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The Interactions between Cormorants
and Wild Fish Populations
Analytical Methods and Applications
Maria Ovegård
Faculty of Natural Resources and Agricultural Sciences
Department of Aquatic Resources
Lysekil
Doctoral Thesis
Swedish University of Agricultural Sciences
Lysekil 2017
Acta Universitatis agriculturae Sueciae
2017:12
ISSN 1652-6880
ISBN (print version) 978-91-576-8797-5
ISBN (electronic version) 978-91-576-8798-2
© 2017 Maria Ovegård, Uppsala
Print: SLU Service/Repro, Uppsala 2017
Cover: Cormorant eating cod, Denmark.
Photo by Helge Sørensen, www.birdphotos.dk
Cover pages for manuscripts:
Photos by Florian Möllers, http://florianmoellers.com/
The Interactions between Cormorants and Wild Fish populations.
Analytical Methods and Applications
Abstract
Predation is the core in ecology, as a function in food webs which regulate both
populations and communities. Seabirds are at the top of the food chain and key players
in many aquatic food webs. So are humans, and in certain cases conflicts of resources
arise. Cormorant predation on fish is probably one of today’s most well-known and
wide spread human-wildlife conflict. Different species of cormorants have
independently increased in numbers in several areas of the world. For some species,
their predation has created a human conflict concerning resource competition (real or
perceived competition) with both commercial and recreational fisheries. Though there
is extensive research on cormorant diet we are far from reaching a consensus about how
cormorant predation affects the environment.
The aim of this thesis was to investigate how cormorants interact with wild fish
communities and human fisheries. This was achieved by investigating cormorant diet
composition, changes in diet over time, and between areas. The thesis also includes the
first meta-analysis on cormorant diet, in which previous research investigating the
effects of cormorant abundance on fish parameters were analysed.
The results shows that cormorants generally have negative effects on fish
populations, and control measures to limit predation generally have positive effects.
Especially vulnerable to cormorant predation are species within the Percidae and
Cyprinidae families. To some degree fish species and sizes in the diet overlap with
those in fisheries catches (commercial and recreational). The predation on smaller sized
fish however, is for some fish species more important in terms of competition with
fisheries, as it results in less recruitment to commercial sizes. The diet analyses support
earlier studies on temporal and spatial variation in the diet of cormorants.
Essential knowledge for the management of fish, fisheries and cormorants is how
cormorants affect fish populations. A misdirected effort in cormorant research is
emphasized. Most studies fail to identify effects as they don’t relate diet with
cormorant abundance and predation pressure. There is a need for systematically
designed research, where cause and effects are studied. Future research should also
consider an ecosystem approach, where indirect effects of predation are considered.
Keywords: cormorant, diet, fishery, meta-analysis, Phalacrocorax, tag, wildlife-conflict.
Author’s address: Maria Ovegård, SLU, Department of Aquatic Resources, Institute of
Coastal Research, Turistgatan 5, 453 30, Lysekil, Sweden
E-mail: maria.ovegard@ slu.se
Dedication
To my supporting family and friends whom I love very much.
And she gazed at the sky, the sea, the land,
The waves and the caves and the golden sand.
She gazed and gazed, amazed by it all,
And she said to the whale, “I feel so small”
Julia Donaldson, The snail and the Whale
Contents
List of Publications 7
1 Introduction 9
1.1 Interaction in food-webs and predator hypotheses 9
1.2 The Cormorant 11
1.3 P. c. sinensis - foraging behaviour and distribution 13
1.4 Scientific dilemma – how can the effect of predation be measured? 16
1.5 Controversial predator under management and political debate 17
2 Goals and outline of the thesis 21
3 Methods 23
3.1 Diet analyses – sampling and description of diet 23
3.2 Fish community – gillnet fish surveys 25
3.3 Direct and indirect predatory effects on fishery catch 25
3.4 Effect of predation on fish populations 26
4 General Results and Discussion 29
4.1 Cormorant interactions with wild fish populations 29
4.2 Cormorant interaction with fish of human interest 33
4.3 A Global Perspective on conflicts - in short 34
4.4 Meta-analysis 36
4.5 Managing animals or human conflicts - personal reflections 37
4.6 Conclusions and main results 38
4.7 Future perspectives 39
5 Sammanfattning 41
References 45
Thanks and Acknowledgements 54
7
List of Publications
This thesis is based on the work contained in the following papers, referred to
by Roman numerals in the text:
I Boström, M.K., Lunneryd, S-G., Hanssen, H., Karlsson, L. and Ragnarsson,
B. (2012). Diet of the great cormorant (Phalacrocorax carbo sinensis) at two
areas in the Bay Lövstabukten, South Bothnian Sea, Sweden, based on
otolith size-correction factors. Ornis Fennica 89, 157-169.
II Boström, M.K., Östman, Ö., Bergenius, M.A.J. and Lunneryd, S.G. (2012)
Cormorant diet in relation to temporal changes in fish communities. ICES
Journal of Marine Sciences 69(2), 175-183.
III Östman, Ö., Boström, M.K., Bergström, U., Andersson, J. and Lunneryd, S-
G. (2013) Estimating competition between wildlife and humans-a case of
cormorants and coastal fisheries in the Baltic Sea. PLoS ONE 8(12), 1-8.
(DOI: 10.1371/journal.pone.0083763).
IV Ovegård, M.K., Öhman, K. and Mikkelsen J. S., and Jepsen, N. (2017)
Cormorant predation overlaps with fish communities and commercial-
fishery interest in a Swedish lake. Marine and Freshwater Research (DOI:
10.1071/MF16227).
V Ovegård, M.K., Jepsen, N., Bergenius, M., and Petersson E. (2017) A
review and meta-analysis of the effects of cormorant predation on fish
populations. Manuscript.
Publications I-IV are reproduced with the permission of the publishers.
8
The contribution of M. Ovegård to the papers included in this thesis was as
follows:
I Participated in planning and designing the project that was initiated by
Sven-Gunnar Lunneryd. Conducted field work with personnel at
Älvkarleby field station and Hanna Ståhlberg, collected and identified
pellet material, conducted the statistical analyses, primary author of the
manuscript and handled the review process.
II Initiated, planned and designed the study with Sven-Gunnar Lunneryd,
analysed most diet material, conducted the statistical analyses with support
of Örjan Östman, primary author of the manuscript and review process.
III Planned and designed the field work with Sven-Gunnar Lunneryd,
identified most diet material, wrote the manuscript as secondary author,
Örjan Östman conducted the analyses and handled the review process
IV Initiated, planned and designed the study as project leader, participated in
field work together with Kristin Öhman, Niels Jepsen, Jørgen Mikkelsen
and Anders Nilsson (local fisherman), identified diet material with Kristin
Öhman, conducted statistical analyses, primary author of the manuscript
and handled the review process.
V Initiated the study with Erik Petersson, planned and designed the study
with co-authors, managed the literature review and conducted the analyses
with the support of Erik Petersson. Primary author of the manuscript.
9
1 Introduction
The cormorant, Phalacrocorax spp., can on a global scale be considered a
model genus for human-wildlife conflict (Klenke et al., 2013; Wild, 2012;
Doucette et al., 2011; Vetemaa, 1999). There is a wide spread conflict between
humans where concerns for the conservation of a bird species stand against
protection of harvestable natural fish resources. The core of the conflict
regarding cormorants relates to its ability to quickly colonize new areas and
exploit new food resources. In many cases they forage in large numbers and
will consequently, in a short time, consume large numbers of fish. Cormorants
are present in salt-, fresh- and brackish waters on all continents (Sibley, 2001).
Different areas of the world have similar conflicts regarding cormorants,
although the particular species of cormorant in question differ (Doucette et al.,
2011; Wires et al., 2003).
The great cormorant (Phalacrocorax carbo) is one of the most studied and
well-known conflict species, along with the double-crested cormorant
(Phalacrocorax auritus) in North America. Both species have had a similar
steep increase in numbers (Seefelt, 2012), almost during the same period of
time. They are also considered to have similar feeding behaviour, and thus
similar potential effects on fish communities. Despite a persistent belief that
these species affect fish populations negative, there is relatively little known
about their interactions in ecosystems and food webs (Doucette et al., 2011).
This thesis aims to contribute to that knowledge using the great cormorant as
the study species.
