Effects of Altered Offshore Food Webs on Coastal Ecosystems Emphasize the Need for Cross-Ecosystem Management

Abstract

By mainly targeting larger predatory fish, commercial fisheries have indirectly promoted rapid increases in densities of their prey; smaller predatory fish like sprat, stickleback and gobies. This process, known as mesopredator release, has effectively transformed many marine offshore basins into mesopredator-dominated ecosystems. In this article, we discuss recent indications of trophic cascades on the Atlantic and Baltic coasts of Sweden, where increased abundances of mesopredatory fish are linked to increased nearshore production and biomass of ephemeral algae. Based on synthesis of monitoring data, we suggest that offshore exploitation of larger predatory fish has contributed to the increase in mesopredator fish also along the coasts, with indirect negative effects on important benthic habitats and coastal water quality. The results emphasize the need to rebuild offshore and coastal populations of larger predatory fish to levels where they regain their control over lower trophic levels and important links between offshore and coastal systems are restored.

Full text

REVIEW PAPER
Effects of Altered Offshore Food Webs on Coastal Ecosystems
Emphasize the Need for Cross-Ecosystem Management
Britas Klemens Eriksson, Katrin Sieben, Johan Eklo
¨f,
Lars Ljunggren, Jens Olsson, Michele Casini,
Ulf Bergstro
¨m
Received: 21 December 2010 / Revised: 28 April 2011 / Accepted: 13 May 2011 / Published online: 24 June 2011
Abstract By mainly targeting larger predatory fish,
commercial fisheries have indirectly promoted rapid
increases in densities of their prey; smaller predatory fish
like sprat, stickleback and gobies. This process, known as
mesopredator release, has effectively transformed many
marine offshore basins into mesopredator-dominated eco-
systems. In this article, we discuss recent indications of
trophic cascades on the Atlantic and Baltic coasts of
Sweden, where increased abundances of mesopredatory
fish are linked to increased nearshore production and bio-
mass of ephemeral algae. Based on synthesis of monitoring
data, we suggest that offshore exploitation of larger pred-
atory fish has contributed to the increase in mesopredator
fish also along the coasts, with indirect negative effects on
important benthic habitats and coastal water quality. The
results emphasize the need to rebuild offshore and coastal
populations of larger predatory fish to levels where they
regain their control over lower trophic levels and important
links between offshore and coastal systems are restored.
Keywords Mesopredator release 
Human transformation Commercial fisheries 
Cod Baltic Sea Swedish coast
INTRODUCTION
Fishery induced declines in populations of larger predatory
fish have generated dramatic changes in the food web
composition in offshore and coastal seas (Pauly et al. 1998;
Lotze et al. 2006). In particular, decreased stocks of
predatory fish have generated strong increases in their prey,
medium-sized or ‘‘meso-’’ predators (i.e., ‘‘mesopredator
release’’), changing the interactions between higher trophic
levels considerably (e.g., Myers et al. 2007; Baum and
Worm 2009). In some instances, there are documented
cascading effects from such mesopredator increases on
lower levels in the pelagic food web, including community-
wide decreases of zooplankton, and increases in jellyfish
and phytoplankton (e.g., Frank et al. 2005; Daskalov et al.
2007; Casini et al. 2008).
Effects of overfishing have traditionally been synony-
mous with effects on commercially important stocks, and
on the consequences for either the market actors or coastal
human societies that have experienced dramatic changes in
their livelihood. There has also been a strong concern for
many of the larger pelagic species, which have a high
societal impact and cultural value. Management actions
have therefore been centered on protecting the economic
viability of commercial stocks and on restoring biological
diversity of apex predators, such as whales, dolphins, seals,
sharks, and tuna. Today, most management organizations
promote ecosystem-based management (EBM). EBM is an
adaptive management approach that focuses on the com-
plexity of interactions within and between ecological and
social systems, acknowledging that diversity of species and
their traits are important for ecosystem performance and
stability (Christensen et al. 1996). For coastal societies,
EBM is a favorable long-term strategy because it considers
multiple ecosystem services and manage the capacity of
ecosystems to tolerate disturbances and stress, rather than
focusing on one interest group by managing a single
function or the production of one species (Christensen et al.
1996; Leslie and McLeod 2007).
