For Peer Review - core.ac.uk · For Peer Review 2 43 Abstract 44 45 The eastern Baltic cod stock has recently started to recover, after two decades of severe 46 depletion, however

For Peer Review

Spatial management of marine resources can enhance the

recovery of predators and avoid local depletion of forage fish

Journal: Conservation Letters

Manuscript ID: CONL-12-0017.R2

Manuscript Type: Letters

Date Submitted by the Author: n/a

Complete List of Authors: Eero, Margit; Technical University of Denmark, National Institute of Aquatic

Resources Vinther, Morten; Technical Unoversity of Denmark, National Institute of Aquatic Resources Haslob, Holger; Helmholtz Centre for Ocean Research Kiel, Huwer, Bastian; Technical University of Denmark, National Institute of Aquatic Resources Casini, Michele; Swedish Institute of Agricultural Sciences, Departement of Aquatic Resources Storr-Paulsen, Marie; Technical University of Denmark, National Institute of Aquatic Resources Köster, Friedrich; Technical University of Denmark, National Institute of Aquatic Resources

Keywords: predator-prey overlap, stock recovery, species distribution, food limitation, ecosystem based fisheries management, Baltic Sea, cod, forage fish, local depletion

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Spatial management of marine resources can enhance the recovery of predators and avoid 1

local depletion of forage fish 2

3

Margit Eero1, Morten Vinther

1, Holger Haslob

2*, Bastian Huwer

1, Michele Casini

3, Marie Storr-4

Paulsen1, Friedrich W. Köster

1 5

6 1Technical University of Denmark, National Institute of Aquatic Resources, Charlottenlund 7

Castle, DK- 2920, Charlottenlund, Denmark 8 2Helmholtz Centre for Ocean Research Kiel (GEOMAR), Düsternbrooker Weg 20, 24105, Kiel, 9

Germany 10 3Swedish University of Agricultural Sciences, Department of Aquatic Resources, Institute of 11

Marine Research, 45330 Lysekil, Sweden 12

*present address: Thünen-Institute of Sea Fisheries, Palmaille 9, 22767, Hamburg, Germany 13

14

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Emails: [email protected] (M.E.); [email protected]( M.V.); [email protected] (H.H); 16

[email protected] (B.H.); [email protected] (M.C.); [email protected] (M.S-P.); 17

[email protected] (F.W.K) 18

19

Running title: spatial management of marine ecosystem 20

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Key words: Baltic Sea, cod recovery, ecosystem based fisheries management, food limitation, 22

forage fish, local depletion, predator-prey overlap, species distribution 23

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Type of article: a letter 25

Number of words: 147 (abstract); 2839 (main text) 26

Number of references: 40 27

Number of figures: 5 28

Number of tables: 0 29

30

Corresponding author: 31

32

Margit Eero 33

Technical University of Denmark 34

National Institute of Aquatic Resources 35

Charlottenlund Castle, 2920 Charlottenlund, Denmark 36

Tel.:+45 3588 3318 37

Fax: +45 3588 3333 38

Email: [email protected] 39

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Page 1 of 24 Privileged Communication

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Abstract 43

44

The eastern Baltic cod stock has recently started to recover, after two decades of severe 45

depletion, however with unexpected side-effects. The stock has not re-occupied its former wide 46

distribution range, but remains concentrated in a limited area in the southern Baltic Sea. The 47

biomass of forage fish, i.e. sprat and herring, is historic low in this area, which in combination 48

with increasing cod stock results in locally high predation mortality of forage fish and 49

cannibalism of cod. In line with low prey availability, body weight and nutritional condition of 50

cod drastically declined. In the southern Baltic Sea, cod competes with pelagic fisheries for the 51

limited resources of sprat and herring, while the largest biomass of these species is currently 52

found outside the distribution range of cod. Accounting for spatial overlap between species is 53

crucial in developing ecosystem based fisheries management to enhance the recovery of predator 54

