ICES Journal of Marine Science, 61: 959e965 (2004)doi:10.1016/j.icesjms.2004.06.016

Short communication

Predation by herring (Clupea harengus) and sprat (Sprattussprattus) on Cercopagis pengoi in a western Baltic Sea bay

Elena Gorokhova, Towe Fagerberg, and Sture Hansson

Gorokhova, E., Fagerberg, T., and Hansson, S. 2004. Predation by herring (Clupea harengus)and sprat (Sprattus sprattus) on Cercopagis pengoi in a western Baltic Sea bay. eICES Journal of Marine Science, 61: 959e965.

Cercopagis pengoi is a pelagic cladoceran that has recently colonized the Baltic Sea and theLaurentian Great Lakes and is recognized as a species with the potential to affect naturalfoodwebs. To study the consumption of C. pengoi by zooplanktivorous fish, stomachcontents of herring (size range 52e252 mm) and sprat (57e116 mm) from a coastal area ofthe northern Baltic proper were examined in parallel with zooplankton samples. The overallproportion of fish preying on C. pengoi was high both for sprat (70%) and for herring(61%), and it accounted for 8G 23% and 20G 33% of prey dry weight in the diets. Thepredation on Cercopagis depends on its abundance and on fish size; herring showeda tendency to become more selective for Cercopagis with increasing size. The majority ofdiapause eggs found in sprat (69%) were immature and appeared digested, while this wasthe case only for 2% of the eggs found in herring. These results suggest that Cercopagis hasbecome a significant component in the diet of zooplanktivorous fish and, therefore, itsabundance may be controlled by fish predation.

� 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.

Keywords: Cercopagis pengoi, diapausing eggs, diet, herring Clupea harengus, invasivespecies, predation, selectivity, sprat Sprattus sprattus.

Received 21 August 2003; accepted 15 June 2004.

E. Gorokhova, T. Fagerberg, and S. Hansson: Department of Systems Ecology, StockholmUniversity, SE-106 91 Stockholm, Sweden. Correspondence to E. Gorokhova: tel.: C46 8164256; fax: C46 8 158417; e-mail: elenag@system.ecology.su.se

Introduction

Cercopagis pengoi is a pelagic cladoceran that has

recently colonized the Baltic Sea (Ojaveer and Lumberg,

1995; Uitto et al., 1999; Bielecka et al., 2000), including

coastal waters of the Stockholm Archipelago (Gorokhova

et al., 2000). Furthermore, the species has recently ap-

peared in the Great Lakes (MacIsaac et al., 1999), where it

is spreading rapidly (Therriault et al., 2002). The invasion

has raised concerns that it may change the foodweb

structure of native ecosystems (Vanderploeg et al., 2002).

Indeed, when the closely related cercopagid Bythotrephes

longimanus colonized North American lakes, it undoubt-

edly influenced these ecosystems (Yan et al., 2002). When

established, Cercopagis may in a similar way affect resi-

dent zooplankton communities by selective predation, and

this has recently been reported from the Gulf of Riga

(Ojaveer et al., 1999) and Lake Ontario (Benoit et al.,

2002). This may result in decreased grazing pressure on

phytoplankton and enhanced algal blooms. Cercopagis

may also impact fish populations by competing with

1054-3139/$30.00 � 2004 International Coun

0-group fish for small prey, or conversely by becoming

prey itself for older fish (Vanderploeg et al., 2002).

Indeed, zooplanktivorous fish both in the Baltic and in the

Great Lakes have been found to prey on Cercopagis when

available (Ojaveer and Lumberg, 1995; Ojaveer et al.,

1998; Antsulevich and Valipakka, 2000; Bushnoe et al.,

2003). However, the extent to which fish consume

C. pengoi may vary between size classes and species.

Small fish may be unable to use it as prey due to gape

size limitations, while large individuals may consume

a significant proportion of Cercopagis production and

even control its population development.