Ecosystems are connected by flows of energy, materials
and organisms. Spatial subsidies across ecosystem borders
are important for population dynamics and community
structure in many recipient ecosystems (Polis and Strong
1996). An important vector that transports resources
between offshore and coastal ecosystems is constituted by
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AMBIO (2011) 40:786–797
DOI 10.1007/s13280-011-0158-0

migrating animals that utilize both systems during their life
cycles (e.g., Varpe et al. 2005). The existence of such
migrations implies that changes in offshore food webs may
profoundly impact coastal ecosystems. For example, in the
early 1990s, negative effects of increased predation from
offshore populations of killer whales (Orca orca) were
reported from the coast of Alaska (Estes et al. 1998). Killer
whales increased their foraging along the coast and thereby
limited the coastal populations of sea otters (Enhydra
lutris). This released the main prey of sea otters—herbivo-
rous sea urchins—from predation control, resulting in
severe overgrazing of giant kelp; the habitat-founding
species in the ecosystem. There is an increasing realization
that major changes in offshore pelagic food webs might
impact the functioning of coastal ecosystems, including a
reduced production of the crucial ecosystem services they
provide.
In this study, we suggest that observed effects of coastal
mesopredators on lower trophic levels may in fact be
triggered by fishery induced changes in offshore food
webs. We base this hypothesis on analyses of fish moni-
toring data from two different areas: the marine Atlantic
west coast of Sweden, and the brackish Baltic east coast of
Sweden, combined with published information on con-
comitant food web changes, highlighting how changes in
offshore food web composition appear to give rise to
complex responses also in the coastal ecosystems.
INCREASE OF MESOPREDATORS ON THE
SWEDISH ATLANTIC COAST
Declines in offshore predator populations may increase the
abundance of nearshore mesopredators by direct decreases
in predation rates, but also by complex, indirect food web
interactions. On the Atlantic coast of Sweden (Skagerrak
and Kattegat) the coastal mesopredator community is
dominated by wrasses, gobiids and the common shore crab
(Carcinus maenus) (Pihl and Wennhage 2002; Pihl et al.
2006; Swedish Board of Fisheries unpublished). Long-term
monitoring data from a coastal area in the southern basin,
Kattegat (Swedish Board of Fisheries, Vendelso
¨), suggests
that these important mesopredators have all become
increasingly abundant.
Vendelso
¨(latitude 57°180, longitude 12°70) is a refer-
ence area for the nuclear power plant of Ringhals. The
discharge of heated cooling water from the power plant is
not expected to affect the Vendelso
¨area (Bergstro
¨m et al.
2009). In 1976, a standardized fyke net monitoring pro-
gram was initiated in Vendelso
¨(HELCOM 2008). Since
1976, six stations have been fished at Vendelso
¨between 9
and 12 consecutive nights both in April and August every
year, generating an effort of 108 to 144 fyke net nights per
year. At each of the six stations, two fyke nets have been
placed perpendicular to the shore, covering a transect from
2 to 5 m depth. At each sampling occasion, the abundance
of all fish and larger crustaceans have been registered, as
well as water temperature, sechi depth and salinity (for
more info, see Thoresson 1996). The August sampling
better represents changes in wrasse and shore crab popu-
lations (20 and 5 times higher catch in August compared to
April, respectively). However, gobiids are as common in
April as in August, and we therefore included both sam-
pling periods in our analyses of coastal mesopredators.
Data were square root or log10 transformed if necessary to
improve linearity and temporal trends were analyzed with
linear regression. We tested all analyzed time series for
autocorrelation to the 15th lag using the autocorrelation
function (STATISTICA, version 8.0; StatSoft, Inc. 2007).
All coastal and later analyzed offshore time series, showed
significant first-order autocorrelations (dependence on the
first lag), which may cause an underestimation of the
standard error and a higher risk of Type 1 error. We
therefore adjusted sample sizes for first-order autocorrela-
tion by calculating effective sample sizes: effective sample
size (N*) =sample size (N)9(1 -r
c
)/(1 ?r
c
), where r
c
is the first-order autocorrelation coefficient (Dawdy and
Matalas 1964). In the results, F* and p* indicate that
sample sizes are corrected for significant first-order
autocorrelations.
Since 1976, the abundance of the dominating wrasses,
corkwing wrasse, Symphodus melops, and goldsinny wrasse,
Ctenolabrus rupestris has steadily increased in the catches
(linear regression: N=34, R=0.49, F
1;11 =10.26, p*=
0.009), as has the common shore crab (linear regression:
N=34, R=0.49, F
1;12 =22.29, p*\0.001) and black
goby, Gobius niger (linear regression on square root trans-
formed data: N=34, R=0.72, F
1;8=34.80, p*\0.001;
Fig. 1a). During the same time (1976–2009), the powerplant
at Ringhals has also increased its effect and there is a s
ignificant increase in water temperatures in the area
affected by cooling water (Bergstro
¨m et al. 2009;www.
fiskeriverket.se). At Vendelso
¨, there is a marginally signif-
icant trend towards increasing water temperatures in August
(R=0.33, F
1,32
=3.84, p=0.059), but not in April
(R=0.28, F
1,32
=2.80, p=0.103). However, the tem-
perature increase at Vendelso
¨in August corresponds to ca a
0.5°C per decade, which is comparable to the general
increase in surface water temperatures in the whole Kattegat
area and significantly lower than the temperature increase
measured at the nuclear power plant (Swedish Board of
Fisheries 2008; Bergstro
¨m et al. 2009;www.fiskeriverket.se).
