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DIRECTORATE GENERAL FOR INTERNAL POLICIES

POLICY DEPARTMENT B: STRUCTURAL AND COHESION POLICIES

FISHERIES

DOES OVERFISHING PROMOTE ALGAL BLOOMS?

NOTE

This document was requested by the European Parliament's Committee on Fisheries. AUTHOR Britas Klemens ERIKSSON Department of Marine Benthic Ecology and Evolution, Centre for Ecological and Evolutionary Studies, University of Groningen The Netherlands RESPONSIBLE ADMINISTRATOR Irina POPESCU Policy Department Structural and Cohesion Policies European Parliament E-mail: [email protected] EDITORIAL ASSISTANCE Virginija KELMELYTE LINGUISTIC VERSIONS Original: EN Translations: DE, ES, FR, IT, PT ABOUT THE EDITOR To contact the Policy Department or to subscribe to its monthly newsletter please write to: [email protected] Manuscript completed in November 2011. Brussels, © European Parliament, 2011. This document is available on the Internet at: http://www.europarl.europa.eu/studies DISCLAIMER The opinions expressed in this document are the sole responsibility of the author and do not necessarily represent the official position of the European Parliament. Reproduction and translation for non-commercial purposes are authorized, provided the source is acknowledged and the publisher is given prior notice and sent a copy.

http://www.europarl.europa.eu/studies

DIRECTORATE GENERAL FOR INTERNAL POLICIES

POLICY DEPARTMENT B: STRUCTURAL AND COHESION POLICIES

FISHERIES

DOES OVERFISHING PROMOTE ALGAL BLOOMS?

NOTE

Abstract This note provides scientific evidence for a connection between overfishing and the development of algal blooms, and presents several European case-studies supporting this hypothesis. Overfishing has contributed to the increasing problem of algal blooms in Europe. Over-exploitation of offshore stocks has changed the structure of many marine ecosystems, which has promoted the accumulation of algal biomass. Today, detrimental effects of overfishing on offshore food webs are spreading to coastal ecosystems, causing problems with near shore water quality and habitat loss.

IP/B/PECH/IC/2011-105 November 2011 PE 474.461 EN

Does overfishing promote algal blooms?

CONTENTS

LIST OF ABBREVIATIONS 5

LIST OF FIGURES 7

LIST OF TABLES 9

EXECUTIVE SUMMARY 11

1. INTRODUCTION 15

2. TYPES AND EFFECTS OF ALGAL BLOOMS 19

2.1. What are algal blooms? 19

2.2. Ecological effects of algal blooms 19

2.3. Harmful algal groups 20

2.4. General societal problems and costs 22

2.5. Specific effects on fisheries in Europe 23

3. THE ECOLOGY OF ALGAL BLOOMS 27

3.1. A natural process that increases in frequency with eutrophication 27

3.2. Nutrients and grazing together control algal bloom development 30

3.3. Decreases in top predatory fish coincide with increases in algae 32

3.4. Trophic cascades depend on resources and predator diversity 33

4. DOES OVERFISHING CONTRIBUTE TO ALGAL BLOOMS IN EUROPE? 37

4.1. Modelling effects of overfishing and eutrophication 37

4.2. The North Sea case study 40

4.3. The Black Sea case study 42

4.4. The Kattegat case study 46

4.5. The Baltic Sea – offshore case study 49

4.6. The Baltic Sea – coastal case study 53

5. CONCLUSIONS AND RECOMMENDATION 57

REFERENCES 61

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Policy Department B: Structural and Cohesion Policies

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LIST OF ABBREVIATIONS

ASP Amnesic Shellfish Poisoning

CFP Ciguatera Fish Poisoning

CPUE Catch Per Unit Effort

DSP Diarrhetic Shellfish Poisoning

EBM Ecosystem-Based Management

FK Fish Killing algal blooms

GLM General Linear Model

HAB Harmful Algal Bloom

HBT High Biomass Toxic algal blooms

HBNT High Biomass Non-Toxic algal blooms

NAO North Atlantic Oscillation

PSP Paralytic Shellfish Poisoning

NSP Neurotoxic Shellfish Poisoning

ST Seafood Toxic algal blooms

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LIST OF FIGURES Figure 1: Potential effects of overfishing on marine food-web structure showing a connection between fisheries and algal blooms 16

Figure 2: Groups of organisms and different types of harmful algal blooms. 19

Figure 3: An increased in algal biomass over time in the Black Sea 27

Figure 4: Duration of the algal bloom season in the Wadden Sea 29

Figure 5: Areal extent of the peak cyanobacterial bloom in the Baltic Sea 1997-2009. 30

Figure 6: The relative effect of grazers on the biomass of algae. 31

Figure 7: Fishery induced declines in top predators coincide with abrupt increases in the standing stock of algae in the north Atlantic, Baltic Sea and Black Sea. 32

Figure 8: Nutrient enrichment accumulate on different trophic levels depending on the number of trophic levels in the ecosystem. 35

Figure 9: Generic food web of a temperate pelagic nearshore ecosystem. 38

Figure 10: Generic food web of a temperate pelagic nearshore ecosystem. 39

Figure 11: Trends in landings of large and small fish in the North Sea 41

Figure 12: Trends in landings of large pelagic species in the North Sea 41

Figure 13: Trends in landings of large demersal species in the North Sea 41

Figure 14: Trends in abundance of algae in the North Sea 42

Figure 15: Trends in mean trophic level of landings in the North Sea 42

Figure 16: Trends in landings of tuna and billfishes from Black Sea fisheries 44

Figure 17: Trends in landings of small and medium sized pelagic species in the Black Sea 44

Figure 18: Trends in mean trophic level of landings in the Black Sea 45

Figure 19: Trends in the relative biomass of zoo- and phytoplankton in the Black Sea 45

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Figure 20: Trends in landings of Cod and other large predatory fish in Kattegat 47

Figure 21: Trends in total biomass of cod in Kattegat 47

Figure 22: Trends in the abundances of shore crabs and medium sized fish from coastal monitoring at Ringhals in Kattegat 47

Figure 23: Relation between offshore cod and coastal populations of medium sized predators in Kattegat 48

Figure 24: Relation between spring temperatures and coastal populations of medium sized predators in Kattegat 48

Figure 25: Trends in the dominating fish populations in the Baltic Sea 50

Figure 26: Biomass of zoo- and phytoplankton in the Gotland Sea, S Baltic Sea 50

Figure 27: Intensity of the spring bloom in the Gotland Sea, S Baltic Sea 50

Figure 28: The relative importance of different biological and environmental factors for determining the density of sprat in the Baltic Sea 51

Figure 29: The relative importance of different biological and environmental factors for determining the density of zoo- and phytoplankton in the southern Baltic Sea 52

Figure 30: Decline in perch on the Swedish coast in the southern Baltic Sea 54

Figure 31: Decline in pike on the Swedish coast in the southern Baltic Sea 54

Figure 32: Trends in the abundance of larger coastal predatory fish at Kalmar in the southern Baltic Sea 55

Figure 33: Trends in offshore abundances of cod, sprat and stickleback 55

Figure 34: Abundance of stickleback and the percentage of area overgrown by filamentous algae depending on the density of top predators 56

Figure 35: Removing perch and pike together with eutrophication increase the development of filamentous bloom forming algae 56

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LIST OF TABLES Table 1: Reports of algal bloom incidents in the Mediterranean and the Black Seas 28

Table 2: The relation between larger pelagic predators and lower trophic levels in the Black Sea over time 45

Table 3: The relation between adjacent trophic levels in the Baltic Sea between 1974 and 2006 51

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EXECUTIVE SUMMARY

Background Algal bloom is a collective name for an event of rapid excessive growth of algae and photosynthesizing bacteria. As such, the specific organisms producing algal blooms are only remotely related, and belong to a highly variable group of photosynthesizing aquatic organisms. Algal blooms may cause significant nuisance to humans by affecting valuable parts of ecosystems negatively - a harmful algal bloom (HAB). Summing up available data from European marine waters shows that the total socio-economic impact of harmful algal blooms is at least 850 million euro per year. However, this does not include all countries in Europe and do not account for non-listed events. The frequency of algal blooms has increased with global eutrophication, and in Europe negative effects of harmful algal blooms have increased significantly since the 1950s. Negative effects of algal blooms can be divided into two broad categories:

High density blooms: Large visible accumulations of algae or bacteria that colour the water and cause nuisance by sheer abundance. High biomasses of algae can be detrimental to the ecosystem in various ways, for example by forming drifting algal mats and excess loads of mucus that clog waters and accumulate together with foam on beaches, and by inducing post-bloom anoxia from the decomposition of the large amounts of accumulated organic matter.

Toxin producers: Highly potent algal toxins are produced by a group of unicellular algae dominated by the algal group dinoflagellates. Such toxins are responsible for extensive mortality in fish and shellfish and can have a strong impact on human health by accumulating in the food web, especially through shellfish poisoning. Blooms responsible for shellfish poisoning are often not visible to the bare eye.

Other species have significant direct negative effects on both livestock and humans, by combining high density blooms with low level toxicity.

In the last decade there has been an increasing realization that overfishing may contribute to the problem of algal blooms. In a number of marine systems higher biomass and increased frequency of algal blooms have coincided with dramatic declines in commercial stocks of larger predatory fish. A common phenomenon in these affected systems is that the declines in larger predatory fish have been followed by 1) significant increases in their prey, smaller bodied fish, and 2) decreases in herbivore grazers, which are prey for the smaller bodied fish and themselves consume algae. Thus, there is a potential connection between declines in commercial stocks of fish and increasing algal blooms, mediated by changes in predator-prey relations that in the end decrease the grazing pressure on algae.

Aim The general aim of this briefing note is to outline the background needed to understand the connection between algal blooms and fisheries, and to present scientific evidence indicating that overfishing could contribute to increasing problems with algal blooms. The note presents European case studies indicating that algal blooms are linked to overfishing, and discusses to what extent and under which circumstances fish stock depletion can cause or favor algal blooms.

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The note addresses four specific questions:

What are the consequences of algal blooms for fisheries?

Are there synergistic effects of overfishing and eutrophication?

Which are the types of fish stocks whose depletion tends to facilitate algal blooms?

Which types of algal blooms are related to overfishing?

Key findings Harmful algal blooms have negative effects on fisheries in Europe. The total cost of harmful algal blooms for the European fisheries is estimated to at least 177 million euro per year. This includes negative effects on commercial fisheries, loss to social welfare and cost for monitoring algal blooms for seafood poisoning. Toxic algal blooms generate large costs for the aquaculture sector. Direct losses of sellable products for the mussel sector range from 15 to 62 million euro per year. High density blooms create problems for all types of coastal fisheries. Drifting algal mats and mucilage forming blooms interfere with fishing gear and render fishing gear less effective. Post-bloom anoxia causes significant kill-offs both of aquaculture and wild fish stocks. Anoxia also interferes with reproduction along the coast, which include the main recruitment areas for many offshore populations of fish. Overfishing of larger top predatory fish contributes to an increased frequency and intensity of algal blooms. Algal blooms are natural phenomena that are controlled by a number of environmental factors. However, overfishing contributes to the problem of algal bloom development by weakening an important biological control of overgrowth. This is because removing top-predators by overfishing generates changes in food web configurations, which in general promotes smaller fish and causes a decline in the abundance of grazers on algae, such as zooplankton or invertebrate herbivores. Together with abiotic factors, grazers control the development of algal biomass, and when grazers decline, algal blooms develop easier. Today, detrimental effects of overfishing on offshore food webs are spreading to coastal ecosystems, causing problems with near shore water quality and habitat loss. In the Baltic and the Black Seas it is very likely that overfishing has contributed to an increased problem with harmful algal blooms. Although the ecology and regulation of algal blooms is complex, analyses of time series and coinciding events strongly suggest that overfishing has contributed to the increasing problem and economic cost of algal blooms in the Baltic and Black Seas, by causing large-scale changes to the structure of these marine ecosystems. In the North Sea it is likely that overfishing has contributed to an increased problem with harmful algal blooms. Modeling and analyses of available data in the North Sea indicate that increasing loads of algae may depend on fishery induced changes in the structure of the fish community. In the Kattegat, we lack data on trends in algal blooms, but experiments indicate that the documented long-term decrease in cod has had detrimental effects on seagrass communities by increasing filamentous algal blooms. There is a general problem of data availability in European Seas that limits the ability to estimate the effects of fisheries. There is general lack of trend analyses that include more than one organism group from several sea basins in Europe, but where there are reported problems with both overfishing and algal blooms. This indicates that important information is missing, whereas many European organizations and institutions do not make valuable data publicly available for cross referencing.