1.1 Interaction in food-webs and predator hypotheses
Species interactions create food webs where predation plays a central role
for the energy flow through the food chain, from primary producers to top
predators (Smith & Smith, 2003). Capture fisheries have historically depleted
10
species in a top-down manner, fishing down the food web by targeting the
larger fish (Pauly et al., 1998; Trites et al., 1997). A top predator, in the top of
the food chain, may (and will in most cases) in a similar manner supress the
abundance of a prey, and thus releasing the next trophic level from predation,
which then can increase in numbers. This is called a top-down trophic cascade,
as it results in abundance changes down the food web. (Bottom-up cascades,
on the other hand, occurs when a primary producer is removed (or boosted)
and affects the whole food web from primary, up to top predators (Hunter &
Price, 1992)). For example, in the Baltic Sea it has been suggested that seal
predation on fish, together with human interactions, is an important component
in driving the system by top-down control (Österblom et al., 2007). After
extensive seal hunting, resulting in population reduction, followed a shift from
seal to cod domination. Human overfishing of cod later resulted in a shift
towards clupeid domination in the Baltic Sea, which was the state it was in
when cormorants increased in number. The cormorant is a generalist predator,
able to predate on fish in various sizes and therefore their interaction act at
several trophic levels. Cormorants forage mainly in shallow waters, close to the
coast, compared to seals, which are also foraging in off shore systems
(Boström et al., 2016). Form an ecological management perspective, it is
important to not only consider cormorant predation, but in association with
other piscivorous predators (such as seals) and fishery catch, especially as there
is a conflict around competition with fisheries.
Exactly how predation from one species affects individuals and populations
of other species within an ecosystem is complicated as it depends on the
community structure and other species interactions. Within communities there
are interactions in the form of competition. The level of competition can be
regulated by predators higher in the food-web because individuals or species
benefit if a competitive species is reduced by a predator. Alternatively, removal
of one competitor species may open up for increased competition between
other species. The competitive interaction is based on a limitation of resources,
which can be food supplies or habitats. There are both intraspecific and
interspecific competitions, in which individuals compete within the same
species respectively between species (Persson, 1983). Predators may alter such
competitions and thus alter population structures.
By predating on a limited prey size span predators can alter the size
structure of a prey population (Begon et al., 2002). Predators may have
different effects on a population depending on in which life stage predation is
concentrated. Predation on predominantly young individuals may have
relatively little effect on the population compared to predation on reproductive
individuals (Boyd et al., 2006).
11
Prey fish answer to predators by changing its behaviour, and on a
population level such behavioural change may alter distribution and abundance
(Skov et al., 2013). Spatial heterogeneity in the environment and defence
ability are important factors in population survival (Gilinsky, 1984). On an
evolutionary scale prey may even change to antipredator patterns in their
behaviour and morphology.
According to the predator hypothesis on a generalist and opportunistic
predator, which prey on the most common and easily caught species,
consumption rates should accelerate relative to prey density as the predator
learn to recognise the more abundant prey item. At some point prey
consumption reaches its maximum and the prey number decreases. If other
prey is more abundant the predator should change its target prey. (For example,
cormorants change target prey when a prey becomes scarce, so their predation
is not likely to bring a population down to zero). In those cases consumption
rate may be driven by variability in recruitment and may explain prey
switching behaviour as fish community changes (Schultz et al., 2013). This
could lead to an eventual suppression of recruitment to older age classes,
particularly those recruiting to fishery sizes. The predator thus regulates its
own prey densities. Changes in predator diet may, however, also be caused by
natural fluctuations in fish stocks, fish removal by other predators or by
environmental changes which may affect fish assemblages.
1.2 The Cormorant
Cormorants belong to the pelican order, Pelecaniformis, and the family
Phalacrocoracidae, traditionally within the single genus Phalacrocorax,
(though there are discussions about dividing them further into three groups;
flightless cormorants, long-tailed cormorants and other cormorants (Sibley,
2001)). Within the genus there are approximately 37 different species with a
disputed number of subspecies. The great cormorant (Phalacrocorax carbo) is
the most widespread of all cormorants and can be found on all continents
except South America and Antarctica proper (Johnsgard, 1993). In Sweden,
there are two species of cormorant, the great cormorant (Phalacrocorax carbo,
Linnaeus 1758) and the less common European shag (Phalacrocorax
aristotilis, Linnaeus 1761). The two subspecies of the great cormorant present
in Europe are P. c. sinensis and P. c. carbo and about 90 % of the population is
represented by P. c. sinensis (Klimaszyk & Rzymski, 2016).
The great cormorant were hunted to the brink of extinction in Europe during
the 19th century, but have since the EU bird directive in 1980 benefited from
protection from human persecution (Steffens, 2010) and highly productive,
12
eutrophic, waters. During the last decades there has been a large increase of the
population of P.c. sinensis across Europe (Steffens, 2010; Bregnballe et al.,
2003; Van Eerden & Gregersen, 1995). The population within the EU has
increased from 3 500 pairs in 1960 to 220 000 pairs in 2012 (CorMan;
http://ec.europa.eu/environment/nature/cormorants/home_en.htm, 2017-02-28).
The great cormorant is, like most cormorant species, an opportunistic
piscivore, (Johnsgard, 1993) able to exploit most waters, and therefore the
increases in numbers have led to conflicts with fisheries (Vetemaa et al., 2010;
Carss, 2003; Leopold et al., 1998; Dieperink, 1995). Concern about the
European population of P. c. sinensis has increased markedly in the last
decennium due to their increase in number (Keller & Visser, 1999). From a
bird conservation point of view the development is considered highly
successful and cormorants are now colonising their original habitats, and are
also possibly taking new ground (Bregnballe et al., 2011). This success is on
the other hand seen as a major problem for certain capture fisheries because the
cormorant is perceived as a competitor for fish resources. Many fishermen and
fish farmers claim that cormorants cause them economic loss. They claim that
cormorants deplete fish populations, cause damage (Engström, 1998) (partly by
drowning in fishing gear (Žydelis et al., 2009; Bregnballe & Frederiksen,
2006)), reduce fisheries catch (Andersen et al., 2007) and influence the local
flora and fauna on islands they occupy (Kolb, 2010). They are also claimed to
cause economic losses for fish farms, put and take lakes and pond aquaculture
(Klenke et al., 2013; Lekuona, 2002). There are several cases, where predation
from cormorants has been thought to threaten the conservation of vulnerable
fish stocks and cause ecosystem derogation in freshwater (Skov et al., 2014;
Ryan et al., 2013; Steffens, 2011; Jepsen et al., 2010; Ebner et al., 2007).
During the first half of the 20th century the subspecies P. c. sinensis
occurred only occasionally in Sweden. They established a colony in 1948 on an
island in Kalmarsund, near the island Öland, and spread from there. Already in
the 1980´s, when the numbers had increased to around 1 000 nesting pairs, the
potential effect of cormorant predation was discussed at the local county, and
measures to reduce the number were implemented (Lindell & Jansson, 1993).
However, the population rapidly increased. The fast population growth was
due to high survival and breeding success. Eutrophic waters, with high primary
production and large amount of small fish, are believed to have offered good
food resources (De Nie, 1995; Van Eerden & Gregersen, 1995). Protection
areas were implemented in association with cormorant colonies. A decrease in
the use of pesticides may also have contributed to a higher reproduction rate
(Bregnballe et al., 2011). The national counts in 2006 and 2012 indicate that
the Swedish population is no longer increasing. The population reached its
13
maximum at 42 000 nesting pairs in 2006 and around 40 000 pairs in 2012.
Reasons for levelling off in numbers are most probably the limitation of food
resources (Engström, 2001). Also the growing population of White-tailed eagle
(Haliaeetus albicilla) that are predating on cormorants may keep numbers
down in some areas (HELCOM, 2015; Sevastik, 2002). A reduction in
breeding success may also be due to kleptoparasitism, that is, when other
species steal prey from predators. Seagulls have learned to attack cormorants
and steal fish when they surface to ingest prey (Klenke et al., 2013), which
impacts the net energetic gain for individuals and its nestlings. Seagulls have
also learned to steal eggs from cormorants, when the adults leave the nest in
response to disturbance (personal observation). Another reason for the reduced
breeding success in some areas is human interference to reduce the number of
cormorants. These are both legal and illegal disturbances. In extreme illegal
cases cormorant nests are destroyed and young chicks killed.
1.3 P. c. sinensis - foraging behaviour and distribution
Cormorants are foot propelled divers that usually dive and forage in waters
shallower than 10 meters, but they are able to dive more than 30 meters
(Nelson, 2005). They are commonly submerged for around 20 seconds to a
minute. They feed almost exclusively on fish. Crustaceans and Polychaetes
(Niels Jepsen and personal observations and Lunneryd and Alexandersson
(2005), have however, been observed in the diet. Targeted fish sizes range
from a few cm to a maximum size being limited by what can fit in the
cormorant beak, thus fish of one or two kilo are regularly eaten. This means
that elongated fish can be consumed in larger sizes than high bodied fish or flat
fish. Cormorants have been observed to attempt to eat too large fish, resulting
in suffocation and mortal outcome (Fig. 1). This may be an effect of limiting
food resources, making cormorants prone to eat what is available.
