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ICES COOPERATIVE RESEARCH REPORT
RAPPORT DES RECHERCHES COLLECTIVES
NO. 232
DIETS OF SEABIRDS AND CONSEQUENCES OF CHANGES
IN FOOD SUPPLY
Edited by
Edited by
Robert W. Furness
Institute of Biomedical and Life Sciences
Graham Kerr Building
University of Glasgow
Glasgow G12 8 QQ
UK
and
Mark L. Tasker
Joint Nature Conservation Committee
Dunnet House
7 Thistle Place
Aberdeen AB10 1 UZ
UK
International Council for the Exploration of the Sea
Conseil International pour l’Exploration de la Mer
Palægade 2–4
DK-1261 Copenhagen K
May 1999
Denmark
ICES Cooperative Research Report No. 232
ISSN 1017–6195
TABLE OF CONTENTS
Section
Page
List of Working Group participants ................................................................................................................................
1
A review of issues related to seabird consumption of fish and shellfish stocks, discards and mariculture
as well as the trophic role and ecology of seabirds and waders
G. L. Hunt, W. A. Montevecchi, and M. F. Leopold ...............................................................................................
1.1
1.2
2
2
2
2
3
3
4
4
4
5
Consumption of pre-recruit fish by seabirds and the possible use of this as an indicator of fish stock
recruitment
S. P. R. Greenstreet, P. H. Becker, R. T. Barrett, P. Fossum, and M. F. Leopold..................................................
6
2.1
2.2
2.3
2.4
2.5
2.6
2.7
3
2
Introduction
.........................................................................................................................................
Seabirds as indicators....................................................................................................................................
1.2.1
Seabirds as indicators of prey stocks ..............................................................................................
1.2.2
Seabirds as monitors of pollutants..................................................................................................
Processes affecting the trophic ecology of seabirds ......................................................................................
Seabird and wader interactions with mariculture ..........................................................................................
Seabird impacts on recruitment of fish stocks...............................................................................................
Mortality of seabirds .....................................................................................................................................
Discards and offal .........................................................................................................................................
References
.........................................................................................................................................
1.3
1.4
1.5
1.6
1.7
1.8
2
1
Introduction - background to fish stock assessment......................................................................................
Introduction - background to seabird feeding ecology..................................................................................
Seabirds as samplers of 0-group fish: case studies on cormorants/shags ......................................................
2.3.1
Shags and saithe, Norway...............................................................................................................
2.3.2
Cormorants and flatfish, Dutch Wadden Sea..................................................................................
Pre-recruit herring and common tern reproduction .......................................................................................
2.4.1
Correlations of herring population parameters ...............................................................................
2.4.2
Correlations between pre-recruiting clupeids and diet of common tern chicks..............................
2.4.3
Relationships between recruiting clupeids and the reproduction of terns.......................................
2.4.3.1 Minsener Oldeog .............................................................................................................
2.4.3.2 Banter See, Wilhelmshaven ............................................................................................
2.4.4
Conclusions ....................................................................................................................................
Norwegian spring-spawning herring and north Norwegian seabirds ............................................................
2.5.1 Røst
.........................................................................................................................................
2.5.2 Hornøya .........................................................................................................................................
Conclusions
.........................................................................................................................................
References
.........................................................................................................................................
6
7
7
8
8
8
8
9
10
10
11
12
13
13
14
15
16
Variation in prey taken by seabirds
M. L. Tasker, C. J. Camphuysen, and P.Fossum .................................................................................................... 18
3.1
3.2
3.3
3.4
3.5
3.6
Introduction
.........................................................................................................................................
Database description....................................................................................................................................
Variation in species and size of seabird prey...............................................................................................
3.3.1 General considerations .....................................................................................................................
3.3.1.1
Most frequently recorded food items ..............................................................................
3.3.1.2 Prey size ..........................................................................................................................
3.3.2 Annual variation...............................................................................................................................
3.3.3 Seasonal variation ............................................................................................................................
3.3.4 Spatial variation ...............................................................................................................................
Evidence for selection related to prey body condition ................................................................................
3.4.1 Differential prey selection between species .....................................................................................
3.4.2 Differential selection of prey within species ....................................................................................
Differences between adult and chick diet....................................................................................................
Discussion
.........................................................................................................................................
ICES Coop. Res. Rep. No. 232
i
18
18
18
18
19
19
19
21
21
23
24
24
24
25
Section
3.7
4
4.2
4.3
4.4
4.5
4.6
4.7
5.2
5.3
Introduction
.........................................................................................................................................
4.1.1 The shrimp fishery off Niedersachsen, Germany.............................................................................
Consumption of discards by seabirds ..........................................................................................................
4.2.1 Offshore fisheries in the North Sea ..................................................................................................
Diets of seabirds that scavenge discards in the North Sea...........................................................................
Numbers of seabirds supported by discards in the North Sea .....................................................................
Direct effects of discard consumption on species composition of seabirds in the North Sea......................
4.5.1 Increase in population size of seabird species..................................................................................
4.5.2 Population increase and changes in composition of seabird communities.......................................
Indirect effects of discard consumption on species composition of seabirds in the North Sea ...................
References
.........................................................................................................................................
29
29
31
31
33
33
33
33
36
38
38
Short term effects ........................................................................................................................................
5.1.1 Introduction......................................................................................................................................
5.1.2 Loss of feeding opportunities...........................................................................................................
5.1.3 Change in bird distribution...............................................................................................................
5.1.4 Competition at trawlers ....................................................................................................................
5.1.5 Changing diets..................................................................................................................................
5.16 Reproduction....................................................................................................................................
Medium term effects ...................................................................................................................................
5.2.1 Introduction......................................................................................................................................
5.2.2 Population size of consumper species ..............................................................................................
5.2.3 Population size and species composition .........................................................................................
References
.........................................................................................................................................
42
42
42
42
42
43
43
43
43
43
44
45
Evidence for decadal scale variations in seabird population ecology and links with the North
Atlantic oscillation
J. B. Reid, P. H. Becker, and R. W. Furness ........................................................................................................... 47
6.1
6.2
6.3
6.4
6.5
7
......................................................................................................................................... 25
Exploration of the short-and medium-term consequences of a reduction in the amounts of fish discarded
M. L. Tasker, P. H. Becker, and G. Chapdelaine.................................................................................................... 42
5.1
6
References
Evaluation of the role of discards in supporting bird populations and their effects on the species
composition of seabirds in the North Sea
S. Garthe, U. Walter, M. L. Tasker, P. H. Becker, G. Chapdelaine, and R. W. Furness ........................................ 29
4.1
5
Page
Introduction
.........................................................................................................................................
Materials and methods.................................................................................................................................
Results
.........................................................................................................................................
Discussion
.........................................................................................................................................
References
.........................................................................................................................................
47
47
47
49
49
A review of the causes, and consequences at the population level, of mass mortalities of seabirds ....................... 51
C. J. Camphuysen, P. J. Wright, M. Leopold, O. Hüppop, and J. B. Reid .............................................................. 51
7.1
7.2
7.3
7.4
7.5
7.6
Introduction
.........................................................................................................................................
Presumed causes .........................................................................................................................................
Frequency and seasonal occurrence of wrecks ............................................................................................
Vulnerability of seabird species to wrecks ..................................................................................................
Consequences to populations ......................................................................................................................
References
.........................................................................................................................................
51
51
52
53
55
56
Appendix 7.1 – List of Wrecks ....................................................................................................................................... 64
ii
ICES Coop. Res. Rep. No. 232
The following nationally appointed members of the Seabird Ecology Working Group participated in the meetings from
which this report is derived:
R.T. Barrett
Norway
P.H. Becker
Germany
C.J. Camphuysen
The Netherlands
G. Chapdelaine
Canada
P. Fossum
Norway
R.W. Furness (Chair)
UK
S. Garthe
Germany
S.P.R. Greenstreet
UK
G.L. Hunt Jr
USA
O. Hüppop
Germany
M.F. Leopold
The Netherlands
W.A. Montevecchi
Canada
J.B. Reid
UK
M.L. Tasker
UK
P.J. Wright
UK
ICES Coop. Res. Rep. No. 232
1
1
A review of issues related to seabird consumption of fish and shellfish
stocks, discards and mariculture as well as the trophic role and ecology of
seabirds and waders
G. L. Hunt1, W. A. Montevecchi2, and M. F. Leopold3
1
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA.
Biopsychology Programme, Memorial University, St John’s, Newfoundland, Canada A1C 5S7.
3
IBN–DLO, PO Box 167, 1790 Den Burg, Texel, The Netherlands.
2
1.1
Introduction
The Working Group on Seabird Ecology was requested
by the Biological Oceanography Committee to assess the
issues most likely to be raised within the ICES
community concerning the foraging ecology of seabirds
and waders, and the potential interactions between these
groups of birds and fisheries. In responding to this
request, the Working Group has listed a number of issues
likely to be of importance. The Working Group
recognized that each of these issues by itself is
potentially the subject for new research and/or for a
major review. The Working Group restricted itself to the
identification of issues, and has used this list as the basis
for developing possible future reports by the Working
Group on Seabird Ecology, singularly, or in co-operation
with other ICES Working Groups or Committees.
fishery can be harmed by competition or other trophic
interactions. As these questions and issues are addressed,
both experimental approaches within the North Sea and
comparisons with fisheries experience elsewhere in the
world will be required.
1.2
1.2.1 Seabirds as indicators of prey stocks
1.
In the present listing of issues, we have grouped issues
into several large subcategories, but we have not ranked
either the issues or the subcategories by importance,
since that is probably not feasible except on a local or
species-specific basis. In the first subcategory we list
issues related to the use of seabirds and waders as
indicators of conditions within the ecosystems of which
they are a part. These issues include the distribution and
abundance of prey organisms, the presence of pollutants
and the need to calibrate the signals received from the
birds with the absolute values of the parameters of
interest.
There are also important issues that focus on the basic
ecology of seabirds that are of interest (Hunt et al.,
1996), particularly insofar as they illuminate processes
that control the structure and energy flow within marine
ecosystems. In the second subcategory, we focus on the
use of seabirds as model systems for investigating
processes in marine ecosystems that are of broad interest,
and for which seabirds may be useful windows into
processes that are otherwise difficult to study.
In the remaining subcategories, we list issues concerning
the effects of seabirds and waders on fisheries, and
conversely, the effects of fisheries on seabirds and
waders. It should be noted that, in the cases where birds
and the fishing industry utilise the same resource, there is
the possibility that either, or both, the birds and the
2
Seabirds as indicators
Changes in the distribution, abundance, species
composition and breeding biology of seabirds can
indicate changes in the distribution, abundance, and
size classes of their preferred prey (reviewed by
Montevecchi, 1993).
a)
Seabirds may be sensitive indicators of
interannual and seasonal variation in the timing
of life history events in prey stocks.
b)
Seabird diets may provide indications of
changes in the biodiversity of prey populations
not otherwise monitored by fisheries managers
(Springer et al., 1984; Montevecchi, 1993).
c)
There is a need to calibrate the relationship
between the responses of seabirds and the
variations in abundance or recruitment in prey
stocks of concern.
1.2.2 Seabirds as monitors of pollutants
2.
Seabirds accumulate a wide variety of organic
chemicals and heavy metals and provide an
indication of the prevalence of these pollutants in
the marine ecosystem.
a)
As wide ranging top predators, seabirds
provide sampling opportunities that integrate
pollutant transfers up food chains which is
especially useful in the monitoring of lipophilic
pollutants. They provide a better indication of
possible hazards to humans than does sampling
from low trophic levels. Because their biology
is generally well known, the interpretation of
pollutant burdens is easier. By integrating over
ICES Coop. Res. Rep. No. 232
column, since many species of seabirds are
restricted to forage in the top 2 m?
time and spatial scales they permit more cost
effective sampling. (see reviews in Furness and
Greenwood, 1993).
b)
1.3
1.
How does the abundance of fish predators relative
to the abundance of their prey influence the
availability of food to seabird populations?
b)
5.
Evaluate evidence for decadal-scale variation in the
population sizes, reproductive ecology or food
habits of seabirds in the North Atlantic. Can these
changes be related to the North Atlantic oscillation
and other long-term cycles?
There is a need to evaluate the evidence that
the removal of large piscivorous fish by the
fishery has enhanced prey availability to
seabirds and thereby caused a related increase
in seabird populations.
1.4
1.
Seabird and wader interactions with
mariculture
Shellfish
a)
Blue mussel Mytilus edulis consumption by
waders, especially oystercatchers Haematopus
ostralegus, gulls, and seaducks, especially
eiders Somateria mollissima and scoters, on
both natural and artificial mussel beds in
competition with mussel fisheries (e.g.,
Wadden Sea, coastal U.K., Baltic).
b)
Cockle Cerastaderma edule consumption by
oystercatchers and eiders that compete with
cockle
fisheries
(e.g.,
Wadden
Sea,
Camphuysen et al., 1996).
c)
Spisula consumption by scoters Melanitta spp.
and eiders (e.g., German and Southern Bight).
d)
What are the population-level and local
consequences for seabirds, seaducks and
waders of the availability of commercial stocks
of shellfish, and what changes in these avian
populations would be predicted should the
commercial stocks of shellfish no longer be
available to these birds? This topic was briefly
reviewed in the previous meetings of the
Working Group (Leopold et al., 1996).
There is a need to evaluate the evidence that
changes in the species composition of
predominant fish consumers of zooplankton
has affected seabird populations.
Are preferred foraging areas, with seabird
aggregations, characteristic of some species or
regions, but not of others?
Given that certain forage fish species show strong
relationships to bottom type and other species may
respond to physical processes that concentrate
planktonic prey, what is the importance of bottom
sediment type versus hydrographic processes and
structures in determining foraging location, foraging
success and the role of seabirds in trophic transfer?
a)
4.
7.
At the population level, is most seabird foraging
concentrated in a few critical areas where birds are
present in high concentrations, or is most seabird
foraging accomplished by widely dispersed
individuals (e.g., Wright et al., 1996)?
a)
3.
What are the consequences for seabirds (and other
marine predators) of prey switching as a
consequence of changes in the availability of
preferred prey? How are adult survival and
reproductive performance affected?
Processes affecting the trophic
ecology of seabirds
a)
2.
6.
The pathways of pollutant to seabirds may be
traced by using stable isotope analyses and
fatty acid tracers to identify the trophic
pathways and carbon source areas supporting
seabird populations.
Can we determine or predict where the highest
concentrations of foraging seabirds are likely
to be found, and the temporal stability of these
preferred foraging locations?
What are the winter foods of seabirds at sea? Are
there seasonal changes in the species or types of
prey taken, and if so, are these changes more
marked for planktivorous than for piscivorous
seabirds?
What influences the vertical distribution of forage
fish, in particular their abundance in the upper water
ICES Coop. Res. Rep. No. 232
2.
Finfish mariculture
a)
Salmon
consumption
by
cormorants
Phalacrocorax carbo, gulls, grey herons Ardea
cinerea, ospreys Pandion haliaetus and other
birds taking fish from penned stock.
b)
What are the
local
population-level
consequences to birds of the availability of
farm-raised fish, and the protection of
mariculture by shooting birds that take or
damage product?
3
1.5
Seabird impacts on recruitment of
fish stocks
1.6
Mortality of seabirds
Seabirds predominantly consume small fish, particularly
0-group fish. We believe that in almost all situations the
local impact of this predation is likely to be less than that
from predatory fish, and mostly trivial in terms of fish
stock dynamics, but in some situations it has been
suggested that recruitment to fish stocks might be
affected by seabird predation rates.
The key question is: What are the relative impacts, at the
population level, of various anthropogenic and natural
sources of seabird mortality at sea? In particular in our
context: What is the relative impact of fisheries-related
mortality compared to other sources of mortality? We
appreciate that these topics are to some extent included
in the remit of the Working Group on Ecosystem Effects
of Fisheries.
a)
1.
Consumption of pre-recruit gadids by cormorants
and shags Phalacrocorax aristotelis (Norway,
Barrett et al., 1990).
b)
Consumption of juvenile herring Clupea harengus
by puffins Fratercula arctica and other seabirds
(Norway, Anker-Nilssen, 1992).
c)
Consumption of 0-group flatfishes by cormorants
and other seabirds (Damme, 1995).
d)
Consumption of salmon smolt by gulls, cormorants
and other seabirds (West coast and Alaska, USA).
Although not within the ICES geographical area,
the situation in western North America provides a
useful example of predator build-up at an artificial
feeding opportunity. Similar problems for released
smolts may arise in Canada, the west of Scotland
and in Norway (Greenstreet et al., 1993).
Examination of food samples from gannets Morus
bassanus, which consume low levels of salmon, has
yielded important information about the salmon
migration routes in eastern Canada (Montevecchi et
al., 1988).
Wrecks.
a)
2.
Mariculture
a)
e)
f)
Consumption of forage fish by seabirds and the
potential for competition with fisheries for these
stocks, particularly when local stocks near seabird
colonies are depleted (e.g., sandeels Ammodytes
marinus near Shetland; Sprat Sprattus sprattus near
Firth of Forth, juvenile herring in German and
Southern Bight).
How does the rate and total take of the commercial
harvest of forage fish stocks impact their
availability to seabirds? This question is most likely
to be an issue in ICES IVa west and possibly in
ICES IVb (Tasker and Furness, 1996; Wright and
Tasker, 1996; Wright et al., 1996).
g)
Are the perceived problems for seabirds indicative
of similar problems for other marine predators?
h)
consumption of freshwater fish stocks by
cormorants and sawbill ducks (Russell et al., 1996).
4
3.
4.
1.7
Drowning of cormorants, shags and other birds
in fish pens.
Net fishing
a)
Entanglement of seabirds in set nets, drift nets
and fish traps.
b)
Are there specific areas of the oceans where
seabirds are present in high densities, and thus
particularly vulnerable to entanglement?
Long line fishing
a)
5.
Wrecks or mass mortalities of seabirds may
occur for a variety of reasons, one of which can
be acute local food shortage. This issue is
considered in greater depth later in this report
(Section 7).
Hooking and subsequent death of seabirds, in
particular fulmars Fulmarus glacialis, great
skuas Catharacta skua and gulls in long-line
fisheries in the ICES areas and albatrosses and
large petrels in southern oceans.
Other sources of mortality (e.g., oil, chemical
pollution, weather, etc.). Such effects often act in
synergy. Are these influences greater or less than
effects attributable to fisheries activities, and are
synergies evident?
Discards and offal
Much of the following is addressed in greater detail later
in this report in Sections 4 and 5 on Discards.
1.
To what extent are present populations of seabirds
dependent on discards and offal?
2.
What impacts on seabird and other predator
populations would be expected if food from
discards and/or offal become reduced or
unavailable? What secondary and tertiary impacts
ICES Coop. Res. Rep. No. 232
might be anticipated (e.g., gull predation of other
seabirds in Newfoundland; skua predation on
kittiwakes Rissa tridactyla in Shetland; increased
predation on fish populations of value).