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Overfishing and eutrophication create synergistic effects. Changes in top predator communities and algal blooms co-occur with eutrophication. There is no doubt that an Europe wide eutrophication has promoted algal blooms, but changes in fish community composition have added to the problem of harmful algal blooms. For example, in the modern nutrient rich state of the Baltic Sea, trends in commercial stocks of fish describe trends in algal biomass better than nutrients, indicating that overfishing now contributes significantly to algal blooms. Synergistic effect of overfishing and nutrient enrichment is confirmed by experiments in the field that clearly demonstrates that the development of filamentous algal blooms is facilitated both by nutrients and removal of top-predatory fish, and that they act in concert so that the combined effect of nutrients and removal of predators is often many times stronger than their effects in isolation. Overfishing should mainly promote algal blooms when the target is a single species that dominates the abundance and function of the fish community. Effects on prey species by removing predators are in general much stronger if the predator community is dominated by a single species, such as demersal populations of cod in the Baltic Sea and Kattegat, or pelagic communities of anchovy in the Black Sea. High density blooms of algae are strongest related to overfishing. Available data suggests that non-toxic high density blooms are the type of blooms that should be the most sensitive to overfishing. Thus, overfishing should mainly promote high density algal blooms and generate problems with: 1) drifting algal mats, 2) mucilage and foam production, and 3) post-bloom anoxia. However, generic analyzes of temperate marine food webs also show that further intensified fisheries including smaller pelagic fish can promote toxic algal blooms and jellyfish. This is mirrored in the Black Sea food web, where jellyfish increased dramatically after an intensified fishery on anchovy collapsed in the 1990s.

Recommendation This briefing note demonstrates that traditional management of marine resources has severe limitations since it often ignores interactions both within food webs and between offshore and coastal food webs. Cascading effects of overfishing change predator-prey relations and thereby increases the frequency and intensity of harmful algal blooms, which in turn interfere with profitability of the fishing industry and may generate negative long-term effects on commercially important stocks. However, the cost of fisheries is not limited to the fisheries sector, but also affects coastal communities where increasing problems with algal blooms lead to substantial losses in tourist revenue and costs related to negative effects on human health. The evidence indicates the necessity of an ecosystem-based management approach (EBM) that acknowledges both: 1) effects of fisheries on the rest of the ecosystem, and 2) fluxes between offshore and coastal habitats.

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1. INTRODUCTION Algal bloom is a collective name for rapid excess growth of algae and photosynthesizing bacteria. Algal blooms may cause significant nuisance to humans by affecting valuable parts of ecosystems negatively – harmful algal blooms (Hoagland and Scatasta, 2006). Such negative effects include clogging of beaches and fishing gear, the creation of oxygen free conditions killing bottom living invertebrates and fish, and toxicity of water and food from the sea. There is no doubt that the frequency of harmful algal blooms has increased globally together with anthropogenic loading of nutrients (Hallegraeff, 1993; Sellner et al., 2003; Glibert and Burkholder, 2006; Heisler et al., 2008; Smith and Schindler, 2009). However, in the last decade there has been an increasing realization that depletion of higher trophic level fish stocks may contribute to the problem of algal blooms (Frank et al., 2005; Scheffer et al., 2005; Daskalov et al., 2007; Casini et al., 2008; Moksnes et al., 2008; Eriksson et al., 2009; Eriksson et al., 2011). In a number of marine systems higher biomass and increased frequency of blooms of algae have coincided with dramatic declines in commercial stocks of larger predatory fish. A common phenomenon in these affected systems is that the declines in larger predatory fish have been followed by 1) significant increases in their prey, smaller bodied fish, and 2) decreases in herbivore grazers, which are a prey for the smaller bodied fish and an algae consumer. Thus, there is a potential connection between declines in commercial stocks of fish and increasing algal blooms, mediated by changes in predator-prey relations that in the end decrease the grazing pressure on algae (Figure 1). This briefing note outlines the scientific background needed to understand the connection between algal blooms and fisheries, and presents scientific evidence indicating that overfishing promotes algal blooms. Algae are primary producers at the base of most marine food webs, and as such interact with higher trophic levels through energy transfer. Energy fixed by algae from the sun is channeled up the food web and ultimately control the production of valuable fish stocks. This description of a simple trophic pyramid may seem trivial, but trophic pyramids are not simple linear chains of events where the amount of available abiotic resources is translated into a predestined organic product at higher trophic levels. Instead, complex interactions between different biological organisms create emergent properties that can be considered desirable for humans or not. From a management perspective there are two very important properties of marine food webs that need to be considered to secure a sustainable ecosystem that produce valuable stocks of commercially interesting fish: 1) All consumers depend both on the quantity and quality of the food. Thus, not only the abundance, but also the composition of the algal community determines the structure of the system, i.e. production and composition of the fish community. 2) Higher trophic levels affect lower trophic levels by consuming them, i.e. predatory fish decrease the numbers of their prey, which in turn remove primary biomass by eating plant and algae. This bi-directionality of interactions in food webs led to a long standing scientific debate over if “bottom-up” effects (energy transfer from the basal resources), or “top-down” effects (consumption by higher trophic levels), control the abundance of plants and algae in different ecosystems. Today, we know that consumers, prey and resources often depend on each other, in such way that the accumulation of algae by increasing resources depends on the strength of consumption pressure by herbivore grazers (Worm et al., 2002).

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Figure 1: Potential effects of overfishing on marine food web structure showing a connection between fisheries and algal blooms.

phytoplankton

zooplankton

planktivorous fish

piscivorous fish

sustainable fishing

phytoplankton

zooplankton

planktivorous fish

piscivorous fish

overfishingIncreased fishing

pressure

decreases in large predatory fish

increases in smaller predatory fish

decreases in organisms that eat algae ‐ grazers

increases in primary producing algae

Source: Redrawn from Scheffer et al. (2005), based on Frank et al. (2005).

The documented interaction between aquatic resources and consumers has prompted the suggestion that changes in marine food webs by overfishing may provoke algal blooms. It is important to note from the start, that removing consumers do not necessarily increase the productivity of primary producers. Primary production is controlled by primary resources, such as light and nutrients, and environmental constraints, such as temperature. Thus, removing fish in general do not fuel the growth of algae. This is not what the discussion is about! What science has demonstrated is that consumers have the ability to shape the structure of food webs, within limits defined by certain basic conditions and environmental constraints. Understanding that food web interactions shape ecosystems and have consequences for their function and ability to provide services and goods, have initiated a general call for ecosystem-based management (EBM) of marine resources. EBM is an adaptive management approach that focuses on the complexity 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). To date there is actually limited scientific case-specific evidence for the influence of fishing on algae. This depends on a generally poor interest of exploring links and relations between trophic levels as parts of any marine monitoring programs. Monitoring of algal blooms and their consumers, zooplankton or invertebrate grazers, has not been particularly frequent anywhere, limiting the length of available time series critically. Smaller fish which are an important link between larger commercially interesting fish and algae, have also traditionally received little attention. In addition, there are few published results or open

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databases that have monitored the fish community together with algae and their herbivores, which would enable sharp comparisons of trends between these groups. This reflects sectorial management borders and divisions between academic discipline, such as fisheries vs. water quality and zoology vs. botany, indicating that a shift within management organization structure may be necessary to be able to adequately evaluate ecosystem scale effects of fisheries (Olsson et al., 2008; Osterblom et al., 2010). Even more critically, existing information is to a large extent not made available to external researchers by those organizations collecting the data. Thus, synthesis of ecosystem effects across organism groups and trophic levels are often made impossible by organization structures and private interests. Still, more and more circumstantial scientific evidence indicates that overexploitation of commercial fish stocks may allow algal blooms to develop when the environmental conditions are favorable, by removing a food web constraint on the accumulation of algal biomass. This briefing note provides a brief background on the ecology of algal blooms needed to understand the threat they pose and how they function, and then focuses on presenting relevant cases studies and the latest research on the connection between algal blooms and fisheries. Chapter 2 presents algal blooms and their negative effects for society, and especially details consequences of algal blooms on fisheries. Chapter 3 presents the ecology of algal blooms, describes trends and explains the rationale of the connection between algal blooms and fisheries, and outlines ecological factors that may favor such a connection. Chapter 4 details the potential for synergistic effects of overfishing, excess nutrient runoff and algal blooms in Europe and presents case-specific evidence that overfishing may provoke algal blooms.

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2. TYPES AND EFFECTS OF ALGAL BLOOMS

2.1. What are algal blooms? Algal blooms consist of many different types of algae that are only remotely related. Their life-form can be solitarily unicellular, colony building or filamentous, and they can be planktonic or benthic. Common bloom forming algal groups include dinoflagellates, other flagellates, diatoms, cyanobacteria and filamentous green, brown or red algae (Graneli and Turner, 2006). Due to the wide taxonomic composition, it is difficult to define exactly what an algal bloom is. Instead the definition has to be context dependent. Consequently, alert levels for toxic blooms in monitoring programs can vary as much as from 100-300 cells per liter for dinoflagellates to 150-200 000 cells per liter for diatoms and cyanobacteria (World Health Organization, 2002; Hinder et al., 2011). In this note algal blooms are defined as large accumulations of algae (including cyanobacteria) with harmful effects on the surrounding ecosystem.

2.2. Ecological effects of algal blooms Due to the wide taxonomic composition, algal blooms also have strongly diverging deleterious effects. However, we can broadly classify negative effects into two main types: effects related to high densities per se, and toxin production – chemical effects (Figure 2) (Smayda, 1997; Nastasi, 2010). Figure 2: Groups of organisms generating harmful algal blooms and different

types of harmful algal blooms

Harmful algal blooms

diatoms

dino‐flagellates

flagellatescyano‐bacteria

filamen‐tous algae

Producing toxins/

”red tides”

shellfish poisioning

direct lethal toxicity

ambush predation

Producing high biomass/

”green tides”

mechanical disturbance

shading

anoxia

clogging the water & overgrowth

mucus & foam formation

Source: Granieli et al. (1996)

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High density blooms that color the water and cause nuisance by sheer abundance are reported for many types of bloom forming algae, but are characteristic for cyanobacteria, some flagellates (Phaeocystis, Crysocromulina), diatoms and filamentous algae (green tides). High biomass of algae can be detrimental to the ecosystem in various ways. Mechanical damage by particle irritation can cause infections on gills of both fish and crustaceans, and gill piercing by diatoms can even lead to respiratory failure (Smayda, 1997). Production of extracellular polymers can lead to physical damage on other organisms, for example by clogging of gills and excess loads of mucus that clog waters and accumulate together with foam on beaches (Smayda, 2006). Decomposition of the large amounts of accumulated organic matter after a bloom event may consume all available oxygen, thereby creating local anoxia, which is lethal to bottom living organisms and chase away or kill mobile fauna such as fish and crustaceans (Hallegraeff, 1993; Vahteri et al., 2000; Cloern, 2001; Breitburg, 2002). The toxin producers are a group of 60-80 microalgal species (unicellular algae) of which three-fourths are dinoflagellates (Smayda, 1997; Van Dolah, 2000; Hinder et al., 2011). Algal toxins are highly potent and are responsible for extensive mortalities in fish and shellfish. Algal toxins can accumulate in the food web and thereby have a strong impact on human health, especially through shellfish poisoning. For these toxin producers, low cell densities are sufficient to reach dangerous toxicity levels and toxic harmful blooms are therefore often not visible to the naked eye. On the contrary, cyanobacteria and other flagellates (e.g. Chrysocromulina, Prymnesium) commonly form visible blooms and also produce toxins that have significant direct negative effects on both livestock and humans (World Health Organization, 2002; Edvardsen and Imai, 2006; Peaerl and Fulton III, 2006).

2.3. Harmful algal groups There are five main categories of bloom forming algae, recognized in monitoring and/or in the scientific literature on algal blooms. The chapter below presents a brief overview. For more detailed and complete information see the algal oriented reviews by Smayda (2006) and Graneli and Turner (2006).

2.3.1. Dinoflagellates Dinoflagellates are unicellular organisms consisting of a flagellated cell with a limited but significant ability to move around (Burkholder et al., 2006). They are responsible for four of the five most commonly identified groups of seafood poisoning: paralytic shellfish poisoning (PSP), neurotoxic shellfish poisoning (NPS), ciguatera fish poisoning (CFP) and diarrhetic shellfish poisoning (DSP) (Smayda, 1997; Van Dolah, 2000). In Europe, harmful blooms of dinoflagellates leading to of seafood poisoning is mainly reported from the Atlantic coasts (Smayda, 2006). Dinoflagellates are occasionally reported in connection with nuisances from high density blooms, such as the anoxic Ceratium tripos bloom in New York that killed fish over an area exceeding a million hectares, and together with other algae in mucus forming events in the Mediterranean and the Sea of Marmara (notably Gonyaulax fragilis) (Tufekci et al., 2010). Karenia mikimotoi is another very common dinoflagellate considered a major threat to aquaculture. Reported harmful events include large scale mortality both of shellfish along the French coast, and of shellfish and cultured salmon in Norway (Smayda, 2006). From the Mediterranean, problems with high density blooms of Ostreopsis spp. are regularly reported.