Herring (Clupea harengus L.) and sprat (Sprattus

sprattus L.) are dominant species both in the commercial

fishery and as zooplanktivores in the Baltic Sea. Before the

invasion, their diets consisted mostly of calanoid copepods

(Acartia spp., Eurytemora affinis, and Temora longicornis)

and cladocerans (Bosmina coregoni maritima and Pleopsis

polyphemoides), varying between the coastal and open sea

areas and between northern and southern parts of the Baltic

proper (Rudstam et al., 1992; Mehner and Heerkloss, 1994;

cil for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.

960 E. Gorokhova et al.

Arrhenius, 1996; Antsulevich and Valipakka, 2000). After

its appearance, Cercopagis has become a significant

component in the diet of adult herring but not of the

young-of-the-year (YOY) herring in Estonian and Finnish

coastal waters (Ojaveer and Lumberg, 1995; Ojaveer et al.,

1998; Antsulevich and Valipakka, 2000). These authors

suggested that C. pengoi could improve herring feeding

conditions and growth. However, the extent to which small

fish consume C. pengoi has not been carefully examined

and remains unclear.

The primary objective of this study was to estimate the

contribution of C. pengoi to the diet of herring and sprat in

a coastal area in the northern Baltic proper and to evaluate

the selectivity for Cercopagis of different size classes of

these fish species. In addition, we examined the frequency

and condition of Cercopagis resting eggs in fish stomachs.

The study was carried out during the summer 2002 in

a deep (w30 m), enclosed bay (Himmerfjarden) located in

the southern archipelago of Stockholm. This area was

chosen because (1) the Cercopagis population is estab-

lished in the area since at least 1997 (Gorokhova et al.,

2000), (2) other coastal areas like this are most likely to

become invaded by Cercopagis (Leppakoski and Olenin,

2000), and (3) these habitats are nursery areas for many fish

species, including herring (Axenrot, 2002).

Material and methods

Zooplankton sampling and analyses

Zooplankton were sampled bi-weekly (JulyeOctober 2002,station indicated in Figure 1) from the bottom to the surface

with a 90-mm WP-2 plankton net (B 57 cm). On two

occasions (3 August and 3 September), additional samples

were taken in the upper 5e10 m with a 60-mm plankton net

(B 23 cm). The samples were preserved and analysed

according to the standard protocol of the Baltic Monitoring

Programme (HELCOM, 1988). Dry weights of zooplankton

were calculated according to Rosen (1981) and Hernroth

(1985). When the dates for zooplankton sampling did not

match the dates of fish sampling, zooplankton densities on

the dates of fish sampling were obtained by linear

interpolation between the abundances in the neighboring

days.

Cercopagis individuals were removed from the samples

under a dissecting microscope prior to sub-sampling and

processed separately. Conventional methods of population

analysis of Cercopagidae were employed (Rivier, 1998);

dry weights of Cercopagis were calculated according to

Uitto et al. (1999).

Fish collection and stomach analysis

Fish were collected at three locations (Figure 1) on five

occasions in JulyeSeptember (Table 1). They were caught

during night, in gillnets that were set 4e6 m below the

surface. The nets were 3 m deep and had nine segments

(each 2.5 m) with mesh sizes 5-, 6.25-, 8-, 10-, 12.5-, 15.5-,

19.5-, 24-, and 29-mm bar. Diet analyses focused on, but

were not restricted to, fish from August and September,

because Cercopagis was most abundant during this period.

The collected fish were kept frozen (�18(C) until analysis;sometimes this resulted in deformed caudal fins, and as

a measure of fish size, we used the distance (mm) from the

tip of the nose to the base of the caudal fin. As a measure of

the mouth size, we used the length (mm) of the lower jaw of

the fish. A total of 106 herring and 80 sprat stomachs were

analysed (64 empty; Table 1). When estimating the

presence and condition of C. pengoi resting eggs, all non-

empty stomachs were considered, while for the rest of the

diet analysis, only those with R 8 identifiable objects were

used (95 stomachs).

The effect of fish size on dietary composition was

examined by grouping fish into 50-mm size classes, with

individuals larger than 200 mm forming the group

‘‘O200 mm’’ (Table 1). Herring !100 mm were mainly

YOY fish produced from spawning in the study area (cf.