3.
4.
Do
discards
and
offal
ecological/trophic roles?
play
different
Given that different fisheries produce different
proportions of discards and different ranges of fish
sizes in the discards, to what extent do seabirds
show preferences between fisheries, and how does
the rate of dumping of discards after a trawl affect
their fate? Are seabirds feeding on discards that
might otherwise survive?
5.
Is there a seasonal variation in the importance of
discards to seabirds?
6.
Effects of fishing moratoria/ closed areas/ discard
bans require to be evaluated as these present
valuable experiments permitting responses of
seabirds to be studied.
1.8
References
Anker-Nilssen, T. 1992. Food supply as a determinant of
reproduction and population development in
Norwegian puffins Fratercula arctica. Doctor of
Science thesis in terrestrial ecology, University of
Trondheim. 46 pp.
Barrett, R. T., Rov, N., Loen, J., and Montevecchi, W. A.
1990. Diets of shags Phalacrocorax aristotelis and
cormorants P. carbo in Norway and implications for
gadid stock recruitment. Marine Ecology Progress
Series, 66: 205–218.
Camphuysen, C. J., Ens, B. J., Heg, D., Hulscher, J., Van
der Meer, J., and Smit, C. J. 1996. Oystercatcher
winter mortality in The Netherlands: the effect of
severe weather and food supply. Ardea, 84a: 469–
492.
Damme, C. J. G. van 1995. Predation on juvenile flatfish
by cormorants Phalacrocorax carbo in the Dutch
Wadden Sea. NIOZ Rapport 1995–10, Netherlands
Instituut voor Onderzoek der Zee, Texel. 46 pp.
Furness, R. W., and Greenwood, J. J. D. 1993. Birds as
monitors of environmental change. Chapman and
Hall, London. 368 pp.
Greenstreet, S. P. R., Morgan, R. I. G., Barnett, S., and
Redhead, P. 1993. Variation in the numbers of shags,
Phalacrocorax aristotelis, and common seals, Phoca
vitulina, near the mouth of an Atlantic salmon, Salmo
salar, river at the time of the smolt run. Journal of
Animal Ecology, 62: 565–576.
ICES Coop. Res. Rep. No. 232
Hunt, G. L., Barrett, R. T., Joiris, C., and Montevecchi,
W. A. 1996. Seabird/fish interactions: an
introduction. In: Seabird/fish interactions with
particular reference to seabirds in the North Sea, pp.
2–5. Ed. by G. L. Hunt and R. W. Furness. ICES
Cooperative Research Report 216.
Leopold, M. F., Nehls, G., and Skov, H. 1996.
Consumption of shellfish by seaducks and
oystercatchers. In: Seabird/fish interactions with
particular reference to seabirds in the North Sea, pp.
55–63. Ed. by G. L. Hunt and R. W. Furness ICES
Cooperative Research Report 216.
Montevecchi, W. A. 1993. Birds as indicators of change
in marine prey stocks. In: Birds as monitors of
environmental change, pp. 217–266. Ed. by R. W.
Furness and J. J. D. Greenwood. Chapman and Hall,
London.
Montevecchi, W. A., Cairns, D. K., and Birt, V. L. 1988.
Migration of post-smolt Atlantic salmon (Salmo
salar) off northeastern Newfoundland, as inferred
from tag recoveries in a seabird colony. Canadian
Journal of Fisheries and Aquatic Science, 45: 568–
571.
Russell, I. C., Dare, P. J., Eaton, D. R., and Armstrong, J.
D. 1996. Assessment of the problem of fish-eating
birds in inland fisheries in England and Wales.
Directorate of Fisheries Research, Lowestoft. 130 pp.
Springer, A. M., Roseneau, D. G., Murphy, E. C., and
Springer, M. I. 1984. Environmental controls of
marine food webs: food habits of seabirds in the
eastern Chukchi Sea. Canadian Journal of Fisheries
and Aquatic Sciences, 41: 1202–1215.
Tasker, M. L., and Furness, R. W. 1996. Estimation of
food consumption by seabirds in the North Sea. In:
Seabird/fish interactions with particular reference to
seabirds in the North Sea, pp. 6–42. Ed. by G.l. Hunt
and R.W. Furness ICES Cooperative Research
Report 216.
Wright, P., Barrett, R. T., Greenstreet, S. P. R., Olsen,
B., and Tasker, M. L. 1996. Effect of fisheries for
small fish on seabirds in the Eastern Atlantic. In:
Seabird/fish interactions with particular reference to
seabirds in the North Sea, pp. 44–55. Ed. by G. L.
Hunt and R. W. Furness. ICES Cooperative Research
Report 216.
Wright, P., and Tasker, M. L. 1996. Analysis of fish
consumption by seabirds by age class of prey fish. In
Seabird/fish interactions with particular reference to
seabirds in the North Sea, pp. 42–44. Ed. by G. L.
Hunt and R. W. Furness ICES Cooperative Research
Report 216.
5
2
Consumption of pre-recruit fish by seabirds and the possible use of this as
an indicator of fish stock recruitment
S. P. R. Greenstreet1, P. H. Becker2, R. T.Barrett3, P. Fossum4 and M. F. Leopold5
1
F.R.S. Marine Laboratory, PO Box 101, Victoria Road, Aberdeen AB11 9DB, U.K.
Institut für Vogelforschung, Vogelwarte Helgoland, An der Vogelwarte 21, D–26386 Wilhelmshaven, Germany.
3
Zoology Museum, University of Tromsø, Tromsø, Norway.
4
Institute Marine Research, PO Box 1870 Nordnes, N–5024 Bergen, Norway.
5
IBN–DLO, PO Box 167, 1790 Den Burg, Texel, The Netherlands.
2
2.1
Introduction – background to fish
stock assessment
In order to address the consumption of pre-recruit fish by
seabirds it is necessary to define exactly what is meant
by the terms “recruitment” and “pre-recruit”. These
terms mean different things to different people. Many
consider “recruits” to be those fish maturing in a
particular year to become part of the spawning stock.
Consequently relatively old fish of some considerable
length, two year old cod Gadus morhua of 30 cm or
more for example, could be considered as “pre-recruits”
because they had yet to mature. This definition however,
is not the one adopted by those carrying out assessments
of, for example, the demersal fish stocks. They consider
recruits to be those fish entering the population of a
particular species at the youngest exploited age, i.e. fish
of an age which occur in the catch or discard data. This
varies between species. Thus the youngest haddock
Melanogrammus aeglefinus and whiting Merlangius
merlangus which occur in catches are 0-group fish in the
latter part of the year, while cod and saithe Pollachius
virens of this age are rarely encountered in the catch.
Consequently, assessment working groups consider cod
and saithe recruits to be 1-group fish turning up in the
catches in the year following their birth. As a result of
these between species differences, the VPA population
assessments provide estimates of the numbers of 0-group
whiting and haddock for quarters 3 and 4 in any given
year, but not for the equivalent aged cod and saithe.
The numbers of recruits (0-group whiting and haddock in
year x and 1-group cod and saithe in year x+1, where
year x refers to the year class) can be calculated back
down a time series using straightforward VPA. However,
at the time when each working group meets, an estimate
of the numbers of fish in the current recruiting year class
is required in order to attempt to extrapolate forward to
predict future recruitment. Clearly catch data for these
fish are unavailable. In order to estimate current, or
future recruitment, fisheries survey data are used. The
historic VPA recruitment estimates are regressed against
recruitment indices for the various species derived from
survey data and, using the relationship obtained, the most
recent survey recruitment indices are used to estimated
the current numbers of fish in the recruit age classes. For
species such as cod and haddock, the relationship
between recruitment indices derived from survey data
6
and the VPA recruit estimates are fairly close; the survey
data provides a reasonably accurate estimate of current
recruit numbers. However, for species such as whiting
and saithe, this is not the case. For these species it would
be particularly useful if alternative means of estimating
the numbers of recruits were available. Even in the case
of haddock and cod it is worth exploring whether seabird
diet data might provide a useful independent estimate to
compare with young fish surveys or fisheries-derived
estimates.
Assessments of the major roundfish species are carried
out over a large geographic scale. The stock “units” were
re-evaluated as recently as 1995, following which,
ACFM concluded that, for assessment purposes, the
stocks of whiting and cod in VIId (eastern Channel)
should be combined with those in the North Sea.
Conclusions for the IIIa (Skagerrak) stocks were less
clear cut, but there were indications that the cod and
haddock stocks were linked with those in the North Sea
and that there were therefore grounds for combining
these assessments. Most seabird diet data have been
collected during the breeding season and generally
reflects the diets of birds feeding in the immediate
vicinity of particular colonies. It is questionable whether
data collected on such a limited spatial scale could ever
be used to provide indices of numbers of recruits in areas
as large as the North Sea, Skagerrak and eastern Channel
combined, but we address this issue with real data below.
The backcast VPA estimates of the numbers of recruits
in past years is highly dependent upon estimates of
natural mortality (by definition, these age classes do not
occur in the catch so fishing mortality is zero). Constant
values of natural mortality have been assumed for each
species in carrying out the VPA assessments. If,
however, natural mortality has varied as a result of
between year variation in the diet of seabirds, then the
VPA estimates of the numbers of recruits in each year
could be seriously in error. Furthermore, the predation
loading inflicted by seabirds on young gadid species
(e.g., Barrett, 1991) may be independent of the numbers
of young gadids available to seabirds, and may instead
be dictated by fluctuations in the abundance of pelagic
species such as mackerel Scomber scombrus, herring
Clupea harengus, sprats Sprattus sprattus and sandeels
Ammodytes spp., which tend to be the preferred prey of
most seabird species. Such a situation has been
ICES Coop. Res. Rep. No. 232
demonstrated for common seals Phoca vitulina in the
Moray Firth (Tollit et al., 1997).
2.2
Introduction - background to seabird
feeding ecology
Because most seabirds feed their chicks small fish, often
the juvenile stages of large fish, studies of seabird diet
can provide information on the local abundance of the
youngest age classes (0- and 1-group) of fish in the
immediate area around a seabird colony. As reproductive
success of seabirds depends on the availability of
adequate food resources, several parameters of their
reproductive biology or diet and feeding can be used as
indicators of the availability and distributions of prey
species on which they feed (reviewed by Montevecchi,
1993). However, breeding seabirds only sample fish
within a short distance of their colony. Foraging ranges
vary among species, and according to food abundance,
but tend to be tens of kilometres at most. Thus diet,
provisioning rate, or some surrogate measure such as
chick growth rate, of seabirds at a single colony cannot
sample an entire fish stock. The extent to which local
sampling may reflect the wider situation is uncertain, but
will be considered below.
Fish stocks are sampled on a daily basis by seabirds
whose diet is likely to reflect relative abundance of fish,
both by size (year class) and by species. Among the
different species of seabirds available for research, the
generalists will have diets that are most likely to reflect
the overall, local fish community structure, while
specialists’ diets will reflect yearly or within-season
differences in stocks of a particular species or group of
species. Examples of specialist feeders are the sandeeldependent seabirds of Shetland (Martin, 1989;
Monaghan et al., 1989), the herring-dependent puffins
Fratercula arctica in western Norway (Anker-Nilssen,
1992) and the terns in the south-eastern North Sea that
prey mainly on sandeels and clupeids. Cormorants
Phalacrocorax carbo and gannets Morus bassanus are
good examples of fish-eating seabirds that may take a
large variety of fish species. Diets of cormorants include
both demersal and schooling, pelagic fish. Gannets
sample from the pelagic fish in surface waters. As a
consequence, the local and temporal variation in gannet
or cormorant diet can reflect differences in relative prey
abundance.
It is important to note that there are major differences
between species of seabirds and between populations of
a single species in different regions. For example, the
sandeel ‘crisis’ in Shetland in the 1980s caused different
responses in different seabird species in Shetland. Arctic
tern Sterna paradisaea and kittiwake Rissa tridactyla
diet remained predominantly sandeel during the period of
food shortage, but these birds failed to breed
successfully. In contrast, gannets switched diet to other
fish species and their breeding success was unaffected.
Guillemots Uria aalge continued to feed almost
exclusively on sandeels yet their breeding success was
ICES Coop. Res. Rep. No. 232
also unaffected. Great skuas Catharacta skua switched
diet away from sandeels and their breeding success was
reduced, but not as much as that of kittiwakes. Breeding
numbers of Arctic terns fell drastically as these birds
mostly chose not to breed while sandeels were scarce,
whereas great skuas continued to attempt to breed even
though food was short. Great skuas incurred reductions
in adult survival rate through having to work harder for
food, whereas Arctic terns possibly did not because they
mostly refrained from breeding. Thus each seabird
species may respond in a species-specific way to a
change in food abundance, and may depend on different
prey species, or combinations of species, in different
regions. We show below, that kittiwake populations in
different parts of Norway show opposite responses to
increased local abundance of herring - in one case
kittiwake breeding success increases with herring
abundance and in the other it decreases. Such local
relationships are to be expected since responses depend
both on the ecology of the seabird species but also on the
combination of preferred prey fish species on which the
birds depend.
Total food availability will affect seabird condition in
terms of average body mass, breeding output, growth and
survival of young. Different parameters that can be
measured in seabirds may thus provide information on
total food abundance and the composition of the fish
community on which the birds feed. In situations where
young fish make up most of the diets, seabirds may
provide an additional means to sample younger stages of
fish at a high temporal resolution, and at low cost
compared to traditional ways of monitoring fish. Using
the additional indications provided by seabirds may add
little to assessment costs.
2.3
Seabirds as samplers of 0-group fish:
case studies on cormorants/shags
Cormorants and shags Phalacrocorax aristotelis
regurgitate indigestible prey remains in discrete pellets,
probably on a daily basis (Harris and Wanless, 1993).
These pellets are relatively easily collected and can be
analysed for the presence of fish otoliths, or other
identifiable remains, which can be related to fish size. As
such, these pellets provide an easy means to sample the
diet and to get information on the state of the fish
community at high temporal and spatial resolution.
Unfortunately, few long-term data sets exist for
cormorant diets in relation to prey availability in any one
locality. However, there is evidence that, for example,
double-crested cormorant diet can change considerably
over time, in response to changes in the prey fish
community (Rail and Chapdelaine, 1998).
Here we consider the potential of cormorants and shags
to be used as a tool in assessing the relative abundance of
0-group gadids and flatfish, using case studies made in
European waters. The first is a study on shags feeding
7
mainly on saithe in Norway, the second is on cormorants
feeding mainly on flatfish in the Wadden Sea.
2.3.1 Shags and saithe, Norway
0-group saithe live in shallow, inshore waters that are
notoriously difficult to sample. It is relevant to note that
the relationship between VPA estimates of 1-group
saithe and the numbers of young fish detected in surveys
is very weak (ICES, 1997a). In such a situation,
“systematic surveys of prey harvests of shags breeding
on inshore islands as supplementary inputs to [models on
fish abundance]” could be useful (Barrett, 1991). Pellets
were sampled in the 1985 and 1986 breeding seasons on
Bleiksøy, N. Norway (69°17’N, 15°53’N). Gadid
otoliths, all believed to be saithe, made up 81% and 58%
of all items identified in these two years and the birds
mainly took 0- and 1-group fish. When comparing 1985
to 1986, in the second year the diet contained fewer
saithe with a shift toward a higher proportion of older
fish. This indicates that 1986 was a poor year for 0-group
recruits in the area. This corroborated results of newly
developed 0-group surveys which ran in 1985–92. It is
worth noting here that the data from sampling shag diet
provided indications of low saithe production two or
three years sooner than could be determined from VPA
data (ICES, 1997a).
2.3.2 Cormorants and flatfish, Dutch Wadden
Sea
Cormorant pellets from several major roosts (1993) and
one colony (1992) were sampled in late summer at
locations throughout the Dutch Wadden Sea. Flatfish
were the most important prey, representing 73% of the
total diet by numbers (Leopold et al., 1998). Total
consumption of flatfish was estimated at 28.5 million
fish, of which 44.6% were plaice Pleuronectes platessa,
30.9% dab Limanda limanda, 21.7% flounder
Platichthys flesus and 2.8% sole Solea vulgaris. Flatfish
abundance was estimated from a combination of a
dedicated 0-group flatfish survey and the Demersal
Young Fish Surveys. Cormorant predation was estimated
to range from 30–50% of the total mortality of the 0group fish of these species. Both the figures for
consumption and for fish abundance should be taken
with considerable caution, as the first are as yet
uncorrected for lost otoliths (by digestion) and fish
abundance may have been underestimated. Despite these
uncertainties, and also considering that absolute numbers
of flatfish were low in the years of study, these figures
still suggest that cormorant predation was significant and
that these birds relied on juvenile flatfish to a large
extent. This implies that the cormorants sample 0-group
fish with great efficiency and that at least relative
differences between species of fish should be represented
in the birds’ diet.
however. Cormorants have established several breeding
colonies in the Dutch Wadden Sea in recent years, so
there is now also potential for studies that relate diet to
breeding parameters such as growth rate and survival of
chicks in these parts.
2.4
Pre-recruit herring and common tern
reproduction
Pre-recruit fish have special importance as food for small
seabirds such as terns. These birds have difficulty taking
fish longer than 20 cm. Small fish species or juvenile fish
therefore form the basis of their diet, consequently terns
may be especially useful as indicators of pre-recruit fish
abundance. Their overall energy reserves are low, so
food availability immediately affects body condition and
reproduction in adults (Frank and Becker, 1992;
Wendeln, 1997) and growth of young (Becker and
Specht, 1991; Mlody and Becker, 1991). They transport
single food items in the bill, making it easy to obtain
information on prey identity. Common terns Sterna
hirundo and Arctic terns are distributed widely around
the coasts of the North Sea, and the accessibility of many
colony sites make them ideal as monitors of the temporal
and spatial variations of 0-group fish. Thus the breeding
failures among Arctic terns in Shetland during the 1980s
(Furness, 1987; Monaghan et al., 1989, 1992; Uttley,
1992) coincided with a period of exceptionally low
sandeel recruitment (Bailey et al., 1991). In the southern
North Sea, however, sandeels are not important prey for
terns. Instead, clupeids, especially herring, but also sprat,
are the dominant prey of terns (Frank, 1992; Frick and
Becker, 1995; Tasker and Furness, 1996; Becker, 1996a;
Stienen and Brenninkmeijer, 1998). Thus in this section,
we link common tern reproduction in the Wadden Sea
with IBTS information collected by ICES on herring
stock size. In a long-term project, two colonies in the
German Wadden Sea, Minsener Oldeoog and Banter See,
Wilhelmshaven, have been studied since 1981, to look
for relationships between breeding performance
parameters and fish availability. A preliminary analysis
has already been presented by Becker (1996b).
2.4.1 Correlations of herring population
parameters
Herring larval abundance for the whole North Sea and
for just the south-eastern North Sea are significantly and
positively correlated, indicating that variation in the
abundance of herring larvae over the North Sea as a
whole parallels that in the south-eastern North Sea alone.
