data were combined

with a long-term observational data set to investigate

the impact of herbivorous zooplankton on cyanobacterial

blooms across different levels of fish predation. The

effects of trophic cascades on plankton communities are

complex and system-dependent (Carpenter et al., 2011),

but to disentangle the relative contribution of other driv-

ers from the impacts of direct grazing on cyanobacteria

is beyond the scope of this study. Instead, we here focus

on evaluating whether (1) the grazing impacts of the

naturally occurring zooplankton community on cyano-

bacterial growth differ seasonally at different phyto-

plankton and zooplankton community structures, (2)

whether alterations at higher trophic levels (cyprinid fish

removal) may influence cyanobacterial bloom dynamics

by altering critical herbivore traits of the coexisting zoo-

plankton community (abundance, body size and bio-

mass) and, finally (3), whether results from experimental

tests performed under natural conditions are consistent

with long-term field observations.

Methods

Study site and lake monitoring

Lake Ringsj€on is a eutrophic lake consisting of three con-

nected basins located in Scania, southern Sweden. The

lake became eutrophic in the 1960s and 1970s, since

when there have been regular blooms of potentially

toxic cyanobacterial taxa such as Anabaena, Aphanizome-

non, Microcystis and Planktothrix (Cronberg, Annadotter

& Lawton, 1999). Since the beginning of the 1980s, a

strong control of the external input of nutrients has been

applied, reducing phosphorus loading from more than

30 tonnes to 5–10 tonnes per year. Additionally, since

2005, the lake has been subject to higher trophic level

manipulations in the form of removal of cyprinid fish,

mainly targeting roach (Rutilus rutilus) and bream (Abr-

amis brama). Therefore, chemical variables (phosphorus,

nitrogen, chlorophyll-a and Secchi depth) and major

zooplankton and cyanoabcterial taxa have been moni-

tored since 2000 in the western basin of Lake Rinsgsj€on

(Table 1; see more about the biomanipulation pro-

gramme at the website: http://www.ringsjon.se).

Grazing experiments

Three grazing experiments were performed in the wes-

tern basin of Lake Ringsj€on in June, July and August

2012. These experiments were based on the standard

method described by Lehman & Sandgren (1985), which

has subsequently been used by many others in both field

and laboratory experiments (Bergquist & Carpenter,

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

Zooplankton herbivory on cyanobacteria 961

1986; Vanni & Temte, 1990; Hansson, 1996; Hansson

et al., 2007b; Lebret et al., 2012). This method is similar

to a serial dilution study commonly used to quantify

zooplankton grazing (Landry & Hassett, 1982). Each

experiment was performed in six 10-L transparent plas-

tic containers, which were previously acid-washed with

a 10% HCL solution. The containers were sealed and

were placed 1 m apart in line in the surface water of the

lake using weights, ropes and buoys. There was no

source of nutrients entering or leaving the containers,

which were equally exposed to the same natural temper-

ature and light climate as in the lake.

The six 10-L plastic containers were filled with 9 L of

filtered (150-lm mesh) lake water, containing the natural

phytoplankton community in the lake without grazers

larger than 150 lm in body size (Table 2). The zooplank-

ton collected on the 150-lm mesh were pooled into a

bucket and subsequently added to the six containers to

create a natural grazer gradient of 0.25, 0.5, 1, 2, 4 and 6

times the amount of zooplankton in the lake (Table 2).

The amount of phytoplankton larger than 150 lmretained on the mesh was negligible, so the methods

used did not entail major changes between the phyto-

plankton community structure in the lake and in the

containers. This then allowed the study of algal growth

responses to grazing by creating a non-replicated gradi-

ent of zooplankton biomass. Although the 150-lm mesh

does not remove grazers smaller than 150 lm, their

abundances remained the same across all the enclosures

and changes in algal net growth rates can therefore only

be attributed to the presence of grazers lager than

150 lm. The containers were incubated for 72 h in the

lake to allow changes in phytoplankton community com-

position, while zooplankton biomass remained similar

and effects from the enclosures were minimal.

Phytoplankton samples were taken before and after

72 h of incubation in the lake according to Lehman &

Sandgren (1985). Zooplankton samples at the end of the

experiment were taken by filtering the entire volume of

the containers through a 150-lm mesh. All plankton

samples were immediately fixed in Lugol’s solution and

stored in a controlled temperature room at 4°C. Cyano-

bacteria (class, genus and species level of taxonomic res-

olution), total green algae and diatoms were counted on

a Olympus CK40 (LRI, Lund, Sweden) inverted micro-

scope, and biomasses were estimated according to Ekv-

all et al. (2013). The maximum length of filaments and

the spherical diameter of colonies were used as proxies

to express the size of each cyanobacterial species. The

abundance of zooplankton taxa (cyclopoid and calanoid

copepods, excluding nauplii; Daphnia; and small cladoc-

erans: mainly Bosmina and Chydorus), was determined

using a stereoscopic microscope (Olympus SZ40) at 920

magnification, and biomasses were estimated using

length–weight regressions according to Dumont, Van-

develde & Dumont (1975) and Bottrell et al. (1976).