stocks. 55

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Introduction 59

60

In order to achieve healthy marine ecosystems, an ecosystem-based approach to fisheries 61

management has been widely acknowledged as the fundamental principle for sustainable 62

resource use (Pikitch et al. 2004; McLeod & Leslie 2009). The underlying aim of this approach 63

is ecologically sound resource management that responds to ecosystem processes, including 64

species interactions (Marasco et al. 2007). The concerns of marine animal population’s 65

conservation and recovery are today largely focused on predator species, which have declined 66

worldwide over the past decades (Myers & Worm 2003). Species interactions are considered to 67

influence their recovery mainly through mortality due to predation (MacKenzie et al. 2011; 68

Swain & Mohn 2012). In contrast, the abundance of forage fish as a food resource for predators 69

is usually not included in management strategies aimed to recover the predator stocks. This is 70

probably because declines in predator species have in many cases been followed by a 71

pronounced increase in prey biomass (Myers and Worm 2003; Baum & Worm 2009), and food 72

limitation for recovering predator populations is therefore not expected. 73

74

Nevertheless, the ecosystems where predator species have to recover may have different 75

structural and functional properties from those where they once were abundant (Bakun and 76

Weeks 2006; Hammer et al. 2010). Recovery potential of predators may be affected by factors 77

such has changes in habitats and species interactions, which may include spatial overlap between 78

the predators and prey (Kempf et al. 2010). Especially in a wasp-waist type ecosystem like the 79

Baltic Sea, where a few forage fish species dominate the intermediate trophic level, changes in 80

abundance or distribution of these species can have large implications for higher trophic levels 81


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(Bakun 2006; Smith et al. 2011). In the Baltic Sea, cod has been severely depleted for about 20 82

years during which a major restructuring of the ecosystem has occurred (Möllmann et al. 2009; 83

Casini et al. 2009), including an increase in the biomass of sprat, i.e. one of the major prey 84

species for cod (Köster et al. 2003). Since 2007, the eastern Baltic cod population has started to 85

recover, partly due to effective management measures (Eero et al. 2012). Unexpectedly, and 86

despite the biomass still being relatively low compared to historical levels, recent observations 87

show that the cod has become lean, which indicates food limitation. 88

89

In this paper we apply a spatially resolved multi-species model for the Baltic Sea to elucidate 90

area-specific population dynamics of adult cod and its major fish prey (sprat and herring), 91

including spatially explicit predation mortalities by cod. Further, we document recent changes in 92

body weight and nutritional condition of cod and relate these to the local availability of sprat and 93

herring. Our analyses highlight the need for taking into account species distribution in 94

developing ecosystem based fisheries management strategies, to sustain a sufficient prey biomass 95

in the areas of high predator abundance to enhance its recovery and at the same time avoid local 96

depletion of forage fish. 97

98

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Material and methods 100

101

Spatially resolved biomasses and predation mortalities of cod, sprat and herring 102

103


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The eastern Baltic cod is assessed and managed as one stock unit covering ICES Subdivisions 104

(SD) 25–32 in the Baltic Sea (see Fig. 1 for location of SDs). Sprat is considered as one stock for 105

the entire Baltic Sea (SD 22–32), while the central Baltic herring assessment and management 106

cover SD 25–29&32. In this paper, biomasses and predation mortalities of the three species were 107

estimated separately for four areas in the Baltic Sea, i.e. SD 25, SD 26, SD 28 and SD 27, 29 and 108

32 combined (Fig. 1). For the purpose of investigating the dynamics of predators compared to 109

prey, cod stock size was represented by numbers of individuals instead of biomass, as the body 110

weight incorporated in biomass is already influenced by prey availability. 111

112

The analyses were conducted applying a Stochastic Multi Species (SMS) model (Lewy & 113