In all, this suggests that the increase in effect at the power
plant at Ringhals has not had a major impact on the tem-
perature increase at Vendelso
¨. Note that the densities of
black goby are relatively low in this program, since the
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catchability of the species is low in fyke nets. However,
increasing densities of black goby are also indicated by
catches in an offshore autumn trawl survey (ICES Interna-
tional Bottom Trawl Survey of demersal fish in September,
IBTS), where densities have increased 45 times between the
1990s and the 2000s in Kattegat (ICES subdivision 21; linear
regression on square root transformed data: N=18,
R=0.85, F
1;6=43.97, p*=0.001; Fig. 1b).
The increase in coastal mesopredators coincided with a
long-term decreasing trend of cod populations in the
international offshore bottom trawl survey in Kattegat
(Gadus morhua; IBTS average catch weight kg per trawl
hour in September: linear regression on square root trans-
formed data, N=18, R=-0.65, F
1;10 =11.70, p*=
0.001, Fig. 1b; IBTS in February: linear regression,
N=18, R=-0.77, F
1;7=43.26, p*\0.001, Fig. 1c).
Cod is the dominant larger demersal predator in the area
and was subjected to a strong commercial fishery during
the decline from 1970s to the 2000s. Juveniles of offshore
populations of cod settle in nearshore habitats and the
larger individuals predate significantly on gobiids, shore
crabs and wrasses (Pihl 1982; Pihl and Ulmestrand 1993;
Salvanes and Nordeide 1993). Notably, the catch of cod in
the offshore bottom trawl survey was negatively correlated
with the catch of mesopredators in the coastal fyke net
monitoring program (Pearson’s product moment correla-
tion; wrasses [sqrt transformed data] r=-0.61, N=32,
t=4.24, p\0.001; shore crab: r=-0.51, N=32,
t=3.22, p=0.003; black goby [sqrt transformed data]:
r=-0.64, N=31, t=4.58, p\0.001; Fig. 2a), sug-
gesting a link between declining cod populations and the
increase in mesopredators. However, general changes in
climatic variability have been proposed to have generated
changes in the composition of fish communities during the
same time period in the North Sea, with increasing tem-
peratures as a main driver (Alheit et al. 2005). Temperature
is important for the year-class strength of many fish spe-
cies. To compare possible drivers of mesopredator abun-
dances, we therefore constructed multiple regression
models for the coastal mesopredator groups at Vendelso
¨;
including offshore cod (catch weight kg per trawl hour in
February) and average temperatures during the fyke net
sampling in April and August as explanatory variables. The
temperature in August did not significantly explain any
variation in mesopredator abundances and was deleted
from all models. Instead, offshore biomass of cod together
with water temperatures in April contributed significantly
to all models (Fig. 2; Table 1). The results indicate that
spring temperatures are probably important for the abun-
dance of mesopredators in the area. However, in contrast to
cod biomass local spring temperatures did not change over
time. Thus, the results suggest that decreasing predation
pressure by juvenile cod, alongside with changed climatic
variability may have contributed significantly to the
increased abundances of mesopredators along the coast.
Black goby, shore crabs and wrasses all have the
potential to regulate the abundance of crustacean and
gastropod herbivores (‘‘mesograzers’’), potentially result-
ing in cascading effects on vegetation (Norderhaug et al.
2005, Newcombe and Taylor 2010). Concomitant with the
observed changes in food web composition, beds of eel-
grass (Zostera marina L.)—the dominating foundation
species on shallow soft-bottoms—declined with 60% on
the northern Swedish Atlantic coast since the 1980s and up
to 85% in northern Kattegat (Kunga
¨lv; Baden et al. 2003;
Nyqvist et al. 2009). These losses have been attributed to
blooms of mat-forming filamentous algae (e.g., Clado-
phora spp., Ectocarpales and Ulva spp.) generated by a
combination of increased nutrient supply (via coastal
eutrophication) and low grazing pressure, mediated by high
predation pressure on functionally important grazers from
high densities of mesopredators (Fig. 3; Moksnes et al.