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2.3.2. Other flagellates Flagellates, other than dinoflagellates, that form harmful blooms with significant negative effects for humans mainly include the classes Prymnesiophyceae and Raphidophyceae (Edvardsen and Imai, 2006). Prymnesiophytes is a class of flagellates with a cosmopolitan distribution that occasionally form harmful blooms; in Europe harmful blooms are mainly reported from the North Sea. Prymnesium parvus can reach densities up to 800 million cells per liter (Smayda, 2006). It regularly causes local fish-kills along the British coast but also occurs in high densities all the way into the southern Baltic Sea. Chrysochromulina polylepis is a toxic prymnesiophyte associated with fish-kills. In 1988, a bloom of C. polylepis on the Atlantic coasts of Sweden and Norway had significant harmful effects on both wild organisms and fish aquaculture over an area of 75 000 km2 (Maestrini and Graneli, 1991; Granéli et al., 1996; Dahl et al., 2005). Phaeocystis spp. is a prymnesiophyte that recurrently forms blooms in the north Atlantic and which produces high amounts of mucilaginous material that can be seen as thickets of foam on the water surface and beaches (Lancelot et al., 1998; Smayda, 2006). In 2001, 10 million kg of mussels where killed by an anoxia event after a Phaeocystis bloom in the Oosterschelde, an estuary on the Dutch Atlantic coast (Peperzak and Poelman, 2008). Raphidophytes contain three notorious fish killing taxa: Chattonella spp., Heterosigma akashiwo and Fibrocapsa japonica. Fish-kills in connection with blooms of raphidophytes have been reported from the Adriatic and along the French, Dutch and British coasts (de Boer, 2006). Several large scale fish kills in northern Europe were first linked to Chattonella verruculosa but turned out to be the silicoflagellate named Pseudochattonella verruculosa. The first fish killing bloom by this species was observed in April-May 1998 in Skagerrak in the North Sea. Since then Pseudochattonella has been held responsible for several fish mortality events in this area.

2.3.3. Diatoms Diatom blooms are generally not toxic, but harmful effects on farmed fish are frequently reported in Europe by high density blooms of ca 14 species of diatoms (Smayda, 2006). Diatoms have silicone frustules – a hard silicone based outer skeleton – and often exhibit spines which can cause mechanical damage on gills during blooms (Smayda, 1997). There are also frequent reports of post-bloom effects by anoxia and mucus formation (Smayda, 2006). In addition, amnesic shellfish poisoning (ASP) is caused by a diatom (Pseudo-nitzschia multiseries). Pseudo-nitzschia multiseries blooms are regularly reported along the North Sea coast of Europe, and cause temporal closures of both scallop and mussel fisheries (Smayda, 2006).

2.3.4. Cyanobacteria Cyanobacteria are often called blue-green algae, but are photosynthesizing bacteria that can form colonies. Cyanobacteria blooms are most common in brackish water habitats and intercontinental seas such as the Baltic Sea, the Sea of Marmara and estuaries (Peaerl and Fulton III, 2006). They commonly form high density blooms of more than 200 000 individuals per liter, but they also produce toxins. There are three common groups of cyanotoxins: hepatotoxins that cause liver injury, neurotoxins that act on the nervous system and dermatoxins that cause irritant and allergic responses on contact (World Health Organization, 2002).

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2.3.5. Filamentous algae Filamentous algae are responsible for near-shore green tides, and are a mixture of filamentous green, red and brown algae, including species such as Cladophora spp., Ectocarpus spp., Pilayella spp., Ulothrix spp., Ulva spp. and Urospora spp., but also contain colonial diatoms such as Melosira spp. (Eriksson et al., 2009; Eriksson et al., 2011). They are not toxic, but create both thick overgrowth and massive drifting algal mats that outcompetes benthic macrophytes and cause localized anoxia of inlets. Filamentous algal blooms also clog fishing gear, boats and beach installations, and are a threat to local tourism. In Europe, harmful events by drifting algal mats and filamentous algal blooms are mainly reported from the Baltic Sea, Kattegat and Skagerrak (Bonsdorff et al., 1997; Pihl et al., 1999; Vahteri et al., 2000; Baden et al., 2003; Eriksson et al., 2009; Eriksson et al., 2011), but also in connection with beach deposition along the Atlantic coast (World Health Organisation, 2002).

2.4. General societal problems and costs There are a number of demonstrated negative societal effects of algal blooms that have a significant economic impact on coastal communities (Hoagland et al., 2002; World Health Organization, 2002; ECOHARM, 2003; Hoagland and Scatasta, 2006). Toxic algal blooms affect human health through contact, ingestion and through air spray (World Health Organization, 2002). This has negative economic consequences for tourism and the seafood industry (Hoagland et al., 2002; ECOHARM, 2003; Hoagland and Scatasta, 2006). High biomasses of algae create anoxia when decomposing, which has significant negative effects both on fish stocks and shellfish (Hallegraeff, 1993; Breitburg, 2002). For fish, juvenile stages such as larvae and eggs may be particularly affected by anoxia because of limited movement (Breitburg, 2002). High biomass blooms of algae also affects fish gear by making nets heavy and prone to damage by clogging, which includes overgrowth and mucus formation (World Health Organization, 2002). High biomass of algae also renders coastal waters and beaches unattractive to humans, both by visibly clogging the water and by foul smells when the high amounts of organic material decompose (World Health Organization, 2002). The European Commission supported program ECOHARM (2003) analyzed socioeconomic losses due to harmful algal blooms in Europe. ECOHARM divide harmful algal blooms into seafood toxic blooms (ST), fish killing blooms (FK), high biomass toxic blooms (HBT) and high biomass non-toxic blooms (HBNT). The results show that seafood toxin is the most reported HAB nuisance in Europe, followed by high biomass non-toxic blooms. ECOHARM calculated that the average annual economic loss of HABs in Europe was 813 million US dollars (2005 dollars). This was divided between effects on public health (11 million $), commercial fisheries (147 million $), recreation and tourism (637 million $) and the cost for monitoring and assessment of toxic blooms (18 million $) (see also Hoagland and Scatasta, 2006). The distribution of effects was unevenly distributed throughout Europe, and ECOHARM divided European countries into HBTN and ST countries depending on which type of bloom that was most commonly reported. HBTN countries were: Estonia, Finland, France, Germany, Latvia, The Netherlands, Poland and Sweden. This indicates that problems with high biomass non-toxic blooms are the main concern in the Baltic Sea countries including the Wadden Sea and estuaries on the Dutch coast. In France, the HBTN problem was mainly associated with beach accumulations of filamentous algae, but there were also a high number of reported incidents with seafood toxins (the 5th highest rate in Europe). ST countries were: Denmark, Ireland, Italy, Norway, Portugal, Spain and the UK. Together with France this indicates that seafood poisoning is mainly an Atlantic and Mediterranean problem. Note that there was no assessment of the Black or Marmara Sea.

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2.5. Specific effects on fisheries in Europe The total cost of harmful algal blooms on fisheries in Europe includes direct negative effects on commercial fisheries, loss of social welfare and the cost for monitoring algal blooms to prevent seafood poisoning. According to ECOHARM (2003), the total annual cost for European fisheries is estimated to 177 million euro. It is difficult to pinpoint certain species that create harmful algal blooms that are more or less important for the fisheries to manage, because costs are shared between harmful events generated by all above presented groups of algae. However, we can divide specific examples where we have good scientific documentation into type of effects to outline a general picture, as long as we take into account that there are additional threats and many local exceptions.

2.5.1. Seafood toxic blooms Algal blooms is one of the top three causes of aquaculture loss, together with disease and weather damage (Rutter, 2010), and 99% of all reports of seafood toxic blooms in Europe involve shellfish (ECOHARM, 2003). The direct loss of revenue for the mussel aquaculture sector is between 15 and 62 million euro per year in Europe, not counting the cost for monitoring and social welfare. Seafood toxic blooms are mainly a problem along the Atlantic and Mediterranean coasts of Europe, naturally concentrated in the countries with significant aquaculture (ECOHARM, 2003). The main concerns are different dinoflagellate blooms that can generate seafood poisoning and mortality of wild and cultured stocks, such as Dinophysis spp., Alexandrium spp. and Karenia mikimotoi (Smayda, 2006). Another large cause of concern is the toxin producing diatom Pseudo-nitzschia multiseries that blooms regularly along the North Sea coast of Europe (Smayda, 2006). All these species regularly cause temporal closures of shellfish fisheries along the European coasts. There is also an increasing awareness of the threats to seafood populations by the raphidophytes Heterosigma akashiwo and Fibrocapsa japonica (de Boer, 2006).

2.5.2. High biomass blooms The main problems with high biomass blooms seem to be concentrated in intercontinental, enclosed seas and estuaries (ECOHARM, 2003). A significant exception seems to be the beach accumulations of Pheocystis and filamentous algae on the North Sea coasts of France, Belgium and the Netherlands (World Health Organization, 2002). High biomass blooms can have different effects on fisheries, including mechanical disturbance, starvation and suffocation (see above, Smayda, 1997; Van Dolah, 2000). However, in European case-studies, clogging by drifting algal mats or mucus in the water, and post-bloom anoxia are the negative effects most commonly reported to have significant economic consequences for the fishery sector.

Drifting algal mats Documented negative effects of drifting algal mats on fishing are mainly reported from the Baltic Sea area. For example, in 2005 in Finland, 65% of the professional fishermen using stationary fishing gear (fish traps or gill nets), and 35% of the fishermen using trawls, reported that they have suffered economic damage from drifting algal mats of cyanobacteria (Viitasalo et al., 2005). During blooms, they spent a significant time cleaning their equipment and argued that catches decreased because fish avoided fishing gear clogged with algae.

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Drifting filamentous algal mats may also lead to large scale declines in the quality of recruitment habitats for fish that use shallow bays and vegetation as nursery areas (Pihl et al., 2006; Ljunggren et al., 2010). Habitat quality has a great influence on the recruitment of fish (Alheit and Niquen, 2004; Leggett and Frank, 2008). In Kattegat and Skagerrak, strong declines in eelgrass (Zostera marina) beds due to increasing loads of filamentous algae have impaired important recruitment habitats for both off-shore and near-shore populations of cod (Gadus morhua) (Pihl et al., 1999; Baden et al., 2003; Pihl et al., 2006). In the Baltic Sea, clogging of shallow bays by high loads of drifting filamentous mats interfere locally with the recruitment of the coastally dominating predatory fish perch (Perca fluviatilis), which lay eggs in shallow vegetation (Ljunggren et al., 2010).

Mucilage forming blooms Negative effect of mucilage on fishing gear is mainly reported from the Adriatic and Marmara Seas (Zengin et al., 2009; Turk et al., 2010; Zengın et al., 2011). In the Mediterranean and Marmara seas, algal blooms forming a gelatinous creamy mass in the water contain a rich community of different species, including cyanobacteria, diatoms and dinoflagellates (Tufekci et al., 2010; Turk et al., 2010). Notably, the diatoms Skeletonema costatum and Cylindrotheca closterium and the dinoflagellate Gonyaulax fragilis are very common mucus producing species (Tufekci et al., 2010). Mucus events have been reported for centuries from the Adriatic Sea, but have increased in the last decades (Turk et al., 2010). In the Marmara Sea, fishery landings declined almost by half during heavy mucilage blooms in 2007-2008, compared to 2006: from 75 000 to 44 450 and 38 400 tons, respectively (Zengin et al., 2009; Zengın et al., 2011). Fishery gear became too heavy from a gelatinous mass of algae mixed with jellyfish, causing the nets to break and preventing them to be hauled on board. This affected all types of fisheries in the Marmara Sea and is estimated to have eradicated 91% of the yearly profit (Zengin et al., 2009; Zengın et al., 2011).