Cormorants undertake feeding bouts at least two to three times a day. They
forage solitary or in large groups and may follow conspecifics to locate
lucrative feeding areas (Nelson, 2005). It is thought that fishing in larger
groups is an adaptation to murky waters with less visibility (Van Eerden &
Voslamber, 1995). The group work effectively together by moving in a row
and taking turns in diving to stir up the fish from the bottom so they can be
seen and caught. However, exactly how cormorants locate food, visually,
hearing or sensory, is not entirely known (Grémillet et al., 2012). They are
commonly surfacing to swallow prey but they may also swallow smaller prey
under the water. During the breeding season cormorants have been shown to
14
change their target prey. In the Gulf of Finland cormorants were observed to
feed small chicks with smaller and more easily digested fish, such as eelpout
(Zoarces viviparus), compared to more scaly roach (Rutilus rutilus) and perch
(Perca fluviatilis) during the later phase of breeding (Lehikoinen, 2005). It has
also been observed that foraging occurs closer to the colony when they rear
small chicks and that they can forage at larger distance before and after. It is
not uncommon that they forage 15 to 20 kilometres from the colony (Nelson,
2005), but a distance up to 40-60 kilometres has been documented (Van Eerden
et al., 2012). The theory of Ashmole´s halo may apply to cormorants (Andrews
et al., 2012), where the foraging distance from the colony increases due to a
decrease in prey availability near the colony through the breeding season (Birt
et al., 1987).
Figure 1. A mortal outcome from a struggle between a cormorant and an eel. Usually the fish get
stuck in the throat of the cormorant, but in this case the eel strangled the cormorant. Photo:
Kristina Lager.
Cormorants are commonly said to consume around 500 grams of fish per
day. The amount of food varies however, depending on gender, species,
temperature and breeding state requirements (Carss, 1997). Cormorants
overwintering in colder areas with cooler waters spend more energy and
require more food. Details of energy demand and food requirements can be
found in Carss et al. (2012), Ridgway (2010), Keller and Visser (1999), Carss
15
(1997), Feltham and Davies (1997), Grémillet et al. (1996), Gremillet et al.
(1995), and Platteeuw and Van Eerden (1995), and will not be covered in this
thesis.
The subspecies P.c. sinensis range from Europe and east/south east through
central Asia to Serbia, China and India (Nelson, 2005). They breed in colonies,
sometimes several hundred pairs, in trees, bushes or on the ground near
shallow marine or fresh water systems. In northern Europe breeding occurs
between April and August. European cormorants tend to have a south/south-
western winter migration. Birds tagged in Sweden have been found as far south
as Africa (Bird Ringing Centre, Fig. 2). The distribution of the great cormorant
during winter has been correlated with a mean winter temperature warmer than
-5.5ºC (Van Eerden et al., 2011). As cormorants move long distances the
conflict of cormorant predatory effect can be argued to be a European rather
than a local concern. And this has led to the EU to fund several pan-EU
cormorant projects; Redcafe, Intercafe and CorMan.
Figure 2. Recoveries of tags from cormorants tagged in Sweden, up until 2016 (n=3711). Source:
Bird Ringing Centre, Swedish Museum of Natural History.
16
1.4 Scientific dilemma – how can the effect of predation be
measured?
Though cormorant diet has been studied for decades there is insufficient
knowledge about cormorant food habits, and in particular how they affect wild
fish populations (Russell et al., 2003). Conclusions from research results are
not consistent. Some studies conclude that cormorants can have negative effect
on fish stocks (e.g. Čech & Vejřík, 2011; Fielder, 2010; Vetemaa et al., 2010;
Fielder, 2008; Rudstam et al., 2004; Leopold et al., 1998; Kirby et al., 1996b;
Barret et al., 1990), while others conclude less or no effect of cormorant
predation (e.g. Dalton et al., 2009; Diana et al., 2006; Engström, 2001; Suter,
1995). The inconsistent results between studies partly relate to the ability of
cormorants to make use of most fish communities, and that fish community
structure differ spatially and temporally. There are many factors affecting fish
communities, beside predation (Heikinheimo et al., 2016). Both abiotic and
biotic processes cause natural fluctuations in fish stocks or environmental
change, which in turn may influence stocks. The significance of cormorant
predation on natural fish populations is difficult to estimate because the true
fish population size and structure is often unknown, or the knowledge
incomplete. Fish surveys are useful in identifying changes in fish communities
over time, but as no fishing method captures all fish and sizes representatively
they are limited in that they cannot be used to identify exactly how the
community is structured. There are too many variables to measure and account
for, when attempting to identify effects of predation.
Though the highly various and complex ecological systems are one reason
for the inconsistency between studies on the effects of cormorant predation, the
main reason probably relates to differences in perceptions of what an effect is.
How “large” should a predation effect be to be considered significant, and how
can this be measured? A large quantity or even proportion of predated fish does
not necessarily mean that cormorants affect a fish population, in terms of
damage of human resources, as compensatory mechanisms may set in.
There are several methods available and used to quantify cormorant
predation (see section 3.1). The most direct way to quantify predation on a
known fish stock is to tag fish and recover tags in cormorant residues (Skov et
al., 2014; Jepsen et al., 2010). Even though these methods results in the
knowledge of how large a proportion of a given fish population the cormorants
consume, the question of effects on the fish not eaten by cormorants remain.
(Note that there is a possibility to model cormorant predation and abundance in
relation to fish population parameters). A combination of tagging studies,
preferably by telemetry, and good survey data on the fish population can
17
provide very precise estimates of effects, but naturally this works best in small,
restricted waterbodies like lakes or streams.
From a strict scientific point of view the significance of effects are best
studied by using carefully designed experiments, with treatments and controls.
As ecological systems are highly variable, it is important to conduct studies
with replication in several waters and, preferably, to study fish communities
before, during and after cormorant predation. But in most cases it is practically
impossible to predict areas where cormorants will establish in the future. What
can be done is to relate fish community changes to cormorant abundance, or
manipulate the number of predating cormorants, either by using fish refuges or,
more drastically, move cormorants from a fish community by e.g. hazing or
shooting. The latter options infer cormorant population disturbance, in one way
or another, which calls for legal consent. With cormorants being a source for a
human-wildlife conflict such research project first needs to be considered on
the political agenda. In Denmark, the negative effect of cormorants is
documented and treated as a fact in the national management plan. A study is
being conducted at present (2016-2018), where salmon smolt survival is related
to lowered levels of cormorant predation. Radio-, PIT- and acoustic telemetry
is used to monitor the survival of smolt and relate this to efforts to reduce
predation, by shooting cormorants in the river and the estuary as well as
destroying colonies.
1.5 Controversial predator under management and political
debate
Managers and stakeholders are irresolute in decision processes around
cormorant management, partly because of the difficulty in collecting scientific
data on true effects of cormorant predation on fish population, communities
and fisheries, but mainly because of the human-wildlife conflict and a
difficulty in interpreting the legal frames.
Human-wildlife conflicts are in reality not conflicts between humans and
wildlife, but conflicts between humans around a wildlife species issue
(Dickman, 2010; Madden, 2004). The source of the conflict is often the
consumption of resources by wildlife that is of value for humans (Chamberlain
et al., 2013; Madden, 2004). The social aspect may be a more important driver
in such conflicts than the actual effect on prey of the wildlife (Dickman, 2010).
Effects may be perceived and not even real, for such conflicts to arise (Klenke
et al., 2013). Deeply rooted attitudes and strong opinions are difficult to alter,
even with scientific proof. When cormorants started to increase in number in
Europe, they were a welcomed and exotic sight for many. As they increased
18
further people relying on fish catch as an income started to become concerned.
Fishery representatives in Europe consider cormorant predation harmful to
their business and believe there is a need for a reduction of cormorant
predation on a European scale (Marzano et al., 2013). This viewpoint is shared
by EIFAAC (European Inland Fisheries and Aquaculture Advisory Council)
and EAA (European Anglers Alliance).
The subspecies P. c sinensis is not assessed for the IUCN Red List but is
included in the species P. carbo, which is now listed as LC (Least Concern),
due to its large range and extremely large population size
(www.iucnredlist.org, 2016-12-19). In Europe cormorants are protected under
international laws and treaties such as the EEC Directive 2009/147/EC
(codified version of 79/409/EEC) on the Conservation of Wild Birds 1979, the
Bern Convention on the Conservation of European Wildlife and Natural
Habitats 1979, and the Bonn Convention on the Conservation of Migratory
Species of Wild Animals 1979 (CMS). Originally the subspecies P. c. sinensis
was listed under Annex 1 in the directive of Conservation of Wild Birds, which
includes bird species on which special conservation measures, by protecting
their habitats, are needed (Article 4). In 1997 it was removed from that list
(commission directive 97/49/EC) because P. s. sinensis had reached favourable
conservation status. It means that the level of protection is no more than for
most other bird species. Member states can decide on measures to manage
cormorants under conditions stated in Article 9. Article 9 can be used if it is in
the interest of public health and safety, air safety, to prevent serious damage to
crops, livestock, forests, fisheries and water, and for the protection of flora and
fauna (Article 9 in the Directive 2009/147/EC on the conservation of wild
birds).