Vinther 2004), which is regularly used for scenario forecasts and management strategy 114

evaluations in the Baltic and North Sea. The SMS includes estimation of predation mortalities 115

from observation of catches, survey indices and stomach contents. The predation mortalities of 116

sprat and herring represent predation by cod. Predation mortality on young age-groups of cod 117

represents cod cannibalism. The data on stock distribution by year and quarter were derived from 118

research surveys supplemented with information from commercial catches. A description of the 119

model procedures related to estimation of predation mortalities and area-specific stock sizes is 120

provided in Supplement 1, including the sources where further information on the model can be 121

found. 122

123

Mean weight and energy status of cod 124

125


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Changes in mean weight of cod by age in SD 25 were analysed using international data from 126

commercial catches for 1976–2010. Anomalies in cod weight by age and year were calculated as 127

difference from the long-term mean. To supplement the information on changes in mean weight 128

with indices of energy status of cod, Fulton’s condition factor (K) and hepatosomatic condition 129

index (HSI) were calculated. Analyses of Fulton’s condition factor (K) were based on data on 130

total length (Lt) and whole weight (W) of individual cod sampled on Danish and German 131

research cruises in SD 25, in the 1st and 2

nd quarter of the year, in the period from 1994 to 2011. 132

The analyses included adult cod between 40 and 60 cm in length (approximately 400–2000 fish 133

per year). The cod with Fulton’s K below 0.8 were classified as being in low condition, 134

according to Marteinsdottir and Begg (2002). Hepatosomatic condition index (HSI) was 135

calculated for pre-spawning time based on data from German research cruises in the 2nd

quarter 136

of the year (1996–2011), as the ratio between liver weight (WL) and ovarian free body weight, 137

i.e. total weight (W) minus ovary weight (WO) (Marteinsdottir & Begg 2002): 138

139

O

L

WW

WHSI

−= *100 140

The hepatosomatic index was estimated only for females, at 40–60 cm and >60cm in length 141

(based on approximately 200–400 and 10–20 fish per year, respectively). 142

143

Cod stomach data 144

145

On German research surveys in the 2nd

and 3rd

quarter in 1999–2011, cod stomachs have been 146

recorded as empty or containing food items. The proportion of non-empty stomachs in each year 147


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was calculated as an average of the data for the two quarters, for all length-groups combined. 148

The analyses excluded juveniles as well as individuals at a stage of active spawning. 149

150

Results 151

152

The abundance of adult cod (age-groups 4 and older) in the entire eastern Baltic Sea (SD 25–32) 153

is currently estimated to be only about a half of the historic high stock size observed in the early 154

1980s. However, in SD 25, the present density of cod is close to the highest level in the time-155

series since the 1970s (Fig. 2). Since 2007, the number of cod in this area sharply increased, 156

whereas in the northeastern Baltic Sea (SD 26–32), the abundance of cod has been relatively low 157

since the 1990s. Thus, most of the adult cod is currently concentrated in SD 25. In contrast, only 158

about 10–15 percent of the herring and sprat biomass is distributed in SD 25. Largest 159

concentrations of both species are found in SDs 28–32, i.e. out of the current distribution area of 160

cod. 161

162

The relatively low biomass of clupeids (sprat and herring) in combination with an increasing cod 163

stock in SD 25 has resulted in a steep decline in the ratio of prey to predators, with the lowest 164

biomass of clupeids relative to the abundance of cod in 2009–2010 (Fig. 3). Concurrent with the 165

decline in prey biomass, mean weight of larger cod (age-groups 4–7) sharply declined to record 166

low values since 2007 (Fig. 3). In line with reduced prey availability, the proportion of cod with 167

food in the stomachs declined from 50 percent in the early 2000s to 20 percent in 2011 (Fig. 3). 168

Moreover, in the 1990s–early 2000s, almost no cod in SD 25 were found in low somatic 169

condition, i.e. had Fulton’s K values below 0.8, whereas in 2011, 15 percent of cod at 40–60 cm 170