Post-bloom anoxia Anoxia mainly affects intercontinental enclosed seas and estuaries. Deteriorating oxygen conditions by degrading high algal biomasses is easier to develop when the water shows density stratification during summer, which limits the exchange of bottom water (Cloern, 2001; Breitburg, 2002). Anoxia is a significant threat to all aquaculture and benthic communities of invertebrates. For example, in 2001 an anoxia event after a Pheocystis bloom killed-off 10 million kg of cultured mussels (Mytilus edulis) in the Oosterscheelde, an estuary on the Dutch Atlantic coast, causing an estimated loss of 15 to 20 million euro (Peperzak and Poelman, 2008). Anoxia is also a threat to wild stocks of fish. Commonly, surface waters act as a refuge for adult fish during bottom water anoxic events (Breitburg, 2002). However, occasionally oxygen depletion locally extends into shallow waters. In 1997, anoxia in connection with a dinoflagellate bloom (Prorocentrum minimum) rapidly spread to the whole water column over an 25 km area in Mariager Fjord in northern Denmark, which lead to large kill-offs of both fish and invertebrates (Fallesen et al., 2000). Anoxia is a potential large-scale threat to the recruitment of wild stocks of fish. Drifting algal mats can cause local anoxia in shallow bays, killing eggs and larvae of coastal fish (Pihl et al., 1996; Ljunggren et al., 2010). In addition, pelagic eggs can sink into anoxic bottom layers in the water (Breitburg, 2002). Notably, due to the stratification of the Baltic

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Sea, cod egg survival depends on the availability of water with a salinity which is high enough to create buoyancy (so that the eggs do not sink to the bottom), and with a sufficient oxygen content. This is called the reproductive volume of water available (Österblom et al., 2007). During strong declines of the cod stock in the late 1980s, salinity was very low in the bottom waters and up to 95% of the cod eggs where found at oxygen levels below what was required for survival (Breitburg, 2002; Österblom et al., 2007). The salinity and oxygen content of the water in the Baltic Sea depend on inflows of oxygen rich water with a high salinity from Atlantic, but the volume of anoxic bottom waters is also promoted by the large-scale decomposing of plankton (HELCOM, 2009). Thus, algal blooms could directly contribute to the decline in cod recruitment, but this is so far poorly investigated.

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3. THE ECOLOGY OF ALGAL BLOOMS

3.1. A natural process that increases in frequency with eutrophication

Algal blooms are natural phenomena in most marine systems, with annual cycles of spring and summer accumulations of different species. They are generally controlled by the abiotic resources light and nutrients, and the environmental conditions temperature and turbulence. When resources are available and temperatures are high enough to promote rapid growth, algal blooms may develop. High density blooms usually require calm weather conditions, because wind induced turbulence hinders the accumulation of algae in the water. For the past 30 years increased resource availability through worldwide eutrophication has contributed significantly to a global increase in algal bloom frequency and bloom related nuisances (Hallegraeff, 1993; Van Dolah, 2000; Cloern, 2001; Sellner et al., 2003; Heisler et al., 2008). There are two general problems with documenting trends in algal blooms. First, there are serious limitations in the data we can use to document trends in algal blooms. Algal blooms are difficult to monitor, and relevant monitoring efforts have been done only in the past decades. Second, blooms are extreme events and therefore display tremendous variability. Limited monitoring and only from the recent past therefore means that we often cannot separate natural variability from trends in time. However, in Europe, both direct and circumstantial evidence suggests that problems with harmful algal blooms in general have increased. Figure 3: An increased summer peak in algal biomass over time in the Black Sea. Bars show the maximum value in chl a profiles, which indicate the maximum intensity of algal blooms. Note that in 1995 and 1996 sampling frequency is very low, and June and July were not sampled at all. This means that blooms likely were underestimated in 1995 and 1996. Also note that if bars are missing, there are no data from those years.

0

1

2

3

1960 1965 1970 1975 1980 1985 1990 1995

Chl a

(mg per m

3 ) Chl A maximum

Source: Redrawn from Yunev et al., 2005

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In the Black Sea, the abundance of bloom forming algae increased together with the onset of modern eutrophication (Zaitsev, 1992). Average phytoplankton biomass doubled in the 1980 and the frequency and intensity of phytoplankton blooms have increased dramatically since the 1970s (Zaitsev, 1992; Kideys, 1994; Daskalov, 2002; Yunev et al., 2002; Yunev et al., 2005) (Figure 3). The relative contribution of dinoflagellates has increased from 10% in the 1960-70s to 30% in the 1980s, and with this the occurrence of red tides and the abundance of some harmful dinoflagellate species increased significantly (notably Prorocentrum cordatum and Noctiluca miliaris) (Kideys, 1994). Table 1: Reports of algal bloom incidents in the Mediterranean and the Black Seas.

Year Species of algae reported responsible for bloom

Late 1960s North Adriatic: Prorocentrum

1970s North Adriatic: Noctiluca, Gonyaulax, Prorocentrum, Gyrodinium, Glenodinium

1980s

North Adriatic: Katodinium, Noctiluca, Glenodinium, Prorocentrum, Gyrodinium, Gonyaulax, Scrippsiella, Massarthia

Spain 1984: Gonyaulax Black Sea 1986: Prorocentrum Mediterranean 1989: Gymnodinium

1990s

Black Sea: Pseudo-nitzschia, Nitzschia, Cheatoceros, Ditylum, Cylindrotheca, Rhizosolenia, Heterocapsa, Protoperidinium, Scripsiella, Emiliania, Gonyaulax, Prorocentrum

Black Sea 1993: Dinoflagellates Tunisia1994: Karenia Spain 1994 and 1996-1999: Alexandrium Greece 1994 and 1997: Prorocentrum, Noctiluca, Erythropsidinium France 1998: Alexandrium Greece 1998: Chattonella France 1999: Prorocentrum Tyrrhenian Sea 1998, 2000-2001: Ostreopsis

2000s

Black Sea: Skeletonema, Cerataulina, Prorocentrum, Gymnodinium

Spain 2003: Alexandrium, Gymnodinium Greece 2000-2004: Prorocentrum, Noctiluca, Gymnodinium, Alexandrium, Dinophysis, Pseudo-nitzschia Ligurian Sea 2005-2006: Ostreopsis Tunisia 2006: Coolia North Adriatic 2007: Ostreopsis Italy 2010: Ostreopsis Puglia 2010 Sicilia 2010

Source: Nastasi 2010

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In the Mediterranean Sea, both in northwest (Catalonia) and northeast (Adriatic Sea), a high frequency of potentially harmful algal blooms have been detected the past decades (Degobbis 1989, Vila et al. 2001a, Vila et al. 2001b). In the Adriatic Sea primary production doubled between the 1960s and 1980s, and large scale mucus events linked to blooms of diatoms (Skeletonema costatum) caused economic problems for the coastal communities (Solic et al., 1997; Thornton et al., 1999; Cloern, 2001). Since the 1980s, massive algal bloom have been reported in both the Mediterranean and Black Seas from the dinoflagellates Ostreopsis, Prorocentrum, Noctiluca, Gymnodinium, Alexandrium, Dinophysis and Gonyaulax, as well as the diatoms Pseudo-nitzschia and Skeletonema (Table 1; Nastasi, 2010). In the Atlantic, reported occurrences of potentially toxic algal blooms and shellfish poisonings increased in the 1980s and 1990s all along the European coast (for example by Raphidophytes, see de Boer, 2006). Furthermore, mucilaginous blooms that accumulate as foam on beaches are a nuisance along the coasts of France, Belgium, the Netherlands and Germany (Riegman et al., 1992; World Health Organization, 2002). The frequency of such blooms of Phaeocystis, are suggested to have increased along the southern North Sea coasts (Lancelot et al., 1987; Passow and Wassmann, 1994; Riebesell et al., 1995). In the Dutch Wadden Sea, there are indications that primary production and standing stock of benthic algae doubled between the 1960 and 1980s (Cloern, 2001; Eriksson et al., 2011), and the duration of Phaeocystis blooms have increased dramatically (Figure 4) (Cloern, 2001). In Kattegat, on the border between the North Sea and the Baltic Sea, primary production was double in the 1980s compared to the 1950s (Richardson and Heilmann, 1995). At the same time the transparency of the water and oxygen concentrations in the bottom water declined strongly, which indicates a higher number of plankton in the water absorbing the light and consuming the oxygen when decomposing (HELCOM, 2009). To the north from Kattegat, in the Skagerrak, local seagrass communities are reported to have decreased 60% by massive developments of filamentous algal blooms (Pihl et al., 1999; Baden et al., 2003). Figure 4: Duration of the algal bloom season in the Wadden Sea.

0

50

100

150

200

250

300

350

1970 1975 1980 1985 1990

Days

Duration of the bloom season in days

Source: Redrawn from Cloern (2001)

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Figure 5: The areal extent of the peak algal bloom of cyanobacteria in the Baltic Sea between 1997 and 2009.

0

2000

4000

6000

8000

10000

12000

14000

1997 1999 2002 2004 2006 2008

km2

Areal extent of algal blooms

Source: Hansson and Öberg 2009 - SMHI

In the Baltic Sea, both nitrogen and phosphorus concentrations increased substantially in the water from the 1960s to the 1980s, and water transparency has decreased in all subregions in the past 100 years (HELCOM, 2009). Cyanobacteria blooms are a natural part of the Baltic system, but before the 1940s nuisances in connection with blooms were rarely reported (Finni et al., 2001). This is confirmed by sediment deposits showing that blooms of cyanobacteria increased strongly in the latter half of the 20th century (Poutanen and Nikkila, 2001). Satellite monitoring show strong development of cyanobacteria blooms during the 1990s and 2000s (Figure 5) (Kahru et al., 1994; Hansson, 2005), and the taxa Nodularia and Aphanizomenon, which produces toxins, have formed the largest blooms in the 2000s (HELCOM, 2009). In general, bottom oxygen concentrations decreased dramatically from the 1960s to the 1980s in the Baltic Sea area, and have stayed low throughout the 1990s and 2000s with substantial areas affected by long-term anoxia (HELCOM, 2009). In addition, problems with filamentous algal mats related to eutrophication are reported from most coastal areas in the Baltic Sea (Bonsdorff et al., 1997; Bonsdorff et al., 2002).

3.2. Nutrients and grazing together control algal bloom development

There is no doubt that nutrient enrichment has increased the problem of algal blooms in Europe (see chapter 2.1). However, in the past decades a scientific consensus has developed based on a large number of experiments, which showed that consequences of nutrient enrichment in marine systems depends also on the grazing pressure by zooplankton or invertebrate herbivores (Worm et al., 2002). This has prompted the idea that herbivore grazers may act as a controlling factor, limiting or preventing negative effects of eutrophication by consuming the excess production of algal biomass (Worm and Lotze ,2006; Eriksson et al., 2007). Grazers have significant effects on the accumulation of algal biomass, but the effect is context dependent and fluctuates in space and time. Ecological synthesis, calculating mean effects over many different experiments from different areas, show that removing grazers or adding nutrients increase algal biomass strongly in all types of marine systems – often more than two times (Worm et al., 2002; Gruner et al., 2008). In a synthesis by Gruner et

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al. (2008), removing grazers increased the relative effect of nutrients on rocky shores (significant interaction effect). This means, for example, that nutrients may increase algal biomass 40% with grazers, but increase biomass 80% without grazers. On soft bottoms nutrients on average doubled biomass with or without grazers, but grazers still decreased the total biomass by half. Worm and Lotze (2006) performed a coordinated nutrient and grazer experiment in eutrophied bays in the Baltic Sea and Nova Scotia, and found that grazers decreased biomass of bloom forming filamentous algae by ca. 80% in all examined areas, but that nutrients still had a positive effect on biomass accumulation in spite of high grazing pressures. Thus, negative eutrophication effects can be prevented by grazing, but occasionally nutrient enrichment overrides grazer control and algal biomass starts to accumulate. Still, natural levels of grazing in general limit the abundance of algae to significantly lower levels than compared to without grazers. From the accumulated body of aquatic experiments manipulating grazers world-wide, we can make a general evaluation of the strength of grazer control both in benthic and pelagic ecosystems. Summarizing 650 experiments, 507 benthic and 143 pelagic, shows that the presence of grazers limits benthic algal biomass to ca. 50% of the standing biomass that accumulate when removing the grazers, and pelagic algal biomass to ca. 70% (Figure 6). Thus, there is a strong scientific consensus that grazers improve the resistance of coastal communities to negative effects of eutrophication. Figure 6: The relative effect of grazers on the biomass of algae in benthic and

pelagic systems. The y-axis show the log-response ratio of removing the grazers – thus, a positive response means that algal biomass increased when removing the grazers. A log response ration of 0.69 means that biomass doubled. In the figure, removing grazers increased the biomass of benthic algae with 100%, and pelagic algae with 40%. The study is based on synthesis of 650 different experiments from all over the world.