2008; Baden et al. 2010). Field experiments using cages
show that predation by local mesopredators decrease the
biomass of potential mesograzers by more than 95% in this
system (Moksnes et al. 2008; Baden et al. 2010). Cage
experiments also demonstrate that the black goby indirectly
increases the biomass accumulation of ephemeral algae in
seagrass patches up to five times by controlling the most
efficient grazers: adult ([9 mm) individuals of the
amphipod Gammarus locusta (Moksnes et al. 2008).
Today, gammarid and isopod mesograsers occur in very
low abundances in eelgrass beds, where they were abun-
dant in the 1980s (Jephson et al. 2008; Moksnes et al. 2008;
Baden et al. 2010). Seagrass beds decrease turbidity by
stabilizing sediments, and act as nursery ground for a
number of commercially important fishes in the area (such
as cod; Pihl et al. 2006). Thus, the decreases in offshore
populations of larger demersal fish and the following dra-
matic increase in populations of mesopredators described
here for Kattegat, might have impacted crucial components
of these nearshore ecosystems, including their nursery
function for the top predators already impacted by fishing.
However, even though these results indicate that altered
cross ecosystem interactions have fundamentally impacted
the coastal ecosystem, there is still a strong need to clearly
link such time-series of higher trophic levels with the
experimental results from lower trophic levels in seagrass
meadows.
INCREASE OF MESOPREDATORS
ON THE SWEDISH BALTIC SEA COAST
There are also indications from the coast of the central
Baltic Sea that offshore fisheries on cod may have
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coastal monitoring
0
5
10
15
20
25
30
1976 1980 1984 1988 1992 1996 2000 2004 2008
# wrasses & crabs cpue
0
0.3
0.6
0.9
# black goby cpue
wrasses
shore crab
black goby
(a)
offshore autumn monitoring
0
10
20
30
40
50
1976 1980 1984 1988 1992 1996 2000 2004 2008
cod cpue
0
0.02
0.04
0.06
0.08
0.1
0.12
black goby cpue
black goby
cod
(b)
*
obs: sampling
started in 1991
offshore winter monitoring
stock assessement
0
50
100
150
200
250
300
350
1976 1980 1984 1988 1992 1996 2000 2004 2008
cpue
0
5
10
15
20
25
30
35
40
biomass (kg 106)
cod other
cod
(c)
Fig. 1 Trends in larger
predatory fish and
mesopredators in Kattegat,
ICES subdivision 21, the North
Sea. aAbundances of
mesopredators in the coastal
monitoring at Vendelso
¨by the
Swedish Board of Fisheries:
black goby (Gobius niger—
black line), wrasses (Symphodus
melops and Ctenolabrus
rupestris—green line) and shore
crab (Carcinus maenus—
orange line). Cpue denote catch
(numbers) per night per fyke
net. Note that Symphodus
melops was five times more
common than Ctenolabrus
rupestris and therefore
dominated the trend for wrasses.
bAutumn abundances of black
goby (white bars) and cod
(Gadus morhua—black line)in
offshore trawls by the
International Bottom Trawl
Survey (IBTS). All autumn
trawls are from September. The
early autumn is the main season
when cod predates on black
goby in nearshore habitats.
Regular autumn trawls are only
available within IBTS from
1991. Cpue denote catch in kg
per trawl hour. Note that this
survey is aimed at offshore
demersal fish, and the black
goby is therefore only
represented by a fraction of its
true abundance. In 2006,
corresponding nearshore
abundances of black goby
averaged 92 individuals per
beach-seine haul in vegetated
shallow bays along the Swedish
Atlantic coast (Pihl et al. 2006).
Asterisk indicates that there is
no data from the autumn of
2000. cWinter abundances of
cod (black line) and other larger
demersal predators (haddock:
Melanogrammus aeglefinus;
ling: Molva molva; and pollack:
Pollachius pollachius)in
offshore trawls (IBTS), and
stock assessment of the total
biomass of cod in the Kattegat
over time. Scientific winter
trawls for demersal fish have
been performed in February
since 1978. Cpue denote catch
in kg per trawl hour
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cascading effects on coastal food webs. Interestingly, these
cascading effects seem dependent on offshore-inshore
migrations of mesopredators, combined with changes in
interspecific competition, as well as release in predation
pressure (Ljunggren et al. 2010). On the Swedish coast of
the central Baltic Sea, juvenile three-spined stickleback
0
5
10
15
20
25
30
35
40
offshore cod cpue
# coastal wrasses and crabs cpue
# black goby x 10
-2
cpue
(a)
0
5
10
15
20
25
30
35
40
0 100 200 300 400
3456789
Temperature °C
# coastal wrasses and crabs cpue
# black goby x 10
-2
cpue
(b)
Fig. 2 Relation between
coastal abundances of the
mesopredators black goby
(Gobius niger—black dots),
wrasses (group of small bodies
fish—green dots), and shore
crabs (Carcinus meneas—
orange dots) on the Kattegat
coast of Sweden, and aoffshore
abundances of cod (Gadus
morhua) in winter (February),
and bcoastal temperatures in
spring (April). Offshore cod was
sampled by the International
Bottom Trawl Survey (IBTS).