Though the directive of Conservation of Wild Birds is rather clear in that it
now opens up for regulating cormorant predation, the level of evidence is not
stated. There is an attempt to describe the directive in relation to cormorants in
the EU derogation report (Great cormorant, Applying derogations under
Article 9 of the Birds Directive 2009/147/EC). It is up to the member states to
decide on the level of evidence of cormorant predation effects, before
regulation measures can be implemented. Most member states have
management plans on national level and in some instances also local level.
Cormorant damage on fisheries is easiest to measure and report by
estimating wounded fish in fishing gear. It is more difficult to measure and
prove if cormorants induce changes in fish communities to the degree that they
cause damage to fisheries catch and income, a concern that for some fishermen
is considered more worrying than damage in fishing gear (Strömberg et al.,
2012). This damage may be of even higher importance than damage of fish
19
catch. The same challenge is found in seal management in Sweden, where the
fishery gets compensated for seal damaged catch, but the degree of damage on
fish stocks is not considered. However, there is relatively new evidence, based
on models, showing an importance of fish predation on fish populations. Seal
predation can prevent the recovery of overexploited fish stocks (Cook et al.,
2015; Swain & Benoit, 2015). In Denmark, where the nesting cormorant
population used to be the highest in Europe, it is stated in their national
management plan (2016) that cormorant predation can prevent recovery of
coastal fish populations and even drive populations of freshwater fish to an
unsustainable level.
20
21
2 Goals and outline of the thesis
The objective of this thesis was to achieve further understanding of cormorant
predation and predatory effects on fish population and community structures.
The thesis work had two main focuses:
1. Investigate the diet of cormorants on the Swedish Baltic Sea coast
(papers I and II).
- Examine spatial and temporal differences in diet.
2. Investigate how cormorant predation effect fish populations and
fisheries. (papers III, IV and V)
- Explore the competition between cormorants and humans (papers
III and IV)
- Summarize previous research measuring the effects of cormorants
on fish and examine the variations in those effects (paper V).
In the process of my thesis work I encountered several methodological
challenges and difficulties. Diet analysis methodology was discussed in my
licentiate thesis (Boström, 2013). In this thesis I discuss the challenges in
research related to the identification of effect of cormorant predation on fish
populations (see discussion and paper V).
22
23
3 Methods
To complete this thesis, the diet of the great cormorant (Phalacrocorax carbo
sinensis) was examined in four areas, whereof three in the Baltic Sea (I, II, III)
and one freshwater lake (IV). Patterns of change in diet between areas and
periods were analysed (I, II). The results from diet studies could then be used
to estimate the competition between cormorants and coastal fisheries (III). The
direct competition on fish of the same sizes were accounted for, as well as the
indirect competition by cormorant predating on smaller sized fish, resulting in
a decrease in the number of fish recruiting to catchable sizes (for fishery). As
coastal systems are open, and fish move over long distances, it is a challenge to
relate cormorant predation to response in fish populations. Therefore a study
was conducted in a freshwater lake (IV). To quantify predation, fish were
tagged and tags were recovered in colonies and roosting areas. In both the lake
and the coastal areas trends in fish community structure were examined and
related to cormorant predation (II, III, IV). For this, fish survey data (II, III),
collected by the Swedish Board of Fisheries
1
, were used, and an own survey
was conducted (IV). Finally, cormorant predatory effects on fish and fisheries
were evaluated, based on published literature. This was achieved by a
structured literature search and meta-analysis (V).
3.1 Diet analyses – sampling and description of diet
Bird diet composition can be determined with several methods; observational
studies, tagging prey, visually examining food remains in stomachs, pellets,
regurgitates or faeces, and biochemical methods such as analysis of DNA,
1
. Before 1 July 2011 The Swedish Board of Fisheries was responsible for these fish surveys,
but after that date the Department of Aquatic Resources at the Swedish University of Agricultural
Science has this responsibility. The section of the board dealing with research and monitoring
were simply incorporated to the university as a new department.
24
stable isotopes and fatty acids (Barrett et al., 2007). The type of methods to use
depends on the hypothesis in question. If the size of prey is important, visual
analysis of food remains or tagging prey is a necessity. Biochemical methods
have the advantage that a large sample can be analysed with little effort,
compared to visual methods. However, these methods have their limitations.
With DNA you can get semi-quantitative proportions of prey, but it is not
possible to measure prey size, and the application to quantify prey is in its
developmental phase (e.g. Huang et al. (2016). With stable isotopes you can
identify which trophic level(s) and geographical area a predator feed in. Fatty
acids can also give a semi-quantitative estimate of prey proportions, but with
the advantage that you can investigate diet over longer time spans (time span
depends on which structure you sample). If your objective is a deeper
understanding of predator interaction with prey and food webs, it is advisable
to complement biochemical methods with visual analyses. Though not studied
in this thesis, with visual analysis it is possible to examine the life stage of
prey.
In this thesis diet was investigated through visual analysis of pellets (paper
I), regurgitated fish (paper I) and from stomach content from shot birds (papers
II, III, IV) (For study areas, see map in Fig. 3). The methods, limitations,
application of size correction factors on otoliths, regression use on otolith size
to attain fish sizes and methodological differences in relation to questions of
ecosystem impacts and effects on fish populations, are described in Boström
(2013) and will not be covered in detail in this thesis.
Diet composition can be described as frequency of occurrence, numerical or
biomass contribution. Either the total contribution of prey for all samples
examined or the contribution of prey can be weighted per sample. The later
method was used in papers I, II and IV. It has the advantage that the
contribution of prey in each sample is considered to be equally large, with each
sample containing 100 % prey. If one diet sample contains only a little amount
of prey it is equally weighted as a diet sample with large amount. For example,
if one sample contains 10 prey items of which 1 is species A and another
sample contain 100 prey items of which 10 items are species A, both samples
contain 10 % of the species within each sample; and thus species A has the
same weight in both samples though it was found in less amount in the first
sample. The method accounts for a potentially skewed distribution in diet
composition and also allows estimating uncertainties due to random processes
by bootstrapping (Haddon, 2001).
With complex predator and prey dynamics it is of importance to take into
account, that short term studies only give a short term picture of the diet and
effect of a predator. As cormorants are opportunistic generalists they can adapt
25
to variable sources of food. Fish can be dynamic in behaviour and movement
during its life time and move long distance to reproduce or feed. Migration
behaviour may also be a response of predator presence (Skov et al., 2013;
Kortan & Adámek, 2011). In paper I, II and IV the diet of cormorants were
investigated during the entire breeding season. In paper III sample collection
was spread out over the entire year to identify the predation in the non-
breeding season. Spatial and temporal differences in the diet were examined
with one-way non-parametric permutational multivariate analyses of variance
Permanova by using Bray-Curtis similarity indices on relative biomass or
number of prey. Variations were examined with constrained canonical analysis
of principal coordinates (CAP) biplots using the Bray-Curtis similarity index.
Differences between breeding phases (Paper I and II), gender and age (Paper
II) were examined.
3.2 Fish community – gillnet fish surveys
National gillnet fish surveys were used to examine the degree of change in fish
communities between years, in relation to cormorant abundance and diet
(Paper II and IV). Fish surveys were conducted by the Swedish Board of
Fisheries as part of the national and regional monitoring programme. The
survey along the coast is conducted annually (Paper II and III), while in Lake
Roxen (paper IV) the data was limited to only a few years. Therefore an
additional survey in Lake Roxen was conducted in 2013. Procedures in the
field are explained for coastal survey in Söderberg et al. (2004) and Thoresson
(1996), and for lake survey in (Kinnerbäck, 2001) and Appelberg et al. (1995).
It is important to note that gillnet survey methodology relies on the active
movement of fish into nets and therefore sedentary species are poorly
represented. Also smaller sized fish and elongated fish, like eel and eelpout, are
not caught representatively.
Gillnet catches were examined by using catch per unit effort (numbers or
biomass) with principal coordinate analysis (PCO) (Paper II) and Student´s t-
test (Paper IV). Differences in fish sizes, among surveys, were investigated
using one-way ANOVA (paper IV).
3.3 Direct and indirect predatory effects on fishery catch
Cormorants may prey on fish of the same species and sizes as those targeted by
the fishery. They may also add to the natural mortality of fish in earlier life
stages, before recruiting to commercial size (as seen for perch Gagliardi et al.
(2015)). These kinds of direct and indirect competitions were investigated in
26
paper III, using length distribution of fish in cormorant diet and commercial
fishery catch, together with total cormorant predation and total fishery catch. A
model to measure competition between human catch and cormorant predation
was constructed, based on consumption levels and mortality rates, where both
commercial and recreational fishery were accounted for. Published literature
was used for estimates on the natural mortality, which were included in the
equations. For details of equation modifications see paper III.