0

0.5

1

benthic pelagic

The r

ela

tive e

ffect

of gra

zers

on

alg

al b

iom

ass

(lo

ga

ritm

ic s

cale

)

Source: Author

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3.3. Decreases in top predatory fish coincide with increases in algae

Increased production potential by human induced eutrophication is paralleled by large scale changes in higher trophic levels by overfishing. In a number of marine systems strong declines in top predators and subsequent cascading changes in lower trophic levels coincide with abrupt increases in the standing stock of algae, notably the Black Sea, the Baltic Sea and the Scotian shelf in the western Atlantic (Figure 7) (Daskalov, 2002; Frank et al., 2005; Daskalov et al., 2007; Casini et al., 2008; Eriksson et al., 2011). For all these systems declined grazer control triggered by overfishing seems to contribute to large scale increases in algal biomass. Increased accumulation of algal biomass should increase the probability of algal blooms. Below I outline the chain of events from the western Atlantic and discuss the factors that could contribute to a linkage between higher trophic levels and algal blooms, while the specific European case studies including a food web analysis for the North Sea are detailed in Chapter 4. Figure 7: Fishery induced declines in top predators coincide with abrupt

increases in the standing stock of algae in the north Atlantic, Baltic Sea and Black Sea.

phytoplankton

larger zooplankton

planktivorous fish

demersal top predators

(mainly cod)

overfishingIncreased fishing

pressure

decreases in large predatory fish

increases in smaller predatory fish

decreases in organisms that eat algae ‐ grazers

increases in primary producing algae

phytoplankton/ dinoflagellates

larger zooplankton

planktivorous fish (mainly anchovy)

pelagic top predators

overfishing

Scotian shelf Black Sea

phytoplankton

larger zooplankton

planktivorous fish (sprat)

cod

overfishing

Baltic Sea

Source: Frank et al. (2005), Daskalov (2007), Casini et al. (2008)

On the Scotian shelf, in the northwest Atlantic (Nova Scotia, Canada), a collapse in the heavily fished benthic fish community between 1985 and 1995 corresponded to a general change in phytoplankton abundance from low in the 1960-70s to high in the 1990-2000s (Frank et al., 2005). The benthic fish community was dominated by cod (Gadus morhua), but also other exploited larger demersal fish species declined, such as haddock (Melanogrammus aeglefinus), hakes (Urophycis tenuis, Merluccius bilinearis) and pollock (Pollachius virens). After the collapse of the main larger predators, many of their prey species increased significantly, including the total biomass of small pelagic fishes, crabs and shrimp (Frank et al., 2005). During this change towards smaller planktivorous fish, the zooplankton community also changed from high to low abundances of large bodied species

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(Mountain and Kane, 2010; Pierik et al., 2011). Larger zooplankton is the preferred food source by the smaller pelagic fish and there was a 45% higher abundance of larger zooplankton in the early 1980 compared to the 1990s, while the abundances of smaller bodied zooplankton remained constant. Correlation analyses showed that yearly changes in benthic fish since the 1970s were mirrored negatively by small pelagic fish and phytoplankton, and positively by larger zooplankton: there was a significant negative correlation between the biomass of benthic fish and small pelagic fishes (r=-0.61, n=33), a significant positive correlation between the biomass of benthic fish and larger zooplankton (r=0.45, n=23), and a significant negative correlation between the biomass of benthic fish and phytoplankton (r=-0.72, n=24) (Frank et al., 2005). These reciprocal changes in the abundance of the trophic levels indicate that the decline in larger demersal fish may have promoted an increase in phytoplankton abundance by indirectly decreasing the abundance of larger zooplankton species and consequently decreasing the general grazing pressure. Changes in food web structure, where declines in top predators are followed by alternating changes in trophic levels – such as increases in smaller predators, decreases in herbivores and increases in plant or algal biomass - are defined as “trophic cascades” (Pace et al., 1999). There are few experiments on an ecosystem relevant scale that causally link predators and algae in marine systems. However, the circumstantial evidence of system wide marine trophic cascades are accumulating (Estes et al., 1998; Jackson et al., 2001; Daskalov, 2002; Frank et al., 2005; Casini et al., 2008; Eriksson et al., 2011), and there are a number of small scale experiments that support the importance of fish predators for algal biomass (Shurin et al., 2002; Borer et al., 2005; Borer et al., 2006; Eriksson et al., 2009; Sieben et al., 2011a, 2011b). Trophic cascades are well known in lake management where whole lake experiments have shown that releasing top predator fish in formerly turbid phytoplankton dominated lakes can significantly reduce algal biomass and cause a transformation to clear water lakes (Carpenter et al., 2001). Thus, biomanipulation of higher trophic levels has become a useful tool to limit the development of algal blooms in eutrophied lakes (Sondergaard et al., 2007).

3.4. Trophic cascades depend on resources and predator diversity Ecosystem effects of predator declines have been thoroughly explored in the past decades, both in modeling exercises and field studies. Today we know that cascading changes in the structure of food webs following declines of higher trophic level predators are common in a variety of ecosystems, including lakes (Carpenter et al., 1985), streams (Power, 1990), kelp forests (Estes et al., 1998), estuaries (Jackson et al., 2001), rocky intertidal systems (Menge, 2000), continental shelves (Frank et al., 2007), and also in the open ocean (Ward and Myers, 2005). However, we also start to realize that trophic cascades depend on complex interactions between environmental conditions, resource supply, individual species traits and food web complexity (Strong, 1992; Polis and Strong, 1996; Menge, 2000; Oksanen and Oksanen, 2000; Shurin et al., 2002; Borer et al., 2005; Borer et al., 2006; Hopcraft et al., 2010). Thus, predator effects on food web configuration are highly context dependent, and properties of the ecosystem will determine any responses to overfishing of top predators. However, there are a few generalities we can make that could indicate which systems are vulnerable to trophic cascades, and hence, where overfishing could contribute to algal blooms. Trophic cascades are enhanced by productivity (Pace et al., 1999), which means that declines in top predator fish may interact with marine eutrophication. Trophic cascades actually imply that every second trophic level is resource controlled and every second level consumer controlled (Oksanen and Oksanen, 2000), resulting in a positive relationship

33


between primary production and every second trophic level. Thus, in a marine system with four effective trophic levels (1) algae, 2) herbivores, 3) smaller predators that eat herbivores and 4) top predators that eat smaller predators) herbivores and top predators should increase with nutrient enrichment. In contrast, if we reduce the system to three effective trophic levels by overfishing of the top predators, algae and the smaller predators should increase with nutrient enrichment (Oksanen and Oksanen, 2000; Eriksson, 2011) (Figure 8). This mirrors documented examples of cascading effects from declines in top predatory fish coinciding with increasing algal biomass in the Black and Baltic Seas (see case studies below; Daskalov, 2002; Casini et al., 2008), where overfishing and eutrophication have occurred simultaneously. Both terrestrial and marine field studies support a positive relationship between large-scale productivity and trophic cascades (Sinclair et al., 2000; Elmhagen and Rushton, 2007; Vasas et al., 2007; Hopcraft et al., 2010), and small-scale experiments from the marine benthos specifically support that nutrient enrichment promotes the propagation of trophic cascades from top-predatory fish to algae (Moksnes et al., 2008; Eriksson et al., 2009; Sieben et al., 2011b). For example, Vasas et al. (2007) created a model food web based on published studies from the North Sea, and showed that overfishing and eutrophication had synergistic effects promoting harmful algal blooms (see 4.2 case study North Sea). Sieben et al. (2011b) showed that removing benthic top predators with the use of cages, induced a trophic cascade that increased the biomass of benthic algae dramatically, but only in combination with nutrient enrichment (see 4.6 case study Baltic Sea). Thus, consequences for the development of algal blooms by removing top predators depend on resource availability. Trophic cascades are stronger in the marine benthos than in the marine plankton (Strong, 1992; Shurin et al., 2002; Borer et al., 2005). In general, positive effects on plant or algal biomass by predation removing herbivores are stronger in water than on land (Strong, 1992). However, this is mainly the cause of very strong cascading effects on algae in the marine benthos (Shurin et al., 2002). In a review of all marine trophic cascade studies published at that time, Borer et al. (2005) showed that medium sized predators that consume herbivores had significant positive effects both on marine phytoplankton and benthic algae, but that while predators increased plankton biomass with ca. 30%, predation increased the biomass of benthic algae multiple times. Thus, we can expect that removal of top predators have stronger effects on filamentous algal blooms than on phytoplankton blooms. Furthermore, trophic cascades with strong reciprocal predator prey effects are mainly expected in systems where interaction strengths are determined by a few functionally dominant species (Strong, 1992; Pace et al., 1999). A compilation of 108 predator removal experiments show that predators on average removed 57% of prey individuals or biomass (personal data). This corresponds well to the average removal of producer biomass by herbivores analyzed in a synthesis of 191 experiments (Gruner et al., 2008). However, the effect of predation on the biomass of their lower trophic level prey was consistently negative only in systems where one predator species alone dominated the predator community. In those communities with one dominating predator, predation on average removed two thirds of the prey biomass, while at higher predator diversities there were no significant negative effects of predation. This indicates that while predators obviously remove biomass, their predation pressure is often not strong enough to control prey biomass when predator diversity is high, probably due to negative interactions between the predators themselves. Thus, we can expect strong effects of overfishing in marine systems where the fish community is dominated by a few highly abundant and functionally important species. This corresponds well with the Black Sea system where

34


anchovy dominates the pelagic fish community and the Baltic Sea system where cod dominates the top predator community and clupeids (sprat and herring) the planktivorous fish community (see case studies 4.3 and 4.5). Figure 8: Increased biomass production from nutrient enrichment accumulate

on different trophic levels depending on the number of trophic levels in the ecosystem.

Smaller predators

Algae

nutrients

Herbivores

Herbivores

Smaller predators

Top‐predators

Algae

4 trophic levels

3 trophic levels

Source: Frank et al., (2005); Daskalov (2007); Casini et al. (2008)

35


36


4. DOES OVERFISHING CONTRIBUTE TO ALGAL BLOOMS IN EUROPE?

From a methodological stand point, it is almost impossible to find conclusive evidence for the effects of such large scale processes as overfishing. Effects of fishing will be superimposed on and interact with a number of important environmental variables. Since we cannot manipulate systems on the scale of ocean basins, we need to use analyses of trends and modeling based of field data in combination with small scale experiments to explore the most likely scenarios and evaluate the most likely effects. Evidence for effects of fisheries on algal blooms, although mainly circumstantial, shows that overfishing most likely contributes to algal blooms in some European marine systems., We thus need to conclude that overfishing contributes to algal blooms, but the magnitude and severity of the blooms changes both in time over the season, and in space, between and within marine systems.

4.1. Modelling effects of overfishing and eutrophication To specifically test joint effects of fishing and marine eutrophication, Vasas et al. (2007) constructed a network model of a generic temperate nearshore pelagic ecosystem. The network model consisted of a topological food web, which is a simple description of relations between different important species groups and information on who eats whom. This gives the basic organization of the ecosystem, and can be used to study the general behavior of the system when exposed to clear cut perturbations, but cannot be used to predict specific abundances or any dynamic behavior. Identification of the functionally most important nutrient pools and species groups, as well as relations between species groups, was obtained by a general review of 25 studies of trophic transfer, i.e. consumption of a nutrient pool or species group or contribution to a nutrient pool by release of nutrients or sedimentation, and by using field data from the North Sea (Rousseau et al., 2000). Thus, the results of this analysis are relevant for any coastal ecosystem in Europe, but are especially relevant for the North Sea. Based on the literature review, Vasas et al. (2007) identified 19 species groups and 7 nutrient pools as relevant for the function of temperate pelagic nearshore communities. This included four bloom forming algal groups: 1) large diatoms, 2) large non-toxic dinoflagellates, 3) inedible algae, including the harmful algae and bacteria that forms toxic or inedible algal blooms; the analysis for example included harmful algal species of cyanobacteria (Nodularia spumigena), dinoflagellates (Noctiluca, Alexandrium spp., Karenia brevis), prymnesiophytes (Prymnesium parvus, Chrysochromulina polylepis, Phaeocystis spp.), raphidophytes (Heterosigma akashiwo). Relevant for this analysis, the network also included large zooplankton that eat larger edible diatoms and dinoflagellates (groups 1 and 2), planktivorous fish (smaller pelagic plankton eating fish), piscivorous fish (larger pelagic fish eating fish), and jellyfish, i.e. jelly-like zooplankton that are members of Cnidaria (true jellyfish) and Ctenophora (comb jellies) (Figure 9).