Algal responses to grazing were determined by linear

regression analyses (F-test, one-tailed, n = 6) with net

growth rate (r) as the dependent variable (y-axis) and

the fixed increase of zooplankton biomass as the inde-

pendent variable (x-axis) according to Lehman & Sand-

gren (1985). Owing to the seasonal changes in

zooplankton abundances in the lake, this led to different

gradients of zooplankton biomass in each of the experi-

ments (June, July and August). This allowed mimicking

of the natural plankton succession in the lake and inte-

gration of these natural changes into the strength of the

regression analyses for each of the experiments. Net

growth rates (r) were calculated as r = ln(Nt/N0)/Δt,

where N0 and Nt express the biomass (mg L�1) at the

beginning and after the end of the 72-h incubations (rep-

resented by Δt). Since zooplankton can cause negative

(direct grazing) and positive (nutrient recycling) impacts

on the algal community, this method reveals the net

effect of these two (and other) processes on the growth

of each phytoplankton taxon. Thus, negative slopes indi-

cate that algal mortality caused by zooplankton grazing

was greater than any positive effect, and positive slopes

Table 1 Morphological and chemical characteristics of the western

basin of Lake Rinsgj€on. Numbers in brackets are of overall values

for Lake Rinsgj€on including all three basins. Chemical variables are

shown for the period of high fish abundance (2000–2004) and low

fish abundance (2005–2011) created by biomanipulation starting in

2005. Values represent summer means (�SD) including June, July

and August of each assessed year. Bold type indicates significant

differences between the two predator regimes (P < 0.05; Student0st-test, unpaired, one-tailed)

Parameters (unit) Ringsj€on western basin

Morphological

Mean depth (m) 3.1

Maximum depth (m) 5.4

Surface area (km2) 14.8 (40.0)

Catchment area (km2) 24.7 (347.0)

Total volume (mm3) 46.6 (184.2)

Retention time

(years; 1984–1993)0.3 (1.0)

Chemical High fish

abundance

(2000–2004)

Low fish

abundance

(2005–2011)

TP (lg L�1) 97 � 19 69 � 14

TN (lg L�1) 1540 � 221 1250 � 141

Chl-a (lg L�1) 64 � 28 49 � 13

Secchi depth (cm) 71 � 14 91 � 17

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

962 P. Urrutia-Cordero et al.

indicate that the positive effect from the presence of

grazers compensates for algal mortalities. The slope of

this regression also provides an estimate of the filtering

rate on each algal species (mg algae filtered per lg zoo-

plankton per day). Grazing scores were estimated across

the three grazing experiments to indicate the consistency

and direction of the responses of each phytoplankton

taxon to the natural zooplankton assemblage, calculated

by summation of positive significant (P < 0.05) slopes

(+1), negative significant (P < 0.05) slopes (�1) and no

significant (P > 0.05) relationships (0).

Long-term field study

We investigated the impact of different predator

regimes on the abundance, body size and biomass of

major zooplankton taxa (cyclopoid and calanoid cope-

pods, excluding nauplii; Daphnia; small cladocerans:

mainly Bosmina and Chydorus). Similarly, we studied

changes in biomass of the dominant phytoplankton

groups, that is total cyanobacteria, green algae and dia-

toms, as well as major cyanobacterial taxa (Anabaena,

Aphanizomenon, Planktothrix, Microcystis and dominant

Microcystis species). This was performed by comparing

the period prior to (hereafter named ‘high fish abun-

dance’) and after (hereafter named ‘low fish abundance’)

the start of the biomanipulation in 2005 using an inde-

pendent Student’s t-test (unpaired, one-tailed). Given

the absence of targeted taxa in distinct months of the

monitoring data, we used summer means (June, July

and August) of each year over the period 2000–2011 as

replicates for the analyses. Furthermore, we used the

same data set to investigate the effects of changing zoo-

plankton abundance, body size and biomass, on the bio-

mass of major cyanobacterial taxa (Anabaena,

Aphanizomenon, Microcystis and Planktothrix) through lin-

ear regression analyses (F-test, one-tailed, n = 11).

Counts and biomasses of cyanobacterial and zooplank-

ton taxa were obtained using the methods described

above for the grazing experiments. No monitoring data

were available for 2002 or 2012, and these years were

therefore excluded from the analyses.

Table 2 Zooplankton and cyanobacterial commu-

nities used in the grazing experiments (T0), and

representative of the seasonal community dynam-

ics in Lake Rinsgj€on in 2012. Means (� SD) sizes

and size ranges of zooplankton and cyanobacterial

taxa (n = 30 individuals) are represented by ‘maxi-

mum linear dimensions’ (maximum length of fila-

ments and spherical diameter of colonies) across

the three grazing experiments in June, July and

August. Note that only dominant cyanobacteria

are shown at species level

Biomasses of

zooplankton (lg L�1)

and phytoplankton

taxa (mg L�1)Mean size (lm)

Size range

(lm)

June July August

June–July–August

June–July–August

Zooplankton taxa

Calanoida 33.6 0.2 10.2 638 � 110 390–1274Cyclopoida 31.0 7.9 89.5 598 � 24 359–910Daphnia 15.6 0.3 14.0 585 � 15 306–1107Small cladocerans

(Bosmina and Chydorus)

5.1 9.5 90.2 289 � 4 182–650

Total zooplankton 85.3 17.9 203.9 � �Phytoplankton taxa

Species

Anabaena crassa 0.83 7.19 1.83 70 � 7 20–205Anabaena flos-aquae 0.02 0.11 0.07 43 � 9 15–125Anabaena lemmermanii 0.02 0.08 0.02 44 � 8 20–100Aphanizomenon gracile 0.01 0.11 1.24 110 � 41 10–310Aphanizomenon klebahnii 0.01 0.38 0.80 102 � 6 37–265Microcystis botrys 0.13 0.07 0.19 105 � 8 50–260Microcystis viridis 0.37 0.35 0.94 101 � 7 25–250Microcystis wesenbergii 0.14 0.13 0.59 83 � 11 25–260Planktothrix agardhii 0.01 0.09 2.28 278 � 59 15–655

Genera

Anabaena 0.89 7.90 2.01 � �Aphanizomenon 0.02 0.49 2.04 � �Microcystis 0.65 0.57 1.77 � �Planktothrix 0.01 0.09 2.28 � �Classes

Total cyanobacteria 1.72 11.82 10.40 � �Total green algae 2.59 0.13 0.25 � �Total diatoms 0.51 0.55 4.41 � �

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

Zooplankton herbivory on cyanobacteria 963

Results

Lake zooplankton and phytoplankton community used in

the grazing experiments

Total biomass of the natural grazer community decreased

considerably from June to July, but recovered in August

reaching a value of above 200 lg L�1 (Table 2). In June,

calanoid and cyclopoid copepods were the dominant

taxa, constituting 39 and 36% of the total zooplankton

biomass, respectively (Table 2). However, while cala-

noids were nearly absent in July and August (1–5%),

cyclopoids comprised around 50% of the total zooplank-

ton biomass, thereby dominating together with small cla-

docerans (Table 2). Daphnia only reached relevant

numbers in June (18%), and abundances were low in July

and August (1–7%) (Table 2). Average body size of the

zooplankton community remained nearly constant

among cyclopoids, Daphnia and small cladocerans from

June to August, but calanoid copepods showed high vari-

ation between months (Table 2). Calanoid copepods were

the largest zooplankters present in the zooplankton com-

munity followed by Daphnia and cyclopoid copepods,

and further by the small cladocerans (Table 2).

Cyanobacteria were scarce in June with a community

dominated by Anabaena and Microcystis, when other

algal competitors, such as green algae and diatoms, were

together present in higher abundances (Table 2). How-

ever, cyanobacteria increased dramatically in July, domi-

nated by the species Anabaena crassa (Table 2), whereas

green algae and diatoms decreased considerably

(Table 2). In August, the cyanobacterial community was

more diverse with Anabaena, Aphanizomenon, Microcystis

and Planktothrix together constituting more than 75% of

the total cyanobacterial biomass (Table 2). The average

size of most cyanobacterial species showed little varia-

tion among months, except for Aphanizomenon gracile

and Planktothrix agardhii (Table 2). However, more varia-

tion was found among species belonging to the same

genus, with the filamentous forms Anabaena flos-aquae

and A. lemmermanii generally smaller than A. crassa

(Table 2). Of the filamentous forms, the species Plankto-

thrix agardhii showed the greatest average length of fila-

ments (Table 2). The colonial cyanobacterium Microcystis

showed little size variation among the three represented

species M. viridis, M. wesenbergii and M. botrys (Table 2).

Grazing experiments

In June, the natural grazer community only affected neg-

atively the net growth rate of Anabaena flos-aquae and

total diatoms (Table 3), while Anabaena crassa, Plankto-

thrix agardhii and Microcystis botrys, together with the

total Microcystis, Planktothrix and cyanobacterial biomass,

showed a positive growth response to increasing grazer

biomass (Fig. 1, Table 3). In July, the growth rate of An-

abaena crassa was also affected positively, while the total

Microcystis biomass and green algae showed a signifi-

cant, negative response to the natural grazer community

(Fig. 1, Table 3). In August, the natural grazers were

able to significantly suppress the net growth rate of

Anabaena crassa, Microcystis viridis, Microcystis wesenbergii

and Planktothrix agardhii, together with the total biomass

of Anabaena, Microcystis, Planktothrix, green algae and

diatoms (Fig. 1, Table 3). As in June, the natural grazer

community stimulated the growth of M. botrys in

August, which was thereby the taxon least vulnerable to

grazing with an overall grazing score of +2 (Table 3).

Long-term field study

In contrast to calanoid copepods (Fig. 2a, b, c), both the

abundance and body size of cyclopoid copepods were

larger under the lower predation regime (Fig. 2a, b).

This led to a drastic increase in cyclopoid copepod bio-

mass during the period of lower predation pressure

(Fig. 2c). Similarly, the size of Daphnia (mostly repre-

sented by Daphnia cucullata) in the lake increased signifi-

cantly (Fig. 2b), although no changes in biomass were

observed due to a slight tendency to decrease in abun-

dance (Fig. 2a, c). The abundance of small cladocerans

was higher under the lower predation regime, although

no changes were observed in body size or biomass

(Fig. 2a, b, c).

Total cyanobacteria decreased considerably during the

period of lower predation pressure (Fig. 2d), while no

changes were observed in green algae and diatoms, the

other most prominent phytoplankton groups in the lake

(Fig. 2d). Although the biomasses of Anabaena, Aphani-

zomenon and Planktothrix did not differ between the two

periods (Fig. 2e), the start of biomanipulation brought

about a drastic decrease in Microcystis biomass (Fig. 2e).

All the three dominant Microcystis species (M. viridis,

M. wesenbergii and M. botrys) showed a highly significant

decrease in biomass under the lower fish predation

regime (Fig. 2e).

Linear regression analyses revealed a negative

response of Microcystis growth to the increase in body

size of cyclopoids (nearly significant, P = 0.056) and,

accordingly, in their biomass (Fig. 3b). No significant

relationship was found between Daphnia abundance and

the biomass of Microcystis (Fig. 3c). Similar to the

response to cyclopoid copepods, Microcystis showed a

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

964 P. Urrutia-Cordero et al.

Table

3Responsesofcyan

obacteriaat

differentlevelsoftaxonomic

resolution(species,

gen

era,

classes),totaldiatomsan

dgreen

algae

tozo

oplanktongrazingin

each

oftheexperi-

men

tsperform

edin

June,

July

andAugust.Bold

typeasterisks(*)an

ddouble

asterisks(**)

show

significant(P

<0.05

andP<0.01,resp

ectively)linearregressionan

alyses(y-axis:

net

algal

growth

rate,x-axis:zo

oplanktonbiomass;

n=6).Grazingscoresindicatetheconsisten

cyan

ddirectionoftheresp

onsesofcyan

obacteriato

thenaturalzo

oplanktoncommu-

nityacross

allexperim

ents,calculatedas

thesu

mofpositivesignificant(P

<0.05)slopes

(+1),neg

ativesignificantslopes

(�1)

andnosignificantrelationsh

ips(0),resp

ectively.Neg

a-

tiveslopes

andscoresindicatetaxathat

aresu

ppressed

,an

dpositiveslopes

andscorestaxathat

overallben

efitfrom

thegrazerpresence.NS=notsignificantrelationsh

ip

Grazing

score

June

July

August

R2

F-

value

(1,4)