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in length was at such low condition (Fig. 4). Also, the average hepatosomatic condition (HSI) of 171

cod is currently the lowest in the time-series since 1996 (Fig. 4). 172

173

The high density of cod in SD 25 is reflected in a pronounced cannibalism taking place in this 174

area, compared with much lower or negligible predation mortalities of young cod (age-groups 0–175

2) estimated for the other areas (SD 26–32) (Fig. 5). Similarly, predation pressure on sprat and 176

herring is highest in SD 25, with intermediate levels in SD 26 and almost no predation in SD 27–177

32 (Fig. 5). Fisheries in the Baltic Sea are targeting all three species and are conducted in the 178

entire distribution area of the stocks. Sprat and herring in SD 25 are currently harvested at a 179

similar rate than the stock components distributed in SD 26–32 (Fig. 5). Consequently, the small 180

stock components of sprat and herring located in SD 25 are exposed to a high pressure both from 181

exploitation and predation. In contrast, the abundant resources of clupeids in the northern areas 182

(SD 28–32) are less utilized (Fig. 5). 183

184

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Discussion 186

187

The ecological consequences of declines in marine predator populations are well-documented, 188

including trophic cascade effects, which have in some cases led to major restructuring of food 189

webs (Pace et al. 1999; Shurin et al. 2002). In contrast, the ecological effects of the return of a 190

predator to such ecosystem are less clear. The Baltic Sea is an example of an ecosystem that has 191

undergone major structural changes subsequent to a more than ten-fold decline in cod biomass 192

from the late 1980s to the 1990s (Möllmann et al. 2009; Casini et al. 2009). Before the late 193


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1980s, cod was widely distributed in the entire Baltic Proper (Aro 2000; Eero et al. 2007). The 194

collapse of cod involved a contraction of the stock to SD 25 in the southern Baltic Sea (Fig. 2). 195

The hydrographic conditions in the eastern spawning grounds (in SDs 26&28) did no longer 196

allow for regular survival of cod eggs, and SD 25 has been basically the only area supporting 197

successful reproduction of the eastern Baltic cod since the mid-1980s (Köster et al. 2009). The 198

recent recovery of cod in SD 25 has resulted in the highest cod abundance recorded in this area 199

in the time series since the 1970s (Fig. 2), which is also higher than the historical estimates going 200

back to the 1950s (Eero et al. 2007). The stocks of the main pelagic prey for cod, sprat and 201

herring, have on the other hand increased in the northern Baltic since the early 1990s (Casini et 202

al. 2011). Our study suggests that in this largely modified ecosystem set-up, the carrying 203

capacity for cod in SD 25 may have been reached, indicated by record low weight and 204

deteriorated condition of adult cod. 205

206

Variations in cod growth in other regions of the North Atlantic have been linked to density-207

dependent effects and hydrological conditions, or a combination of both (Swain et al. 2003 and 208

references therein). The growth of the eastern Baltic cod has been described earlier as density 209

dependent and affected by the relative availability of clupeid prey (Baranova 1992). In addition, 210

oxygen concentration affects cod metabolism with impacts on growth and condition (Hinrichsen 211

et al. 2011). Therefore, variable hydrographic conditions by sub-regions in the Baltic Sea 212

prevent direct comparisons of cod weight and condition between sub-areas in relation to prey 213

availability. However, the sharp decline in cod weight in SD 25 since 2007, concurrent with a 214

rapid local increase of the stock size, can hardly be due oxygen conditions affecting cod 215

physiology and growth directly, as oxygen conditions deteriorated already since the 1990s 216


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(Hinrichsen et al. 2011). This suggests that the recent dramatic change in cod growth in SD 25 is 217

due to food limitation and density-dependence. 218

219

In addition to clupeid prey, adult cod is cannibalistic and preys as well on benthic invertebrates 220