Larval abundance and the IBTS herring index are also
correlated (1-ring, Table 2.1, ICES, 1997b, c). The 1995
value, however, does not fit the regression line. The
IBTS herring estimate of the 1995 year class appears to
be an outlier (ICES, 1997b).
Clearly, studies that only lasted 1–2 years cannot be used
to describe long-term changes in fish stocks. Acquiring
longer time series of diet analyses seem promising,
8
ICES Coop. Res. Rep. No. 232
Table 2.1. Spearman correlation coefficients between various parameters estimating the clupeid stock in the North Sea (IBTS). n =
17 year classes (1979–1995).
IBTS herring index
North Sea
IBTS sprat North Sea
IBTS sprat index
North Sea
IBTS clupeids
Herring larvae density
–.07
IBTS clupeids
.76 ***
Herring larvae density
.43
–.44
.14
Herring larvae abundance
.77 ***
–.04
.62 **
2.4.2 Correlations between pre-recruiting
clupeids and diet of common tern chicks
Clupeids are the most important common tern food in the
Wadden Sea. On Minsener Oldeoog and Baltrum, they
represent 29–70% of the chick diet (mean=49%, 9 years;
Frank, 1992, 1998; Frick and Becker, 1995; Ludwigs,
1998). In the colony Banter See in Wilhelmshaven, 3–
15% of the chicks' food (mean=10%, n=6; unpubl. data)
and 11–48% of the courtship food are clupeids
(mean=24%, n=7 years; Wendeln, 1997 and unpubl.).
The common terns feed on 0-group herring, 1-group
herring, and on 1-group sprat which are about 6–13 cm
long during spring in the Wadden Sea.
It is difficult to distinguish visually between herring and
sprat in the bill of a tern. Herring was, however, the
dominant species in the local waters: in stow net catches
during 8 years (1985–1996) on Minsener Oldeoog, sprat
dominated the clupeids (92%) in 1994 only,
corresponding to a very high IBTS sprat index (year
.52 *
.59*
class 1993, ICES 1997c). In the other years, herring
dominated (92–99%; Behnke, 1996; Ludwigs, 1998) in
the stow net catches, and in the samples of dropped
clupeids recovered from the vicinity of nests.
In the Wadden Sea colonies, the amount of clupeids in
chick diet was positively correlated with the herring
larvae density in the south eastern North Sea (c.f. Figure
2.1, Minsener Oldeoog, rs=0.70, p<0.05, n=9, Table 2.2;
with IBTS herring index rs=0.45, n=9, n.s.; but not with
IBTS sprat index rs=0.03, n=9, n.s.). In the Banter See
colony, the amount of clupeids in chick diet was
positively correlated with herring larvae abundance
(rs=0.95, p<0.05, n=6, Table 2.3) and IBTS herring index
(rs=0.89, p<0.05, n=6). A high clupeid proportion in tern
diet apparently indicates a good stock of pre-recruiting
clupeids, especially herring.
There was no significant correlation between herring
larvae density and amount of clupeids in tern diet in the
same year.
Figure 2.1. Data sampling of herring recruits and common tern reproduction. Key tern diet is herring spawned in autumn two
calendar years (20 months) before the tern breeding season. These herring are sampled by the IBTS surveys during spring as larvae
the year before the tern breeding season, and as 1-ringers in the same season as tern breeding.
ICES Coop. Res. Rep. No. 232
9
Table 2.2. Spearman correlation coefficients between clupeid stock data of the North Sea (IBTS) and seabird data (common tern,
Minsener Oldeoog, 1981–1997)
Herring larvae density South East
(n=17)
Herring larvae abundance North Sea
(n=17)
% clupeids in chick diet (n=9)
.70 *
.32
growth rate of chicks (n=14)
.74 **
.58 *
growth rate of fledged chicks (n=11)
.77 **
.73 *
% chick losses by food shortage (n=17)
–.58 *
–.49 *
age of fledging (n=13)
–.56 *
–.46
chick fledged/pair
.23
.17
no. breeding pairs
–.32
–.47
Table 2.3. Spearman correlation coefficients between clupeid stock data of the North Sea (IBTS) and seabird data (common tern,
common tern, Wilhelmshaven, 1991–1997). n = 7 except % clupeids in chick diet.
IBTS herring
index
IBTS sprat index
IBTS clupeids
Herring larvae
density
Herring larvae
abundance
North Sea
North Sea
North Sea
South East
North Sea
% clupeids in chick diet (n=6)
.89*
.43
.43
.66
.95**32
growth rate of chicks
.21
.89**
.75
.79*
.61
growth rate of fledged chicks
.36
.68
.49
.94*
.77 *
.75
.61
.50
.32
chick fledged/pair
–
2.4.3 Relationships between recruiting
clupeids and the reproduction of terns
2.4.3.1 Minsener Oldeoog
Between 1981 and 1997, tern breeding success fluctuated
greatly between 0 and 1.6 chicks per pair per year, owing
to variation in the annual food availability as well as to
the influence of predators (Becker, 1998).
Comparison of herring larvae density and common tern
chick losses through starvation, over a 17 year period
(1981–1997), showed that common terns lost fewer
10
chicks and survivors grew better. (Chick growth rate
being interpreted as a surrogate for food provisioning
rate) in years with high rate of herring larvae density
(Figure 2.2). There are significant correlations between
herring larvae production two years before and common
tern chick growth rate, fledging age and chick loss
(Table 2.2, Figure 2.3). The linear modelling of chick
growth rate vs herring larvae index for the south east
North Sea was y=2.95x + 5.517. Consequently, an
increase of the larvae index by 0.1 would increase the
chick growth rate by 0.3 g/d, and reduce the chick losses.
No significant correlations were found with sprat index.
ICES Coop. Res. Rep. No. 232
Figure 2.2. Time trends of herring larval density (south-east North Sea, x1000; year class=year–2; IBTS) and losses of common tern
chicks (in %x10) on Minsener Oldeoog, Wadden Sea, from 1981–1997; Becker, unpublished data.
Figure 2.3. Correlation of herring larval density (south-east North Sea, x1000; year class=year–2; IBTS) with growth rate of
common tern chicks that fledged on Minsener Oldeoog, Wadden Sea, from 1981–1997; Becker, unpublished data.
2.4.3.2 Banter See, Wilhelmshaven
The number of fledglings per pair per year varied
between 0.2 and 2.4 chicks (1991–1997; Becker, 1998).
The correlations of reproductive parameters with herring
stock density were similar to those at Minsener Oldeoog
(Table 2.3, Figure 2.4). Chick loss through predation was
not so important as on Minsener Oldeoog, and the
ICES Coop. Res. Rep. No. 232
reproductive success increased positively with herring
availability (but n.s., Table 2.3). Chick growth was
especially good in 1994, the year with high sprat
abundance (see also Minsener Oldeoog Figure 2.3). Thus
sprat abundance can confuse the relationship with
herring abundance, but in most years sprat abundance
was too low to cause this problem.
11
Figure 2.4. Correlation of herring larval density (south-east North Sea, x1000; year class=year–2; IBTS) with growth rate of
common tern chicks that fledged at Banter See, Wilhelmshaven, from 1991–1997; Becker, unpublished data.
The regression of chick growth rate on the herring larvae
index (Figure 2.4) was y=4.0x+6.845. Thus an increase
in the herring index value of 0.1 would improve chick
growth by 0.4g/d. Using the herring larvae density or
abundance for the same year the terns bred, the
correlations described above were not significant at
either colony.
However, to conclude that tern breeding ecology can be
used as a measure of herring juvenile abundance, some
important points have to be clarified:
•
Decisive for the terns was the herring year class two
calendar years before the respective breeding
season (i.e. 1-ring in the breeding season, Figure
2.1), or the sprat year class one year before the tern
breeding (age 1 in the breeding season). This may
indicate that the 1-group herring is more important
for tern reproduction than 0-group. This should be
investigated further.
•
The correlations of tern data with the herring larvae
abundance estimates are much closer than those
with IBTS herring index (1-ring). This suggests that
the sampling of larvae gives a better annual figure
of the herring population 1 year later than the
sampling of 1-ringers in the current year. Fish
catches of 1-ringers may be taken more by chance
than larvae sampling.
The dependence of the reproduction of terns on prerecruit clupeids should be verified at another colony
site, for example on Griend in the Dutch Wadden
Sea where terns are also studied (by Stienen and
Brenninkmeijer).
2.4.4 Conclusions
Although not related to herring larval production in the
same year (these larvae being too small to provide much
food for terns), the data show that the reproduction of
terns on the southern North Sea coast is strongly linked
to the annual stock of juvenile herring, their main food
source. Consequently, terns can be used in addition to the
fisheries' data to indicate abundance of the young herring
stock. Conversely, fisheries' data on clupeids may be
used to predict growth and reproductive success of terns.
A reduced common tern breeding population in the
Wadden Sea in 1996 and 1997 (Südbeck et al., 1998)
also may be due to the reduced occurrence of juvenile
clupeids. Despite the short foraging range of breeding
common terns (max ca 7 km), the correlation with
herring abundance over the entire south-eastern North
Sea is quite strong. This suggests that herring are fairly
uniformly distributed over this region, or at least that
local abundance near these tern colonies is closely
related to abundance at the wider scale.
12
•
•
To investigate interactions between seabird
reproduction and fish stocks, breeding seabird
numbers or overall breeding success are often
considered, but parameters more directly linked to
ICES Coop. Res. Rep. No. 232
food availability such as chick growth, rate of chick
starvation or fledging success should be assessed as
they may be expected to provide a more direct and
sensitive indicator of food supply (Table 2.2). The
data presented also underline the importance of
long term data series as the key tool to understand
interactions between seabirds and fish.
2.5
Norwegian spring-spawning herring
and north Norwegian seabirds
The Norwegian spring-spawning stock of the AtlantoScandian herring has shown huge fluctuations in size
during the last half century. Between 1957–1971, it
collapsed from ca. 18 million tonnes to an estimated
12000 tonnes, remained very low (<1 million tonnes)
until 1985, and has since been increasing (ICES, 1997a).
Norwegian seabirds feed their chicks mainly on small
fish, samples of which are easy to obtain. Several studies
have documented that several seabird species feed
significant amounts of 0- and 1-group herring to their
chicks and studies along the coast of Norway have
shown that the amounts of herring in the samples vary
considerably from year to year (Barrett et al., 1987;
Barrett, 1996). This has been highlighted in two longterm studies on two colonies in North Norway, Hernyken
at Røst (67o26'N, 11o52'E) and Hornøya in East
Finnmark (70o22'N, 31o10'E). Close correlations exist
between the amount of herring fed to chicks and
independent assessments of amounts of young herring in
the sea (Anker-Nilssen, 1992; Anker-Nilssen and Øyan,
1995; Barrett and Krasnov, 1996).
2.5.1 Røst
There is clear evidence that seabirds breeding at Røst,
Lofoten Islands breed successfully only when larval and
0-group stages of herring are abundant. In years with low
abundance of herring, puffins and common guillemots
have produced few chicks of poor quality,
or no chicks at all, and kittiwakes have had reduced
breeding success (Bakken, 1989; Anker-Nilssen, 1992;
Anker-Nilssen and Øyan, 1995; Anker-Nilssen et al.,
1997).
There is, however, no clear causal relationship between
breeding success and abundance of herring larvae.
Between 1979–1994, herring content in puffin chick diet
varied between 0% and 89% wet mass, with sandeels,
saithe and haddock making up most of the remainder.
There is no simple relationship between the amount of
herring fed to the chicks and 0-group abundance. This is
possibly due to a preference for other prey species such
as sandeels or saithe which tended also to be abundant in
years with high herring abundance (e.g., 1983, 1992,
1994).
Figure 2.5. The relationship between the abundance indices of age-0 herring in the Barents Sea and adjacent waters in early autumn
and the fledging success of puffins at Røst, northern Norway, in 1975–1996. Eight points are located close to the origin. From AnkerNilssen et al. (1997).
ICES Coop. Res. Rep. No. 232
13
Although Anker-Nilssen et al. (1997) demonstrated a
strong positive relationship between breeding success
and independently obtained indices of 0-group herring
abundance over a 22 year period (1975–1996, Figure 2.5,
rs=0.898, p<0.001), there was a clear threshold above
which fledging success was at a maximum and could not
increase with increases in herring abundance. This
suggests that any changes above e.g., 1.0 in the
presently-used logarithmic index of herring 0-group
abundance (ICES 1997a) will not be detectable in puffin
breeding success alone.
A similar
positive
relationship between kittiwake breeding success and 0group herring abundance at Røst was also found between
1980–1996 (Figure 2.6, rs=0.815, p<0.001, AnkerNilssen et al., 1997), but again there is a threshold above
which breeding success does not increase further.
Because the species composition of the diet does not
relate directly to the availability of herring, and due to
the shape of the relationship curves between availability
of 0-group herring and breeding success, it is impossible
to predict levels of herring 0-group fish at scales finer
than high (log. index >1.0) or low (< 0.3) from breeding
success data.
Figure 2.6. The relationship between the abundance indices of age-0 herring in the Barents Sea and adjacent waters in early autumn
and the breeding success of kittiwakes at Røst, northern Norway, in 1980–1996. From Anker-Nilssen et al. 1997.
Puffin diet data from several northwestern Norwegian
colonies have, however, indicated the presence of some
0-group herring in the Barents Sea in years when surveys
failed to document any (1981, 1982, 1986, 1987,
index=0, Barrett et al., 1987; Barrett, 1996; ICES,
1997a).
2.5.2 Hornøya
Whereas seabirds breeding at Røst depend heavily on
herring to feed their chicks, the main diet of seabird
chicks in the southern Barents Sea consists of varying
proportions of herring, sandeels and capelin Mallotus
villosus (Barrett and Krasnov, 1996). Sandeels and
capelin are caught mainly as adult fish (Barrett and
Furness, 1990; Barrett and Krasnov, 1996). It has proved
impossible to relate amounts of capelin caught by
puffins, kittiwakes or common guillemots with
independent measures of capelin abundance, probably
due to the differences in spatial scale at which the
parameters were measured (Barrett and Krasnov, 1996).
There was, however, a suggestion that the kittiwakes
found smaller capelin (mean 114±40 mm) in 1989 than
in all but one of the other years (130–140 mm, 1980–
1994), due to low recruitment of capelin after the
collapse of the stock in 1987.
14
The herring, however, are consumed by seabirds as 1group fish, and while there were no relationships
between the previous years’ 0-group herring abundance
indices and the amount of herring in the chick diet on the
Kola Peninsula, there were clear positive correlations for
kittiwakes, common guillemots and puffins further west
on Hornøya (Figure 2.7). There are also positive
correlations between herring content in the diet of
common guillemot and puffin chicks and independent
assessments (ICES, 1997a) of 1-group herring in the
Barents Sea (r2=44%, df=9, p=0.027 and r2=76%, df=8,
p<0.0001 respectively; Barrett, unpubl.). The correlation
for kittiwakes was not significant (r2=32%, df=10,
p=0.07). Food data collected nearly every year since
1980 showed that herring first appeared in food samples
in 1985, was absent in the late 1980s and appeared again
in 1990. In 1993 and 1994 herring constituted >90% of
kittiwake diet samples and 30–50% of the puffin and
common guillemot diet samples. The appearance in 1985
corresponds with the only large cohorts of 0-group
herring spawned in the 1980s (1983, 1984), whereas the
presence in all diets in the early 1990s corresponds with
several years of successful spawning (1989–1994, ICES
1997a).
ICES Coop. Res. Rep. No. 232
Figure 2.7. The relationship between the percent of herring in common guillemot, kittiwake and puffin chick diets on Hornøya, north
Norway (solid squares) and Kharlov, northwest Russia (open circles), and the log index of 0-group herring abundance in the previous
year. Each graph has several points at the origin, not plotted. From Barrett and Krasnov (1996).
Contrary to the situation at Røst, it seems that increased
amounts of herring in chick diet corresponds to a decline
in the breeding success of kittiwakes at Hornøya
(r2=0.821, p>0.01, n=10, Anker-Nilssen et al., 1997).
There were, however, no significant relationships
between kittiwake breeding success and indices for the
1-group or the previous years’ 0-group herring
abundance. At present, the only parameters for seabirds
on Hornøya which corroborate the fisheries’ assessments
of the 0- and 1-group cohorts of herring in the Barents
Sea are the amounts of herring in the diets of chicks of
kittiwake, common guillemot and puffin.
2.6
Conclusions
We conclude that there are some case studies of seabirds
that show fairly strong correlations between diet
composition or food provisioning (or a surrogate
ICES Coop. Res. Rep. No. 232
measure of this such as chick growth rate) and the
abundance of pre-recruit fish. Fisheries-derived and
survey-derived estimates of recruitment apply to entire
stocks or to very large geographical areas, so are on a
much larger spatial scale than the distribution of fish
providing food to seabird chicks at a particular colony.
Nevertheless, correlations between common tern
breeding parameters and herring abundance in the southeastern North Sea provide an example of a correlation
where it seems that the local performance of terns does
reflect the changes in herring abundance over a larger
scale. This may not always be the case. Thus it would be
essential to be very cautious if using seabird data to infer
the level of recruitment into a fish prey population over a
wide area. In addition to the relationships discussed here,
good examples can be found in the literature, as for
example Montevecchi and Myers (1995), Montevecchi
(1993).
15
2.7
References
Anker-Nilssen, T. 1992. Food supply as a determinant of
reproduction and population development in
Norwegian puffins Fratercula arctica. Doctor of
Science thesis in terrestrial ecology, University of
Trondheim. 46 pp.
Anker-Nilssen, T., Barrett, R. T., and Krasnov, J. 1997.
Long- and short-term responses of seabirds in the
Norwegian and Barents Seas to changes in stocks of
prey fish. Proceedings of a symposium on forage
fishes in marine ecosystems. Alaska Sea Grant
College Program AK–SG–97–01: 683–698.
Becker, P. H. 1996a. Flußseeschwalben (Sterna hirundo)
in Wilhelmshaven. Oldenburger Jahrbuch, 96: 263–
296.
Becker, P. H. 1996b. Relationships between fish
populations and reproductive biology of common
terns in the Wadden Sea. In: Seabird/fish interactions,
with particular reference to seabirds in the North Sea,
pp. 65–67. Ed. by G.L. Hunt and R.W. Furness. ICES
Cooperative Research Report 216.
Becker, P. H. 1998. Langzeittrends des Bruterfolgs der
Flußseeschwalbe und seiner Einflußgrößen im
Wattenmeer. Vogelwelt, 119: 223–234.
Anker-Nilssen, T., and Øyan, H. S. 1995.
Hekkebiologiske langtidsstudier av lunder på Røst.
NINA Fagrapport, 15. 48 pp.
Becker, P. H., and Specht, R. 1991. Body mass
fluctuations and mortality in common tern Sterna
hirundo chicks dependent on weather and tide in the
Wadden Sea. Ardea, 79: 45–56.