However, it is important to note that aquatic systems are more complex and
these estimates do not include all indirect effects of predation on fisheries. For
example, cormorants may injure fish and also force fish to use sub-optimal
feeding strategies (like shown by, amongst others, Skov et al. (2013)), and
cormorant predation may affect piscivorous fish by removing their prey.
3.4 Effect of predation on fish populations
In chapter 3.1 the methods in describing cormorant diet were explained. It is
one thing to measure and estimate predation (in numbers or biomass) and
another thing to estimate the “effect” of predation on wild fish populations,
communities or ecosystems. Effect is here defined as change in fish parameters
e.g. size, number, biomass, survival etc. in relation to cormorant abundance or
presence. It is measurements on the effect on the surviving fish population that
is of importance in effect studies, not “only” measurements of mortality caused
by cormorants, (though survival and mortality are correlated).
Several studies in Denmark (e.g. Jepsen et al. (2010), Koed et al. (2006),
Dieperink et al. (2001), Dieperink (1995)) and North America (e.g. Hawkes et
al. (2013), Sebring et al. (2013), Lovvorn et al. (1999)) have used tags on fish
to estimate predation by cormorants. As mentioned in section 1.4., tag fish and
recover tags in cormorant colonies or roosting areas is considered the most
direct way of measuring predation (Jepsen et al., 2010). Tag studies give
precise estimates on which fish individuals cormorants have eaten, but not
direct information on the effects of the fish population surviving cormorant
predation. However, predation effect, as defined above, can be measured with
tag studies if designed to consider cormorant abundance/predation pressure in
relation to fish parameters of the individuals surviving cormorant predation.
For applications on a wild fish population the available size range of fish must
be covered and tagged respectively, which may be challenging as fishing gear
don’t catch all sizes.
Most research on cormorant diet is descriptive diet studies, which do not
prove or disprove the effect of cormorant predation, in a clear statistical sense.
In paper V a systematic search for published articles on cormorant predation
27
was conducted. From these, articles including a statistical setup, where effect
sizes and direction (positive or negative) of effect could be extracted, was
identified and used in a meta-analysis. A meta-analysis enables to combine
results from different studies as long as they address a similar question. This
means that studies that are variable in; what fish parameter they measured
(individual size, numbers, biomass, size at age etc.), in which habitat type
studies were conducted and on what cormorant and fish species studies
targeted, can be used. An overall quantitative estimate between all studies, the
effect size, can be calculated. Increased sample size provides an increased
statistical power. A meta-analysis also enables the exploration of sources of
variation in effects. The meta-analysis included in this thesis is the first ever
attempted on cormorant predatory effects.
28
29
4 General Results and Discussion
4.1 Cormorant interactions with wild fish populations
The results from this thesis (papers I and II) support earlier findings (e.g.
Lehikoinen et al. (2011), Lehikoinen (2005) and Neuman et al. (1997)) that
diet of cormorants vary both spatially and temporally (Fig. 3). In Lövstabukten
the diet differed between colony islands only 6 km apart (Paper I), which
probably was a result of birds foraging in different areas. The diet changed
more (Paper I) or less (Paper II) during the breeding season, which can be the
result of varying demands during different stages of chick rearing (Lehikoinen,
2005). While rearing small chicks, smaller, more easily digestible fish species
may be preferred. Or, as proposed in paper I, the change in the diet over time
may be due to fish prey availability in relation to fish behaviour and
abundance. For example, the timing of eelpout present in cormorant diet, in
both paper I and II, matched the migration of eelpout into shallower waters.
Changes in diet between years were also identified (papers II, IV). The
clearest change was the large amount of sticklebacks in the diet of cormorants
in the Mönsterås area observed in 2009 (92 % in numbers). A study in the
same area in 1992 found no sticklebacks in the cormorant diet (Lindell, 1997).
Instead perch dominated the diet in 1992 (Table 1). The fish community, based
on net surveys, indicate a change from a dominance of roach and perch in the
mid 1990´s towards dominance by herring and species of cyprinids, other than
roach. However, survey nets used in coastal areas do not catch sticklebacks
representatively, because the smallest mesh sizes, 17 mm, are too large to catch
sticklebacks. But stickleback presence has increased in the coastal area of the
Baltic proper since the early 1990´s (Ljunggren et al., 2010). Perch on the
other hand has decreased (Vetemaa et al., 2010).
30
Figure 3. The three most commonly occurring species in the diet of cormorants in the four study
areas (Paper I-IV). In all areas samples were collected throughout the breeding seasons and during
the time of cormorant presence (in such numbers that sample collections were possible). In paper
III collections were made all year round.
Table 1. The diet of cormorants in the archipelago close to Mönsterås in 1992 (Lindell, 1997) and
2009 (paper II) in numerical percentage. For 2009 estimates included and excluded sticklebacks
to get an idea of the importance of sticklebacks compared to other species. Other fish preys of
importance in 2009 were gobies and flatfish which, with stickleback removed, contributed 23.6
and 7.3%, respectively (modified from paper II).
Species
Sticklebacks
included 1992
Sticklebacks
excluded 2009
Sticklebacks
included 2009
Perch
41
0.2
0
Cyprinids
36
8.7
0.7
Ruffe
6
0.2
0
Eelpout
7
50.8
3.9
Sticklebacks
-
excluded
92.3
Other Species
10
40.1
3.1
31
A coastal trophic cascade (Ljunggren et al., 2010) may have followed a
shift in the offshore system (Casini et al., 2008), (the shift in the offshore
system is described in section 1.1) which may be the reason for the change in
cormorant diet. Cascades may, in turn, be due to overharvesting by humans,
and maybe to some degree also the predation from predators, that during the
same time period increased in numbers (seals (Harding & Härkönen, 1999),
mainly in the offshore system and cormorants (Bregnballe et al., 2003), mainly
in the coastal system).
Long term changes in cormorant diet were also suspected in cormorants
foraging in Lake Roxen (paper IV). Net surveys conducted in 1990, 2001, 2010
and 2013 show a change in the fish community structure, and the fishery catch
decreased during the same time. Cormorants inhabited the lake in 1992 and
have been blamed for these changes. As the eutrophic state of the lake has
improved during the years (paper IV) an increase in the number of larger
piscivore fish predators was expected. But generally, there were fewer but
larger piscivorous individuals in 1990 than in the following surveys. The
number of perch, ruffe and roach decreased from 2001. The only species with a
significant continuous decrease (table 2 paper IV) in both biomass and number
was ruffe, belonging to the Percidae family. In the last survey however, in
2013, perch were larger in individual size, but still caught in smaller number,
i.e. more piscivorous perch (Fig. 4).
Piscivorous predators have been shown to enhance growth and size
structure of prey populations, which is probably a result of decreased density
and intra specific competition (Pierce et al., 2006). For example, Dorr and
Engle (2015) found that harvest loss of catfish (Ictalurus punctatus) due to
cormorant predation occurred, but was to some degree mitigated by
compensatory growth of individual catfish.
Fish in the Percidae family are from other studies known to be vulnerable to
cormorant predation. Cormorants may have been, together with high fishery
catches before cormorants arrived, and the improved eutrophic state, one of the
factors for changes observed in Lake Roxen. In Oneida Lake in New York,
USA, cormorant predation caused an increase in sub-adult mortality and
caused declines in the Percidae species walleye (Sander vitreus) and yellow
perch (Perca flavescens) (Coleman et al., 2016; Rudstam et al., 2004). There
are some contradicting conclusions about cormorants being the reason for
declines in yellow perch in Les Cheneaux Islands region, of northern Lake
Huron discussed in Diana (2010). Conclusions and indifferences are mainly
based on different perceptions of importance of level of predation. Despite this,
an increase in abundance of perch followed cormorant control efforts,
strengthening the fact that cormorants had a negative effect. In Lake Ontario
32
there has been a decrease in fish abundance of the Percidae species smallmouth
bass (Micropterus dolomieui). The high mortality of age 3 to 5 year old fish
has been related to cormorant abundance (Lantry et al., 1999). Gagnon et al.
(2015) found that perch and ruffe were less abundant near cormorant colonies
along the Finish coast in the Baltic Sea. As ruffe in Lake Roxen is not targeted
by the fishery, cormorants are probably the main reason for their continuous
decrease in both number and biomass.
Figure 4. CPUE of perch, ruffe and roach in net surveys conducted in Lake Roxen (Paper IV).
33
Considering that cormorants eat around 500 grams (+/- depending on life
stage and energy demand) of fish per day, are central foragers during breeding,
and breed in large numbers, it is difficult to argue that a significant number of
cormorants don’t have an effect on a local fish community level. Effect are
especially likely in lakes, where fish movement is limited, and foraging in
other lakes mean an extra energy loss for cormorants due to a larger flight
distance. Cormorants in Lake Roxen were observed to have foraged further
than 21 kilometres away, as Baltic fish species were found in diet samples.