Arrhenius and Hansson, 1996), while sprat in this size

range were one-year-old fish. The stomach content was

Figure 1. Study sites: zooplankton and fish were collected in

JulyeSeptember 2002 in a coastal area of the northern Baltic

proper. Station H4, Himmerfjarden Bay, w30-m depth; 58(59#N17(44#E e zooplankton collection site; Stations 1, 2 and 3 e fish

collection sites.

961Predation by herring and sprat on Cercopagis pengoi

Table 1. The frequency of occurrence for Cercopagis in the fish stomachs (%), number of prey per stomach (individuals, meanG s.d.), dry

weight of zooplankton prey per stomach (DW, mg, meanG s.d.), and number of fish in each size class from each sampling occasion that

was used for stomach content analysis (total number of fish/individuals with empty stomachs).

Species,

size classes

Frequency of

Cercopagis, %

Number of prey

per stomach;

meanG s.d.

DW of prey

per stomach,

mg; meanG s.d.

Sampling date, 2002

9 July 28 July 13 Aug 1 Sep 16 Sep

Herring (Clupea harengus)

5e10 cm 54 716G 792 3.3G 6.1 d d 11/1 31/10 14/2

10e15 cm 89 429G 564 10.0G 5.3 d d 12/4 20/10 9/1

15e20 cm 50 36G 15 96.5G 105.2 2/0 1/0 d 6/1 1/1

O20 cm 0 16G 1 5.4G 4.1 2/0 d d 2/0 1/1

Total 61 546G 716 12.7G 52.0 4/0 1/0 23/5 59/21 25/5

Sprat (Sprattus sprattus)

5e10 cm 62 589G 564 2.9G 2.9 d d 7/2 1/0 18/11

10e15 cm 71 1327G 1420 8.7G 9.4 d d 10/3 11/7 27/10

Total 70 1044G 1221 6.4G 8.1 d d 17/5 18/7 45/21

analysed using a dissecting microscope and an inverted

microscope and identifying each prey item to the lowest

possible taxonomic level. Cercopagis were recorded in two

ways: (1) by weighing or (2) by counting the identifiable

individuals or their body parts. The first method was used

when the stomach contained a large bolus of individuals

bundled together and the remnants of their bodies were

relatively intact. Each bolus was transferred to a pre-

weighed tin cup, dried at 60(C for 72 h, and weighed

(G2 mg). The number of individuals in the bolus was

calculated by assuming an individual dry weight of 20 mg(Uitto et al., 1999). It is possible that this underestimated

the number of individuals, as some of them were partly

digested, but we are confident that separating individuals

(hundreds to thousands) and counting their remains would

have introduced an even greater error. The second method

was used when the remnants of Cercopagis were not

aggregated and could be counted directly.

The number of Cercopagis resting eggs was determined

from those visible in a bolus and those found free in the

sample. Furthermore, the maturity of each egg was noted

using the characteristics of Bythotrephes diapausing eggs

(Jarnagin et al., 2000), i.e. amount of yolk present,

coloration and thickness of the outer shell. The eggs were

categorized as (1) mature e those with dispersed droplets,

a bright-yellow coloration, thick and distinct shells and (2)

immature e those which were clear or weakly colored on

periphery, with very few or no droplets and thin outer

shells.

Selectivity estimates and statistics

The selection of prey types was estimated using the

Chesson (1983) selectivity index (ai); the index ranges

from 0 to 1, corresponding to complete avoidance and full

selection. In this study the three most abundant prey groups

were considered, i.e. cladocerans (other than C. pengoi),

copepods, and C. pengoi. As data on the in situ mysid

abundance were unavailable, this prey was excluded from

the selectivity estimates.