Bailey, R. S., Furness, R. W., Gauld, J. A., and Kunzlik,
P. A. 1991. Recent changes in the population of the
sandeel (Ammodytes marinus Raitt) at Shetland in
relation to estimates of seabird predation. ICES
Marine Science Symposium, 193: 209–216.
Behnke, A. 1996. Vergleich verschiedener Fang- und
Analysemethoden zur Fluktuation von KleinfischBeständen im Wattenmeer. Diplomarbeit University
of Oldenburg. 104 pp.
Bakken, V. 1989. The population development of
common guillemot Uria aalge on Vedøy, Røst.
Fauna norvegica Series C, Cinclus, 12: 41–46.
Frank, D. 1992. The influence of feeding conditions on
food provisioning of chicks in common terns Sterna
hirundo nesting in the German Wadden Sea. Ardea,
80: 45–55.
Barrett, R. T. 1991. Shags (Phalacrocorax aristotelis L.)
as potential samplers of juvenile saithe (Pollachius
virens L.) stocks in northern Norway. Sarsia, 76:
153–156.
Barrett, R. T. 1996. Prey harvest, chick growth, and
production of three seabird species on Bleiksøy,
North Norway, during years of variable food
availability. In: Studies of high-latitude seabirds. 4.
Trophic relationships and energetics of endotherms in
cold ocean systems, pp. 20–26. Ed. by W. A.
Montevecchi. Canadian Wildlife Service Occasional
Paper 91.
Barrett, R. T., Anker-Nilssen, T., Rikardsen, F., Valde,
K., Røv, N., and Wader, V. 1987. The food, growth
and fledging success of Norwegian puffin chicks
Fratercula
arctica
in
1980–1983.
Ornis
Scandinavica, 18: 73–83.
Barrett, R. T., and Furness, R. W. 1990. The prey and
diving depths of seabirds on Hornøy, North Norway
after a decrease in the Barents Sea capelin stocks.
Ornis Scandinavica, 21: 179–186.
Barrett, R. T., and Krasnov, J. V. 1996. Recent responses
to changes in stocks of prey species by seabirds
breeding in the southern Barents Sea. ICES Journal
of Marine Science, 53: 713–722.
16
Frank, D. 1998. Bruterfolgsmonitoring an der
Flußseeschwalbe als Instrument ökologischer
Begleituntersuchungen zu einer Pipeline-Verlegung.
Vogelwelt 119: 235–241.
Frank, D., and Becker, P. H. 1992. Body mass and nest
reliefs in common terns Sterna hirundo exposed to
different feeding conditions. Ardea, 80: 57–69.
Frick, S., and Becker, P. H. 1995. Unterschiedliche
Ernährungsstrategien
von
Flußund
Küstenseeschwalbe (Sterna hirundo und S.
paradisaea)
im
Wattenmeer.
Journal
für
Ornithologie, 136: 47–63.
Furness, R. W. 1987. The impact of fisheries on seabird
populations in the North Sea. In: The status of the
North Sea environment; reasons for concern, Vol. 2,
pp. 179–192. Ed. by G. Peet. Werkgroep Noordzee,
Amsterdam.
Harris, M. P., and Wanless, S. 1993. The diet of shags
(Phalacrocorax aristotelis) during the chick-rearing
period assessed by three methods. Bird Study, 40:
135–139.
ICES 1997a. Report of the northern pelagic and blue
whiting fisheries working group. ICES CM
1997/Assess:14. 188 pp.
ICES Coop. Res. Rep. No. 232
ICES 1997b. Report of the herring assessment working
group for the area south of 62 N. ICES CM
1997/ASSESS:8. 392 pp.
ICES 1997c. Report of the International Bottom Trawl
Survey in the North Sea, Skagerak and Kattegat in
1996: Quarter 1. ICES CM 1997/H:8. 52 pp.
Leopold, M. F., van Damme, C .J. G., and van der Veer,
H. W. 1998 Impact of cormorant predation on
juvenile flatfish in the Dutch Wadden Sea.
Netherlands Journal of Sea Research, 40: 93–108.
Ludwigs, J. D. 1998. Kleptoparasitismus bei der
Flußseeschwalbe (Sterna hirundo) als Anzeiger für
Nahrungsmangel. Vogelwelt, 119: 193–203.
Martin, A. R. 1989. The diet of Atlantic puffin
(Fratercula arctica) and northern gannet (Sula
bassana) chicks at Shetland colony during a period of
changing prey availability. Bird Study, 36:170–180.
Mlody, B., and Becker, P. H. 1991. KörpermasseEntwicklung und Mortalität von Küken der
Flussseeschwalbe (Sterna hirundo L.) unter
ungünstigen Umweltbedingungen. Vogelwarte, 36:
110–131.
Monaghan, P., Uttley, J. D., and Burns, M. D. 1992.
Effect of changes in food availability on reproductive
effort in Arctic terns Sterna paradisaea. Ardea, 80:
71–81.
Monaghan, P., Uttley, J. D., Burns, M. D., Thaine, C.
and Blackwood, J. 1989. The relationship between
food supply, reproductive effort and breeding success
in Arctic terns Sterna paradisaea. Journal of Animal
Ecology, 58: 261–274.
Montevecchi, W. A., and Myers, R. A. 1995. Prey
harvests of seabirds reflect pelagic fish and squid
abundance on multiple spatial and temporal scales.
Marine Ecology Progress Series, 117: 1–9.
Rail, J. F., and Chapdelaine G. 1998. Foods of doublecrested cormorants Phalacrocorax auritus in the gulf
and estuary of the St Lawrence River, Québec
Canada. Canadian Journal of Zoology, 76: 635–643.
Stienen, E. W. M., and Brenninkmeijer, A. 1998.
Population trends in common terns Sterna hirundo
along the Dutch coast. Vogelwelt, 119: 165–168.
Südbeck, P., Hälterlein, B., Knief, W., and Köppen, K.
1998. Bestandsentwicklung von Fluß- und
Küstenseeschwalbe an den deutschen Küsten.
Vogelwelt, 119: 147–163.
Tasker, M., and Furness, R. W. 1996. Estimation of food
consumption by seabirds in the North Sea. In:
Seabird/fish interactions, with particular reference to
seabirds in the North Sea, pp. 6–42. Ed. by G.L. Hunt
and R.W. Furness. ICES Coop. Res. Report 216.
Tollitt, D. J., Greenstreet, S. P. R., and Thompson, P. M.
1997. Prey selection by harbour seals Phoca vitulina
in relation to variations in prey abundance. Canadian
Journal of Zoology, 75: 1508–1518.
Uttley, J. D., 1992. Food supply and allocation of
parental effort in Arctic terns Sterna paradisaea.
Ardea, 80: 83–91.
Wendeln, H. 1997. Body mass of female common terns
(Sterna hirundo) during courtship: relationships to
male quality, egg mass, diet, laying date and age.
Colonial Waterbirds, 20: 235–243.
Montevecchi, W. A. 1993. Birds as indicators of change
in marine prey stocks. In: Birds as Monitors of
Environmental Change, pp. 217–266. Ed. by R.W.
Furness and J.J.D. Greenwood. Chapman and Hall,
London.
ICES Coop. Res. Rep. No. 232
17
3
Variation in prey taken by seabirds
M. L. Tasker1, C. J. Camphuysen2, and P. Fossum3
1
Joint Nature Conservation Committee, 7 Thistle Place, Aberdeen AB10 1UZ, U.K.
Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands.
3
Institute Marine Research, PO Box 1870 Nordnes, N–5024 Bergen, Norway.
2
3.1
Introduction
Seabird diet in the ICES area has been described by
studies that have used a variety of techniques; principally
these are: analysis of regurgitated samples from living
birds or from the contents of regurgitated pellets,
observations of prey being carried to chicks and analysis
of stomach contents of dead birds killed either
deliberately or accidentally, for instance in an oil spill or
as by-catch (Duffy and Jackson, 1986). Each technique
used has some bias attached; these biases may be large
and unquantifiable. Analyses of regurgitated samples or
of otolith pellets are likely to miss small prey items with
few or no hard parts. Observations of prey brought to
colonies may not represent adult diet, and may also be
biased by the difficulty of identifying prey from a
distance. Killing live birds may be the least biased
method, but there may in turn be problems in ensuring
that a representative sample of birds is taken. There may
also be substantial cultural difficulties in killing birds
(e.g., Coleridge, 1854). Analysis of the stomach contents
of oil spill victims may be biased by behavioural changes
of birds prior to death. It may therefore often be difficult
to distinguish real patterns in seabird diet from patterns
caused by the study method.
There have been many studies of seabird diet; rather than
review these exhaustively for evidence of dietary
variation at various spatial and temporal scales, these
studies have been gathered into a database which is
described below. Examples to describe the various
aspects of variation have then been drawn from this
database to form this section of the report. We also draw
attention to Tasker and Furness (1996) who reviewed
dietary variation of seabirds in the North Sea.
3.2
Database description
A relational database was established by members of the
working group to facilitate this and future reviews of the
diet of seabirds. For all seabirds within the ICES and
NAFO areas, dietary information was collected from
published (including ‘grey literature’) and unpublished
sources, and coded in a standard format. The first version
of this database was launched (SEABDIET 1.0) at this
meeting. Each reference is coded with the ICES or
NAFO area in which the samples were collected, such
that most frequent prey items can be searched from the
database using area codes. It contains 838 study reports
(diet studies of a given predator at a given time and
18
place) covering 38 species of birds and 518 different
prey types. For the present review, a list of 1680
references dealing with seabird diets was consulted.
These references are not included in the present
document, but are available in digitised format for future
consultation. We are aware that the database is still
incomplete and it will be enlarged in the future.
3.3
Variation in species and size of
seabird prey
3.3.1 General considerations
Several general points should be noted in relation to this
review. First, prey abundance may be very different from
prey availability. While ‘prey populations’ may remain
constant over time or may be equally abundant in
neighbouring areas, spatial differences or temporal
changes in prey availability can influence whether or not
such prey is taken. Secondly, there has been a tendency
to study those organisms that appear in seabird diets,
rather than the full range of potential prey items. There is
rarely any insight as to why a potential prey item is not
taken. Food aversions, other than the complete
unsuitability of prey (too large, out of reach), are
normally ignored. A third point is that modern
technology has challenged a number of common
assumptions on foraging performance. Seabirds tagged
with satellite and/or radio transmitters or other data
loggers can be followed and detailed activity and prey
consumption on their feeding trips recorded (Wanless et
al., 1985; Wilson et al., 1986; Burger and Wilson, 1988;
Wanless et al., 1992; Briggs et al., 1993; Weimerskirch
and Robertson, 1994; Falk and Møller, 1995; Georges et
al., 1997). These studies, despite the possible negative
effects of some devices on foraging performance, have
demonstrated that the feeding range of some seabirds is
considerably greater than previously assumed, and that
the diving depth of birds previously assumed to be
surface feeders may be comparatively large. All of these
studies indicate that assumptions on the size of foraging
niches are usually too limited.
Some studies may assume that a change in prey
consumption by a predator population from one study to
the next represents a change in the availability of the
original prey stock. However, optimal diet models
predict that predators will select the most ‘profitable’
prey in terms of yield per unit handling time of each food
type encountered and rank this relative to profitabilities
ICES Coop. Res. Rep. No. 232
of other types. The implication is that a forager should
always accept the most profitable food type and that it
should accept successively less profitable types only
when encounter rates with higher ranking types fall
below critical levels (Hughes, 1993). This would mean
that the representation or the absence of a given prey in
the diet could have been caused by changes in the
availability of another prey species perhaps as a
consequence of changes in the local abundance (Tollitt et
al., 1997). Optimal diet theory predicts that the diet of a
species should expand and contract according to the
quality and availability of alternative foods.
3.3.1.1 Most frequently recorded food items
Most seabirds, even those with highly specialised
foraging methods, appear to feed on a great variety of
prey types, though primarily on small pelagic fishes,
squids and crustaceans (Montevecchi 1993). However,
relatively few prey items are taken as staple foods
(represented in at least 50% of the diet samples in a
study), while many organisms are only rarely recorded in
dietary studies. A survey of the available literature on
seabird diets contained in SEABDIET 1.0 found that 13
prey species or groups have each been recorded in at
least five studies as ‘staple food’ in any species of North
Atlantic seabird, either in the form of discards from
fisheries or as prey taken during more ‘natural’ feeding .
Sandeels (in particular Ammodytes marinus), capelin
Mallotus villosus, polar cod Boreogadus saida, clupeid
fish (herring Clupea harengus and sprat Sprattus
sprattus), a variety of small crustaceans (mainly
Euphausiids and amphipods), and squid (usually
unidentified Cephalopods, Loligo spp and Gonatus spp),
in decreasing order of importance, were the most
frequently encountered staple foods (at least 10 studies).
Staple foods (>50% of the diet by mass) or common prey
(26–50%), at any year of study in a given area, are in this
study considered ‘preferred prey’, whereas infrequently
taken prey items (2–25%) or rare prey are considered
‘alternative prey’.
3.3.1.2 Prey size
The size of fish prey of North Atlantic seabirds generally
varies between 100 and 300 mm, although larger as well
as smaller prey are also taken (Table 3.1). Not
surprisingly, larger seabirds tend to feed on larger prey
than smaller species, as clearly demonstrated in the
studies of the use of discards by scavenging seabirds in
the North Sea (Table 3.2) (Camphuysen et al., 1995) but
also in other multi-species diet studies (e.g., Swennen
and Duiven, 1977; Knopf and Kennedy, 1981; Götmark,
1984; Sanger and Ainley, 1988; Camphuysen, 1990,
1996). There are notable exceptions. Gannets Morus
bassanus, the largest seabird breeding in the North
Atlantic, are capable of taking larger prey than most
other seabirds (e.g., roundfish of 300–450 mm). They
can, however, take small sandeels and capelin; these
have been recorded as staple food in Scottish and
ICES Coop. Res. Rep. No. 232
Newfoundland colonies in response to the sometimes
abundant supply of these fish in these areas
(Montevecchi and Porter, 1980; Martin, 1989).
Table 3.1. Size range (fish length in mm) of fish prey in some
North Atlantic seabirds (SEABDIET 1.0 database).
Species
Min
Red-throated diver
Great northern diver
Fulmar
Gannet
Shag
Great skua
Black-headed gull
Common gull
Lesser black-backed gull
Herring gull
Great black-backed gull
Kittiwake
Arctic tern
Common tern
Guillemot
Brünnich's guillemot
Razorbill
Black guillemot
Puffin
42
35
40
70
80
100
35
60
40
20
20
50
30
30
20
126
20
40
10
Max
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
200
500
330
550
160
360
210
210
470
530
450
360
160
160
270
184
237
220
170
These results show firstly that smaller scavenging
seabirds under similar conditions select smaller food
items than larger seabirds, and secondly that larger
seabirds may select considerably larger roundfish than
are generally available. It has been shown that the
tendency for smaller seabirds to take small prey is at
least partly motivated by the presence of other, more
powerful scavengers or more dominant conspecifics. An
increase in handling time would increase the risk that a
fish was lost through kleptoparasitism (Hudson, 1989;
Hudson and Furness, 1989). Size selection under natural
conditions in foraging seabirds is an aspect which
deserves more attention in future studies.
3.3.2 Annual variation
There are few long-term studies of seabird diets.
Examples of dietary change between years are more
numerous and the following examples illustrate the scale
of change which has been observed.
Large changes in staple foods from one prey
species/group to another are not uncommon in seabird
populations. Changes in diet composition may be sudden
or more gradual. Sudden changes are usually more easily
linked with a drastic change in foraging conditions or
prey abundance than are gradual changes. An excellent
example of a combination of rather sudden and gradual
shifts is provided by diet studies of great skuas
Catharacta skua in Shetland (Furness, 1997). In the late
19
1970s, when the breeding population of great skuas on
Foula reached its highest level ever, the diet of great
skuas was dominated by sandeel (Table 3.3). After 1979,
sandeels were suddenly considerably less important and
over 50% of the samples studied comprised a mixture of
whitefish, most probably obtained as discards. A shift
from sandeel towards whitefish discards had been
observed also in 1974 and 1975. Since 1983, seabird
predation by great skuas has increased significantly.
Interestingly, when sandeel gradually returned in the diet
of great skuas in the 1990s, and while discards remained
in the diet, the habit of bird predation persisted.
The collapse of sandeel stocks around Shetland in the
1980s provided a number of examples of annual
variation in seabird diet, involving several species of
seabirds in a single area. Surface feeding birds, such as
arctic terns Sterna paradisaea and kittiwakes Rissa
tridactyla, experienced great difficulty in obtaining
sufficient prey, and breeding failures or abandoned
breeding attempts were widespread in the archipelago
(Monaghan et al., 1989; Hamer et al., 1991, 1993). Other
seabirds, such as the gannet, showed marked shifts in
their diets in response to this crash towards a wider prey
spectrum that included much herring and gadids (Martin,
1989). Species, such as the guillemot Uria aalge and
shag Phalacrocorax aristotelis, which dive to pursue fish
underwater, were hardly affected by the collapse and
continued feeding chicks with sandeels and to reproduce
with reasonably high fledging rates.
Table 3.2. Median length (cm) of roundfish and median width of flatfish (0.5 cm) consumed by scavenging seabirds (arranged by
body mass) in relation to the size of roundfish and flatfish offered in sessions of experimental discarding in the North Sea (from
Camphuysen et al., 1995).
Species
body mass (g)
roundfish
consumed
flatfish
offered
Kittiwake
300–500
15
18
Common gull
300–500
14
15
Fulmar
700–900
16
Lesser black-backed gull
700–1000
Herring gull
consumed
offered
3.5
6.5
18
3.5
6.5
18
18
4.5
6.5
800–1200
18
19
5.0
6.5
Great skua
1300–1800
25
19
Great black-backed gull
1100–2000
24
18
6.5
6.5
Gannet
2800–3200
25
19
6.5
6.5
Table 3.3. Representation of sandeel A. marinus, whitefish discards, birds and other prey (% frequency of occurrence in all samples
studied per year) in the diet of great skuas on Foula (Shetland Islands), simplified after Furness (1997).
Year
sandeel
discards
birds
other
Year
sandeel
discards
birds
other
1973
71
27
2
0
1985
1
72
20
7
1974
24
71
5
0
1986
0
81
14
5
1975
21
69
6
4
1987
9
77
10
4
1976
72
26
2
0
1988
1
72
24
3
1977
59
35
4
2
1989
2
67
29
2
1978
64
35
1
0
1990
1
38
38
23
1979
41
54
3
2
1992
15
66
25
7
1980
17
74
6
3
1993
31
87
11
10
1981
18
77
4
1
1994
19
81
13
34
1982
13
80
3
4
1995
73
63
3
24
1983
9
70
17
4
1996
55
73
42
23
1984
0
74
23
3
20
ICES Coop. Res. Rep. No. 232
In northern Norway, changes in the stocks of capelin in
the 1970s and 1980s were tracked by changes in
breeding performance of seabirds in the area (Wright et
al., 1996). In 1986, when the capelin stock was at its
lowest, several species of seabird produced very few
young. Massive declines in both the number of breeding
guillemots at northern Norwegian colonies and of
guillemots on their wintering grounds were recorded.