There were also cormorants foraging both in Lake Roxen and in the nearby
Lake Glan. This change in foraging areas opens up the question of at which
prey density level cormorants change foraging strategy and target species.
Enstipp et al. (2007) studied prey capture rate in relation to prey density for
double crested cormorants and juvenile rainbow trout (Oncorhynchus mykiss)
and found that the capture rate decreased disproportionately at a level below 2
g×m-3. The study was undertaken in captivity, but if it occurs in a natural
setting that might be the level at which cormorants move to other foraging
areas (or change prey species).
4.2 Cormorant interaction with fish of human interest
The process of a predator eating a prey means an interaction in the form of
removal of an individual from a prey population. Depending on how many
individuals, and at what life stage the prey individuals are removed, the effects
can be more or less important on a population level. Cormorants are likely to
impact fish communities, but the effects do not have to impact fishery catches
negatively. Cormorants are known to prosper in eutrophic waters and it is
argued that eutrophic waters are the very reason for the fast increase in
cormorant number (De Nie, 1995; Van Eerden & Gregersen, 1995). They often
eat fish of smaller sizes than what is targeted by the fishery (Östman et al.,
2012), but are able to feed on as large fish individuals as can fit in their beak
and thus sizes which may overlap with commercial and recreational fishery
catch.
When comparing cormorant predation on fish with commercial and
recreational fishery catches some overlap in fish species and size was identified
(paper III). This can be considered a direct competition on resources.
Cormorants were estimated to consume the equivalent of 44 % in Karlskrona
archipelago and 10 % in Mönsterås archipelago of the commercial and
recreational fishery catch in biomass, of cod, flounder (Platichthys flesus),
herring (Clupea harengus), perch, pike (Esox lucius) and whitefish (Coregonus
lavaretus) combined. The cormorant consumption estimates of harvestable
34
sized fish were 14 % respective 5 % for Karlskrona and Mönsterås. The direct
competition did not result in large decreases in catchable sized individuals, <
10 % for all species. But when accounting for indirect effects, by consuming
smaller individuals, the estimated removal of fish that could have reached
catchable size at least doubled. The results stress the importance to include the
predation (or removal) of fish individuals of smaller sizes in predation
estimates, that has not yet reached maturity and therefore not reproduced
(paper III). The impact on fisheries catches more than four folded compared to
the estimated direct competition for perch, pike and whitefish.
The estimated competition with fisheries differed between areas, mainly as
a result of differences in target species between fisheries. In Karlskrona
archipelago the commercial fishery targeted herring and cod, while in
Mönsterås the targeted species were herring and eel. Recreational fishery in
Karlskrona targeted pike and perch while in Mönsterås they targeted pike and
flounder. In general, results showed that the estimated impact of cormorant
predation was higher for stocks important for recreational fishery (perch and
pike) than for commercial (cod, herring and eel), which seems reasonable as
most commercial species are more offshore species and cormorants forage
closer to the coastline.
Results in paper III show that competition between human catch and
cormorant predation is very dynamic in relation to predation pressure, fisheries
pressure, natural mortality, competition etc. Not accounted for in study III was
the removal of available prey for commercial fish species, and sizes, caused by
cormorants. This is another indirect way, in which cormorant predation may
affect the survival and condition of fish available for the fishery.
4.3 A Global Perspective on conflicts - in short
Cormorant predation has been studied on all continents and for most
cormorant species. The literature search for the meta-analysis covered all
cormorant species, except four species; the red-faced (P. urile), Socotora (P.
nigrogularis), red-legged (P. gaimardi) and the flightless cormorant (P.
harrisi), of which the first three are considered vulnerable or near threatened.
Of the 448 articles found, around 50 % was based on studies in Europe,
mainly England, Italy and Germany and concerned primarily the great
cormorant in fresh water, lakes or ponds. Freshwater aquaculture ponds have
been identified as the main area of conflict by the INTERCAFE project (Seiche
et al., 2012), in particularly with carp (Cyprinus carpio) pond areas in Central
Europe. But the literature search reveal that most studies in Europe are diet
analysis on cormorants related to sea and lake areas, not ponds.
35
Around 30 % of the articles concerned cormorants in North America and
most of them studied the double crested cormorant, which has increased in
number in a similar manner as the great cormorant has in Europe. Most
research seem to originate from the Great Lakes and the Mississippi channel
cat fish (Ictalurus punctatus) aquaculture in the Mississippi delta area, the two
areas where cormorants seem to be causing the most conflict (Wild, 2012).
About 4 % of the articles were studies from South America and most on the
imperial cormorant (P. atriceps) in marine systems and the neotropical
cormorant (P. brasilianus) in freshwater environments. The predation of the
South American cormorant species do not seem to cause major human conflict,
as most studies concern their diet and no identified studies showed predatory
effect on fish.
Most of the literature from Africa (5 %) was based on studies in South
Africa on the cape cormorant (P. capensis) in marine systems and the white
breasted cormorant (P. c. lucidus) in both lakes and sea areas. Studies related
to the cape cormorant mainly concern the welfare of the species in relation to
fisheries depleting food resources. Linn and Campbell (1992) identified no
effect of predation on fisheries as white breasted cormorant foraging areas and
diet did not overlap with fisheries catch in Lake Malawi. Most probably there
is no large cormorant conflict in Africa, or research is lacking.
About 4 % of the articles were based on studies in Asia which included
several species with low number of publications on each. Most studies were
conducted in Japan on the great cormorant subspecies P. c. hanedae. They
have since the 1970´s increased rapidly in numbers and distribution, and
caused conflicts with fishery interests (Takahashi et al., 2006). Most of the
conflict occur in the inland recreational fishery and are about the ayu
(Plecoglossus altivelis), which is one of the most popular recreational and
commercial species (Kameda & Tsuboi, 2013). But there are also positive
associations between human and cormorant. The Japanese and Chinese have,
and are still to some degree, utilized cormorant guano as fertilizer and trained
cormorants to catch fish.
About 3 % of the articles covered studies conducted in Australia, of which
most concerned lakes or rivers and the little pied cormorant (P. melanoleucus).
Negative effects of cormorant predation have been seen on stocked fish and
farm fish, but conclusions from studies in open sea areas vary (Barlow & Bock,
1984).
In Antarctica there are no cormorants and thus no conflict with humans, but
the closely related shags are present in the Antarctic peninsula and about 2 %
of the articles found concerned these, mainly the blue-eyed shag (P. atriceps)
and the Antarctic shag (P. a. bransfieldensis). Most studies described the diet
36
of cormorants and one related fish abundance to declining number of birds
(Casaux & Barrera-Oro, 2016).
Though cormorants are widespread in distribution and research on
cormorant diet has been carried out on all continents and most cormorant
species, the conflict is, at least today, limited to a few cormorant species. Most
studied areas concern smaller sized systems, such as ponds, lakes and rivers.
4.4 Meta-analysis
As discussed in chapter 1.4., the way to answer if cormorants have an effect
on fish or fishery is to relate fish population change to cormorant abundance.
The meta-analysis of cormorant predation effect revealed that, in modern
times, since the cormorant started to increase in numbers, their food habits
have been extensively studied. The underlying reason for studying cormorant
diet has in most cases been to get a picture of how their diets overlap with
human catch. Research has mainly focused on quantifying predation, but
quantities do not necessarily provide information on effect. Studies on diet
mainly present percentage of fish, either by number, biomass or frequency of
occurrence. Diet composition may be compared to fishery catch, but is seldom
compared to known fish populations, (except in tagging studies), as there is a
lack of cormorant diet studies in relation to independent fish monitoring.
Studies where effect sizes (Koricheva et al., 2013) could be extracted were
those which studied fish parameters in relation to cormorant presence or
abundance. In some cases cormorant abundance was due to human induced
limitations of number of foraging birds by the use of refuges, hazing or
shooting. If the response was more or larger fish in relation to cormorant
abundance the effect was considered positive. If less and smaller fish was a
result of more cormorants the effect was considered negative.
Only 22 articles were identified where effect size could be extracted and the
combined effect of those was negative -0.3103, 95 % C.I. -0.4260 to -0.1952).
Thus, cormorant predation in general has a negative effect on fish and
decreasing predation has a positive effect on a prey population. There was no
significant difference in effect size between, cormorant species, study type,
effect type or habitat/foraging area. But there was a significant difference in
effect sizes between fish species. The most vulnerable species was perch,
walleye and a combined effect for species in the Cyprinidae family. This
further supports that species in the Percidae family are the most vulnerable to
cormorant predation (as discussed in chapter 4.1.).
Though the meta-analysis covered cormorant predation on a global scale the
identified studies only included great cormorants (P. c. carbo and P. c.