Equation

P-

value

Direction

R2

F-

value

(1,4)

Equation

P-

value

Direction

R2

F-

value

(1,4)

Equation

P-

value

Direction

Species

A.crassa

0.66

7.90

Y=0.00

04*X

+0.08

91

0.024*

+0.55

4.94

Y=0.00

30*X

�0.33

05

0.045*

+0.64

7.22

Y=�0

.000

1*X

+0.13

38

0.028*

�1

A.flos-aqu

ae0.54

4.76

Y=�0

.000

6*X

+0.19

68

0.048*

�0.19

0.96

NS

0.19

1�

0.16

0.76

NS

0.21

7+

�1

A.lemmermanii

0.46

3.41

NS

0.07

0+

0.03

0.14

NS

0.36

2�

0.02

0.08

NS

0.39

3�

0

Aph

.gracile

0.26

1.45

NS

0.14

8�

0.05

0.19

NS

0.34

2�

0.15

0.69

NS

0.22

7�

0

Aph

.klebanhii

0.50

4.02

NS

0.05

8+

0.01

0.02

NS

0.44

6+

0.05

0.22

NS

0.33

2+

0

M.botrys

0.80

16.46

Y=0.00

14*X

�0.12

03

0.008**

+0.42

2.92

NS

0.08

1+

0.82

18.90

Y=0.00

08*X

�0.18

35

0.006**

+2

M.viridis

0.01

0.04

NS

0.43

0�

0.06

0.23

NS

0.32

7�

0.89

31.51

Y=�0

.000

3*X

+0.20

18

0.003**

��1

M.wesenbergii

0.46

3.43

NS

0.06

8+

0.51

4.21

NS

0.05

5�

0.70

9.16

Y=�0

.000

2*X

+0.22

77

0.020*

��1

P.agardh

ii0.66

7.89

Y=0.00

08*X

�0.07

09

0.024*

+0.29

1.61

NS

0.13

7�

0.77

13.71

Y=�0

.000

4*X

+0.25

96

0.011*

�0

Gen

era

Anabaena

0.06

0.24

NS

0.32

4+

0.43

3.05

NS

0.07

8+

0.60

6.11

Y=�0

.000

1*X

+0.11

79

0.035*

��1

Aph

anizom

enon

0.20

1.00

NS

0.18

7+

0.01

0.03

NS

0.43

4+

0.11

0.49

NS

0.26

2�

0

Microcystis

0.57

5.33

Y=0.00

04*X

�0.00

68

0.041*

+0.59

5.70

Y=�0

.001

2*X

+0.23

42

0.038*

�0.75

12.23

Y=�0

.000

1*X

+0.17

98

0.013*

��1

Planktothrix

0.66

7.89

Y=0.00

08*X

�0.07

09

0.024*

+0.29

1.61

NS

0.13

7�

0.77

13.71

Y=�0

.000

4*X

+0.25

96

0.011*

�0

Classes

Cyan

obacteria†

0.88

29.73

Y=0.00

03*X

+0.06

53

0.002**

+0.09

0.39

NS

0.28

2+

0.92

45.19

Y=�0

.000

1*X

+0.16

65

0.001**

�0

Diatoms

0.70

9.43

Y=�0

.000

4*X

�0.00

84

0.018*

�0.88

28.99

NS

0.08

2�

0.91

41.82

Y=�0

.000

2*X

+0.17

60

0.001**

��2

Green

algae

0.46

3.41

NS

0.06

8�

0.42

2.87

Y=�0

.002

6*X

+0.10

48

0.003**

�0.92

47.87

Y=�0

.000

2*X

+0.20

65

0.001**

��2

†Grazingratesontotalcyan

obacteriaad

aptedfrom

Ekvallet

al.(201

4).

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

Zooplankton herbivory on cyanobacteria 965

negative response to increasing Daphnia body size

(Fig. 3c). However, there was no significant correlation

between body sizes of cyclopoid copepods and Daphnia

(R2 = 0.01, F1,9 = 0.02, P > 0.05), which suggests that the

negative relationships between Microcystis biomass and

the body sizes of cyclopoid copepods and Daphnia were

independent of each other. No significant relationships

were found between Microcystis and either calanoid

copepods or small cladocerans (Fig. 3a, d).

Discussion

Our results show that the naturally occurring zooplank-

ton community that typically exists in nutrient-rich lakes

(Jeppesen et al., 2000; Hansson et al., 2007a) may have

contrasting effects on the growth of large-sized, poten-

tially toxic cyanobacteria, both seasonally and under dif-

ferent levels of fish predation. Our grazing experiments

show that a community dominated by selective herbi-

vores like calanoid and cyclopoid copepods may pro-

mote the growth of filamentous and colonial Anabaena,

Microcystis and Planktothrix species in early summer. In

contrast, a combination of cyclopoid copepods and small

cladocerans grazed efficiently on cyanobacteria when the

latter were present at higher densities in late summer.

The capacity of the natural grazer community to graze

efficiently on cyanobacteria is in accordance with our

long-term observations, suggesting a drastic decline in

Microcystis, the most dominant cyanobacterial taxon,

after zooplankton abundance and body size increased

following reduced fish predation. Although the mecha-

nisms through which trophic cascades may alter phyto-

plankton biomass and ecosystem functioning are

complex and not dependent on grazing alone (Carpenter

et al., 2011), our results show that direct grazing on cy-

anobacteria may be a strong driver of cyanobacterial

Fig. 1 Examples of responses of total cyanobacteria, total Microcystis and M. botrys to the natural grazer community in the grazing experi-

ments in June, July and August. Fitted regression lines (n = 6), model equations, F-values, R2 values and P-values are given for significant

relationships (P < 0.05).