Since 1989, capelin stocks have increased and bird
numbers have started to recover. In this instance, there
was no alternative in the late 1989s to capelin in the diet,
so that switching was not possible. Since then, herring
stocks have increased in the area, and this species has
reappeared in bird diets. This may be a reversion to the
situation in the 1930s and 1940s when Belopol'skii
(1957) recorded herring as important constituent of the
summer diet of many seabirds breeding in the region.
importance of sandeels, clupeids and gadids in guillemot
diets in the post- (August–October) and pre-breeding
seasons (March–April). Camphuysen (1996) summarised
published information on guillemot diets outside the
breeding season in the North Sea and demonstrated
consistent features, such as a greater importance of
sandeels in late spring and early autumn, substantial use
of prey that were available for only a short time (small
scad in the southern North Sea), and a greater importance
of clupeids and gadids in winter. Future versions of the
diet database, SEABDIET, will facilitate a more detailed
summary of seasonal changes in diets, for a considerably
larger number of species. To achieve that, a substantial
amount of so far unpublished data will need to be
computer coded.
3.3.3 Seasonal variation
Spatial variation in seabird diets is particularly
interesting on the small scale, as it indicates that local
populations use different, but perhaps overlapping, food
resources. A demonstration of regional variation in
seabird diets was provided by Lilliendahl and
Solmundsson (1997), who described summer food
consumption of six seabirds in Iceland (Table 3.5). For
razorbill Alca torda, guillemot and Brünnich’s guillemot,
sandeels predominated in the diet (>50% in percent wet
prey mass) to the south, west and east of Iceland, while
capelin was their main prey (generally >90% of wet prey
mass) in the north-west and north-east. Euphausiids were
of significance mainly for Brünnich’s guillemots,
particularly to the east and north-west. Capelin formed
nearly 100% of the prey of kittiwakes to the north, while
sandeels predominated in the south and mixtures
(capelin/sandeel and capelin/sandeel/Euphausiids and
other prey) in respectively the west and east sectors.
Fulmars Fulmarus glacialis have a more mixed diet in all
sectors, although the overall trend of capelin
consumption in the northern sectors and sandeels
representing a significant part of the diet in the south and
west can be seen also in this species. Much of this
variation in seabird diet can be linked to oceanographic
differences between regions.
Much of the dietary work carried out on seabirds has
been from or around colonies in the breeding season.
Even within that window of courtship, incubation,
raising chicks and fledging of young, rather radical shifts
in the diet (both of adults and in the prey delivered to the
chicks) have been demonstrated. For example, the
gradually altering energetic demands of the growing
chick(s) has to be met with by the provisioning adults
(Harris and Wanless, 1986; Anker-Nilsson and Nygård,
1989; Annett and Pierotti, 1989; Beers and Habraken,
1993; Hill and Hamer, 1994; Anker-Nilssen and Øyan,
1995). So, even in the absence of obvious changes in
food resources, there may be differences in the
exploitation of their prey by seabirds, which have to
meet constantly changing energy and nutrient
requirements during breeding. In the post-breeding
season, most seabirds become more mobile, because the
constraints imposed by central place foraging are no
longer in effect. In winter, the energetic requirements
may be elevated due to harsh environmental conditions,
such as severe storms or very cold weather. Even from a
purely energetic point of view, seasonal changes in diet
and food preferences are likely to occur. Since many fish
are known to show rather different distribution and
activity patterns in the course of a year (e.g., spawning,
buried phases in sand, migration), dietary changes in
seabirds will probably be even more obvious between the
seasons.
Elliot et al. (1990) demonstrated substantial changes in
the diet of Brünnich’s guillemots Uria lomvia, such as
shifts from predominantly fish in birds in the autumn to
crustaceans in birds wintering off Newfoundland and
Labrador (Table 3.4). Blake et al. (1985) produced
similar information from various locations off the
Scottish east coast, showing shifts in the relative
ICES Coop. Res. Rep. No. 232
3.3.4 Spatial variation
Because the birds studied by Lilliendahl and
Solmundsson (1997) were shot at sea (presumably at or
near feeding locations) rather than at colonies, these
results show the use of a common resource by predators
with different foraging capabilities and prey preferences.
So, while capelin is virtually absent from the diet of the
three auk species east of Iceland, both fulmars and
kittiwakes still consumed considerable amounts of these
fish. As the latter are surface foragers and the former are
deep diving seabirds (but capable of feeding near the
surface as well as over 100m deep), we might conclude
that these auks prefer sandeel over capelin as prey in
these waters.
21
Table 3.4. Seasonal changes in diets of Brünnich’s guillemots in Labrador and Newfoundland from birds shot at sea (% frequency in
total number of stomachs examined per season per region), after Elliot et al. (1990).
Study area
Prey (genus/group)
E Newfoundland
Decapoda
Euphausiacea
Gammarus
Hyperiidae
Thysanoessa
Boreogadus
Gadus
Mallotus
Mollusca
Nereis
Cephalopoda
Decapoda
Euphausiacea
Gammarus
Hyperiidae
Thysanoessa
Boreogadus
Gadus
Mallotus
Mollusca
Cephalopoda
Decapoda
Euphausiacea
Hyperiidae
Boreogadus
Gadus
Mallotus
Cephalopoda
Decapoda
Euphausiacea
Gammarus
Hyperiidae
Parathemisto
Thysanoessa
Boreogadus
Gadus
Mallotus
Nereis
Decapoda
Euphausiacea
Gammarus
Hyperiidae
Boreogadus
Gadus
Mallotus
Mollusca
Cephalopoda
Labrador
NE Newfoundland
S Newfoundland
SE Newfoundland
22
Nov
Dec
0
3
1
5
6
57
9
18
37
10
87
40
10
5
13
6
85
26
65
13
2
Jan
3
100
1
3
32
3
29
3
Feb
100
22
92
4
3
Mar
1
85
1
31
96
9
10
1
2
1
3
69
1
9
82
1
12
9
43
1
7
80
5
80
25
3
14
11
7
66
3
29
3
7
4
27
51
18
54
74
88
4
7
16
55
5
5
10
92
2
26
33
5
8
7
5
ICES Coop. Res. Rep. No. 232
Table 3.5. Summer prey (% wet mass, rounded figures to nearest 5%) of seabirds feeding in five sectors off Iceland, as an example
of spatial variation in diets. Shown are prey fractions representing at least 5% of wet mass (after Lilliendahl and Solmundsson
(1997).
Species
Prey
Fulmar
Capelin
Kittiwake
South
West
North-west
North-east
East
5
25
15
45
40
5
10
Sandeel
60
Euphausiids
5
Other
35
55
70
75
45
Capelin
15
55
95
100
40
Sandeel
80
45
Euphausiids
5
10
35
10
Other
Guillemot
5
Capelin
Sandeel
30
90
Euphausiids
Other
Brunnich’s guillemot
Razorbill
90
65
5
5
5
10
5
10
Sandeel
75
Euphausiids
5
25
Other
10
5
Capelin
10
95
95
5
90
Capelin
Sandeel
Puffin
90
15
70
100
50
80
50
95
5
100
Euphausiids
5
5
Capelin
30
25
65
20
5
10
5
40
45
5
5
Sandeel
100
Euphausiids
Other
Camphuysen et al. (1995) experimentally discarded fish
from survey vessels in seven subregions in the North Sea
and Skagerrak in four seasons. There was considerable
variation in the selection of discarded items by different
species of scavengers in different areas through the year
in relation to the type and size of discards. Spatial
variation in consumption rates (% of the discarded
fraction of the fish caught actually taken by seabirds)
showed that competition for fishery waste is
considerably more intense in some areas and less in
others. This variation could not always be explained by
the relative abundance of scavenging seabirds in relation
to the number of fishing vessels in those areas. Specific
dietary preferences of species of birds meant that some
species did not occur at fishing vessels in some seasons
because other food resources were exploited instead. For
example, kittiwakes were abundant and widespread all
year round, but were most common scavenging around
fishing vessels only in winter and autumn. The reverse
ICES Coop. Res. Rep. No. 232
90
55
was true for the even more abundant fulmar, which
obtained the greater part of discarded fish only in
summer and spring (see also Camphuysen and Garthe,
1997). In brief, these studies demonstrated a mixture of
spatial and seasonal trends in discard consumption by
different seabirds, which was at least partly related to
changes in dietary preferences or changing feeding
opportunities in these birds.
3.4
Evidence for selection related to prey
body condition
The quality of prey varies both between species and
within species.
23
3.4.1 Differential prey selection between
species
In an analysis of dietary selection, Harris and Hislop
(1978) described the biomass and quality of various prey
species fed to young puffins Fratercula arctica at ten
colonies around Scotland during six years in the early
1970s. This dietary information was compared with the
"availability" of these prey as described in experimental
mid-water trawl catches made in areas off north and east
Scotland. There are obvious methodological problems
involved that are acknowledged by the authors. In terms
of biomass, sandeels and sprats predominated in the diets
of chicks at most colonies in most years. Rocklings
Ciliata mustela and whiting Merlangius merlangus
formed a more important part of the diet at western
rather than eastern Scottish colonies. In calorific terms,
large sprat (>100mm long) had a considerably higher
energy density (10.9 kJ/g wet weight) than any other
prey species and were twice the value of saithe and
whiting (5.1 kJ/g and 4.05 kJ/g respectively). Between
these limits, in decreasing order, came rockling, small
sprats (43–93mm long), sandeels and small larval forms.
The percentage fat increases significantly in both sprat
and sandeel with the length of fish (Love, 1970). The
diet of these puffin chicks, when looked at in calorific
terms, accentuates the importance of sprat and devalues
the importance of whiting.
There was a broad similarity between the composition of
trawl catches and puffin chick diets, with some
exceptions. Sandeels were one hundred times as
numerous as sprats in the trawl catches, but only three
times as common in puffin chick loads, suggesting that
puffins differentially select sprat. Rockling were
uncommon in the trawl, but this may have been due to
the young of this species living near the surface, above
the level at which the trawl was fishing. Conversely,
Norway pout Trisopterus esmarkii and long rough dab
Hippoglossoides platessoides were common in the trawl,
but only recorded once each in puffin diets.
A later study, around the Isle of May off eastern
Scotland, found that as the North Sea sprat stock
declined, these were replaced in the diet by herring,
whose stock was increasing (Hislop and Harris, 1985).
3.4.2 Differential selection of prey within
species
Several authors have suggested that seabirds may
differentially select individuals of the same species with
higher calorific values. The most obvious selection
would be for different sized individuals of the same
species (e.g., Harris and Hislop, 1978). Wright and
Bailey (1993) showed that diving birds tended to bring in
a higher proportion of older age-classes sandeels than
would be expected if they were selecting fish randomly.
Becker (unpubl.) examined the changes in size classes of
fish brought to chicks by common terns at
Wilhelmshaven. There was a clear and significant
24
difference in size of fish fed to chicks of different ages
(Table 3.6) (Chi2 for herring/sprat = 78.1, p<0.001; Chi2
for smelt = 93.3, p<0.001).
It may also be that seabirds prey selectively on ripe, prespawning fish rather than spent or non-spawning fish of
the same size. Furness and Barrett (1985) found that
guillemots at a colony in northern Norway took
predominantly gravid female capelin, containing 6.6%
lipid and 15.2% protein, which compared with spent fish
containing only 2.5% lipid and 14% protein. These
authors could not demonstrate whether guillemots prey
selectively on the young ripe late-spawning capelin in
the area or whether the behaviour of these capelin makes
them more available to the birds. Montevecchi and
Myers (1996) also indicate some prey selection by
guillemots on Funk Island, Newfoundland. Almost all
capelin delivered to chicks between 1977 and 1994 were
gravid female, providing higher energy densities than
found with male or spent female capelin (Montevecchi
and Piatt, 1984). In contrast, Montevecchi and Myers
(1996) found that gannets landed about equal proportions
of male and female capelin. Guillemots hunt by pursuit
diving underwater, so may have a greater opportunity to
assess the state of individual fish than would the plungediving gannet. In addition, greater selectivity is to be
expected among single prey loading species (e.g.,
guillemots or terns) than among multiple prey loading
species (e.g., gannets, puffins).
3.5
Differences between adult and chick
diet
A simultaneous study of diet as assessed by three
methods was carried out by Harris and Wanless (1993)
on shags on the Isle of May in the Firth of Forth during
the chick-rearing period. Regurgitated samples were
collected from chicks, stomach contents of adults were
sampled by flushing with water and mucous pellets
(which contain hard parts of prey) were retrieved from a
roost site. The roost site samples (mostly non- and failed
breeders) were from a wider spectrum of prey than the
chicks. Stomach contents of adults returning to feed
chicks were very similar to those regurgitated by the
chicks (i.e. almost entirely sandeels), however Wanless
et al. (1993) concluded that adults ate a wide spectrum of
fish from other fish families and probably digested these
before returning to the colony. Fish in these families had
low calorific densities compared to sandeels indicating
that adults transported highest calorific items for their
chicks.
Courtship feeding of females by their mates is a feature
of the biology of several seabirds. We contrasted the
sizes of fish fed to common tern females and to chicks
(Table 3.7). In general females were fed on a
significantly wider size range of fish than were chicks
(Chi2 for herring/sprat = 80.1, p<0.001; Chi2 for smelt
Osmerus eperlanus = 70.2, p<0.001).
ICES Coop. Res. Rep. No. 232
Table 3.6. Proportions (%) of size classes (multiples of bill length) of fish fed to different ages of common tern chicks
at Wilhelmshaven in 1995 (P.H. Becker, unpubl.).
Smelt
Age
0–7 days
8–14 days
Sprat/herring
>14 days
0–7 days
8–14 days
>14 days
Fish size class
1
19.7
2.7
2.9
37.7
15.3
3.6
2
62.5
48.1
36.5
56.9
60.2
60.8
>2
17.8
49.2
60.6
5.4
24.4
35.5
Sample size
152
187
170
130
98
166
Table 3.7. Proportions (%) of size classes (multiples of bill length) of fish fed to female and chick common terns at Wilhelmshaven
in 1995 (P.H. Becker, unpubl.).
Fish size class
Smelt
Sprat/herring
Females
Chicks
Females
Chicks
1
19.6
6.9
20.7
17.6
2
32.6
43.1
31.1
56.9
3
34.6
41.3
32.4
23.1
>3
13.2
8.7
15.8
2.5
Sample size
613
813
241
615
3.6
Discussion
From the examples of annual, seasonal and spatial
variation in seabird diets provided in this chapter it may
seem that we have a reasonable overview of its
variability in most common species of seabirds in the
ICES area. In fact, this is not the case. Of 767 studies in
which the study season was specified, 64% were
conducted during the breeding season or in summer.
Only 8% of all studies were conducted in the prebreeding season, 12% during post-breeding (early
autumn) and 15% in winter. Logistic problems have
prevented large scale studies of the diets of most pelagic
seabirds outside the breeding season, simply because
most birds are ‘out of reach’ (away from land). From the
examples given earlier and from many published papers
on variability in seabird diets, it should be emphasised
that the results obtained in one area, in one season, in any
one year are not necessarily valid with that same predator
species in other circumstances. However, on the larger
scale it will soon be possible to come up with some
generalisations. There is no need to become side-tracked
as a result of the immense variation in prey, since most
items form only a very small part of the diet. Rather few
species/types are ‘preferred’ prey for seabirds while very
many should be labelled ‘occasional prey’. It is very
important, however, that additional information is
collected on seabird prey preferences, particularly
outside the breeding season and away from the colonies.
have tried to address the aspect of prey selection from a
known resource of potential prey. There are very obvious
methodological problems involved with the assessment
of food resources (a function of prey stock size,
suitability and availability) for piscivorous seabirds, but
in the absence of any insight it remains speculative why
certain seabirds rely on sandeels in one year and perhaps
clupeids in the next. Size selection (e.g., Swennen and
Duiven, 1977, 1991; Camphuysen et al., 1995),
differential selection of prey of a certain ‘quality’ or
calorific value (e.g., Harris and Hislop, 1978, Wright and
Bailey, 1993) and prey choice or dietary shifts in relation
to the prey stock (e.g., Doornbos, 1979; Vader et al.,
1990) are very important aspects which all deserve a lot
more attention in future studies.
3.7
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in the southern Barents Sea. In: Auks at sea, pp. 175–
180. Ed. by S. G. Sealy. Studies in Avian Biology 14.
Wanless, S., Corfield, T., and Buckland, S. T. 1992.
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in relation to habitat and prey. In: European seabirds,
Proceedings of the Seabird Group conference,
Glasgow 27–29 March 1992, p. 26. Ed. by M. L.
Tasker, Seabird Group, Sandy.
Montevecchi, W. A., and Myers, R. A. 1996. Dietary
changes of seabirds indicate shifts in pelagic food
webs. Sarsia, 80: 313–322.
Wanless, S., Harris, M. P., and Morris, J. A. 1985.
Radio-monitoring as a method for estimating time
budgets of guillemots Uria aalge. Bird Study, 32:
170–175.
Montevecchi, W. A. and Piatt, J. 1984. Composition and
energy contents of mature inshore spawning capelin
(Mallotus villosus): implications for seabird
predators. Comparative Biochemistry and Physiology
A, 78: 15–20.
Wanless, S., Harris, M. P., and Russell, A. F. 1993.
Factors influencing food load sizes brought in by
shags Phalocrocorax aristotelis during chick rearing.
Ibis, 135: 19–24.
Montevecchi, W. A., and Porter, J. M. 1980. Parental
investments by seabirds at the breeding area with
emphasis on northern gannets, Morus bassanus. In:
behavior of marine animals vol. 4, pp 323–365. Ed.
by J. Burger, B. L. Olla, and H. E. Winn. Plenum,
London.
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Weimerskirch, H., and Robertson, G. 1994. Satellite
tracking of light-mantled sooty albatross. Polar
Biology, 14: 123–126.
Wilson, R. P., Grant, W. S., and Duffy, D. C. 1986.
Recording devices on free-ranging marine animals:
does measurement affect foraging performance?
Ecology, 67: 1091–1093.
27
Wright, P. J., and Bailey, M. C. 1993. Biology of
sandeels in the vicinity of seabird colonies at
Shetland. Fisheries Research Services Report 15/93.
Marine Laboratory, Aberdeen. 64 pp.
28
Wright, P., Barrett, R. T., Greenstreet, S. P. R., Olsen,
B., and Tasker, M. L. 1996. Effect of fisheries for
small fish on seabirds in the eastern Atlantic. In:
Seabird/fish interactions, with particular reference to
seabirds in the North Sea, pp 44–55. Ed. by G. L.
Hunt, and R. W. Furness ICES Cooperative Research
report No. 216.