37
sinensis) and double crested cormorants (P. c. auritus). This, per se, is an
indication that these two species are the source for most human-cormorant
conflicts. It also mainly covers small enclosed systems, such as farms, dams,
rivers and lakes where experimental manipulation with test and controls are
relatively easy to apply. Such habitats often lack suitable refuges for fish and
may thus be more vulnerable to cormorant predation (Gagliardi et al., 2015)
than other systems. There is still a lack of evidence for cormorants damaging
wild fish populations and fisheries in open aquatic systems, because
appropriate experiments have not been conducted to demonstrate cause and
effect (Hustler, 1995).
4.5 Managing animals or human conflicts - personal reflections
There are many feelings and personal opinions around cormorant
management, especially from persons whose livelihood or recreation depend
on fish resources. During my work with cormorants I have encountered people
with views all from “exterminate all cormorants”, “cormorants are natural
predators that are back in our environment and should be left alone”, to “what
is a cormorant”. Well, working with such a conflict species is, and has been, a
challenge.
From an ecologist point of view I believe we should aim for sustainable
populations and manage species from an ecosystem perspective (ecosystem
based management). Increasing the commercial or recreational fishery catch
alone is not incitement enough to deplete populations of cormorants. To
maintain and protect a small scale local fishery, an occupation traditionally
handed down in generations, may be a reason to mitigate cormorant predation
(not exterminate cormorants). Or the economic and social benefits from
recreational fishing may be another reason to discuss mitigation measures. It is
essential to consider top predator consumption when formulating advice for
fishery management (Cook et al., 2015), as well as general wildlife
management. The overall objective should be sustainable fishery and viable
populations of both fish populations and all kinds of piscivorus predators.
However, there is a sociological concern in cormorant management that
cannot be ignored. Management implementation in the form of reducing
cormorant predation can reduce the animosity towards cormorants and might
be a method to reduce unethical illegal actions (such as killing chicks). The
great cormorant has the potential of fast reproduction, if conditions are right
and if the population not yet has reached the point of food resources limiting
reproduction. This theoretically means that if cormorants decrease in number
from a food limited state, they will increase their reproduction (as each
38
cormorant gets more available food). Controlling populations in some areas
will not affect the population as a whole.
A reasonable strategy would be to identify where, when and with which
species conflict occur and implement predation limitation in vulnerable areas.
In some circumstances sacrificing fish to cormorants in some areas can be
beneficial to protect fish in vulnerable areas (Kirby et al., 1996a). Predation
limitation in an area can be achieved by modifying cormorant behaviour,
instead of killing, e.g. by scaring them from foraging in vulnerable areas.
At all times ethical considerations should be taken into account. Illegal
actions, such as destroying nests with young and killing chicks should be
publically unacceptable. Not only is it ethically questionable, but it impedes
cormorant research and makes it problematic to evaluate effect of both
cormorant predation and implemented limitations of cormorant predation.
There is a need to “manage” the human view of cormorants and turn the
negative picture around and, by all stake holders, start regard cormorants as a
valued and respected species in our nature.
4.6 Conclusions and main results
From the results in this thesis it can be concluded that cormorant predation
on fish has a negative effect on fish populations and fishery catch, (both direct
and indirect). Successful management actions to reduce cormorant predation
have positive effect on fish populations. These effects vary between study area
and fish species, as cormorant diet and fish community structure vary.
In the meta-analysis in paper V it was identified that cormorants generally
have negative effects on fish populations and that management actions to
reduce predation are very probable to have positive effect on fish populations.
Paper V, together with results from paper IV, show that fish in the Percidae
family are the most vulnerable to cormorant predation. In paper III it was
shown that the cormorant can compete with fishery. Smaller sized fish, which
have not yet recruited to catchable sizes in fishery, are more important in terms
of competition with fishery, than the predation of the same sizes the fishery
catch. There are also strong indications from results in paper IV and V that
cormorant predation can restructure the size distribution of a fish population by
predating on a limited size span. This can affect recruitment to larger sizes and
reproduction.
Studies demonstrate variations in diet (paper I, II, IV) and effect (III, V),
due to differences in fish community structure and target species in fishery.
39
4.7 Future perspectives
Though there is an extensive number of research articles concerning
cormorant predation there is a need of further research. A clearer picture of the
interaction of cormorants in ecosystems, their function in food webs and effect
in fishery catch, especially in open aquatic systems is needed. Research should
focus on the effect of cormorant predation and test hypothesis with
experimental set ups, instead of conducting elaborate, extensive and descriptive
studies. The reason for this is that only using percentages of predation per
species, or on a fish population, may not be considered to be enough proof of
an effect. For example, though a tagging study manages to identify 60 %
mortality of a fish species due to cormorant predation, it may still be
argumentations about what the effects are on the fish not eaten by cormorants
(unless the study is taken further). In conservation biology today we urgently
need effective mitigation strategies in order to resolve human conflicts
(Dickman, 2010). Increased knowledge and awareness are important tools in
the process. The meta-analysis in this study was conducted to accommodate
the requests from stake holders to investigate predation effect with hypothesis
testing.
Another way to mitigate the conflict, and increase knowledge of predation
effect could be to implement cormorant predation limitations and study the
effect in fish response. Reducing wildlife damage alone may fail to produce
long-term conflict resolution (Dickman, 2010). Therefore, close monitoring,
evaluation of effect and an adaptive management, with fast decision and action
process, is necessary, together with open and continuous communication
between stake holders and the public. With an increased concern of the
conservation of aquatic ecosystems and to sustain fishing efforts, conservation
would benefit from close collaboration between seabird and fishery science.
40
41
5 Sammanfattning
Fiskätande sjöfåglar i toppen av näringskedjan kan påverka ekosystem genom
att reglera fiskpopulationer och förändra fisksamhällens struktur. Eftersom
människan också nyttjar fisk i toppen av näringskedjan uppstår ibland
konflikter om resurser.
Det finns omkring 40 arter av skarv i världen. Framför allt två av dessa har
under slutet av 1900-talet oberoende av varandra ökat snabbt i antal, vilket
orsakat konflikter om resurser. I Europa gäller det storskarven av underarten
mellanskarv (Phalacrocorax carbo sinensis), och i Nordamerika gäller det
öronskarv (P. auritus). Båda arter är så kallade generalister, vilket innebär att
de snabbt anpassar sig till tillgängliga resurser. Beroende på vilket livsstadium
skarvar befinner sig i äter de olika mängd fisk, men generellt brukar man säga
att dessa två arter äter omkring 500 gram per dag per skarvindivid.
Denna avhandling gjordes för att öka kunskapen om skarvars interaktion
med fisk och fiske. När projektet satte igång saknades det kvalitativ
information om mellanskarvens föda på den svenska kusten i Östersjön, och till
viss del i sjöar. Tidigare studier var begränsade till ett lågt antal undersökta
spybollar. Födovalet studerades på tre platser, (Lövstabukten, utanför
Mönsterås och Karlskrona) och förändringar i föda över tid undersöktes. För
att få bättre kunskap om hur skarv konkurrerar med yrkes- och fritidsfisket
beräknades, utifrån födovalsstudierna, hur mycket skarvar äter av storlekar som
fångas av fisket (fångstbar fisk). Dessutom undersöktes en indirekt konkurrens
i och med att skarvar också äter mindre fiskindivider än vad fisket fångar.
Detta gjordes genom att beräkna hur skarvarnas predation på mindre fiskar
påverkar överlevnaden till fångstbar storlek.
I sjön Roxen hade man sett att det skett förändringar i fisksamhället, och en
del av förändringarna skedde under en period då antalet häckande skarvar
ökade. Skarvföda undersöktes i relation till provfiskefångster,
yrkesfiskefångster och näringshalter (fosfor och kväve) för att beskriva
42
variabler i relation till förändringar i fisksamhället. Dessutom märktes fisk för
att kvantifiera predationen på definierade populationer av abborre, gös och ål,
vilka är några av de kommersiella arterna i sjön.
Den övergripande mängden forskning på skarv beskriver födoval och
kvantifierar andelen fisk de tagit från fiskpopulationen i antal eller biomassa.
Få studier baseras på uppställningar där man testar en hypotes och undersöker
påverkan av predation på de fiskar som inte ätits av skarv, vilket egentligen är
vad man vill veta för att identifiera effekten av skarvpredation. Alltså studier
som undersöker påverkan på fiskparametrar, så som fångst per ansträngning,
biomassa, antal, storlekar på fisk individer etc., i relation till skarvabundans.
Ett exempel är att jämföra fiskparametrar i områden med skarv (försök) med
områden utan skarv (kontroll). Fördelen med den sortens studier är att man
statistiskt kan utvärdera skarvens effekter på fisk, och bortse från andra
variabler som kan påverka fisken, eftersom de variablerna agerar på båda
områdena. För en sådan studie kan man beräkna effekten, eller storleken av
påverkan, d.v.s. hur positiv eller negativ effekten är.