Using estimated ai values, intra- and inter-specific

differences in selectivity for Cercopagis were evaluated

with a log-linear analysis (Upton, 1978). The analysis was

based on a three-way frequency table with the dimensions:

species (herring and sprat), length (longer or shorter than

the median length, 97 mm), and position (ai higher or lowerthan the median value for Cercopagis). Position was treated

as a dependent variable, while species and length were

independent variables. The number of fish that fit into

a certain cell (e.g., herring! shorter than median

length! ai lower than median value; Table 2) is the

frequency that is compared with the expected frequencies

derived from the total number of observations and row/

column sums.

Results

Food availability

During the study period, Cercopagis densities were always

low (!48 ind. m�3, Figure 2A), comprising !0.1% of the

total zooplankton abundance and 0.4e1.2% of the biomass.

Zooplankton were dominated by rotifers (Keratella coch-

learis and Synchaeta spp., 19e80% of total zooplankton

abundance) and copepods (mostly juvenile stages of

Acartia bifilosa and Eurytemora affinis, 14e70%). Clado-

cerans (Bosmina coregoni maritima, Pleopsis polyphe-

moides, and Podon intermedius) contributed at most 10% to

the total abundance, with usually less than 1e2% (Figure

2B). Cladocerans and copepods were abundant in Ju-

neeJuly, decreasing during August, while the rotifers

showed a very drastic decline during the mid-August

(Figure 2B). Cercopagis was common from midsummer

962 E. Gorokhova et al.

Table 2. The three-way frequency table for the log-linear analysis. To test for differences in prey selectivity between the species,

aCercopagis-values for each fish (Chesson selectivity index) were classified as below or above the median-aCercopagis-value (0.335).

Fish length a Below median-a a Above median-a

Herring Below the median 24 13

Above the median 8 16

Sprat Below the median 5 8

Above the median 11 10

The frequencies of observations above and below the median were then analysed by log-linear statistics. The first step (A) was to generate

a saturated model, in which all possible interactions are included. This model has 0 degrees of freedom (d.f.) and explains all variations in

counts in the frequency table (c2-valueZ 0). In the following steps (BeD), interactions between categories are removed, producing

models that are less efficient in explaining the observed frequencies. As the category position was a response variable, it was only species

and length that could be excluded from interactions. The goal was to find interactions, the exclusion of which has significant negative

effects on the remaining model. The only significant result was obtained when species and size effects on selectivity are combined

(B; shown in bold face).

Considered interactions

between variables d.f. c2 Change in d.f. Change in c2 p-value

A e complete model

included: species! length! position 0 0

B e three-way

interaction excluded

included: species! positionC length! position 1 4.37 1 4.37 0.037

C e three-way

and species! position excluded

included: length! position 2 4.41 1 0.04 O0.05

D e three-way

and length! position excluded

included: species! position 2 6.52 1 2.15 O0.05

and showed a distinct peak on 10 September. The

proportion of gametogenic females was also highest in this

sample (16%, Figure 2A). Most of the gametogenic females

(88%) had one-egg broods and hence we used a 1:1 ratio for

egg:female, when using egg number to estimate the number

of Cercopagis in a fish stomach.

Stomach contents

Copepods (Acartia and Eurytemora) and cladocerans

(mostly Bosmina) were dominant prey for sprat and the

smallest of herring (Figure 3). Besides zooplankton, herring

O114 mm had also eaten mysids (Neomysis integer) and

small fish (data not shown). Irrespective of their size

(herring of 52e252-mm length, sprat of 57e116-mm

length), both fish species fed on Cercopagis and it occurred

in 61% of the analysed herring and in 70% of the sprat.

Herring stomachs contained up to 1299 and those of sprat eup to 116 C. pengoi. The proportion of Cercopagis in the

diet was highest in 100e150-mm herring (Table 1, Figure

3), among which some fish had nothing but Cercopagis in

their stomach. The higher proportion of Cercopagis in

herring stomachs (Figure 3A) may at least in part be

explained by their relatively larger mouth compared to that

of sprat (Figure 4). Thus, although rare in the water column,

Cercopagis contributed substantially to the stomach content

of both fish species (Figure 3). The proportion of

Cercopagis in diets increased with its abundance, with

the strongest correlation derived for 100e150-mm herring

(Pearson’s rZ 0.68, p! 0.003).