ICES Coop. Res. Rep. No. 232
4
Evaluation of the role of discards in supporting bird populations and their
effects on the species composition of seabirds in the North Sea
S. Garthe1, U. Walter2, M. L. Tasker3, P. H. Becker4, G. Chapdelaine5 and R. W. Furness6
1
Institut für Meereskunde, Düsternbrooker Weg 20, 24105 Kiel, Germany.
Forschungzentrum Terramre, Schleusenstrasse 1, 26382 Wilhelmshaven, Germany.
3
Joint Nature Conservation Committee, 7 Thistle Place, Aberdeen AB10 1UZ, U.K.
4
Institut für Vogelforschung, Vogelwarte Helgoland, An der Vogelwarte 21, D–26386 Wilhelmshaven, Germany.
5
Canadian Wildlife Service, 1141 route de l’Eglise, PO Box 10100, 9th floor, Ste-Foy, Quebec G1V 4H5, Canada.
6
Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, U.K.
2
4.1
Introduction
In this report, we use the term discards to describe the
animal waste generated by fishing operations which is
jettisoned at sea. This therefore includes undersized fish
and shellfish, fish which cannot be taken to market
because quotas are exceeded or the catch is of low
relative value to other hauls etc., offal and waste from
cleaning fish at sea and other biota such benthos.
The amounts of discards (including offal) from offshore
fisheries in the North Sea have been evaluated by several
workers. Recent evaluations were summarised by ICES
(1996). Garthe et al. (1996) compiled information from a
variety of sources on the amounts discarded in six
sections of the North Sea (Table 4.1).
4.1.1 The shrimp fishery off Niedersachsen,
Germany
Shrimping is the most important fishing activity off
Niedersachsen. The fleet consists of 118 cutters (Prawitt,
1995),
which
fish
between
March
and
November/December (Gubernator, 1994) for the brown
shrimp Crangon crangon (5–8 cm body length).
Shrimping is carried out with beam trawls close to the
coast and inside the Wadden Sea. Large numbers of
undersized shrimps, other benthic invertebrates and fish
species are incidentally caught owing to the poor
selectivity of the fine meshed shrimp nets (minimum
mesh opening 20 mm).
In order to quantify total amounts discarded in three
categories (undersized shrimps, other invertebrates and
fish) the discard to commercial shrimp mass ratios in 103
unsorted catch samples (November 1992–November
1993) were analysed (Walter, 1997). These ratios,
combined with the landings statistics of brown shrimps
for the same month, was used as a basis to estimate the
total amount of discards from the shrimp fleet of
Niedersachsen in the main part of the fishing season of
1993.
Shrimps of marketable size comprised 11 % of mass of
the catch, the remainder was mostly undersized shrimps
(64 %), other invertebrates (8 %) and fish (11 %). The
most abundant fish were flatfish such as plaice
Pleuronectes platessa, flounder Platichthys flesus and
dab Limanda limanda, and roundfish such as clupeids
and gadids. Among the invertebrates, shore crab
Carcinus maenus and swimming crab Liocarcinus
holasadus were most frequent (Walter, 1997).
Table 4.1. Estimated quantities of discards and offal in six sub regions (see Figure 4.1) in North Sea offshore trawl fisheries in 1990
(in tonnes) (Garthe et al., 1996, see also ICES, 1996) and the SE North Sea shrimp fisheries.
Roundfish
Flatfish
Elasmobranchs
Benthic
invertebrates
Offal
Total
NW
54,890
13,130
3,380
7,760
11,750
90,910
NE
53,310
14,290
3,270
8,270
11,450
90,590
CW
26,760
14,960
1,610
7,860
5,970
57,160
C
48,010
61,450
2,710
30,580
11,690
154,440
CE
48,520
68,230
2,710
33,820
11,990
165,270
S
30,710
127,240
1,320
61,410
9,950
230,630
SE shrimp fishery
10,800
8,000
0
137,800
0
156,600
273,000
307,300
15,000
287,500
62,800
945,600
Total
ICES Coop. Res. Rep. No. 232
29
Figure 4.1. Map of the six sub regions of the North Sea used by Garthe et al. (1996).
The monthly median of the ratio of undersized to
marketable shrimps varied considerably (between 1:2–
1:10), with the lowest value in spring and the highest
ratio in August (Figure 4.2). The majority of undersized
shrimp are discarded alive. The proportion of
invertebrates (other than brown shrimps) to marketable
shrimps varied between 0.05:1 and 1.1:1. The equivalent
ratios for fish showed less variation (0.5:1–1.4:1) than
invertebrates (excluding undersized shrimps) (Walter,
1997).
Total discards of approximately 4,000 tonnes of fish
(1,750 t of flatfish and 2,290 t of roundfish), 27,000
tonnes of undersized shrimps and a further 2,000 tonnes
of other invertebrate species were calculated for the
shrimper fleet in the main fishing season (April–
November) in 1993.
30
There is no direct information on discards from shrimp
fisheries elsewhere in the North Sea. Shrimping is
carried out off the coasts of France, Belgium, England,
and the three Wadden Sea countries (Netherlands,
Germany and Denmark). The results of the study off
Niedersachen might be extrapolated to the remainder of
the brown shrimp fishery off the Wadden Sea coast of
the North Sea, in order to provide an approximate
estimate of total bycatch. The total landings of brown
shrimps in the coastal area of the Wadden Sea average to
20,000 tonnes per year (1983–1992) (Lozàn, 1994). If
the mean discards/marketable shrimp ratios in the catch
samples off Niedersachsen (0.4 for flatfish, 0.54 for
roundfish, 6.4 for undersized shrimps and 0.49 for other
invertebrates) is applied to the rest of the fishery, then a
total of more than 150,000 tonnes of discards would be
produced by all shrimpers of the three countries (Table
4.1).
ICES Coop. Res. Rep. No. 232
It should be noted that Table 4.1 does not include
amounts discarded from a number of inshore fisheries
(e.g., shrimp fisheries off countries other than those of
the Wadden Sea), from static gear fisheries or from
industrial fisheries (likely to be relatively small
amounts). The total amount of fishery waste discarded in
the North Sea probably exceeds 1,000,000 tonnes.
4.2
Consumption of discards by seabirds
4.2.1 Offshore fisheries in the North Sea
The proportion of discards consumed by seabirds in the
North Sea was studied experimentally by Camphuysen et
al. (1995) (summarised in Table 4.2). These proportions
are broken down by species to quantify tonnages of five
categories of discard (offal, roundfish, flatfish,
elasmobranchs and benthic invertebrates) consumed by
the most important scavenging seabird species in the
North Sea (Table 4.3 based on Camphuysen et al., 1995;
Garthe et al., 1996), based on the numbers of discard
items consumed by birds. Calculations using discard
mass as the basis would certainly lead to somewhat
different results since, for instance, kittiwakes Rissa
tridactyla take the smallest roundfish and gannets Morus
bassanus the largest roundfish (Camphuysen et al.,
1995). Inshore shrimp fisheries off Niedersachsen
(Lower Saxony)
In the coastal area off Niedersachsen, scavenging
seabirds follow shrimp trawlers in large numbers
throughout the whole fishing season (Walter and Becker,
1997). Up to 3,000 birds may be found astern of an
individual shrimper (Berghahn and Rösner, 1992; Walter
and Becker, 1994, 1997).
The main scavenging species are herring gull Larus
argentatus and black-headed gull L. ridibundus, which
together represent 93% of all recorded birds (Walter and
Becker, 1997). Both species showed the same seasonal
pattern, with low numbers until June and larger numbers
in late summer and autumn. Common gulls L. canus,
lesser L. fuscus and great black-backed gulls L. marinus
and common terns Sterna hirundo and arctic terns S.
paradisaea were less numerous than herring and blackheaded gulls. Common gulls occurred throughout the
whole fishing season, but only in substantial numbers
behind shrimpers in March and in autumn. Lesser blackbacked gulls and common/arctic terns were summer
visitors and occurred in relatively low numbers between
April and September. Great black-backed gulls were
scarce before July, increasing slightly in numbers in late
summer and autumn.
Table 4.2. Proportion of experimental discards and offal consumed by birds (in %) in six offshore regions (all seasons) and four
seasons (all sub regions), respectively, in the North Sea offshore trawl fisheries (from Garthe et al., 1996), and in the shrimp fishery
of Niedersachsen (Walter, 1997).
Roundfish
Flatfish
Elasmobranchs
Benthic invertebrates
Offal
Sample size
NW
90
28
12
9
99
9,132
NE
89
41
12
3
98
3,281
CW
84
32
12
1
92
5,316
C
75
14
12
1
90
8,519
CE
63
10
12
3
54
3,396
S
71
8
12
4
100
1,200
Winter
92
35
12
17
100
6,028
Spring
76
22
12
8
94
10,354
Summer
70
10
12
3
94
8,526
Autumn
82
20
12
3
97
5,936
21,848
2,345
34
902
5,715
30,844
79
41
sample size
Shrimp fishery
ICES Coop. Res. Rep. No. 232
23 (excl. shrimp)
4291
31
30
A: undersized shrimps
Mass ratio of discard category: commercial shrimps
20
10
0
12
B: other invertebrates
8
4
0
5
4
C: fish
3
2
1
0
Month
Apr
N samples 9
May
Jun
Jul
Aug
Sep
Oct
13
15
15
15
15
12
Nov
9
Figure 4.2. Average seasonal discards/commercial shrimp ratio of three main discard components, undersized shrimps, other
invertebrates and fish (April–November 1993, total number of catch samples = 103) (from Walter, 1997).
Table 4.3. Tonnes of discards consumed by seabird species from the North Sea offshore fisheries as a whole (based on Garthe et al.,
1996; Camphuysen et al., 1995; Walter and Becker, 1997).
Offal
Roundfish
Flatfish
Elasmobranchs
Benthic
invertebrates
Total
Fulmar
39,800
53,400
4,500
200
6,300
104,200
Gannet
300
35,900
15,300
200
0
51,700
Great skua
100
2,000
0
0
0
2,100
0
100
0
0
0
100
100
800
100
0
0
900
Lesser black-backed gull
1,300
14,500
6,200
1,100
500
23,300
Herring gull
2,600
21,100
5,100
0
500
29,300
300
12,600
4,800
200
600
18,500
Kittiwake
10,500
66,000
2,200
400
1,100
80,200
Total
55,000
206,000
38,000
2,100
9,000
310,000
Black-headed gull
Common gull
Great black-backed gull
32
ICES Coop. Res. Rep. No. 232
Feeding rates by number of items consumed were
determined following the method of Hudson and Furness
(1988). Differences between the length distribution of
commercial
and
experimental
discards
were
compensated for (Walter and Becker, 1997). In total,
5,500 tonnes of discards from the shrimper fleet of
Niedersachsen were consumed by the birds in 1993. This
comprised 41% of the discarded flatfish mass (=710
tonnes), 79% of roundfish (=1,820 tonnes), 23% of four
invertebrate species (Carcinus maenas, Liocarcinus
holasadus, Asterias rubens, Allotheutis subulata; 420 t)
and 10% of the undersized shrimps (2,500 t).
4.3
Diets of seabirds that scavenge
discards in the North Sea
Discards form only a proportion of the diet of seabirds in
the North Sea. Full quantification of seabird diet has not
been carried out, but it is known that this proportion
varies by species, by location and by season. Based on a
compilation of many studies, Tasker and Furness (1996)
make some assumptions on diets for an input to a model
of North Sea fish consumption by seabirds. Their results
for the main scavenging species are summarised in Table
4.4.
4.4
Numbers of seabirds supported by
discards in the North Sea
In order to assess how many seabirds can be sustained
from discards and offal, Garthe et al. (1996) derived an
"average scavenger community" from seabird counts
(Camphuysen et al., 1995). This is based on the typical
composition of those eight common seabird species
known to consume fishery waste regularly and is
calculated in proportion to the numerical and seasonal
abundance of the species in the North Sea There are
considerable variations in the distribution of the
scavengers in the North Sea, with respect to both area
and season (Camphuysen et al., 1995; Stone et al.,
1995). Fulmars Fulmarus glacialis are most numerous in
the north (particularly around Shetland), with much
lower numbers in the south and east. Highest numbers
are present in late summer/early autumn. Gannets leave
the North Sea in autumn and winter as do lesser blackbacked gulls. Herring gulls and great black-backed gulls,
in contrast, move into the North Sea during the winter.
Kittiwakes are also highly numerous, but stay in the
North Sea in considerable number the entire year.
Common gulls are present only in winter in the south and
the eastern parts, black-headed gulls are scarce in
offshore areas at all times, in contrast to inshore areas of
the south-eastern North Sea where they are common
(Stone et al., 1995; Berghahn and Rösner, 1992; Walter
and Becker, 1997).
About 5.9 million individuals in the North Sea
scavenging seabird community could possibly be
sustained by offshore fisheries (this figure assumes that
all offal and discarded organisms are consumed by
ICES Coop. Res. Rep. No. 232
seabirds – an assumption supported only by some discard
experiments (Garthe et al., 1996)). Discarding is not
uniform, thus different numbers of varying species might
be supported in separate parts of the North Sea. Garthe et
al. (1996) divided the offshore areas into six sub regions
(Figure 4.1).
The largest number of seabirds that could potentially be
supported by fishery waste is in sub region S
(1,500,000), followed by CE (1,200,000) and C
(1,100,000). Lower numbers might be supported by
fisheries in sub regions NW and NE (800,000 individuals
in each of the two regions) and CW (500,000) (Garthe et
al., 1996).
Additionally, the shrimp fishery in inshore waters off
Niedersachsen supports a large number of seabirds. The
consumed part of the shrimper discards represents an
energy value of 2.5 x 1013J per year (Walter and Becker,
1997). The mean daily energy demand of a 'model'
seabird (species energy demand may be weighed against
their relative frequency astern the shrimpers) amounts to
1,145 kJ or to 418,000 kJ/year. A total of 60,000 birds
may potentially have been supported by the discards of
the fleet off Niedersachsen in 1993.
In the south-eastern North Sea shrimp fishery,
consumption rates by mass were applied to the estimated
discard quantities. A total consumption of 27,000 tonnes
of all discard categories were calculated. The most
important scavenger species were herring gulls which
took 55% of all consumed discards, and black-headed
gulls (39%). Using standardised energy content of the
different discard categories (Walter and Becker, 1997)
the total amount consumed by seabirds represents an
energy value of 1.22 x 1014J. This amount of energy is
sufficient to support a potential number of about 340,000
birds (Table 4.5).
4.5
Direct effects of discard
consumption on species composition
of seabirds in the North Sea
4.5.1 Increase in population size of seabird
species
About 30% of total food consumed by seabirds in the
North Sea is estimated to be discards (including offal)
(Tasker and Furness, 1996). These foods are therefore of
direct importance in sustaining populations of some
seabirds. Furness and Hislop (1981) showed that discards
formed up to 70 % of the diet of adult great skuas
breeding in Shetland and 28 % of chick diet even when
their preferred prey, lesser sandeels Ammodytes marinus,
were abundant. When sandeel abundance declined in the
late 1980s, discards formed up to 82 % of adult diet and
77 % of chick diet (Hamer et al., 1991) (Table 4.6).
Breeding success was much reduced in the absence of
sandeels (Furness, 1987) and chick growth rate is
considerably reduced when the proportion of discards in
the diet is high (Table 4.7).
33
Table 4.4. Foods consumed by seabirds which scavenge discards in the North Sea (after Tasker and Furness, 1996 and Walter and
Becker, 1997).
Species
Discards and offal
Other food
Fulmar (summer)
30% offal, 30% discards
10% zooplankton, 30% sandeels
50% offal, 25% discards
25% zooplankton
Gannet
10% discards
30% sandeels, 30% herring, 30% mackerel
Great skua1
62% discards
26% sandeel, 10% birds, 2% other
Black-headed gull2
10% discards
50% other, 40% terrestrial food
Common gull2
10% discards
50% other, 40% terrestrial food
Lesser black-backed gull2
60% discards
40% other
Herring gull
10% offal, 30% discards
30% invertebrates, 30% terrestrial foods
Great black-backed gull
60% discards
20% sandeels, 20% other prey
(winter)
Kittiwake IVa W (summer)
(winter)
100% sandeels
25% offal, 25% discards
25% zooplankton, 25% sprat,
IVa E, IVb, IVc (summer)
(winter)
20% zooplankton, 60% sandeels, 20% sprat
25% offal, 25% discards
25% zooplankton, 25% sprat
Notes:
1. A 16 year average from non-breeding birds, based on studies on breeding grounds (Hamer et al., 1991).
2. Estimates from Arbouw and Swennen (1985), Dernedde (1993), Freyer (1995), Gorke (1990), Hartwig et al. (1990), Noordhuis
and Spaans (1992), Spaans et al. (1994).
Table 4.5. Total numbers of seabird that could theoretically be supported by discards and offal in the North Sea (offshore fisheries:
from Garthe et al., 1996; shrimp fisheries: Walther and Becker, 1997).
offshore fisheries
Fulmar
3,200,000
0
Gannet
210,000
0
21,000
0
0
204,000
84,000
7,000
Lesser black-backed gull
130,000
4,000
Herring gull
670,000
115,000
Great black-backed gull
250,000
0
1,300,000
0
0
9,000
5,900,000
339,000
Great skua
Black-headed gull
Common gull
Kittiwake
Common/arctic tern
Total
However, with the exception of these cases, there is
limited evidence that fishery waste forms the essential
part of the diet of any other population of seabirds.
Nevertheless, the availability of discards is believed to
affect feeding strategies of the scavengers. For instance,
Blaber et al. (1995) suspect that the greater availability
of discards of similar taxa may have led to greater
overlap in the diets of the seabird species of the Northern
Great Barrier Reef, Australia. Blaber et al. (1995) also
found that the diet of several species changed due to the
supply by discards, which has occurred also in the North
34
shrimp fisheries
Sea (e.g., Hudson, 1986; Camphuysen, 1993; Walter and
Becker, 1997). Since fisheries are carried out throughout
the study area and throughout the year, interrupted only
locally during gales and storms, one is rarely able to
demonstrate any effects of fishing activities on feeding
ecology and reproductive output of discard consumers.
This might be the reason for the weak link between
studies showing the utilisation of discards at sea and
studies focusing on possible effects of fishing
activities.The distribution of scavenging birds, both on
land and at sea, is affected by the availability of discards.
ICES Coop. Res. Rep. No. 232
Fishing activity strongly enhanced the number of
Audouin's gulls Larus audouinii resting on the
Columbrete Islands off east Spain (Castilla and Pérez,
1995), and herring and great black-backed gulls on
Helgoland, south-eastern North Sea (Geiss, 1994;
Hüppop, 1995).
Table 4.6. Food items in pellets produced by non-breeding great skua on Foula between 1 and 15 July, for the years from 1973 to
1989 except 1985 (from Hamer et al., 1991).