Cpue for cod denote catch per
trawl hour. Coastal abundances
of mesopredators and
temperatures are from the
coastal monitoring at Vendelso
¨
by the Swedish Board of
Fisheries (fish data includes
April and August samplings).
Cpue for mesopredators denote
catch per night per fyke net
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Table 1 Multiple regression results for coastal mesopredatory fish at Vendelso
¨(Kattegat), including offshore cod biomass and local temper-
atures in spring (April) and late summer (August) as additative explanatory variables
Full model Univariate results: spring biomass
offshore cod
Univariate results: coastal spring
temperatures
RF
2,29
PPartial correlation F
1,29
PPartial correlation F
1,29
P
Wrasses (sqrt transformed data) 0.69 13.40 \0.001 -0.60 16.61 \0.001 0.41 5.87 0.022
Common shore crab 0.63 9.35 0.001 -0.49 9.00 0.005 0.43 6.43 0.017
Black goby (sqrt transformed data) 0.83 32.33 \0.001 -0.70 27.14 \0.001 0.69 26.12 \0.001
August temperatures never contributed significantly to the models and were therefore deleted
Fig. 3 Shallow seagrass
(Zostera marina) bed on the
Swedish Atlantic coast
(Fiskeba
¨ckskil), with heavy load
of filamentous macroalgae
(Ectocarpales and Ulva spp.).
Field experiments in the area
show that the summer/autumn
algal accumulation may partly
be caused by an intense
predation from highly abundant
mesopredators on the most
effective herbivore; adult
Gammarus locusta amphipods
(e.g., Moksnes et al. 2008).
Photo: Johan Eklo
¨f
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(Gasterosteus aculeatus)—a smaller predatory fish feeding
on crustacean and gastropod mesograzers (Eriksson et al.
2009; Sieben et al. 2011b)—completely dominate many
sheltered coastal communities in early summer (Eriksson
et al. 2009; Ljunggren et al. 2010). Stickleback changes
distribution over the ontogeny, and after their first summer
the majority migrate offshore (unpublished data). Since the
1980s, the offshore food web in the central Baltic Sea has
changed dramatically, indicating a strong basin-wide
mesopredator release phase (Alheit et al. 2005;O
¨sterblom
et al. 2007; Casini et al. 2008;Mo
¨llmann et al. 2008).
Initially, the offshore Baltic Sea cod populations declined
by 75% during the 1980s, due to climate induced poor
recruitment conditions combined with high fishing pressure
(Fig. 4a; ICES 2010a). This generated a trophic cascade in
the open sea, including a four-fold increase in the domi-
nating pelagic mesopredator sprat (Sprattus sprattus bal-
ticus), a 50% decrease in summer zooplankton biomass,
and a doubling in phytoplankton biomass (Casini et al.
2008). Recently, offshore abundances of stickleback have
increased exponentially (Fig. 4a; Ljunggren et al. 2010),
suggesting a dramatic increase of this mesopredator also in
the coastal habitat. Coastal monitoring of migrating fish is
poor, but a combination of unique data from an open
archipelago of the Swedish Baltic coast (the Kalmar sound)
indicates that the changes in fish community structure in
the open Baltic Sea have also affected nearshore areas. In
the 1970–1980s, high abundances of cod were commonly
registered near the shore, but from the early 1990 cod has
vanished (Fig. 4b) concomitant with the overall collapse of
the Baltic cod stock (Fig. 4a). This suggests that the gen-
eral decline in Baltic cod may have limited the distribution
to offshore areas, excluding the coastal zone. From 1990,
there has also been a continuous decline in the densities of
the dominating larger nearshore predators—European
perch (Perca fluviatilis) and northern pike (Esox lucius)—
in the same area (Fig. 4b). Thus, the recent strong increase
in stickleback may have been enabled by release from
predation both from coastal and offshore predators: the
overwintering stickleback population may have gained
from the declines in offshore cod, whereas the spawning
and juvenile stickleback populations may have gained from
declines of both stationary coastal predators (perch and
pike) and a decreased distribution of Baltic cod. This
emphasizes that changed distributions and simultaneous
migrations of both larger and mesopredatory fish may be
important pathways linking human impacts on offshore
food webs with coastal ecosystems (Fig. 5).