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

966 P. Urrutia-Cordero et al.

growth and that this may be enhanced through the sus-

ceptibility of copepods (selective grazers) and Daphnia

(generalist grazers) to alterations in fish predation.

Unlike the effects of trophic cascades through changes

in Daphnia abundances (Hansson et al., 1998), the capac-

ity of copepods to alter cyanobacterial bloom dynamics

has hitherto been largely unexplored (Ger, Hansson &

L€urling, 2014). We have demonstrated, by taking advan-

tage of a whole-lake manipulated food chain, that a

community dominated by copepods can also signifi-

cantly suppress cyanobacterial growth.

The impact of copepod-dominated zooplankton com-

munities on cyanobacteria is still controversial (Ger,

Hansson & L€urling, 2014), showing contrasting results

with respect to bloom formation and stability (Moriarty

et al., 1973; Wang et al., 2010; Lacerot et al., 2013). The

positive growth response by cyanobacteria to the natural

grazer community in our experiments occurred at low

cyanobacterial densities in early summer, most likely

due to altered competition patterns as a result of selec-

tive grazing on other phytoplankton taxa, such as dia-

toms (cf. Wang et al., 2010). This may help to explain the

seasonal shift in phytoplankton community composition

and dominance of cyanobacteria observed from June to

July in Lake Ringsj€on (cf. Wang et al., 2010). These

responses can also be linked to the high biomass contri-

bution of calanoid copepods in the June experiment, as

those are known to avoid consuming cyanobacteria

when the supply of better quality food sources is high

(Ger et al., 2010; Ger & Panosso, 2014). In contrast, with

an advanced succession of species and at higher cyano-

bacterial densities, a community dominated by cyclo-

poid copepods and small cladocerans was able to

restrict the growth of cyanobacterial species not previ-

(a) (b) (c)

(d) (e) (f)

Fig. 2 Monitoring data for zooplankton (calanoid copepods, cyclopoid copepods, Daphnia and small cladocerans) abundance (a), size shown

as maximum length (b), biomass (c) as well as biomasses of major phytoplankton groups (d; cyanobacteria, green algae, diatoms and other

taxa), cyanobacterial genera (e; Anabaena, Aphanizomenon, Planktothrix and Microcystis) and Microcystis species (f), and comparing the periods

of high fish abundance (black bars; 2000–2004) and low fish abundance (grey bars; 2005–2011) created by biomanipulation starting in 2005

in Lake Ringsj€on. Values are for summer means (�SD) including June, July and August of each assessed year. Asterisks (*) and double

asterisks (**) show significant differences (P < 0.05 and P < 0.01, respectively; Student0s t-test, unpaired, one-tailed). Note that in a)

(cyclopoid copepods) the asterisk within parentheses denotes P = 0.053.

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

Zooplankton herbivory on cyanobacteria 967

ously grazed by the natural zooplankton community.

Although known to feed efficiently on motile planktonic

cells (Bouley & Kimmerer, 2006), raptorially feeding co-

pepods like cyclopoids can also feed efficiently on colo-

nial and filamentous cyanobacteria (Moriarty et al., 1973;

Kurmayer & Juttner, 1999). The grazing impact on

(a)

(b)

(c)

(d)

Fig. 3 Linear regression relationships between Microcystis biomass and calanoid copepods (a), cyclopoid copepods (b), Daphnia (c) and small

cladocerans (d), abundances, body sizes and biomasses throughout the period 2000–2011 in Lake Ringsj€on. Values represent summer means

(June, July and August) of each monitored year. Black circles represent years prior to the start of the biomanipulation in 2005 (high fish

abundance) and open circles the years afterwards (low fish abundance). Fitted regression lines, model equations, F-values, R2 values and

P-values are given for P-values below the 5% significance level. This information is also shown for the relationship between Microcystis

biomass and body size of cyclopoid copepods (dotted regression line) given its close level of significance (P = 0.056).

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

968 P. Urrutia-Cordero et al.

cyanobacteria by small cladocerans, such as Chydorus

and Bosmina, is weak and, in contrast to copepods, they

generally feed on food particles smaller than cyanobacte-

ria (Burns, 1968; Wilson, 1973). Nonetheless, cyclopoid

copepods are able to break down cyanobacterial colonies

or filaments into smaller pieces, which may be an indi-

rect mechanism facilitating subsequent grazing by smal-

ler cladocerans (Moriarty et al., 1973; Haney, 1987).

Altogether, our results suggest a significant grazing

impact by the naturally occurring zooplankton commu-

nity on cyanobacteria, in spite of size and morphologi-

cal-based constraints conferred by filaments and

colonies. However, direct grazing intensity can vary sea-

sonally; for example, the lack of significant grazing on

cyanobacteria in our experiments in July can be

explained by the low zooplankton abundances in the

lake, and thereby also in the experiments, most likely

resulting from the strong predation by newly hatched

0 + fish (Hansson et al., 2007b; Ekvall, Urrutia-Cordero

& Hansson, 2014). The marked differences between June

and August are, however, in accordance with optimal

foraging theory and suggest a strong opportunistic for-

aging behaviour by zooplankton on cyanobacteria in situ-

ations of low abundance of high-quality prey

(MacArthur & Pianka, 1966; DeMott & Moxter, 1991),

such as those created during high cyanobacterial prolif-

eration (in this case late summer).