37


Figure 9: Generic food web of a temperate pelagic nearshore ecosystem. Circles outline trophic groups of organisms or nutrients, and the arrows shows who eats whom. The sustainable food web (a) is based on trophic relations described for modern seas in Europe without strong declines in commercial stocks of fish. The overfishing of larger predatory fish scenario (b) is the predicted change in relation between trophic groups when the food web is exposed both to overfishing of larger fish eating fish and eutrophication. In overfishing of larger predatory fish scenario we expect strong increases in smaller planktivorous fish and blooms of non-toxic algae.

pisci‐vorous fish

plank‐

tivorous

fish

large zoo‐

plankton

large nontoxic algae

toxic algae

jelly fish

nutrients

plank‐tivorous fish


nutrients

jelly fish

toxic algae

large zoo‐plankton

piscivorous fish

Overfishing of larger

predatory fish

Sustainablemodern food‐web

”larger fish that eat fish”

”smaller fish that eat zoo‐plankton”

a) b)

Source: Vasas et al. (2007)

Effects of overfishing of top predators: Analysis of the generic network predicted that overfishing of larger predators should favor blooms of larger non-toxic diatoms and dinoflagellates, but only under simultaneous nutrient enrichment (Vasas et al., 2007). Decreases in larger predators increased the biomass of planktivorous fish and thereby indirectly decreased the abundance of larger zooplankton which feed on the non-toxic diatoms and dinoflagellates (Figure 9b). Thus, overfishing of larger predatory fish should generate a linear trophic cascade in predator prey relations that favors non-toxic high density algal blooms.

38


Figure 10: Generic food web of a temperate pelagic nearshore ecosystem. Circles outline trophic groups of organisms or nutrients, and the arrows shows who eats whom. The sustainable food web (a) is based on trophic relations described for modern seas in Europe without strong declines in commercial stocks of fish. In the ”fishing down the food web scenario” (b), the food web is exposed to overfishing of the smaller pelagic stocks of commercial fish. This is common when stocks of larger fish collapse and fisheries instead turn to smaller planktiovorous fish (e.g. Black Sea). In the ”fishing down the food web” scenario we expect increasing abundances of jelly fish and toxic algal blooms.

nutrients

jelly fish

toxic algae

large zoo‐

plankton

largenon‐toxicalgae

piscivorous fish

planktivorous fish

”Fishing down the food web”pisci‐

vorous fish

plank‐

tivorous

fish

large zoo‐

plankton


toxic algae

jelly fish

nutrients

Sustainablemodern food‐web

”larger fish that eat fish”

”smaller fish that eat zoo‐plankton”

a) b)

Source: Vasas et al. (2007) Effects of overfishing of planktivorous fish: Analysis of the generic network predicted that overfishing of planktivorous fish should favor blooms of inedible algae and jelly fish, irrespective of eutrophication (groups 3, 4 and 5) (Figure 10) (Vasas et al., 2007). The reason for this is that when removing the planktivorous fish, larger zooplankton increased strongly which led to a decrease in their main prey, larger non-toxic diatoms and dinoflagellates. This in turn meant that inedible algae were released from nutrient competition with the edible algae, and increased. At the same time, jellyfish were released from competition by planktivorous fish, and also increased. Thus, overfishing of piscivorous fish should favor toxic algal blooms and jellyfish, by releasing them from competition. In conclusion, the generic food web model of a temperate pelagic nearshore ecosystem by Vasas et al. (2007) predicts that: 1) overfishing of larger predatory fish together with eutrophication should facilitate the development of non-toxic high biomass algal blooms; and 2) overfishing of smaller planktivorous fish – “fishing down the food web” – should facilitate the development of toxic algal blooms and an increased abundances of gelatinous

39


zooplankton. This simple analysis provides a template for understanding how overfishing can contribute to the temporal trends in the case studies below.

4.2. The North Sea case study In the North Sea, declines in larger predatory fish due to overfishing are well documented since the 1970s (Pauly et al., 1998; Christensen et al., 2003). However, from 1980 there is also a general change in the North Sea ecosystem that includes changes in the fish community composition and increases in the abundance of phytoplankton (Reid et al., 2001; Weijerman et al., 2005; McQuatters-Gollop et al., 2007). Catches of predatory fish with a maximum length larger than 90 cm have decreased steadily since 1970, from a peak of 1000,000 to 200,000 tons in 2000 (Figure 11). Fisheries on tunas and billfishes, the larger pelagic predators, collapsed already in the early 1960s, while fisheries for sharks and rays peaked during the 1960 with a continuous decline from the 1970s and on (Figure 12). Today, the commercially dominating larger predators are the demersal species cod and saithe (Pollachius virens). Catches of cod and saithe peaked during the 1970s when catches were two and a half times larger than today. Since around 1980, catches of cod and saithe have declined strongly (Figure 13). In the mid-1970s the composition of the catch changed significantly, because the decline in larger fish was paralleled by a strong increase in the catch of fish smaller than 30 cm (Figure 11). Together with the general decline in the stocks of the larger predators, the shift towards smaller fish is due to a strong increase in industrial fisheries for sandlances (seaaroundus.org). Around 1980, the structure of the North Sea ecosystem changed, most notably by a rapid increase in algal biomass (Figure 14)(McQuatters-Gollop et al., 2007). Comparing 1947-1979 with 1980-2003 shows on average a 13% higher concentration of phytoplankton pigments in the water of the open North Sea, and a 21% higher concentration in the coastal regions of the North Sea (McQuatters-Gollop et al., 2007). Analyses of large scale climatic variables have suggested a number of potential environmental variables affecting the whole region of northwestern Europe which triggered this shift in biological structure, most notably salinity, weather conditions and large-scale changes in water clarity (Reid et al., 2001; Weijerman et al., 2005; McQuatters-Gollop et al., 2007). This has led to the suggestion that changes in large scale climatic conditions have induced a large scale regime shift in the North Sea, affecting all trophic levels from plankton and open sea fish to benthic invertebrates and coastal fish (Beaugrand, 2004). However, the shift also coincides with a decline in the mean trophic level of the catch, which depends on the combined effects of an increased fishery for smaller fish and the declines in larger predators (Figure 15). Thus, we see parallel changes in the fish and the phytoplankton community, where an intensified fishing and declines of larger fish, especially of cod, correlate with increases in phytoplankton biomass. This corresponds to the predicted joint effects of overfishing of larger predatory fish and eutrophication in the North Sea (Vasas et al., 2007). In conclusion, although highly speculative, the trends in the North Sea indicate that we need to explore if both fishery- and climate-induced changes have contributed to the increase in phytoplankton biomass, with a potentially increased risk for algal blooms.

40


Figure 11: Trends in landings of large and small fish in the North Sea

0

200

400

600

800

1000

1200

1400

1600

1950 1960 1970 1980 1990 2000

catch tonnes x 10

3small < 30 cm

large > 90 cm

Source: Seaaroundus.org

Figure 12: Trends in landings of large pelagic species in the North Sea

0

10

20

30

40

50

60

1950 1960 1970 1980 1990 2000

catch tonnes x 10

3

Sharks & rays

Tuna & billfishes


Figure 13: Trends in landings of large demersal species in the North Sea

0

50

100

150

200

250

300

350

400

1950 1960 1970 1980 1990 2000

catch tonnes x 10

3

Atlantic cod

Saithe


41


Figure 14: Trends in abundance of algae in the North Sea

2

2.5

3

3.5

4

4.5

1950 1960 1970 1980 1990 2000

Chl a

(mg m

‐3)

coastal North Sea

open North Sea

Source: McQuatters-Gollop et al. (2007)

Figure 15: Trends in mean trophic level of landings in the North Sea

3.1

3.2

3.3

3.4

3.5

3.6

1950 1960 1970 1980 1990 2000

mean trophic level

Mean trophic level


4.3. The Black Sea case study In the Black Sea, a strong decline in larger predators culminating in the early 1970s was followed by a sharp increase in phytoplankton biomass that peaked in the early 1980 at a relative increase of 100% (Daskalov, 2002; Daskalov et al., 2007). Since the shift in fish composition in the 1970s, the frequency and intensity of phytoplankton blooms have increased dramatically (Zaitsev, 1992; Kideys, 1994; Daskalov, 2002; Yunev et al., 2002; Yunev et al., 2005). All through the 1960s the dominating top predators in the Black Sea were heavily exploited, including dolphins and large migratory species such as the bonito (Sarda sarda), tuna and swordfish (Daskalov, 2002). However, in the late 1960s fisheries on larger species collapsed and their stocks were heavily depleted or disappeared. Today we see a slow recovery of tuna and billfishes in the catch statistics, mainly because of an increasing catch of Atlantic bluefish tuna in the Turkish and Russian fisheries (Figure 16). After the decline of the larger pelagic species, their main prey species, small and medium sized pelagic

42


species such as anchovy (Engraulis encrasiccolus), sprat (Sprattus sprattus) and Mediterranean horse mackerel (Trachurus mediterraneus), increased strongly in the early 1970s which attracted the commercial fisheries (Figure 17)(Kideys, 1994; Daskalov, 2002). Consequently, the average trophic level of catches in the Black sea decreased significantly throughout the second half of the 20th century, supporting a shift in fish community composition from large to medium and small pelagic species (Figure 18). Following the shift in the fish community from larger predatory to smaller planktivorous fish, zooplankton biomass decreased strongly and phytoplankton increased accordingly (Figure 19)(Daskalov, 2002; Daskalov et al., 2007). Planktivorous fish mainly eat larger zooplankton, and changes in community compositions of zooplankton suggest that the decline in biomass in part depends on that larger species were replaced by smaller species of crustacean plankton (Zaitsev, 1992; Kideys, 1994). The phytoplankton community also changed character, as larger phytoplankton dominated by dinoflagellates increased in relative abundance compared to smaller phytoplankton, dominated by diatoms (Kideys, 1994; Daskalov, 2002). Notably, in the Black Sea we see a second cascading event that establishes even higher abundances of phytoplankton biomass and algal bloom frequency in the 1990s. After the switch of the commercial fisheries from larger top predators to smaller pelagic species in the 1960s, the anchovy fishery increased strongly to become the commercially most important planktivorous fish in the Turkish fisheries. Between 1988 and 1991, the catches of anchovy dropped to 25% percent of the catches in the 1980s. The decline in anchovy catch is confirmed by a sharp decrease in the general total biomass of smaller planktivorous fish in the Black Sea (Daskalov et al., 2007). However, the zooplankton community did not recover. Instead two species of jelly-like zooplankton that compete with the planktivorous fish for their main zooplankton prey increased strongly. This suggests that fishing may have promoted algal blooms in the Black Sea in two separate overfishing events, both leading to declined zooplankton grazer pressure on phytoplankton. There is strong circumstantial evidence that overfishing and eutrophication have jointly contributed to a trophic cascade increasing the biomass of phytoplankton in the Black Sea (Daskalov, 2002; Daskalov et al., 2007). First, there is an inverse correlation between adjacent trophic levels over time (1950-60 to 2003), whereas there is a positive correlation between non-adjacent trophic levels (Table 2) (Daskalov, 2007): notably there is a significantly negative relation between the abundance of larger pelagic predatory fish and phytoplankton biomass (n=43, r=-0.39). Second, Daskalov (2002) constructed a food web model (a dynamic mass balance model) of the pelagic system in the 1960s by mapping mean biomass, production, consumption rates and diets of 15 important food web groups. This included dolphins, larger predators, planktivorous fish, fish larvae, different gelatinous zooplankton, and large and small zoo- and phytoplankton. Daskalov (2002) then ran model simulations of fishing and eutrophication. A fishing only scenario, where fishing pressure was assumed to have increased three-fold over a 30 year period, correctly reproduced the alternating changes in trophic levels observed in the 1970-80s in the Black Sea food web, including 1) increases in planktivorous fish, 2) decreases in zooplankton biomass, caused by decreases in the relative abundance of larger zooplankton species and 3) increased phytoplankton biomass, caused by increases in the relative abundance of larger phytoplankton species. Note that the applied fishing pressure is a minimal estimation to avoid exaggeration of effects. Still, the “fishing only” model only produced an increase in phytoplankton biomass with ca. 30%, which underestimate the observed increase of 100%. However, assuming both a three-fold increase in fishing and an increased primary production of the system by eutrophication, correctly predicted an increase in phytoplankton biomass of between 95 and 100%.