Selectivity

There were statistically significant inter-specific differences

in selectivity for Cercopagis between herring and sprat

(Chesson selectivity index; Table 2). The difference was

that the selectivity for Cercopagis increased with fish size

for herring, but not in sprat.

Resting eggs

Resting eggs of Cercopagis were found in the stomachs of

all size classes of the both species (Figure 5), sometimes in

large quantities, e.g. 1299 eggs in a 113-mm herring. They

were more frequent in herring than in sprat, with the highest

frequency of eggs occurring (89%) in 100e150-mm herring

963Predation by herring and sprat on Cercopagis pengoi

(Figure 5A). Most of the eggs in sprat (69%) were immature

(Figure 5B), while this was the case only for 2% of the eggs

found in herring stomachs (6% if the stomach with 1299

eggs was excluded from the calculations). Most of the

0

15

30

45

Parthenogenic females

Gametogenic females

Males

Cerco

pag

is

a

bu

nd

an

ce

, in

d. m

-3

18 Ju

n

23 Ju

n

30 Ju

l

3 A

ug

13 A

ug

28 A

ug

3 S

ep

10 S

ep

23 S

ep

9 O

ct

0

100

200

300

400

500

Rotatoria

Cladocera

nauplii

C I-III

C IV-adults

Sampling date

Zo

op

lan

kto

n ab

un

dan

ce, in

d. 10

3 m

-3

Copepoda

A

B

* * * * *

Figure 2. Abundance and population structure of Cercopagis

pengoi (A) and the native zooplankton community (B) during the

study period. Note the different scales on the Y-axes. Asterisks

indicate fish sampling occasions.

immature eggs found in sprat appeared as at least partially

digested, with only thin empty outer shells containing

essentially no yolk.

Discussion

It has been suggested that Cercopagis will compete for

herbivorous zooplankton with young stages of planktivo-

rous fish, if these are unable to prey on Cercopagis due to

its long caudal spine (Vanderploeg et al., 2002). In our

study, however, fish down to a size of 52 mm fed on

Cercopagis, including YOY herring. Despite its rarity in

plankton (!1% of total zooplankton abundance and

biomass), Cercopagis was ingested with high frequency

by all fish !200 mm (Table 1). The predation on

Cercopagis appears to depend on its abundance and to

some extent on fish size; in particular, herring showed

a tendency to become more selective for Cercopagis with

increasing size. Thus, the colonization by Cercopagis has,

at least in some areas, led to a shift in the feeding ecology

0 50 100 150 200 250 300

0

10

20

30

40

Herring: a=0.134; b=0.58; r2=0.97

Sprat: a=0.08; b=3.10; r2=0.60

F1,179

= 26.4455; P < 0.0001

Body length, mm

Jaw

len

gth

, m

m

Figure 4. Relationships between mouth size measured as lower jaw

length (mm) and body length (BL, mm) in herring and sprat;

regression line: jaw lengthZ aBLC b. The difference between the

slopes is extremely significant.

Size classes, cm

Herring

Copepods

Cladocerans

Mysids

Cercopagis

Sprat

5-10 10-15

B

5-10 10-15 15-20 >20

0

25

50

75

100A

% o

f fo

od

b

io

mass

Figure 3. Diets of different size classes of herring (A) and sprat (B), expressed as percentages (based on dry weight) of different prey types

in their stomachs. Contribution of Cercopagis is shown separately from the rest of the cladocerans.

964 E. Gorokhova et al.

Herring

A

5-10 10-15 15-20 >200

15

30

45

60

Freq

uen

cy, %

Sprat

B

5-10 10-15

Mature

Immature

Size classes, cm

Figure 5. Proportions of fish stomachs that contained Cercopagis resting eggs and relative distribution of mature and immature eggs in

herring (A) and sprat (B) of different size.

of herring and sprat, the major zooplanktivores in the

Baltic. Moreover, this shift occurs not only in adult herring

(as suggested by Ojaveer et al., 1998), but also in sprat and

in fish as young as metamorphosed YOY herring.