In addition, our grazing experiments show unequal

grazer effects by the natural grazing community upon

different Microcystis species with similar size and form,

suggesting that chemical defences may also alter selec-

tive foraging patterns in natural environments (DeMott

& Moxter, 1991). Hence, while the natural grazers had a

negative effect on M. viridis and M. wesenbergii, the net

growth rate of M. botrys was consistently promoted.

Ekvall et al. (2013) identified the species M. botrys as a

major explanatory variable of a 300% increase in toxin

(microcystins) concentrations in a mesocosm experiment.

Additionally, in a survey of 13 waterbodies from nine

European countries, Via-Ordorika et al. (2004) found that

of the Microcystis species investigated, M. botrys repre-

sented the highest proportion (90%) of toxic subpopula-

tions – that is, colonies containing microcystins and the

gene mcy responsible for its synthesis (Tillett et al.,

2000). Microcystins are potent hepatotoxins that nega-

tively affect the growth and fitness of herbivores (Hans-

son et al., 2007a; Urrutia-Cordero et al., 2013), and

selective grazers, like copepods, have developed adap-

tive feeding strategies allowing the detection of toxic

secondary metabolites, such as microcystins (Kurmayer

& Juttner, 1999; Ger et al., 2011, 2014). Although we did

not quantify microcystins or other potential bioactive

compounds acting as grazing deterrents (Urrutia-

Cordero et al., 2013; Agha & Quesada, 2014a; Agha et al.,

2014b), our results suggest that selective feeding on

other taxa may favour the most toxic species (in this

case, M. botrys) by altered competitive patterns. These

results are consistent with observations that selective

feeding facilitates grazer coexistence with toxic cyano-

bacteria by feeding on the least toxic algal species

(DeMott & Moxter, 1991). Future studies should focus

on determining whether selective zooplankters may feed

on toxic species in oligo- or monospecific cyanobacterial

blooms, represented by only one or a few dominant

taxa, and when little alternative food is present (DeMott

& Moxter, 1991; Ger et al., 2010; Ger & Panosso, 2014).

Cyclopoid copepods were 111% more abundant and

18% larger during the period of lower fish predation in

Lake Ringsj€on, which subsequently translated into a

253% increase in body mass. Similarly, Daphnia individ-

uals increased by 31% in body size. While no cascading

effects were observed on algal competitors such as dia-

toms, green algae or other taxa, the combination of our

grazing experiments and field observations suggests that

a stronger zooplankton herbivory following reduced fish

predation contributed significantly to the observed 72%

decrease in Microcystis biomass. As in our grazing exper-

iments, the lake-monitoring data suggest that grazing on

cyanobacteria was most likely highest on the most domi-

nant taxa due to increased encounter rates. Hence, the

strong Microcystis dominance before the biomanipulation

was broken and was shifted to codominance with Anaba-

ena, Aphanizomenon and Planktothrix under the lower pre-

dation regime. Although densities of copepods were

much higher than for Daphnia during the biomanipula-

tion, an increase in grazer body size by both copepods

and Daphnia could also trigger drastic changes in phyto-

plankton community structure (Pace, 1984; Agrawal,

1998). Hence, the 18% and 31% increases in copepod

and Daphnia body sizes are equivalent to 86 and 177 lmlarger individuals, corresponding to the typical average

size of Microcystis colonies in Lake Ringsj€on. Hence, alto-

gether our results suggest a combined impact of cope-

pods (selective herbivores) and Daphnia (generalist

herbivores) on Microcystis blooms and, importantly, this

includes a decline in the most toxic species, M. botrys.

This is of considerable relevance as, in contrast to cope-

pods, cladocerans like Daphnia are generalist, non-selec-

tive feeders that cope with the ingestion of toxic prey

through higher physiological tolerance (Gustafsson,

Rengefors & Hansson, 2005; Chislock et al., 2013a,b). In

spite of the strong response of Microcystis biomass, the

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

Zooplankton herbivory on cyanobacteria 969

dominance of the relatively small-bodied Daphnia cucul-

lata after biomanipulation in Lake Ringsj€on, as well as

the modest changes in chlorophyll-a, nutrients and

water transparency levels, suggest that fish predation

risk was still relatively high and that a stronger reduc-

tion in fish predation should further induce a shift

towards the dominance of a lager zooplankton commu-

nity (Jeppesen et al., 2000).

Our results have important implications for the under-

standing of consumer–prey interactions, but also for the

potential management of other eutrophic lakes through,

for instance, biomanipulation. Although trophic cascades

may affect phytoplankton communities differently

depending on differences in, for example, lake trophic

status (Elser & Goldman, 1991), nutrient recycling

(Vanni & Findlay, 1990), behavioural shifts (Romare &

Hansson, 2003) and many other processes (see Carpenter

et al., 2011), our study suggests that stronger herbivory

on cyanobacteria can be achieved through increased

abundance and body size of both selective and general-

ist grazers (Pace, 1984; Hansson et al., 1998, 2013). The

importance of selective herbivores has traditionally been

neglected in the literature, and here, we demonstrate

that copepods are likely to make an important contribu-

tion to herbivory on cyanobacterial blooms as, in con-

trast to large-bodied Daphnia, they often coexist with

cyanobacteria and abundant fish predators (Jeppesen

et al., 2000). While the presence of effective antiherbivore

cyanobacterial defences has been used to explain most

zooplankton–cyanobacteria interactions (Wilson et al.,

2006; Ger, Hansson & L€urling, 2014), we argue that

overlooking other critical factors, such as predation

(Hansson et al., 2013), resource density (DeMott &

Moxter, 1991) and herbivore counter-adaptations to such

defences (Gustafsson et al., 2005; Chislock et al., 2013a,b),

has led to neglect of the potential capacity of herbivo-

rous zooplankton to ‘mow down’ cyanobacterial blooms.