On the Swedish coast of the central Baltic Sea, there is
evidence that the high densities of three-spined stickleback
indirectly increase the load of bloom forming filamentous
algae in shallow bays by controlling mesograzers (Eriksson
et al. 2009; Sieben et al. 2011b). Today, fish communities
in areas with low abundances of perch and pike can be
dominated by abundant three-spined stickleback: an aver-
age haul with a beach seine may contain up to 3,000
individuals (standardized area 100 m
2
, Fig. 6). In stickle-
back-dominated areas, habitat quality is also impacted:
almost 50% of the bays are overgrown by heavy thickets of
filamentous algae (Eriksson et al. 2009; Fig. 6). Notably,
large-scale exclusions of sticklebacks (thousands of indi-
viduals removed using beach seines from 20 930 m
enclosures) in an often overgrown bay decreased the
recruitment of filamentous algae by 60% (Sieben et al.
2011a). Meanwhile, stickleback abundances are much
lower in areas where perch and pike still are abundant
(average haul up to 60 individuals), and only 10% of the
bays are overgrown by algae. This indicates that declines in
larger predators may allow for massive increases in stick-
lebacks and thereby cause cascading negative effects to
lower trophic levels. This is confirmed by small-scale
experimental exclusion of larger fish and grazers, showing
that declines in larger predators—by inducing a four level
trophic cascade—increase filamentous algal growth with
rates comparable to those caused by nutrient enrichment
alone (Eriksson et al. 2009; Sieben et al. 2011b). Food
competition and egg predation by the high abundances of
stickleback may now even contribute to decreased
recruitment success of perch and pike (Nilsson 2006;
Ljunggren et al. 2010), and potentially ‘‘lock’’ the coastal
food web in an alternative, mesopredator-dominated
regime. Thus, overfishing of offshore cod populations may
have contributed to a shift in nearshore food web structure.
MANAGING INTERACTIONS
BETWEEN NEARSHORE COMMUNITIES
AND OFFSHORE FOOD WEBS
The examples provided above makes it increasingly clear
that traditional management of marine resources has severe
limitations, since it often ignores interactions between the
status of coastal habitats and fisheries, cross-system fluxes,
predator–prey interactions as well as other ecosystem
components (Pikitch et al. 2004). EBM may provide a
better platform for coastal management, where one of the
main objectives should be the incorporation of spatial
considerations, as shown by our synthesis. Offshore and
coastal resources are used at different spatial scales with
the potential for cascading detrimental effects both within
and across ecosystems, e.g., cascading effects from off-
shore exploitation of top predators on nearshore biotopes.
Since cross-ecosystem management also crosses geo-
graphical and sectorial management borders and academic
disciplines (e.g., coastal vs. offshore, benthic vs. pelagic,
fisheries vs. water quality, or zoology vs. botany), a shift
792 AMBIO (2011) 40:786–797
123 ÓRoyal Swedish Academy of Sciences 2011
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within management organization structure may be a crucial
first step (Olsson et al. 2008;O
¨sterblom et al. 2010). With
this we mean that measures for protecting or restoring
coastal ecosystems need a broad approach addressing
cumulative impacts that traditionally are managed by
separate management sectors: including restoration of
offshore food webs, improvements in water quality and
increased habitat protection through implementation of
marine protected areas (Lotze et al. 2006). Furthermore,
changes in offshore and coastal food webs co-occur with
major changes in large-scale hydrodynamics and transport
through human engineering and climate change (Harley
et al. 2006; Eriksson et al. 2010), external nutrient loading
by eutrophication (Cloern 2001) and habitat destruction
through coastal development and dredging (Airoldi and
Beck 2007). Therefore, cascading effects of increases in
mesopredator abundances will most likely interact with
other human-driven changes in environmental conditions
and abiotic resources, eventually altering the functions of
coastal communities (Fig. 5; Olff et al. 2009; Eriksson
et al. 2010). A crucial development of EBM is to
acknowledge and jointly approach these multiple and
potentially interacting drivers of cross-ecosystem changes
(e.g., fisheries, eutrophication, and habitat destruction),
instead of—as in the past—dealing with them in isolation.
For example, overexploitation of offshore fish popula-
tions has triggered governmental actions to rebuild com-
mercially important stocks and ensure sustainable fisheries.