43


In conclusion, considering 1) the high frequency of algal blooms since the 1970s (Zaitsev, 1992; Kideys, 1994; Daskalov, 2002; Yunev et al., 2002; Yunev et al., 2005), 2) the parallel changes in fish community composition and predator-prey relationships (Figure 16 to 19) (Daskalov, 2002; Daskalov et al., 2007), and 3) the results from the food web model by Daskalov (2002) which indicate that declines in decreasing predator control by larger predatory fish together with eutrophication cause a generally higher phytoplankton biomass, it is likely that overfishing and eutrophication jointly contribute to algal blooms in the Black Sea. Notably, the algae predicted to increase from overfishing in the Black Sea were mainly large phytoplankton, such as the larger red tide forming dinoflagellates Prorocentrum cordatum and Noctiluca miliaris, which also increased strongly in the 1970s during the time of the collapse of the fisheries on larger pelagic fish (Kideys, 1994; Daskalov, 2002). Figure 16: Trends in landings of tuna and billfishes from the Russian, Romanian

and Turkish Black Sea fisheries

0

5

10

15

20

25

30

1950 1960 1970 1980 1990 2000

catch tonnes x 10 3

Tuna & Billfishes Atlantic bonito

Atlantic bluefin tuna


Figure 17: Trends in landings of small and medium sized pelagic species in the

Black Sea

0

100

200

300

400

500

600

700

800

900

1950 1960 1970 1980 1990 2000

catch tonnes x 10

3

Perch ‐likes

Herring ‐likes

Anchovies


44


Figure 18: Trends in mean trophic level of landings in the Black Sea

3.1

3.2

3.3

3.4

3.5

1950 1960 1970 1980 1990 2000

trophic level

Mean trophic level


Figure 19: Trends in the relative biomass of zooplankton and phytoplankton in

the Black Sea

‐1.5

‐0.5

0.5

1.5

2.5

3.5

4.5

1950 1960 1970 1980 1990 2000

relative biomass

Zooplankton

Phytoplankton

Source: Daskalov 2002

Table 2: The relation between larger pelagic predators (biomass of e.g. tunas

and billfish) and lower trophic levels in the Black Sea over time.

Number (n) Correlation

coefficient (r) Significance (p)

Planktivorous fish biomass 38 -0.55 <0.01

Zooplankton biomass 43 0.44 <0.01

Phytoplankton biomass 43 -0.39 <0.01

Source: Daskalov et al. (2007)

45


4.4. The Kattegat case study In the Kattegat on the Swedish North Sea coast, a long-term decreasing trend of the dominating demersal predator, cod, coincides with a 60% decline in seagrass beds attributed to increasing blooms of mat-forming filamentous algae (Baden et al., 2003; Moksnes et al., 2008; Baden et al., 2010; Eriksson et al., 2011). Cod is the dominating demersal predator in the area and was subjected to a strong commercial fishery resulting in a continuous decline in catch since the 1970s (Figure 20). Stock assessments indicate a decline in total cod biomass from 25-35 to 5-10 106 kg in the Kattegat between 1976 and 2008 (Figure 21). At the same time, local coastal populations of stationary cod have declined dramatically. In Kattegat, juveniles of the offshore population of cod settle in nearshore habitats and the larger juveniles predate significantly on coastal communities of smaller predatory fish, including gobiids, the common shore crabs (Carcinus maenus) and wrasses (Pihl 1982, Pihl and Ulmestrand 1993, Salvanes and Nordeide 1993). Accordingly, together with the decline in cod populations the abundance of black goby (Gobius niger), shore crabs and the dominating wrasses, corkwing wrasse (Symphodus melops) and goldsinny wrasse (Ctenolabrus rupestris) has steadily increased along the coast (Figure 22) (Eriksson et al., 2011). Black goby, shore crabs and wrasses all have the potential to regulate the abundance of crustacean and gastropod herbivores ("mesograzers"), which in turn graze on the algae that form filamentous algal blooms (Norderhaug et al., 2005; Newcombe and Taylor, 2010). In agreement, comparing the animal communities in seagrass beds between the 1980s and 2000s shows that a crustacean mezograzer community that was abundant in the 1980s, had vanished totally from the seagrass beds in the 2000s (Baden et al., 2011). At the same time the occurrence of cod decreased four times and smaller predators such as black gobies increased six times. Thus, overfishing of cod has potentially resulted in cascading effects that promote filamentous algal blooms by indirectly decreasing the grazing pressure from invertebrate grazers (Moksnes et al., 2008; Baden et al., 2010; Eriksson et al., 2011). There is both circumstantial and experimental support to the hypothesis that the changes in the structure of the Kattegat food web, caused by the fishery induced declines in cod, have contributed to increasing abundances of algal blooms and large-scale decreases of seagrass. First, there is a significant correlation between the decline in offshore cod and the increase in smaller coastal fish (Figure 23). There is also a significant correlation between high coastal water temperatures in spring and higher abundances of smaller coastal fish (Figure 24). However, there is no increasing temperature trend in the coastal waters where fish is monitored, and the correlation with the cod decline is statistically stronger – cod explains 47% of the variation in total abundances of smaller predatory fish and temperature only 28% (compare R values in Figures 23 and 24). This indicates that although temperature is important for survival of coastal fish, the decline in cod is more likely to have caused the increase in smaller predatory fish (Eriksson et al., 2011). Additionally, there is strong experimental evidence that smaller predatory fish promote higher biomass of filamentous algae by feeding on the crustacean grazers in the system (Moksnes et al., 2008; Baden et al., 2010). Removing grazers and predators with different types of cages in the field showed that natural abundance of smaller predators in seagrass beds decreased the presence of crustacean mesograzers with 98%, and affected the growth of the seagrass negatively by increasing the load of the filamentous algae that form nuisance mats in coastal areas of Kattegat.

46


Figure 20: Trends in landings of cod and other large predatory fish in Kattegat

0

50

100

150

200

250

300

350

400

1975 1985 1995 2005

Catch per unit effort

Cod ‐ offshore bottom trawl survey

Other large predators (haddock, ling,pollack)


Figure 21: Trends in total biomass of cod in Kattegat

0

5

10

15

20

25

30

35

40

1975 1985 1995 2005

biomass (kg 106)

Estimated total biomass of cod in Kattegat

Source: Eriksson et al. (2011)

Figure 22: Trends in the abundances of shore crabs and medium sized fish from

coastal monitoring at Ringhals in Kattegat.

0

0.2

0.4

0.6

0.8

0

5

10

15

20

25

30

35

1975 1985 1995 2005

Catch per unit effort

Costal monitoring of:

wrasses

shore crab

black goby


47


Figure 23: Relation between offshore cod and coastal populations of medium sized predators = total abundance of shore crab, wrasses and black goby.

R² = 0.4723

0

10

20

30

40

0 10 20 30 4

total CPUE coastal fish

Total cod biomass kg 1060

Source: Eriksson et al. (2011) Figure 24: Relation between spring temperatures and coastal populations of

medium sized predators = total abundance of shore crab, wrasses and black goby.

R² = 0.2844

0

10

20

30

40

3 4 5 6 7 8 9

total CPUE coastal fish

Water temperature Celsius

Source: Eriksson et al. (2011) Thus, it is highly plausible that that decreases in cod caused by overfishing and the subsequent strong increases in smaller predatory fish along the coast, have contributed to increased loads of filamentous algal blooms. It is notable that the negative effects of increasing filamentous algal blooms have affected seagrass communities dramatically. Juvenile cod was formerly found in high abundances in seagrass beds, which indicate that they are important nursery areas for the offshore cod population. This raises concerns that overfishing of cod generates a negative feedback on cod recruitment in the Kattegat by contributing to loss of coastal recruitment areas.

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4.5. The Baltic Sea – offshore case study In the Baltic Sea, the offshore food web has changed dramatically since the 1980s, with strong declines in the dominating demersal fish stock of cod and increases in phytoplankton biomass and the frequency of algal blooms (Kahru et al., 1994; Poutanen and Nikkila, 2001; Alheit et al., 2005; Hansson, 2005; Casini et al., 2008; Möllmann et al., 2008; HELCOM, 2009). Initially, after an expansive fisheries on cod in the 1970s, the offshore Baltic Sea cod populations declined by 75% during the 1980s (Figure 25) (ICES, 2010). This decline was followed by a four-fold increase in sprat (Sprattus sprattus), which is the main prey fish of cod and which became the dominating pelagic planktivore (Österblom et al., 2007; Casini et al., 2008). Zooplankton is poorly sampled, but data from the Gotland Sea, in the southern Baltic Sea, shows that the summer biomass of the main prey zooplankton species of sprat, (a number of larger copepods and cladocerans (crustaceans)), declined to about 50% in the 1990s compared to the 1980s (Casini et al., 2008). At the same time, phytoplankton biomass estimated by chlorophyll concentrations in the water doubled (Figure 26). Additionally, in the Gotland Sea, phytoplankton biomass in surface waters during the spring bloom from March to May, increased strongly from the 1980s to the 1990s (Figure 27) (Wasmund et al., 1998). There is strong circumstantial evidence that changes in fish community composition have also affected lower trophic levels in the Baltic Sea (Österblom et al., 2007, Casini et al., 2008). First of all, between 1974 and 2006 cod and sprat biomass, sprat and zooplankton biomass, zooplankton and phytoplankton biomass were all significantly inversely related to each other (data by Casini et al. (2008), using zoo- and phytoplankton biomass from the Gotland Sea, southern Baltic Sea; Table 3). In addition, as predicted for a trophic cascade, non-adjacent trophic levels were positively related: low biomass of cod coincided with low biomass of zooplankton, while high biomass of sprat coincided with high biomass of phytoplankton. Second, Casini et al. (2008) compared the effect of each higher trophic level on the lower trophic level, with the effect of various environmental variables, including temperature, salinity and variations in the overall climate (the NAO winter index). The comparison showed consistently that the biomass or abundance of the higher trophic level was the main factor explaining the variation in the lower trophic level: the abundance of cod explained 90% of the yearly variation in sprat; sprat abundance explained 83% of the yearly variation in zooplankton biomass; and zooplankton biomass explained 91% of the yearly variation in phytoplankton (Figure 28 and 29). In conclusion, declines in cod have caused a massive increase in sprat in the open Baltic Sea, due to release of predation pressure, and it is likely that this has generated a trophic cascade with generally lower biomasses of zooplankton and higher biomasses of phytoplankton from the early 1990s onward. The increase in phytoplankton biomass coincides with a sharp increase in spring bloom intensity (Figure 27), and in the 1990s and 2000s there has also been a high frequency and intensity of cyanobacterial blooms in the Baltic Sea (Figure 5) (Kahru et al., 1994; Poutanen and Nikkila, 2001; Hansson, 2005; HELCOM, 2009). Thus, the collective evidence strongly suggests that overfishing of cod has contributed to a general increase in algal blooms.

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Figure 25: Trends in the dominating fish populations in the Baltic Sea

0

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#sprat 10

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Atlantic cod Sprat


Figure 26: Biomass of zoo- and phytoplankton in the Gotland Sea, southern Baltic

Sea.

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1970 1980 1990 2000 2010

Chlorophyll a

(mg dm

‐3)

zooplankton biomass (mg m

‐3) zooplankton

phytoplankton

Source: Casini et al. (2008)

Figure 27: Intensity of the spring bloom in the Gotland Sea, southern Baltic Sea.

Average phytoplankton biomass from 0 to 10 m depth.

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mean biomass (w

t mg m

3) spring bloom

intensity

Source: Wasmund et al. (1998)

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Table 3. The relation between adjacent trophic levels in the Baltic Sea between 1974 and 2006. Biomass of cod and sprat are from total estimations for the Baltic Sea, while biomass of zoo- and phytoplankton are from monitoring data from the southern Baltic Sea (the Gotland Sea).