This is of great relevance given the relative paucity of

information on effective use of low-quality resources like

cyanobacteria by selective feeders, thus aiding our

understanding of foraging choices that drive herbivore–

plant interactions in natural environments.

Acknowledgments

We thank the anonymous reviewers for their helpful

comments. We also thank the municipality of H€o€or for

providing the field data, and Susanne Gustafsson and

Gertrud Cronberg for their help with identification of

algae. This research was funded by the European Union

Interreg IV A project ‘Algae be gone!’, the collaborative

research strategic area ‘Biodiversity and Ecosystem Ser-

vices in a Changing Climate (BECC)’ and LIMNOTIP

through the ERA-Net BiodivERsA, with the national

funder Formas.

References

Agha R., Lezcano M.-A., Labrador M.D.M., Cires S. &

Quesada A. (2014b) Seasonal dynamics and sedimenta-

tion patterns of Microcystis oligopeptide-based chemo-

types reveal subpopulations with different ecological

traits. Limnology and Oceanography, 59, 861–871.Agha R. & Quesada A. (2014a) Oligopeptides as biomarkers

of cyanobacterial subpopulations. Toward an understand-

ing of their biological role. Toxins, 6, 1929–1950.Agrawal A.A. (1998) Algal defense, grazers, and their inter-

actions in aquatic trophic cascades. Acta Oecologica-Inter-

national Journal of Ecology, 19, 331–337.Bergquist A.M. & Carpenter S.R. (1986) Limnetic herbivory:

effects on phytoplankton populations and primary pro-

duction. Ecology, 67, 1351–1360.Bottrell H.H., Duncan A., Gliwicz Z.M., Grygierek E.,

Herzig A., Hillbrichtilkowska A. et al. (1976) Review of

some problems in zooplankton production studies.

Norwegian Journal of Zoology, 24, 419–456.Bouley P. & Kimmerer W.J. (2006) Ecology of a highly

abundant, introduced cyclopoid copepod in a temperate

estuary. Marine Ecology Progress Series, 324, 219–228.Brett M.T. & Muller-Navarra D.C. (1997) The role of highly

unsaturated fatty acids in aquatic food web processes.

Freshwater Biology, 38, 483–499.Burns C.W. (1968) Relationship between body size of filter-

feeding Cladocera and maximum size of particle

ingested. Limnology and Oceanography, 13, 675–678.Carpenter S.R., Cole J.J., Kitchell J.F. & Pace M.L. (2011)

Trophic cascades in lakes: lessons and prospects chapter

4. In Trophic Cascades. (Terborgh J. & Estes J.A. eds).

Island Press, Washington D.C, pp. 55–70.Chislock M.F., Sarnelle O., Jernigan L.M. & Wilson A.E.

(2013a) Do high concentrations of microcystin prevent

Daphnia control of phytoplankton? Water Research, 47,

1961–1970.Chislock M.F., Sarnelle O., Olsen B.K., Doster E. & Wilson

A.E. (2013b) Large effects of consumer offense on ecosys-

tem structure and function. Ecology, 94, 2375–2380.Cronberg G., Annadotter H. & Lawton L.A. (1999) The

occurrence of toxic blue-green algae in Lake Ringsjon,

southern Sweden, despite nutrient reduction and fish

biomanipulation. Hydrobiologia, 404, 123–129.DeMott W.R. & Moxter F. (1991) Foraging cyanobacteria by

copepods: responses to chemical defense and resource

abundance. Ecology, 72, 1820–1834.Dumont H.J., Vandevelde I. & Dumont S. (1975) Dry weight

estimate of biomass in a selection of Cladocera,

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

970 P. Urrutia-Cordero et al.

Copepoda and Rotifera from plankton, periphyton and

benthos of continental waters. Oecologia, 19, 75–97.Ekvall M.K., Martin J.D.L.C., Faassen E.J., Gustafsson S.,

Lurling M. & Hansson L.-A. (2013) Synergistic and spe-

cies-specific effects of climate change and water colour on

cyanobacterial toxicity and bloom formation. Freshwater

Biology, 58, 2414–2422.Ekvall M.K., Urrutia-Cordero P. & Hansson L.-A. (2014)

Linking cascading effects of fish predation and zoo-

plankton grazing to reduced cyanobacterial biomass

and toxin-levels following biomanipulation. PLoS ONE,

9, e112956.

Elser J.J. & Goldman C.R. (1991) Zooplankton effects on

phytoplankton in lakes of contrasting trophic status. Lim-

nology and Oceanography, 36, 64–90.Ger K.A., Arneson P., Goldman C.R. & Teh S.J. (2010) Spe-

cies specific differences in the ingestion of Microcystis

cells by the calanoid copepods Eurytemora affinis and

Pseudodiaptomus forbesi. Journal of Plankton Research, 32,

1479–1484.Ger K.A., Hansson L.-A. & L€urling M. (2014) Understand-

ing cyanobacteria-zooplankton interactions in a more

eutrophic world. Freshwater Biology, 59, 1783–1798.Ger K.A. & Panosso R. (2014) The effects of a microcystin-

producing and lacking strain of Microcystis on the sur-

vival of a widespread tropical copepod (Notodiaptomus

iheringi). Hydrobiologia, 738, 61–73.Ger K.A., Panosso R. & Lurling M. (2011) Consequences of

acclimation to Microcystis on the selective feeding behav-

ior of the calanoid copepod Eudiaptomus gracilis. Limnol-

ogy and Oceanography, 56, 2103–2114.Gustafsson S., Rengefors K. & Hansson L.A. (2005) Increased

consumer fitness following transfer of toxin tolerance to

offspring via maternal effects. Ecology, 86, 2561–2567.Haney J.F. (1987) Field studies on zooplankton-cyanobac-

teria interactions. New Zealand Journal of Marine and Fresh-

water Research, 21, 467–475.