However, single-species management of fish stocks does
usually not account for the complexity of food web inter-
actions, especially those that link different ecosystems. Our
results emphasize that to meet management goals for
coastal areas we need to rebuild predator populations not
only to maximize production of the target species, but to
levels at which their ecological function is restored, both in
offshore and coastal food webs. This includes increasing
the abundance of offshore populations of larger predatory
fish to restore their control over lower trophic levels and to
0
0.5
1
1.5
2
# cod 10
9
0
1
2
3
4
5
6
7
# sprat 10
10
# stickleback 10
4
(cpue)
cod sprat stickleback
(a)
0
500
1000
1500
2000
2500
1970 1980 1990 2000
# piscivorous fish (cpue)
cod pike perch
(b)
Fig. 4 Trends in aoffshore abundances of cod (stock assessment
estimates, ICES 2010a), sprat (acoustic estimates from the ordinary
international acoustic survey, ICES 2010b) and stickleback (trawl
hauls made during the ordinary international acoustic survey), and
bcoastal abundances of larger predators: cod, perch and pike together
with local recruitment of perch and pike (in boxes: the number of
young of the year fish YOY). aSprat and stickleback data are from
ICES subdivision 27, cod data are from subdivisions 25–32. Cod and
sprat are estimated total numbers, while stickleback cpue is number
per trawl hour. bTrap-net monitoring data (catch per night per trap)
of cod, perch and pike between 1970 and 2002 from Ga
˚so
¨(Mo
¨nstera
˚s,
county of Kalmar) on the southeast coast of Sweden. The Ga
˚so
¨data is
part of a larger time-series from four sites around a paper plant
(Mo
¨nstera
˚s bruk) which stops in 2003. Here, we present data
exclusively from Ga
˚so
¨, the site most affected by the open sea, because
it is a good representation of fish both from the fresh-water and
marine communities. Full pike data is presented in Sect. 1in the
electronic supplement to Ljunggren et al. (2010). Estimates of high,
low and no recruitment of perch and pike are also based on Ljunggren
et al. (2010)
AMBIO (2011) 40:786–797 793
ÓRoyal Swedish Academy of Sciences 2011
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restore significant migrations between offshore and coastal
habitats (Fig. 5). It also means rebuilding nearshore pop-
ulations of larger predatory fish to restore their ecological
function along the coast. In our case-studies, this implies
that to improve the quality of coastal habitats, we will need
to combine nutrient reductions and habitat restoration with
fisheries specific targets. On the Atlantic coast of Sweden,
we need to strengthen offshore populations of cod to pro-
mote significant coastal migrations, as well as rebuilding
local nearshore populations of cod. In the Baltic Sea, we
need to strengthen the cod population until its distribution
area expands to include coastal habitats, and we need to
rebuild local populations of pike and perch by protecting
and restoring their spawning areas. These are specific case-
studies that span two different types of coast: one in an
enclosed brackish water sea and one bordering the highly
exploited North Sea continental shelf. However, offshore
fisheries and coastal exploitation are global forces that have
had significant effects on continental seas world-wide
(Lotze et al. 2006, Worm et al. 2006). Examples from both
Fig. 5 Suggested human-driven shifts in the structure of higher
trophic levels in marine food webs and resulting consequences for the
relation between offshore and nearshore fish communities (see also
Eriksson et al. 2010). aHistoric drivers: diverse communities of apex
predators and natural climate forcing influenced offshore fish
communities. Coastal areas had a strong function as recruitment
areas for offshore fish from all trophic levels, which resulted in top-
down control of the near shore fish communities. bPresent drivers:
commercial fishing has skewed the offshore communities toward
dominance by mesopredators. Such mesopredator release events
increase the abundance of planktivorous and/or facultative planktiv-
orous fish (fish that eat both plankton and benthic mesograzers) in
nearshore habitats, which cause food competition and egg predation,
and thereby may limit the recruitment of stationary fish. Declining
populations of stationary piscivores and/or limited migrations of
offshore piscivorous fish to nearshore areas in combination with
increasing resource loads, may enhance bottom-up control of the
nearshore ecosystem. Specific effects of climate change are not well
understood (Harley et al. 2006)
794 AMBIO (2011) 40:786–797
123 ÓRoyal Swedish Academy of Sciences 2011
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the Pacific and the western Atlantic also support that off-
shore trophic cascades or changes in migration patterns of
offshore predators, can have cascading effects on coastal
food-webs (reviewed in Baum and Worm 2009). Thus, the
offshore coastal linkages described in our study systems
may be relevant for a wide range of developed coasts that
border highly exploited offshore systems.