Cercopagis pengoi is present in the northern Baltic proper

from July to October, being most abundant in AugusteSep-tember, i.e. at the same time of year as other zooplankton

decline. This decline also occurred prior to the invasion of

Cercopagis and is probably caused by factors such as

resource availability or fish predation (Johansson et al., 1993;

Adrian et al., 1999). Indeed, the consumption peak by fish

occurs in AugusteSeptember and the major zooplanktivores

are YOY clupeoids (Rudstam et al., 1992; Arrhenius and

Hansson, 1993). Therefore, as fish consumption increases

and densities of native zooplankton decline, Cercopagis

reaches its abundance peak and may become an important

food source for zooplanktivorous fish during this period.

Like most cladocerans, C. pengoi is a cyclic parthe-

nogen, and new population can be established from a single

egg. The primary mode of reproduction is clonal, in-

terspersed with periods ( primarily in autumn) of sexual

reproduction that involves formation of resting eggs

(Rivier, 1998). It has also been suggested that resting eggs

of Cercopagis can survive a passage through the fish

digestive system (Antsulevich and Valipakka, 2000), and

therefore fish could act as a dispersal vector. However, eggs

carried by Instar IeIII gametogenic females are in various

stages of development when consumed by fish, and this

may potentially affect the viability of those eggs following

passage through the gut. We found a tendency in sprat, but

not in herring, to ingest mostly females with immature eggs

(Figure 5) and many of these eggs appeared partially

digested. Because sprat has a smaller mouth compared to

that of herring (Figure 4), it is possible that sprat feeds

preferentially on smaller Instar IeII gametogenic females,

which are more likely to have immature eggs, while herring

selects larger Instar III females with dark, highly visible

mature eggs as shown for many planktivorous fish and

egg-carrying zooplankters. Jarnagin et al. (2000) showed

experimentally that fully mature resting eggs of Bytho-

trephes survived the passage through the alimentary canal

of yellow perch (Perca flavescens), while the hatching

success of immature eggs was decreased. The impact of fish

predation on the production of viable over-wintering eggs

may therefore be influenced by the species composition of

the zooplanktivorous fish and this may influence the

recruitment of Cercopagis the following year.

Once invasive species are established, one of the few

countermeasures that can be taken is to try to suppress the

invader by managing its predators. This approach was taken

in Lake Michigan, to control alewife and rainbow smelt

(Rand and Stewart, 1998). The two dominant zooplanktiv-

orous fish in the Baltic are herring and sprat, the

populations of which are strongly influenced by the fishery

and for which annual catch quotas are set by the

International Baltic Sea Fisheries Commission. Our study

shows that both these species are predators on Cercopagis

and this may need to be accounted for in the management

of the fishery, if we would like to reduce the abundance of

Cercopagis. This would then be an excellent example of an

application of the ecosystem-based approach to fisheries

management, which is a cornerstone in the recently adopted

common fisheries policy of the European Union (Anon.,

2002). It should be acknowledged, however, that it is not

fully understood to which extent herring, sprat and other

zooplanktivores, like for example smelt (Osmerus eperla-

nus), jellyfish, and mysid shrimps, actually control

Cercopagis through predation. Neither do we know if

Cercopagis actually competes with the fish for prey or

constitutes a new and important food web link to higher

trophic levels.

Acknowledgements

This research was supported by research grants from The

Swedish Research Council for Environment, Agricultural

Sciences and Spatial Planning (Formas) and Swedish

965Predation by herring and sprat on Cercopagis pengoi

Environmental Protection Agency. We thank B. Larsson for

his invaluable help in collecting fish for analyses. We also

thank M. Petersson (Ar Research Station, Gotland Univer-

sity, Sweden), L. Lundgren and B. Abrahamsson (Systems

Ecology, Stockholm University, Sweden), and Karolina

Eriksson-Gonzales (Linkoping University, Sweden) for

technical assistance and logistical support.

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