Hansson L.-A. (1996) Algal recruitment from lake sediments

in relation to grazing, sinking, and dominance patterns in

the phytoplankton community. Limnology and Oceanogra-

phy, 41, 1312–1323.Hansson L.A., Annadotter H., Bergman E., Hamrin S.F., Je-

ppesen E., Kairesalo T. et al. (1998) Biomanipulation as an

application of food-chain theory: constraints, synthesis,

and recommendations for temperate lakes. Ecosystems, 1,

558–574.Hansson L.-A., Gustafsson S., Rengefors K. & Bomark L.

(2007a) Cyanobacterial chemical warfare affects zooplank-

ton community composition. Freshwater Biology, 52, 1290–1301.

Hansson L.-A., Nicolle A., Brodersen J., Romare P., Nilsson

P.A., Br€onmark C. et al. (2007b) Consequences of fish pre-

dation, migration, and juvenile ontogeny on zooplankton

spring dynamics. Limnology and Oceanography, 52, 696–706.

Hansson L.-A., Nicolle A., Graneli W., Hallgren P., Kritz-

berg E., Persson A. et al. (2013) Food-chain length alters

community responses to global change in aquatic sys-

tems. Nature Climate Change, 3, 228–233.Jeppesen E., Jensen J.P., Sondergaard M., Lauridsen T. &

Landkildehus F. (2000) Trophic structure, species richness

and biodiversity in Danish lakes: changes along a phos-

phorus gradient. Freshwater Biology, 45, 201–218.Kurmayer R. & Juttner F. (1999) Strategies for the co-exis-

tence of zooplankton with the toxic cyanobacterium

Planktothrix rubescens in Lake Zurich. Journal of Plankton

Research, 21, 659–683.Lacerot G., Kruk C., Lurling M. & Scheffer M. (2013) The

role of subtropical zooplankton as grazers of phytoplank-

ton under different predation levels. Freshwater Biology,

58, 494–503.Landry M.R. & Hassett R.P. (1982) Estimating the grazing

impact of marine micro-zooplankton. Marine Biology, 67,

283–288.Lebret K., Fern�andez Fern�andez M., Hagman C.H.C.,

Rengefors K. & Hansson L.-A. (2012) Grazing resistance

allows bloom formation and may explain invasion suc-

cess of Gonyostomum semen. Limnology and Oceanography,

57, 727–734.Lehman J.T. & Sandgren C.D. (1985) Species-specific rates

of growth and grazing loss among fresh-water algae. Lim-

nology and Oceanography, 30, 34–46.MacArthur R.H. & Pianka E.R. (1966) On optimal use of a

patchy environment. American Naturalist, 100, 603–609.Moriarty D.J., Darlingt J.P., Dunn I.G., Moriarty C.M. &

Tevlin M.P. (1973) Feeding and grazing in Lake-George,

Uganda. Proceedings of the Royal Society Series B-Biological

Sciences, 184, 299–319.Pace M.L. (1984) Zooplankton community structure, but nor

biomass, influences the phosphorous-chlorophyll a rela-

tionship. Canadian Journal of Fisheries and Aquatic Sciences,

41, 1089–1096.Romare P. & Hansson L.-A. (2003) A behavioral cascade:

top-predator induced behavioral shifts in planktivorous

fish and zooplankton. Limnology and Oceanography, 48,

1956–1964.Shapiro J., Lamarra V. & Lynch M. (1975) Biomanipulation:

an ecosystem approach to lake restoration. Proceedings of

a Symposium on Water Quality and Management through

Biological Control, Gainesville, 1975, 85–96.Tillett D., Dittmann E., Erhard M., Von Dohren H., Borner

T. & Neilan B.A. (2000) Structural organization of micro-

cystin biosynthesis in Microcystis aeruginosa PCC7806: an

integrated peptide-polyketide synthetase system. Chemis-

try & Biology, 7, 753–764.Urrutia-Cordero P., Agha R., Cires S., Lezcano M.A., San-

chez-Contreras M., Waara K.O. et al. (2013) Effects of

harmful cyanobacteria on the freshwater pathogenic free-

living amoeba Acanthamoeba castellanii. Aquatic Toxicology,

130, 9–17.

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

Zooplankton herbivory on cyanobacteria 971

Vanni M.J. & Findlay D.L. (1990) Trophic cascades and phy-

toplankton community structure. Ecology, 71, 921–937.Vanni M.J. & Temte J. (1990) Seasonal patterns of grazing

and nutrient limitation of phytoplankton in a eutrophic

lake. Limnology and Oceanography, 35, 697–709.Via-Ordorika L., Fastner J., Kurmayer R., Hisbergues M.,

Dittmann E., Komarek J. et al. (2004) Distribution of micr-

ocystin-producing and non-microcystin-producing Micro-

cystis sp in European freshwater bodies: detection of

microcystins and microcystin genes in individual colo-

nies. Systematic and Applied Microbiology, 27, 592–602.Wang X., Qin B., Gao G. & Paerl H.W. (2010) Nutrient

enrichment and selective predation by zooplankton

promote Microcystis (Cyanobacteria) bloom formation.

Journal of Plankton Research, 32, 457–470.Wilson A.E., Sarnelle O. & Tillmanns A.R. (2006) Effects of

cyanobacterial toxicity and morphology on the popula-

tion growth of freshwater zooplankton: meta-analyses of

laboratory experiments. Limnology and Oceanography, 51,

1915–1924.Wilson D.S. (1973) Food selection among copepods. Ecology,

54, 909–914.

(Manuscript accepted 9 February 2015)

© 2015 John Wiley & Sons Ltd, Freshwater Biology, 60, 960–972

972 P. Urrutia-Cordero et al.