Number (n) Correlation coefficient (r)

Cod vs sprat biomass 33 -0.60

Cod vs zooplankton biomass 33 0.46

Sprat vs zooplankton biomass 33 -0.53

Sprat vs phytoplankton biomass 28 0.62

Zoo- vs phytoplankton biomass 28 -0.47


Figure 28: The relative importance of different biological and environmental

factors for determining the density of sprat in the Baltic Sea. GLM modelling using backwards selection with Mallows C as selection criteria, see original publication for details.

sprat abundancecod abundance

temperature

salinity

NAO winter index

food availability adults

food availability juveniles

sprat biomasscod biomass

temperature

salinity

NAO winter index

food availability adults

food availability juveniles


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Figure 29: The relative importance of different biological and environmental factors for determining the density of zoo- and phytoplankton in the southern Baltic Sea. GLM modelling using backwards selection with Mallows C as selection criteria, see original publication for details.

zooplankton biomasssprat biomass

temperature

salinity

NAO winter index

phytoplankton preyavailability

zooplankton abundancesprat abundance

temperature

salinity

NAO winter index

phytoplankton preyavailability

phytoplankton biomass

zooplankton biomass

temperature

salinity

NAO winter index

nutrient availability


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4.6. The Baltic Sea – coastal case study As in the Kattegat, there are also strong indications from the coast of the central Baltic Sea that filamentous algal blooms have increased as a direct consequence of offshore fisheries on cod, but in this case together with local declines in coastal populations of perch and pike (Eriksson et al., 2009; Ljunggren et al., 2010; Eriksson et al., 2011; Sieben et al., 2011a, 2011b). Since 1990 there has been a continuous decline in the catches of the dominating larger nearshore predators – European perch (Perca fluviatilis) and northern pike (Esox lucius) along the Swedish coast of the Baltic Proper (Figure 30 and 31). The declines of perch and pike are local as the populations in some areas seem fine while the populations in other areas are completely gone. This corresponds to recruitment failures concentrated in open archipelago areas, while sheltered areas along the coast still seem to support both recruitment and strong populations of perch and pike. Accordingly, long-term monitoring from the Kalmar sound, an open archipelago area on the Swedish Baltic coast, shows a general decline of larger predators including formerly strong coastal populations of cod (Figure 32)(Eriksson et al., 2011). Thus, the changes in fish community structure in the open Baltic Sea have also affected nearshore areas. In the 1970-80s, high abundances of cod were commonly recorded near the shore, but since the early 1990s cod has vanished. At present, three-spined stickleback (Gasterosteus aculeatus) – a smaller predatory fish feeding on crustacean and gastropod mesograzers – completely dominates many sheltered coastal communities (Eriksson et al., 2009; Ljunggren et al., 2010). Sticklebacks are poorly represented in coastal monitoring programs because the majority migrates offshore after the recruitment period in summer – they are mainly present in May-June (unpublished data). However, offshore eco-soundings show that stickleback have increased exponentially between 2006 and 2010 (Figure 33) (Ljunggren et al., 2010). Thus, a strong increase in sticklebacks may depend both on decreased predation pressure from weakened coastal populations of cod, perch and pike, and from the declined offshore populations of cod. There is evidence that the high abundances of stickleback are caused by decreased populations of perch and pike, and that this shift in fish community composition indirectly promotes filamentous algal blooms. There is no monitoring of invertebrate grazers or long enough time series of filamentous algae to analyze time trends. However, along the Swedish coast of the Baltic Sea, the development of filamentous algae and abundances of stickleback increases with declining abundances of perch and pike (Eriksson et al., 2009). In areas with low abundance of perch and pike, stickleback dominates the fish communities and almost 50% of the shallow bays are overgrown by filamentous algae (Figure 34). In areas with high abundances of perch and pike, sticklebacks are rare and only 10% of the bays are overgrown. In the Baltic Sea, experiments also demonstrate a causal link between coastal predators and algae. In a stickleback infested bay that is often covered by filamentous algae, a large scale manipulation removing thousands of sticklebacks from 20 by 30 m enclosures decreased the recruitment of filamentous algae by 60%. In an area with healthy predator populations, small scale experiments with cages also show that excluding perch and pike increase the abundance of stickleback several times. This decreased the grazing pressure in algae and consequently the biomass of filamentous algae increased by 100 to 300%. In addition, the influence of removing perch and pike on the production of filamentous algae is significantly strengthened by nutrient enrichment (Figure 35) (Sieben et al., 2011b) – indicating that predator declines and nutrient enrichment contribute together to the problem of filamentous algal mats.

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In conclusion, overfishing and eutrophication together promote the development of filamentous algal blooms in coastal areas in the Baltic Sea. During the 1990s occurrences of drifting algal mats has also become a more common problem (Vahteri et al., 2000). Increasing growth of bloom forming filamentous algae and problems with drifting algal mats are now regularly reported from coastal areas in the Baltic Sea (Bonsdorff et al., 1997; Bonsdorff et al., 2002). Figure 30: Decline in perch on the Swedish coast in the southern Baltic Sea

0

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120

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1994 1996 1998 2000 2002 2004 2006 2008

commercial landings tons

monitoring # cpue

perch Mönsterås gilnet monitoring

Landings Area 27

Source: Ljunggren et al. (2010)

Figure 31: Decline in pike on the Swedish coast in the southern Baltic Sea

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commercial landings tons

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Landings Area 27

Source: Ljunggren et al. (2010)

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Figure 32: Trends in the abundance of larger coastal predatory fish at Kalmar in the southern Baltic Sea.

0

500

1000

1500

2000

2500

1970 1980 1990 2000

# larger predatory fish cpue Perch

Pike

Atlantic cod

Source: Eriksson et al. (2011) Figure 33: Trends in offshore abundances of cod, sprat and stickleback.

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Atlantic cod Sprat Stickleback


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Figure 34: Abundance of stickleback per hand trawl and the percentage of area overgrown by filamentous algae depending on the density of top predators.

A) Bays with vanished populations of perch and pike = low abundances of top predators; and in B) bays with healthy populations of perch and pike = high abundance of top predators

0

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A) Low B) High

Number cpue

Sticklebacks

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Overgrown plots (%)

Filamentousalgae in August

Source: Eriksson et al. (2009) Figure 35: Removing perch and pike together with eutrophication increase the

development of filamentous bloom forming algae

0

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Large fishexcluded

Large fishpresent

Volume dm

3per m

2

No nutrient addition

Nutrient enriched

Source: Sieben et al. (2011), unpublished data

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5. CONCLUSIONS AND RECOMMENDATION This review provides strong evidence that overfishing of larger top predatory fish contributes to an increased frequency or intensity of algal blooms in Europe: Blooms are natural phenomena that are controlled by a number of environmental factors. However, overfishing contributes to the problem of algal bloom development by weakening an important biological control of overgrowth. This is because fishing, by removing top predators, generates changes in food web configurations, which in general promotes smaller fish and causes a decline in the abundance of grazers on algae, such as zooplankton or invertebrate herbivores. Together with abiotic factors, grazers control the development of algal biomass, and when grazers decline, algal blooms develop easier. Thus, effects of fishing on algal blooms vary between systems, time of the season and between years. This is important to note, because it makes the detection and management of effects of fisheries on algal blooms more difficult. Responses of algae will not be linearly related to top-predators, but also depend on other circumstances that make any effects of overfishing more or less strong. Thus, access to matching long-term data including all trophic levels in the marine food web is important to disentangle how much fishing contributes to algal blooms. In the Baltic and the Black Seas overfishing has changed ecosystem configurations and it is very likely that this has contributed to an increased problem with harmful algal blooms: Although the ecology and regulation of algal blooms is complex, there is strong circumstantial evidence that overfishing has contributed to increased problems with algal blooms by simultaneous declines in commercial stocks of larger predatory fish and large-scale increases in algal biomass and harmful algal blooms in a number of European Seas. In the Baltic Sea and the Black Sea analyses of time series and coinciding events strongly support that overfishing has contributed to an increasing problem and economic cost of algal blooms. Notably, trends in the Baltic Sea indicate that detrimental effects of offshore overfishing are spreading to coastal ecosystems, causing problems with nearshore water quality and habitat loss. In the Kattegat, we lack data on trends in algal blooms, but experiments support that effects of a documented long-term decrease in offshore and coastal populations of cod have had detrimental effects on seagrass communities by increasing filamentous algal blooms. In the North Sea, modeling and analyses of available data predicts increasing loads of algae due to documented fishery induced changes in the structure of the fish community. There is a general lack of trend analyses that include more than one organism group from several sea basins in Europe, but where there are reported problems with both overfishing and algal blooms. This indicates that important information is missing, because of data not being publicly available for cross referencing. The ecosystem analyses from the Baltic, Black and North Sea illustrate that to understand the effects of fisheries we need to explore connections between trophic levels. Overfishing and eutrophication creates synergistic effects: double trouble! Changes in top predator communities and algal blooms co-occur with eutrophication. There is no doubt that an Europe wide eutrophication has promoted algal blooms, but later, the effects of changes in fish community composition have added to the problem of harmful algal blooms. For example, in the Baltic Sea, problems with anoxic bottoms generated by

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an increased algal production multiplied during the onset of eutrophication in the 1960s-1970s. However, for the past decades, grazing describes the yearly variation in phytoplankton biomass much better than nutrients (low zooplankton biomass = high phytoplankton biomass; Figure 29). Thus, in the modern nutrient rich state of the Baltic Sea, overfishing has contributed to increases in algal biomass. Furthermore, experiments in the field clearly demonstrate that the development of filamentous algal blooms is facilitated both by nutrients and removal of top-predatory fish, and that they act in concert so that the combined effect of nutrients and removal of predators is often many times stronger than their effects in isolation. Coastal high density algal blooms are strongest related to overfishing There is no clear cut evidence that certain species or types of algal bloom are more or less sensitive to changes in fish community compositions. However, available data suggests some general trends. Of the harmful algal blooms, non-toxic high density blooms are the most sensitive to overfishing, since toxic or inedible blooms should be less sensitive to grazing. Accordingly, the strongest conclusive evidence of overfishing effects comes from coastal bays where declines in larger predatory fish promote non-toxic blooms of filamentous mat-forming algae. Model results based on available knowledge from temperate coastal seas and data from the North Sea also show that larger non-toxic diatoms and dinoflagellates are the main groups that would increase by overfishing on larger predatory fish. Thus, overfishing should mainly promote high density algal blooms and generate problems with 1) drifting algal mats, 2) mucilage and foam production, and 3) post bloom anoxia. However, the analysis of the North Sea food web by Vasas et al. (2007) also showed that intensified fisheries can generate unexpected effects by changing competitive hierarchies between algae and planktivores. The results suggested that, allowing commercial fisheries to replace declining catches of larger predatory fish with intensified fisheries on smaller planktivorous fish – fishing down the food web - promoted toxic algal blooms and jellyfish. This is also mirrored in the Black Sea food web, where jellyfish increased dramatically after an intensified fishery on anchovy collapsed in the 1990s. Overfishing should mainly promote algal blooms when the target is a single species that dominates the abundance and function of the fish community Effects on prey species by removing predators are in general much stronger if the predator community is dominated by a single species. This is typical for the best described European case studies. In the Baltic Sea and the Kattegat, the effects are related to declines in a single predator, cod, which dominated the demersal top-predator communities. In the Black Sea, more top-predators were involved in the initial ecosystem changes in the 1960s-1970s. However, the strongest ecosystem effects, including increases in algae, were generated when the pelagic community of smaller fish collapsed around 1990. This community was dominated by a single species of anchovy that was heavily exploited. This indicated the need to include biodiversity as a management strategy, as keeping a diversified fishery and a species rich fish community will buffer marine systems against harmful cascading effects that promote algal blooms.

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Harmful algal blooms have negative effects on fisheries in Europe. The total cost of harmful algal blooms for the European fisheries is estimated to at least 177 million euro per year. This includes negative effects on commercial fisheries, loss to social welfare and cost for monitoring algal blooms for seafood poisoning. Toxic algal blooms generate large costs for the aquaculture sector. Direct losses of sellable products for the mussel sector ranges from 15 to 62 million euro per year. High density blooms create problems for all types of coastal fisheries. Drifting algal mats and mucilage forming blooms interfere with fishing gear and render fishing gear less effective. Post bloom anoxia causes significant kill-offs both of aquaculture and wild fish stocks. Anoxia also interferes with reproduction along the coast, which include the main recruitment areas for many offshore populations of fish. In the Baltic Sea, increased bottom anoxia may even interfere with offshore recruitment of cod. Recommendation: ecosystem based management This review demonstrates that traditional management of marine resources has severe limitations since it often ignores interactions both within food webs and between offshore and coastal food webs. Cascading effects of overfishing change predator-prey relations and thereby increase the frequency and intensity of harmful algal blooms, which in turn interfere with profitability of the fishing industry and may generate negative long-term effects on commercially important stocks. Thus, negative feedbacks may be detrimental to the long term sustainability of marine resources. However, the cost of fisheries is not limited to the fisheries sector, but also affects coastal communities where increasing problems with algal blooms lead to substantial losses in tourist revenue and costs related to negative effects on human health. The evidence suggests that an ecosystem-based management (EBM) approach is necessary to provide a better platform for an integrated fisheries and coastal management. Two main objectives of a future EMB approach should be 1) the incorporation of ecosystem effects by exploitation of higher trophic levels, and 2) spatial considerations that include fluxes between offshore and coastal habitats. This has two immediate consequences: First, by acknowledging ecosystem effects of fisheries, a necessary first action will be to change management goals. We need to rebuild predator populations not only to maximize production of the target species, but also to bring them to levels at which their ecological function is restored, both in offshore and coastal food webs. This means increasing the abundance of top-predatory fish until their control over lower trophic levels is restored, which includes strengthening grazer control over bloom forming algae. Second, by acknowledging important fluxes between offshore and coastal habitats, the interdependence of different management goals by traditionally separate management sectors will be visible, such as the importance of restoring the function of offshore fish stocks for improvements in water quality by limiting harmful algal blooms, and the importance of increased protection of valuable coastal habitats for the recruitment of many offshore stocks of commercially valuable fish.

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