Year
n
sandeel (%)
Whitefish (%)
(mostly discard)
bird (%)
other (%)
1973
100
71
27
2
0
1974
100
24
71
5
0
1975
100
21
69
6
4
1976
100
72
26
2
0
1977
100
59
35
4
2
1978
100
64
35
1
0
1979
100
41
54
3
2
1980
100
17
74
6
3
1981
100
18
77
4
1
1982
100
13
80
3
4
1983
305
9
70
17
4
1984
100
0
74
23
3
1986
200
0
82
14
5
1987
98
9
77
10
4
1988
200
0
73
24
4
1989
247
4
62
30
4
Table 4.7. The relationship between an index of growth for skua chicks and the proportion of discards in their diet (data from Hamer
et al., 1991).
Year
% Discard
Chick growth
index
Year
1975
28
30
1983
2
3
1976
14
–18
1984
33
4
1977
14
0
1985
33
7
1978
24
28
1986
30
5
1979
24
26
1987
42
–44
1980
28
8
1988
77
–129
1981
6
–40
1989
76
–62
1982
5
15
The food provided by discards may be of importance
particularly during periods of low natural food
availability. There may therefore be positive effects on
body condition, survival (including overwinter survival)
of adult and sub-adult birds as well as on reproductive
parameters such as the onset of laying, egg size, clutch
size, chick growth, chick survival and breeding success.
ICES Coop. Res. Rep. No. 232
% Discard
Chick growth
index
Discards may lower the costs of reproduction for adults,
such that survival and the future reproductive potential
might increase.
Examples from the Mediterranean have documented
various effects of the availability of discards and offal on
breeding phenology, reproductive output, foraging range,
35
diet, activity and behavioural interactions of Audouin's,
yellow-legged Larus cachinnans and lesser black-backed
gulls breeding on the Ebro Delta, north-east Spain (e.g.,
Arcos and Oro, 1996; Oro, 1995, 1996; Oro and
Martinez-Vilalta, 1994; Oro et al., 1995, 1996; Ruiz et
al., 1996).
During the late 1980s, many seabirds in Shetland failed
to breed successfully due to low availability of sandeels.
Only one kittiwake colony (Eshaness) fledged chicks
successfully. This colony was mainly feeding on discards
(Hamer et al., 1993). Removal of fishing offal as a food
source has been shown to be associated with lagged
population declines in herring and great black-backed
gulls in the Gulf of St. Lawrence, Canada (Howes and
Montevecchi, 1992).
4.5.2 Population increase and changes in
composition of seabird communities
There have been considerable changes in the breeding
populations of seabird species in the North Sea during
the past century. There have further been changes in
species composition. While many species which
consume discards have increased their populations, it is
difficult to discriminate between the effects of discards
and other factors such as enhanced bird protection and
increased stocks of small fish. The populations of some
species groups, such as the terns, which had been the
most numerous species on the southern North Sea coasts
in the beginning of the century, have decreased in size
(e.g., Becker and Erdelen, 1987), which may be an
indirect effect of the increase in gull numbers.
The numbers of most scavenging seabird species
breeding in eastern Britain have increased markedly
since at least 1900 (Table 4.8). In the southern North
Sea, breeding numbers of offshore feeding seabirds such
as kittiwakes and fulmars have shown strong population
increases (e.g., kittiwakes: from a few pairs in the early
1950s to 7,460 pairs in 1995; Hüppop, 1995). Herring
gull numbers increased in Germany from about 7,000
pairs in 1910 to 45,600 pairs in 1995 (Vauk et al., 1989;
36
Hälterlein and Südbeck, 1996). Herring gulls in the
Netherlands increased from around 20,000 pairs in 1940
to 90,000 pairs in 1992 (Noordhuis and Spaans, 1992;
Dijk and Meininger, 1995). Lesser black-backed gulls
increased in the Netherlands from first breeding in the
Wadden Sea in 1926 to 34,200 pairs in 1992 (Dijk and
Meininger, 1995) with an additional 12,000 pairs in
Germany in 1995 (Hälterlein and Südbeck, 1996). Blackheaded gulls started to use the German Wadden Sea as
breeding area during the 1940s. Today this gull is the
most numerous seabird in the Wadden Sea (64,000 pairs
in Germany in 1995; Hälterlein and Südbeck, 1996;
170,000 pairs in the Netherlands in 1992, including
inland colonies; Dijk and Meininger, 1995).
Fisher (1953) and Tuck (1961) considered that the
discards of factory trawlers on the Grand Bank of
Newfoundland were responsible for the increase in
fulmars and kittiwakes in the British Isles prior to the
1950s.
Herring gulls and black-headed gulls are the main avian
consumers of the discards of the shrimp fishery. In
Denmark, herring gull numbers increased five years after
the development of the Danish fisheries (Møller, 1981).
From 1973 to 1982 both the landings of the German
shrimp fishery and the discards produced by the
shrimpers increased in parallel with the gull populations
(Figure 4.3). Thereafter the gull populations continued to
grow despite lower shrimp landings; possibly the amount
of fishing continued to increase, but the catch of
marketable shrimps per unit effort decreased with a
consequential increase in amounts of discards.
The increase in populations of discard-feeding seabirds
around the North Sea has changed the balance of seabird
communities towards these species. In the German
Wadden Sea in 1951, the gulls (herring, lesser blackbacked, common and black-headed) comprised 40% of
the seabird community (44,300 pairs) and terns
(common, arctic, Sandwich Sterna sandvicensis and little
S. albifrons) the remaining 60% (Becker and Erdelen,
1987). By 1995, gulls dominated the seabirds breeding
community with 83 % of the total (155,000 pairs)
(Hälterlein and Südbeck, 1996).
ICES Coop. Res. Rep. No. 232
Table 4.8. Numbers of pairs of scavenging seabirds breeding on North Sea coasts (Furness, 1992).
a) Northeast Britain (Shetland, Orkney, Caithness to Cruden Bay)
Year
Fulmar
Gannet
Great skua
Lesser
blackbacked gull
1900
600
3500
41
(3000)
(2000)
1910
1760
3500
82
(2000)
1920
5200
3500
193
1930
11600
3500
1940
28200
1950
Herring
gull
Great
blackbacked gull
Kittiwake
All species
(1000)
(26000)
(37000)
(3000)
(1500)
(34000)
(46000)
(1500)
(4000)
(2000)
(48000)
(64000)
429
(1500)
(5000)
(3000)
(68000)
(93000)
8000
745
(1500)
(10000)
(4000)
(90000)
(142000)
53000
8800
1350
(1500)
(20000)
(6000)
(120000)
(211000)
1960
66000
10000
2100
(1500)
40000
8000
160000
290000
1970
190000
14000
4000
1500
82000
9600
230000
531000
1980
280000
20000
6300
2500
43000
9900
210000
572000
1990
(350000
24000
7500
2500
40000
9900
180000
614000)
b) East coast of Britain from Cruden Bay to the Humber
Year
Fulmar
Gannet
Lesser
blackbacked gull
1900
0
2800
(2000?)
1910
0
3000
1920
20
1930
Great
blackbacked gull
Kittiwake
All species
(400?)
(10?)
(9000)
(14000?)
–
(800)
–
(12000)
(18000?)
3500
–
(1500)
–
(19000)
(26000?)
200
4100
–
(3000)
–
(28000)
(37000?)
1940
600
4400
–
6000
–
38000
(50000)
1950
1200
4800
4000
12000
30
50000
72000
1960
2000
6800
4000
23000
30
65000
101000
1970
5800
8100
4240
45100
31
106000
169000
1980
10000
20000
5000
40000
20
200000
275000
1990
(14000
24000
5300
35000
20
210000
288000)
ICES Coop. Res. Rep. No. 232
Herring
gull
37
Figure 4.3. Development of the gull populations in 28 areas along the German North Sea coast (Becker and Erdelen, 1987, P.H.
Becker, unpubl. data) and landings of edible shrimps of the fleets of Niedersachsen and Schleswig-Holstein (Tiews, 1983; Tiews and
Wienbeck, 1990; Anon., 1990/94) between 1968–1992 (from Walter and Becker, 1996).
4.6
Indirect effects of discard
consumption on species composition
of seabirds in the North Sea
The increase in population size of gulls supported by
discards may have negative effects of other species of
sea- and shorebirds. This may happen through various
mechanisms. Nesting gulls may physically displace other
species by occupying their habitat. Larger predatory
species may depredate smaller species taking eggs,
young and adults (Regehr and Montevecchi, 1996).
In the Wadden Sea the nesting habitat of shorebirds such
as plovers and oystercatchers has been invaded by large
gulls. Some breeding sites which are well suited for
nesting by habitat or food availability may no longer be
available for the terns because of the occupation by gulls
earlier in the season. The Wadden Sea islands of
Memmert and Mellum were important breeding sites for
terns at the start of this century – nowadays more than
10,000 pairs of herring gulls and no terns breed on these
islands (Becker and Erdelen, 1987). Howes and
Montevecchi (1992) describe a similar situation off
Canada.
Frequently, terns can only breed close to gulls, thus
increasing the probability of predation. Common terns
became re-established on Mellum at the end of the
1970s. This was not successful as herring gulls
depredated most tern chicks which led to very low
reproductive output for five years. Subsequently the
colony site was abandoned (Becker, 1995). There are
many other examples of reduced reproductive output of
38
small seabird species caused by gulls feeding on eggs or
chicks (e.g., Kruuk, 1964; Hatch, 1970; Montevecchi,
1977; Wanless, 1988; Hario, 1994; Thiel and Sommer,
1994; Russell and Montevecchi, 1996; Regehr and
Montevecchi, 1996).
In Shetland and Orkney, great skuas Catharacta skua
rely on discards and sandeels for most of their diet, but
will switch to killing other seabirds if sandeels and
discards are in short supply, threatening the viability of
some seabird populations (Furness, 1997; Heubeck et al.,
1997).
4.7
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Howes, L. A., and Montevecchi, W. A. 1992. Population
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the Ebro Delta, NE Spain. Ornis Fennica, 72: 154–
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41
5
Exploration of the short- and medium-term consequences of a reduction in
the amounts of fish discarded
M. L. Tasker1, P. H. Becker2 and G. Chapdelaine3
1
Joint Nature Conservation Committee, 7 Thistle Place, Aberdeen AB10 1UZ, U.K.
Institut für Vogelforschung, Vogelwarte Helgoland, An der Vogelwarte 21, D–26386 Wilhelmshaven, Germany.
3
Canadian Wildlife Service, 1141 route de l’Eglise, PO Box 10100, 9th floor, Ste-Foy, Quebec G1V 4H5, Canada.
2
5.1
Short term effects
5.1.1 Introduction
There are increasing pressures to further manage
fisheries in order to make them sustainable, to reduce
waste and to minimise collateral damage to the
environment. A reduction in the levels of discarding
seems almost inevitable through several possible
policies. Two possibilities seem likely to occur in the
near future, firstly, a general reduction in fishing effort
and hence a general reduction in discards, and secondly
an increase in the mesh size used in fishing gears. These
measures may have different effects on scavengers
(Furness, 1992; ICES, 1994; Hubold, 1994). Seasonal
and longer-term fishery-closures are also likely to occur,
as at present off Canada and Spain.
5.1.2 Loss of feeding opportunities
A general reduction in catch effort will probably lead to
more competition for available discards and larger and
stronger species would be more likely to benefit at the
expense of the smaller, weaker species. In other words,
kittiwake Rissa tridactyla, other small gulls, great skuas
Catharacta skua and fulmars Fulmarus glacialis
(Camphuysen et al., 1995) would suffer, while gannets
Morus bassanus would be relatively unaffected.
An increase in mesh size does not necessarily increase
the size of fish caught as fishermen may take
counteracting measures (Reeves et al., 1992). However,
if the purpose of this potential measure was to be met,
the proportion and amount of small-sized fish present in
discards would decrease considerably. Furness (1992)
calculated reductions in the mass of discarded whiting
Merlangius merlangus at 65%, while haddock
Melanogrammus aeglefinus discard would decrease by
52% if the mesh size increased from 90 to 120 mm in
North Sea fishing fleets. This increase would principally
reduce the small-sized discards (Furness, 1992). This
would lead to a deterioration of feeding opportunities for
the smaller gulls, such as black-headed gull Larus
ridibundus, common gull L. canus and kittiwake which
utilise the smallest discarded fish preferentially
(Camphuysen et al., 1993, 1995; Garthe and Hüppop,
1994).
42
Both measures could lead to reduced feeding
opportunities for immature individuals since adults are
generally more successful than immatures of the same
species (Wunderle, 1992), particularly if immatures
switch to less favourable lengths of discards (Garthe,
1993). Immatures, especially birds in their first year of
life, could suffer from higher mortality.
5.1.3 Change in bird distribution
All those species utilising fishery waste can be assumed
to be somewhat influenced by the distribution of fishing
vessels. Tasker et al. (1987) found positive spatial
correlations between many species including gulls, great
skuas and fulmars and the presence of trawlers.
However, there was substantial variability with respect to
season and area. Camphuysen et al. (1995) found that
great black-backed gulls Larus marinus, herring gulls L.
argentatus and lesser black-backed gulls L. fuscus (in
summer) were the only species which were clearly
positively influenced by the presence of fishing vessels.
There was no evidence of large-scale spatial correlations
between trawlers and fulmars (Camphuysen et al., 1995;
Camphuysen and Garthe, 1997)
Based on the above results, it is possible to speculate that
the distribution of large gulls would be most affected by
a change in fisheries effort whereas that of other species,
such as gannet, would be less affected.
5.1.4 Competition at trawlers
Discharges of fishery waste from fishing vessels attract
scavenging seabirds which compete for preferred items.
For several species of seabirds, the preferred size and/or
type of the discarded items overlaps and because the
numbers of ship-followers are often high, competition
for scraps is often intense. In the competition for the food
resources provided by fishing boats some seabirds are
more successful than others as shown by several studies
(e.g., Hudson and Furness, 1989; Camphuysen et al.,
1995). Different species employ different strategies for
obtaining discards and offal (e.g., Dändliker and
Mülhauser, 1988; Hudson and Furness, 1989;
Camphuysen, 1993; Walter and Becker, 1994;
Camphuysen et al., 1995). Small species, such as
kittiwake, have to catch and swallow prey items rapidly
to avoid interactions with other, physically stronger
ICES Coop. Res. Rep. No. 232
species. If these small species do not succeed with this
strategy they will often lose their prey to larger, more
aggressive, species.
high tide, when foraging sites are flooded (Veen, 1977).
Growth rates of tern chicks will be reduced, and the
breeding success lowered in kleptoparasitised species.
Gannets and great black-backed gulls are least vulnerable
to kleptoparasitism. For these high-ranking species,
kleptoparasitism is an effective strategy for obtaining
food. Large such as gannet, great black-backed gull and
great skua, are virtually absent during spring and summer
in the eastern and southern North Sea. Smaller species
such as fulmar and kittiwake do better when robbing
others in these regions and seasons. A reduction in total
quantities of discards produced and discharged in
commercial fisheries will probably lead to a higher
frequency of kleptoparasitic interactions. The implication
of these size-based dominance hierarchies is that small
species, such as kittiwake, other small gulls and fulmar
will suffer the most.
5.1.6 Reproduction
5.1.5 Changing diets
A reduction in the availability of, and increase in mean
size of, discards will lead to a switch in foraging methods
and diets in gulls. During the breeding season, herring
gulls would change their feeding areas and habits and
exploit food of lower energetic quality such as eggs and
chicks of its own and other species (Regehr and
Montevecchi, 1996). Interactions between Audouin's gull
Larus audouinii and yellow-legged gulls L. cachinnans
at the colony site increase during periods with no fishing
activity (Gonzalez-Solis, 1996). High densities of
breeders and low food supply increases cannibalism
among gulls (Parsons, 1971, 1976; Spaans et al., 1987;
Kilpi, 1989).
Investigations of a kittiwake colony on Great Island,
Newfoundland revealed complex relationships (Regehr
and Montevecchi, 1996). A four-week delay in the
inshore arrival of spawning capelin and a lack of fishery
waste due to the closure of the ground fishing industry in
eastern Newfoundland apparently led to food shortages
in herring gulls and great black-backed gulls. These
species were forced to switch to other prey, including
depredation of the eggs and chicks of kittiwakes. The
low availability of capelin Mallotus villosus (also an
important food of kittiwakes) and the high predation
pressure by herring gulls and great black-backed gulls
led to delayed breeding and led to extremely low
breeding success. They showed that kittiwake
reproductive success was a consequence of indirect and
interactive effects of food supplies on both parents and
predators.
Intra- and interspecific kleptoparasitic feeding may
increase at colonies owing to reductions in the
availability of discards. In windy conditions blackheaded gulls steal more sandeels Ammodytes spp. from
Sandwich terns Sterna sandvicensis than during calm
weather when their intertidal foraging is more successful
(Gorke, 1990). In addition, kleptoparasitism increases at
ICES Coop. Res. Rep. No. 232
Noordhuis and Spaans (1992) showed that as herring
gulls changed diet and obtained fewer discards, there was
a decrease in breeding success and numbers. Some
examples of the dependence of seabirds on fisheries
originate from the Mediterranean. Paterson et al. (1992)
describe severely reduced breeding success in two
Spanish colonies of Audouin's gulls in 1991 that resulted
from a fisheries moratorium (to preserve fish stocks)
during the gull's breeding season. Oro (1996) and Oro et
al. (1995, 1996) demonstrated that the breeding success
of Audouin's, yellow-legged and lesser black-backed
gulls differed significantly between years with different
trawling activity at the Ebro Delta, north-east Spain. The
three species of gulls compensated partly for the
cessation in food supply (discards) after a trawl
moratorium took place by switching to other types of
food. Other parameters of breeding and behaviour were
affected by the availability of fishery waste.
A long-term large-scale fishery moratorium in eastern
Canada has been associated with increased predatory
pressure by great black-backed gulls on kittiwakes and
Atlantic puffins Fratercula arctica, which has in turn
reduced breeding success (Russel and Montevecchi,
1996; Regehr and Montevecchi, 1996).
In summary, if food supply is reduced, reproduction can
be impaired in several ways. The numbers of nonbreeders can increase, the onset of laying can be delayed,
clutch size and egg size can decrease, and hatching
success, growth rate, fledging success and recruitment
can will be reduced (e.g., Pons, 1992). The weakened
condition of adults can lead to higher mortality and
lowered reproductive ability. Mortality of adult gulls,
which is highest during August after the breeding season
(Coulson et al., 1983), may increase due to lowered adult
condition caused by the lack of food from fisheries.
5.2
Medium term effects
5.2.1 Introduction
All effects listed above as short-term will tend to
continue into the medium and long-term if quantities of
waste discarded remain at a relatively low level. Several
further medium-term effects might be expected.
5.2.2 Population size of consumer species
Short-term reductions of reproductive success and
survival of the scavenging species owing to a discard
reduction will over time result in population decreases if
alternative foods are not available. The capacity of the
environment enhanced by the anthropogenic food
43
sources at sea will be lowered to more natural levels, and
the numbers of seabirds using discards and offal will
decline. But as gulls are opportunistic feeders,
individuals will respond by changing their scavenging
diet to other food sources, especially more terrestrial
prey and garbage (Gonzalez-Solis, 1996) and may
increase predation pressure on smaller seabird species.