(Uzars 1994). Utilization of benthic food resources by cod is believed to be reduced at low 221

oxygen concentrations in deeper water layers, when cod is more pelagic (Schaber et al. 2009). At 222

present ecological conditions, the alternative food resources seem not to be able to compensate 223

for the shortage of clupeids in SD 25, indicated by an increasing proportion of empty stomachs 224

and a close correspondence between the availability of sprat and herring and the weight of adult 225

cod in this area (Fig. 3). However, the extent of movement of cod into areas with better feeding 226

conditions and the factors preventing or promoting this need to be investigated to improve the 227

process knowledge of the current ecological status of the Baltic Sea. 228

229

Multi-species and ecosystem models are considered as necessary tools to further develop 230

ecosystem based fisheries management and evaluate the ecosystem consequences of proposed 231

management actions (Sainsbury et al. 2000). Importantly, multi-species tradeoffs and community 232

responses to management schemes need to be examined across broader spatial scales (Kellner & 233

Hastings 2009; Bartolino et al. 2012). The recent developments in the Baltic Sea support the 234

importance of incorporating spatial aspects in the analyses of species interactions, to be able to 235

identify processes, which operate on a local scale, but potentially have wider ecosystem 236

consequences. At the present distribution of the fish stocks in the Baltic Sea, intensive predator-237

prey interactions are taking place only in a limited area in the southern Baltic Sea. The present 238

density-dependence and related high cannibalism of cod can be expected to have negative 239


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impacts on cod recruitment. However, as a counteracting mechanism, low abundance of clupeids 240

reduces predation pressure on cod eggs (Köster et al. 2003). Further, the current food limitation 241

and consequent low weight and condition of adult cod in its main reproduction and distribution 242

area may lower the productivity of the stock (Rätz and Lloret 2003) and limit its further 243

recovery. At the same time, fisheries are competing with cod for the limited resources of sprat 244

and herring in this area, which results in a substantially higher mortality on these local stock 245

components of forage fish compared to the abundant resources distributed in the northern Baltic 246

Sea. 247

248

Forage fish are generally considered a central part of the ecosystem based fisheries management, 249

especially to avoid ecosystem overfishing when forage species, which serve as a prey for other 250

fish and marine top-predators, are also targeted by fisheries (Pikitch et al 2004). However, the 251

spatial scale at which these mechanisms operate is usually not explicitly considered in 252

management strategies, although the importance of spatial heterogeneity and dynamics in marine 253

ecosystems is increasingly recognized (Lorenzen et al. 2010). Spatial fisheries management 254

measures are conventionally implemented in the form of spatio-temporal closures to protect 255

threatened species or habitats, while the use of spatial management measures to protect prey 256

biomass for predator fish is not common. Concerns of local food limitations usually relate to 257

charismatic marine top predators such as sea lions (Witherell et al. 2000) or seabirds (Cury et al. 258

2011), which in some cases has led to fisheries moratoria on local prey populations (Greenstreet 259

et al. 2006). 260

261


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The eastern Baltic cod is one of the first examples of partial recovery of a heavily exploited 262

demersal fish stock in North Atlantic waters in recent decades. The unexpected density 263

dependent effects which have become apparent in the core distribution area of the stock illustrate 264

that novel management measures are increasingly needed to support the recovery of predator 265

species in ecosystems, which in fact may not be any longer structured to sustain large cod stocks 266

(Frank et al. 2005). The present situation in the Baltic, with a high cod stock in the south and 267

large biomass of clupeids in the north, calls for a spatially explicit management of these 268

resources. A decrease in fishing pressure on clupeids in the south would likely enhance cod 269

growth in the area and thus have a positive effect on cod recovery. On the other hand, a relatively 270

higher fishing pressure on clupeids in the north could release clupeid competition in these areas 271