Acknowledgments Johan S. Eklo
¨f was funded by FORMAS (grants
no. 2008-839 and 2009-1086). The contribution of Jens Olsson,
Michele Casini, and Ulf Bergstro
¨m was made within the PLAN FISH
project funded by the Swedish Environmental Protection Agency.
Thanks to Han Olff and Helmut Hillebrand for inspiring discussions
about cross ecosystem and predator removal effects, to Gustav
Johansson for artwork and to Per Olov Moksnes and an anonymous
reviewer for constructive comments on an earlier version of the
manuscript.
Fig. 6 Bloom of filamentous
algae in shallow bays with high
densities of three-spined
stickleback (Gasterosteus
aculeatus) on the Swedish coast
of the central Baltic Sea. Top
From above the surface of a bay
dominated by Fucus vesiculosus
overgrown with predominantly
unbranched green microalgae
(e.g., Ulotrix spp., Urospora
spp.) and colonial diatoms (e.g.
Melosira spp.). Photo: Gustav
Johansson. Bottom Under the
surface in a bay dominated by
Myriophyllum sp. and
Potamogeton sp. overgrown
with filamentous macroalgae
(mainly Cladophora glomerata,
Ectocarpus siliquosus and
Pylaiella littoralis). Photo: Ulf
Bergstro
¨m
AMBIO (2011) 40:786–797 795
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AUTHOR BIOGRAPHIES
Britas Klemens Eriksson (&) is an assistant professor at the
Department of Marine Benthic Ecology and Evolution, the Centre for
Ecological & Evolutionary Studies, University of Groningen. He
holds a PhD in Plant Ecology from Uppsala University. His research
deals with effects of resource exploitation and biodiversity loss on the
function of coastal ecosystems.
Address: Department of Marine Benthic Ecology & Evolution, Centre
for Ecological & Evolutionary Studies, University of Groningen, P.O.
Box 11103, 9700 CC Groningen, The Netherlands.
e-mail: b.d.h.k.eriksson@rug.nl
Katrin Sieben is a doctoral candidate at the Department of Marine
Benthic Ecology and Evolution, the Centre for Ecological & Evolu-
tionary Studies, University of Groningen. Her research focuses on
testing cascading effects of changing coastal fish communities on
lower trophic levels in coastal food-webs.
Address: Department of Marine Benthic Ecology & Evolution, Centre
for Ecological & Evolutionary Studies, University of Groningen, P.O.
Box 11103, 9700 CC Groningen, The Netherlands.
Johan Eklo
¨fis a post-doc at the Department of Marine Ecology at
Gothenburg University, and has a part-time position as researcher at
the Department of Systems Ecology, Stockholm University. He holds
a PhD in marine ecotoxicology from the Stockholm University. He
works with food-web ecology, ecosystem dynamics and management
of shallow benthic ecosystems.
Address: Department of Systems Ecology, Stockholm University, 106
91 Stockholm, Sweden.
Lars Ljunggren is a researcher associated to the Institute of Coastal
Research at the Swedish University of Agricultural Sciences. He
holds a PhD in Fisheries Biology from the Swedish University of
Agricultural Sciences. He works with fisheries and water quality
assessment.
Address: Institute of Coastal Research, Swedish University of Agri-
cultural Sciences, Skolgatan 6, 74242 O
¨regrund, Sweden.
Jens Olsson is a researcher at the Institute of Coastal Research at the
Swedish University of Agricultural Sciences. He holds a PhD in
limnology from the Uppsala University. He works with integrated
ecosystem analysis of coastal systems, coastal fish ecology and
population genetics.
Address: Institute of Coastal Research, Swedish University of Agri-
cultural Sciences, Skolgatan 6, 74242 O
¨regrund, Sweden.
Michele Casini is a researcher at the Institute of Marine Research at
the Swedish University of Agricultural Sciences. He holds a PhD in
marine ecology from the Gothenburg University. He works with fish
stock assessment and management, food-web ecology and ecosystem
dynamics.
Address: Institute for Marine Research, Swedish University of
Agricultural Sciences, Box 4, 45321 Lysekil, Sweden.
Ulf Bergstro
¨mis a researcher at the Institute of Coastal Research at
the Swedish University of Agricultural Sciences. He holds a PhD in
marine ecology from the Umea
˚University. His work concerns habitat
and food web ecology, and applications within management of coastal
ecosystems.
Address: Institute of Coastal Research, Swedish University of Agri-
cultural Sciences, Skolgatan 6, 74242 O
¨regrund, Sweden.
AMBIO (2011) 40:786–797 797
ÓRoyal Swedish Academy of Sciences 2011
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