För att få en övergripande global bild av skarvars påverkan på fisk gjordes
en litterär sökning efter studier som statistiskt undersökt effekter av
skarvpredation. Dessa användes i en meta-analys, vilken är den första som
gjorts på skarvpredation. En meta-analys innebär att man inkluderar alla
effektstudier för att ta fram en total övergripande effekt. Fördelen med meta-
analyser är att man kan lägga samman effekter från undersökningar som
varierar i studiedesign, eg. olika habitat, skarvart, fiskart, fiskparametrar som
mätts etc. och skillnader i effektstorlekar mellan dessa kan undersökas.
Resultaten visar att skarvars föda varierar mellan områden (så kort som 6
km mellan kolonier) och de byter föda över tid. Förmodligen som ett resultat
av ändrat fiskbeteende men det kan till viss del också bero på att skarvar aktivt
väljer föda beroende på behov. När de föder små ungar kanske de väljer
mindre och mera lättsmält fisk att föda ungar med. De äter allt från små spiggar
till gäddor i, för fisket, fångstbara storlekar. Det är gapstorleken som avgör hur
stora fiskar de maximalt kan äta.
Undersökningarna visar att det för vissa arter sker konkurrens med yrkes-
och fritidsfisket. Skarvarna tog 10 % och 44 % av den mängd och storlekar
som yrkesfisket fångster av ål, flundra, strömming, abborre, gädda och sik i
Mönsteås respektive Karlskrona skärgårdar. Denna direkta konkurrens
beräknades minska fiskets fångster med mindre än 10 % för alla arter, förutom
flundra (>30%) och abborre (2-20 %). När predationen av mindre fisk
inkluderades i beräkningarna minskades fångsterna för abborre med 13-34 %
och för gädda 8-19 %. Konkurrensen mellan skarv och fiske varierade mellan
43
de två områdena och för olika arter av fisk, men studien visar att skarvars
predation lokalt kan konkurrera och ha negativ påverkan på vissa fisken.
Övergödning tillsammans med högt fisketryck kan ha bidragit till att
fisksamhället i Roxen initialt förändrades. Från att försörja ett gynnsamt
yrkesfiske med flera fiskare återstår bara en aktiv fiskare i sjön. I och med att
både fisketryck och övergödning minskat förväntades fisksamhället gått från
små planktonätande fiskar mot flera större fiskätande fiskar, men så var inte
fallet. Gärs och mört har minskat i både antal, biomassa och individstorlek.
Däremot visade fångster av abborre 2013 en ökning i individvikt. Skarvarna åt
främst mindre storlekar av abborre och gers. Trenden med färre men större
abborrar kan bero på att fiskproduktionen är stor, men skarvens predation på
mindre fisk gör förmodligen att färre fiskar uppnår reproduktiv ålder. De fiskar
som överlevt förbi den längden skarven främst fokuserar på, kan växa och bli
större och därmed bli tillgänglig för fisket. Märkningen av fisk visade en
skarvdödlighet på över 10 % för gös, 8 % för abborre och 3 % för ål. (Är
man intresserad av att läsa mera om Roxenstudien på svenska hänvisas till
skriften av Boström and Öhman (2014)).
Meta-analysen visade att skarvar generellt har en negativ effekt på fisk
och att förvaltningsåtgärder för att minska predationen har positiva effekter
på fisk. Statistiskt är det inga stora skillnader i effekter mellan
undersökningsområden, olika fiskparametrar som mätts, hur skarvarnas
abundans mätts, länder eller mellan skarvarter (mellanskarv och öronskarv
var de enda arterna som det gjorts studier som uppfyllde kriterier för att
kunna inkluderas i analysen). Däremot var det en signifikant skillnad i
effekter av skarvpredation mellan fiskarter. Abborrfiskar (inkluderar t.ex.
abborre, gös och gers) och arter inom familjen karpfiskar (t.ex. mört) är
extra känsliga för skarvpredation. Skarvpredation på dessa arter hade större
negativ effekt än för andra fiskarter.
Från resultaten kan man dra dessa huvudslutsatser:
1. Skarvens predation kan vara i den kapaciteten att fisk populationer
påverkas negativt (paper V).
2. Skarvpredation kan påverka fisket negativt genom att direkt konkurrera
om fiskar i samma storlekar (paper III, VI).
3. Den indirekta konkurrensen, där skarv äter fiskar innan de rekryteras
till fångstbar storlek, kan ha större betydelse för fisket än den direkta
konkurrensen (III).
4. Eftersom skarvföda, fisksamhällen och fiske varierar i tid och rum är
påverkan mer eller mindre på olika platser och vid olika tider på året (I-
V).
44
Studierna visar också starka indikationer på att skarvarpredation kan
omforma strukturen på en fiskpopulation. Genom att äta specifika storlekar
kan skarvar ändra storleksfördelningen och påverka reproduktion och
rekrytering (III, V).
Med ytterligare belägg och vetskap om att skarven faktiskt kan ha en
negativ påverkan på fisk och fiske yrkar jag på att man tar, inte bara den
mänskliga konflikten om skarv på allvar, men även skarven som predator.
Reduceringar av skarvpopulationer behöver i sig inte innebära att den
mänskliga konflikten minskar. Därför behöver man kontinuerlig övervakning
av effekter på både fisk och skarv efter reduktionsåtgärder. Det krävs en tät och
öppen kommunikation och samarbete mellan allmänheten, politiker, forskare,
och beslutsfattare för att snabbt kunna agera i en adaptiv förvaltningsstrategi
med målsättning av hållbara bestånd av både fisk, skarv och naturresurser.
45
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54
Thanks and Acknowledgements
This thesis would not be without the generous support by Sven-Gunnar
Lunneryd. He got me into cormorant research in 2005. I am forever grateful
for his enthusiasm and interest that rubbed over on me. Sven-Gunnar deserves
a lot of credit for being my mentor for many years, especially in the beginning
of my PhD research. Thank you!
My first experience with cormorants was when I worked in the Fishery
Research Station in Älvkarleby, 2005 and 2006, where the personnel took
care of a young, and maybe too enthusiastic, student. I thank you all for all the
help and support. Nothing was a problem too large to solve.
I have had the opportunity to work with colleges at all three labs at the
Department of Aquatic Research. I would like to acknowledge the help and
support and especially for putting up with my stinky research at times.
Especially colleges that have worked, and still working, in the Seals and
Fisheries group, whom has been a little extra close to the smell at times.
Thanks for helping out with the stinky work Hanna Ståhlberg, Annika
Strömberg, Mikael Ovegård, Kristin Öhman and Annelie Hilvarsson.
Cormorants must be extracting some pheromones or something because three
of us fell in love while digging in cormorant stomachs. Also thanks to
Amanda Whispell who came all the way from USA to help me in the field.
Thanks for being my friend, for interesting discussions and reading my texts.
I have had interesting and developing conversations with many people. But
I would like to mention two especially, though you may not have a degree in
ecology, you certainly have the knowledge and life experience. Thank you Alf
Sevastik, for support in life in general and for the fantastic field experiences
you have given me, and Per Månsson, for your initiatives, enthusiasm and
understanding.
Thanks to all coauthors. It has been a pleasure to work with you and I hope
we will write much more together in the future. Also, thanks to reviewers for
55
constructive comments that has improved manuscripts. I would also like to
thank Karl Lundström for teaching me diet analysis with biochemical
methods (hope for more collaboration) and for commenting on manuscripts
and thesis summary.
A special thanks to the fast response and personal help from the personnel
at the SLU University Library. I am very impressed by your good work and
dedication!
My supervisors have been amazingly supportive. Erik Petersson, thanks
for being the person you are. You are one of the most knowledgeable and
easygoing person I know, which is the perfect combination for a great
supervisor. Niels Jepsen, I know you rather go fishing than editing
manuscripts and commenting on drafts. Though I obviously have a difficulty
with the language, you have taught me (except a lot about tagging and
cormorant predation) to appreciate road kills and stuffed foxes. Thank you.
Mikaela Bergenius, always there (even weekends when it matters) and always
positive, no matter what. I hope we will continue having “parallel” lives. I did
not know you in Townsville, but you have been a great support in Öregrund
and Lysekil. Who knows where we will go next. My three supervisors have
complemented each other well in competence and timing when I needed extra
support. Thank you.
Last but not least, thanks goes to my family and friends for putting up with
me in times of stress. Mom and dad, you are the best. Mikael Ovegård,
thanks for taking the big load at home in the end of my PhD.
Financial support for each study can be seen in the acknowledgement for
each article. The rest of my PhD was financed by the Swedish University of
Agricultural Sciences. Thank you Magnus Appelberg, head of the
department when accepted as a PhD, for giving me the opportunity. And thank
you for letting me take time off for two of my biggest life experiences, crossing
the Atlantic and give birth to Tuva.
Lysekil, February 2017.