(Casini et al. 2011), and release prey-to-predator feedback loops (Bakun and Weeks 2006), 272

which could also be beneficial for cod in case the hydrological conditions would allow cod to 273

spawn in more northern areas. 274

275

With increasing use of the marine environment, spatial aspects in marine management are getting 276

increasingly important including conservation issues which are becoming an integral part of the 277

overall spatial planning (Mackelworth 2012). Implementation of ecosystem approach to fisheries 278

management should be seen in conjunction with this process, given the spatial heterogeneity in 279

fish populations (Norse et al. 2010). The Baltic Sea is currently chosen as a pilot case for taking 280

into account biological interactions in the new fisheries management plans being under 281

development in the European Commission. Thus, the experiences from the Baltic Sea can serve 282

as a basis for similar developments elsewhere. This study is intended to contribute to this process 283

by highlighting the importance of taking into account biological interactions at an appropriate 284


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spatial scale, in order to achieve a healthy balance between species, on both local and regional 285

sea wide scales. 286

287

288

Acknowledgements 289

290

The research leading to these results has received funding from the European 291

Community’s Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. 292

266445 for the project Vectors of Change in Oceans and Seas Marine Life, Impact on Economic 293

Sectors (VECTORS) and EU FP7 Integrated Project 212085 (MEECE). The results of this study 294

contribute to the FP7 project FACTS (024966). MC was partially funded by the Swedish project 295

“Planktivore management—linking food web dynamics to fisheries in the Baltic Sea” (PLAN 296

FISH). The efforts of ICES working groups over past decades producing area-disaggregated data 297

for the Baltic fish stocks, utilized in this paper, are greatly acknowledged. 298

299

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Figure captions 413

414

Figure1. ICES Subdivisions (SD) in the Baltic Sea, indicating the units applied for area-based 415

analyses (SD 25; SD 26, SD 28 and SD 27+29+32). 416

417

Figure 2. Time series of annual average abundance of adult cod (age-groups 4 and older), and 418

total biomass of sprat and herring, by area. 419

420

Figure 3. Anomalies in mean weight of cod (average of age-groups 4–7) in SD 25 (bars) 421

compared with changes in the biomass of clupeids (sprat and herring) relative to the number of 422

adult cod (at age 4 and older) in the same area (line). The stars show the proportion of cod 423

stomachs containing food items. 424

425

Figure 4. The percentage of cod at 40–60cm in length caught in SD 25 in 1994–2011, which 426

were at low somatic condition (Fulton’s K<0.8) (bars); and average hepatosomatic condition 427

index (HSI) of female cod in SD 25 in 1996–2011, by length-groups (40–60cm, >60cm), in the 428

second quarter of a year. The error bars represent standard error of the mean. 429

430

Figure 5. Panels a-c: Spawning stock biomass (SSB) of cod, sprat and herring, including the 431

proportion of catch (shown as sectors of SSB), by area (Subdivisions (SD)), in 2010. Panels d-f: 432

Predation mortality of cod, sprat and herring, for age-groups 0–2, by area (based on average 433

estimates for 2009–2010). 434

435


For Peer Review

Figure 1.


For Peer Review

Figure 2


For Peer Review

Year

1975 1980 1985 1990 1995 2000 2005 2010

Anomalies of cod weight

-0.3

-0.2

-0.1

0.0

0.1

0.2

0.3

0.4

Clupeids / Cod

0

10

20

30

40

50

60

Proportion of stomachs

0.1

0.2

0.3

0.4

0.5

0.6

Cod weight Clupeids / CodStomachs with food items

Figure 3


For Peer ReviewYear

1994 1996 1998 2000 2002 2004 2006 2008 2010

Proportion of cod at low condition (Fulton K<0.8)

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.16

0.18

Hepatosomatic condition index (HSI)

3

4

5

6

7

8

9

Fulton K < 0.8, 40-60 cm

HSI, 40-60 cm

HSI, >60 cm

Figure 4


For Peer Review

Figure 5.


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For Peer Review - core.ac.uk · For Peer Review 2 43 Abstract 44 45 The eastern Baltic cod stock has recently started to recover, after two decades of severe 46 depletion, however