Despite this shift, however, competition between
individuals could be stronger, so that populations may be
reduced anyway.
As an example, on the North Shore of the Gulf of St.
Lawrence the herring gull population decreased from
14,000 pairs in 1988 to 3,000 pairs in 1993 (Figure 5.1),
corresponding with a moratorium on cod fishing
(Chapdelaine and Rail, 1997). While kittiwakes are
considered to be a scavenging species, they could
compensate the lack of discard provisioning because
depredation by gulls will be less as gull populations
decrease (Howes and Montevecchi, 1992). In turn the
breeding success of smaller species should improve
(Regehr and Montevecchi, 1996).
5.2.3 Population size and species composition
During the first years of discard reductions, those species
preyed upon by the larger predatory and scavenging
species are likely to experience a population decline.
This could be through direct predation, or indirectly
through reduced reproductive output due to predation of
chicks and eggs. However, should the populations of the
larger predatory species also decline, there might be
some longer term recovery of the smaller species. The
competition for nesting sites will be less. In consequence
the quality of breeding sites for those species might
improve, and areas abandoned will be resettled. Terns,
for example, can reoccupy their former breeding sites
and populations can recover in the longer term. Overall,
in the absence of other influences, population sizes are
likely to settle to different equilibria than previously.
Furness (1992) estimated a reduction of scavenging
seabirds in Scotland by 500,000 individuals if the
demersal trawl mesh size were to be increased from 90 to
120 cm or if fishery effort was reduced by 30%.
Figure 5.1. Herring gull breeding numbers in sanctuaries on the North Shore of the Gulf of St. Lawrence in relation to total landings
of cod (assumed to provide an index of the quantities of offal and discards made available to seabirds) on the North Shore
Chapdelaine and Rail, 1997)
44
ICES Coop. Res. Rep. No. 232
5.3
References
Camphuysen, C. J. 1993. Een verkennend onderzoek: De
exploitatie van op zee overboord geworpen vis en
snijafval door zeevogels. Het Vogeljaar, 41: 106–
114.
Camphuysen, C. J., Calvo, B., Durinck, J., Ensor, K.,
Follestad, A., Furness, R. W., Garthe, S., Leaper, G.,
Skov, H., Tasker, M. L., and Winter, C. J. N. 1995.
Consumption of discards by seabirds in the North
Sea. Final report EC DG XIV research contract
BIOECO/93/10. NIOZ–Report 1995–5, Netherlands
Institute for Sea Research, Texel. 202 pp.
Camphuysen, C. J., and Garthe, S. 1997. Distribution and
scavenging habits of northern fulmars in the North
Sea. ICES Journal of Marine Science, 54: 654–683.
Chapdelaine, G., and Rail, J.-F. 1997. History of the
herring gull on the north shore of the Gulf of St.
Lawrence and its relationship with fisheries. ICES
Journal of Marine Science, 54: 708–713.
Coulson, J. C., Monaghan, P., Butterfield, J., Duncan, N.,
Thomas, C., and Shedden, C. 1983. Seasonal changes
in the herring gull in Britain: weight, moult and
mortality. Ardea, 71: 235–244.
Howes, L. A., and Montevecchi, W. A. 1992. Population
trends of gulls and terns in Gros Morne National
Park, Newfoundland. Canadian Journal of Zoology,
71: 1516–1520.
Hubold, G. 1994. Maßnahmenkatalog für eine
ausgewogenere und rationellere Bewirtschaftung der
von
der
deutschen
Fischerei
genutzten
Fischereiressourcen im EG Meer. Informationen zur
Fischwirtschaft, 41: 3–18.
Hudson, A. V., and Furness, R. W. 1989. The behaviour
of seabirds foraging at fishing boats around Shetland.
Ibis, 131: 225–237.
ICES 1994. Report of the Working Group on ecosystem
effects of fishing activities. ICES, C.M.
1994/Assess/Env:1. 109 pp.
Kilpi, M. 1989. The effect of varying pair numbers on
reproduction and use of space in a small herring gull
Larus argentatus colony. Ornis Scandinavica, 20:
204–210.
Noordhuis, R., and Spaans, A. L. 1992. Interspecific
competition for food between herring Larus
argentatus and lesser black-backed gulls L. fuscus in
the Dutch Wadden Sea area. Ardea, 80: 115–132.
Dändliker, G., and Mülhauser, G. 1988. L'exploitation
des déchets de chalutage par les oiseaux de mer au
large des Orcades et des Shetland (Nord-Est
Atlantique). Nos Oiseaux, 39: 257–288.
Oro, D. 1996. Effects of trawler discard availability on
egg laying and breeding success in the lesser blackbacked gull Larus fuscus in the western
Mediterranean. Marine Ecology Progress Series, 132:
43–46.
Furness, R. W. 1992. Implications of changes in net
mesh size, fishing effort and minimum landing size
regulations in the North Sea for seabird populations.
JNCC report No. 133. Joint Nature Conservation
Committee. Aberdeen. 62 pp.
Oro, D., Bosch, M., and Ruiz, X. 1995. Effects of a
trawling moratorium on the breeding success of the
yellow-legged gull Larus cachinnans. Ibis, 137: 547–
549.
Garthe, S. 1993. Quantifizierung von Abfall und Beifang
der Fischerei in der südöstlichen Nordsee und deren
Nutzung durch Seevögel. Hamburger avifauniatische
Beitrage, 25: 125–237.
Oro, D., Jover, L. and Ruiz, X. 1996. Influence of
trawling activity on the breeding ecology of a
threatened seabird, Audouin's gull Larus audouinii.
Marine Ecology Progress Series, 139: 19–29.
Garthe, S., and Hüppop, O. 1994. Distribution of shipfollowing seabirds and their utilization of discards in
the North Sea in summer. Marine Ecology Progress
Series, 106: 1–9.
Parsons, J. 1971. Cannibalism in herring gulls. British
Birds, 64: 528–537.
Gonzalez-Solis, J. 1996. Interspecific relationships
between two species of gulls breeding sympatrically:
Larus audouinii and L. cacchinans. Thesis,
University of Barcelona.
Gorke, M. 1990. Die Lachmöwe (Larus ridibundus) in
Wattenmeer
und
Binnenland.
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verhaltensökologischer Vergleich. Seevögel, 11,
Supplement 3: 1–48.
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Parsons, J. 1976. Nesting density and breeding success in
the herring gull Larus argentatus. Ibis, 118: 537–546.
Paterson, A. M., Martinez Vilalta, A., and Dies, J. I.
1992. Partial breeding failure of Audouin's gull in
two Spanish colonies in 1991. British Birds, 85: 97–
100.
Pons, J. M. 1992. Effects of changes in the availability of
human refuse on breeding parameters in a herring
gull Larus argentatus population in Brittany, France.
Ardea, 80: 143–150.
45
Reeves, S. A., Armstrong, D.W., Fryer, R.J. and Coull,
K.A. 1992. The effect of mesh size, cod-end
extension length and cod-end diameter on the
selectivity of Scottish trawls and seines. ICES Journal
of Marine Science, 49: 279–288.
Regehr, H. M., and Montevecchi, W.A. 1996. Interactive
effects of food shortage and predation on breeding
failure of black-legged kittiwakes: effects of fisheries
activities and implications for indicator species.
Marine Ecology Progress Series, 155: 249–260.
Russell, J. O., and Montevecchi, W.A. 1996. Predation
on adult puffins Fratercula arctica by great blackbacked gulls Larus marinus at a Newfoundland
colony. Ibis, 138: 791–794.
Spaans, A. L., de Wit, A. A. N., and van Vlaardingen, M.
A. 1987. Effects of increased population size in
herring gulls on breeding success and other
parameters. Studies in Avian Biology, 10: 57–65.
46
Tasker, M. L., Webb, A., Hall, A. J., Pienkowski, M. W.,
and Langslow, D.R. 1987. Seabirds in the North Sea.
Nature Conservancy Council, Peterborough. 336 pp.
Veen, J. 1977. Functional and causal aspects of nest
distribution in colonies of the Sandwich tern (Sterna
s. sandvicensis Lath.). Behaviour Supplement, 20: 1–
193.
Walter, U., and Becker, P. H. 1994. The significance of
discards from the brown shrimp fisheries for seabirds
in the Wadden Sea – preliminary results. Ophelia
Supplement, 6: 253–262.
Wunderle, J. M., Jr. 1992. Age-specific foraging
proficiency in birds. Current Ornithology, 9: 273–
324.
ICES Coop. Res. Rep. No. 232
6
Evidence for decadal scale variations in seabird population ecology and
links with the North Atlantic Oscillation
J. B. Reid1, P. H. Becker2 and R. W. Furness3
1
Joint Nature Conservation Committee, 7 Thistle Place, Aberdeen AB10 1UZ, U.K.
Institut für Vogelforschung, Vogelwarte Helgoland, An der Vogelwarte 21, D–26386 Wilhelmshaven, Germany.
3
Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, U.K.
2
6.1
Introduction
The North Atlantic Oscillation (NAO) has an influence
not only on the physical oceanography of the North
Atlantic (Levitus et al., 1994; Hurrell, 1995; see also
Web site 1), but also on zooplankton (Fromentin and
Planque, 1996) and fish (Friedland et al., 1993). Thus an
influence of the NAO on higher trophic levels of the
North Atlantic and North Sea may be anticipated.
Seabirds characteristically have high adult survival rates
and deferred maturity, coupled with low reproductive
rates. Thus we may expect some parameters of the
ecology of seabird populations to be buffered against
such environmental fluctuations. In particular, we can
predict that breeding numbers may not respond to the
NAO or may show a long time-lag in response, whereas
breeding success might correlate with the NAO as a
consequence of its influence on preferred prey
populations of the seabirds.
Studies of seabird populations in the California Current
(Ainley et al., 1995) demonstrated that the El NinoSouthern Oscillation (ENSO) caused spectacular changes
in food supply to seabirds, leading to correlations
between seabird breeding parameters and variation in the
Southern Oscillation and/or the Aleutian low pressure
system, both of which affect sea-surface temperature and
thermocline depth. Some seabird species showed
stronger links than others with these physical parameters.
Cormorants and gulls showed stronger variations in
breeding success than did common guillemots Uria
aalge, as might be anticipated given the smaller clutch
size and the greater volume of sea used by foraging
common guillemots.
Montevecchi and Myers (1997) attributed a century-long
increase in northern gannet Morus bassanus numbers in
Newfoundland with warming surface water conditions
and increased availability of mackerel Scomber
scombrus. A major dietary change during the 1990s to
colder-water conditions in the north-west Atlantic led to
a change in prey stocks from warm-water pelagic fish
and squid to cold-water fish. In this report we have
concentrated our efforts on searching for any evidence
that the NAO influences numbers or breeding ecology of
seabirds in the north-east Atlantic. Our analysis is
constrained by the fact that, while there are data sets for
seabird breeding numbers over many decades, data on
breeding success or diet at particular sites rarely provide
more than a run of 10 years, and most sets start during
the 1970s or 1980s.
ICES Coop. Res. Rep. No. 232
6.2
Materials and methods
Four data-sets, or extracts therefrom, were used in
bivariate correlation analyses to detect possible
associations between the NAO and aspects of seabird
breeding ecology.
The UK Seabird Monitoring Programme (Thompson et
al., 1996) monitors seabird populations at several
colonies around the coasts of Great Britain and Ireland.
In addition to breeding numbers and overall success,
various detailed aspects of breeding performance are also
measured, mainly at four key sites. Data on breeding
numbers and breeding success of several species from a
selection of years (between 1986 and 1996) and colonies
were used in the analyses.
The second data-set on bird populations used includes
breeding numbers of various species nesting along the
coast of the German Wadden Sea and Helgoland. This is
a long term data-set, which, for some species dates from
1950 (Becker and Erdelen, 1987; Südbeck and
Hälterlein, 1997; and unpublished data of Becker, Verein
Jordsand and Institut für Vogelforschung). The third
seabird data-set used in the analyses was numbers of
breeding pairs and breeding success of common terns
Sterna hirundo between 1981 and 1997 on Minsener
Oldeoog, an island in the German Wadden Sea (Becker,
1998).
Data on the NAO were slightly amended from Hurrell
(1995). The winter (December through March) NAO
index was used and is based on the difference of
normalised sea level pressures (SLP) between Lisbon,
Portugal and Stykkisholmur, Iceland. The SLP anomalies
at each station were normalised by division of each
seasonal pressure by the long term (1864–1983) standard
deviation.
6.3
Results
No significant correlations were found between the NAO
index and breeding population sizes or breeding success
of various species breeding at several UK seabird
colonies (Tables 6.1 and 6.2). In addition, correlations
between breeding success of kittiwakes Rissa tridactyla
for seven or more years between 1986 and 1996 at 49
colonies in Britain and Ireland and the NAO gave 31
negative and 18 positive correlations.
47
Table 6.1. Relationships between seabird breeding numbers at various UK seabird colonies and the NAO Index. Pearson correlation
coefficients, r, are presented with associated p values. All correlations are non-significant.
Species
Sites
Dates
Guillemot
Razorbill
Skomer, Isle of May,
Skomer, Isle of May
Puffin
Isle of May
r
p
1986–96
1986–96
.051
.165
.883
.629
1983–1993
.142
.738
Table 6.2. Relationships between seabird breeding success at various UK seabird colonies and the NAO Index. Pearson correlation
coefficients, r, are presented with associated p values. All correlations are non-significant.
Species
Sites
Dates
r
p
Fulmar
Fulmar
Fair Isle, Shetland
Isle of May, SE Scotland
1986–96
1986–96
–.058
.088
.866
.796
Fulmar
Fulmar
Farne Islands, NE
1986–96
–.258
.445
Troswick Ness, Shetland
1986–96
.351
.290
Gannet
Fair Isle, Shetland
1986–96
.415
.204
Gannet
Noss, Shetland
1986–96
–.169
.620
Gannet
Bempton, NE England
1986–96 (excluding 1985)
–.087
.812
Shag
Canna, NW Scotland
1986–96
–.239
.480
Shag
Fair Isle, Shetland
1986–96
.141
.678
Shag
Isle of May, SE Scotland
1986–96
–.262
.437
Kittiwake
St. Kilda, NW Scotland
1986–96 (excluding 1995)
–.397
.256
Kittiwake
Isle of May, SE Scotland
1986–96 (excluding 1987)
.076
.834
Guillemot
Fair Isle, Shetland
1987–96
–.237
.510
Guillemot
Isle of May, SE Scotland
1986–96
.082
.810
Razorbill
Isle of May, SE Scotland
1986–96
.369
.265
Table 6.3. Relationships between seabird breeding numbers on the German Wadden Sea coast and the NAO Index. Pearson
correlation coefficients, r, are presented with associated p values. An asterisk (*) indicates statistical significance.
Species
Dates
Fulmar
most years, 1953–96
.371
.022 *
Cormorant
1971–96
.183
.370
Herring gull
most years, 1950–93
.456
.004 *
Lesser black-backed gull
most years, 1950–93
.480
.002 *
Common gull
most years, 1950–93
.566
.000 *
Kittiwake
most years, 1953–96
.423
.008 *
Black-headed gull
most years, 1950–93
.565
.000 *
Sandwich tern
most years, 1909–96
.264
.015 *
Arctic tern
various, 1982–96
.316
.317
Common tern
various, 1982–96
.485
.156
Arctic/common tern
most years, 1950–93
.145
.385
Guillemot
most years, 1953–96
.536
.001 *
Razorbill
most years, 1953–96
.414
.010 *
48
r
p
ICES Coop. Res. Rep. No. 232
Table 6.4. Relationships between common tern breeding numbers and success on Minsener Oldeoog, German Wadden Sea, and the
NAO Index between 1981 and 1997. Pearson correlation coefficients, r, are presented with associated p values. Both correlations are
non-significant.
Measure
r
p
No. Breeding pairs
.233
.368
Chicks fledged per pair
.252
.329
Four were significant at the 5% level, two of these were
positive and two were negative correlations. We
conclude from this result that there is no reason to
believe that the factors that the NAO index represents
affects kittiwake breeding success.
NAO index is unlikely in the case of the black-headed
gull, as unlike the other species considered, the blackheaded gull is not closely linked with fish foods gathered
at sea, but feeds mainly on Nereis in the Wadden Sea,
and additionally inland (Gorke, 1990).
No significant relationship was found between the NAO
index and breeding numbers of cormorant, Arctic tern or
common tern in the German Wadden Sea as a whole.
However, there were significant associations between the
NAO and numbers of other breeding seabirds here
(Table 6.3). In some cases, the relationship was very
strong.
If the common cause of recent seabird population
increases (the Dutch and German Wadden Sea data
indicate that these date from the 1970s) is not the NAO
then a more local explanation need be sought. It is likely
that the general, sustained increase is due to recovery of
these populations following a major pollution incident in
the Dutch and German parts of the Wadden Sea in the
late 1960s when large amounts of organochlorine
pesticides contaminated these waters from the Rhine
river (Becker, 1991). The immediate effect of this was
widespread mortality of seabirds in the Wadden Sea
resulting in depressed population sizes, from which there
has been a gradual increase in breeding seabirds. This
population recovery has coincided with an increase in
strength of the NAO since the 1970s but there remains
no evidence of a causal link between the two.
No correlation was detected between either breeding
numbers or breeding success of common terns on
Minsener Oldeoog in the German Wadden Sea and the
NAO (Table 6.4).
6.4
Discussion
No correlations were found between the breeding success
of seabirds and the NAO index during the last decade. As
expected, no significant relationships were found
between numbers of seabirds breeding around the UK.
Significant correlations were detected, however, between
breeding numbers of fulmar Fulmarus glacialis, herring
gull Larus argentatus, common gull L. canus, lesser
black-backed gull L. fuscus, black-headed gull L.
ridibundus,
kittiwake,
Sandwich
tern
Sterna
sandvicensis, razorbill Alca torda and guillemot on the
German coast, and the winter NAO index.
That so many significant correlations should be found
between breeding numbers and the NAO when no
relationship was suspected, is puzzling. Such a finding
would be expected if high correlations also existed
among population sizes of these species. Indeed, such
high, positive correlations do prevail among population
levels of all these species (all pairwise Pearson
correlation coefficients, r>0.75, p<0.001). This indicates
that a common factor may account for the observed
results. Such a common factor, of course, could be the
influence of the NAO on food resources. However, the
feeding requirements and general feeding ecology of
those species involved is so diverse as to render this
unlikely. Furthermore, if the NAO were to contribute to
processes underlying seabird population patterns, then
seabird life history parameters would lead to the
expectation that there would be a time lag in the
manifestation of NAO effects. An identical effect of the
ICES Coop. Res. Rep. No. 232
6.5
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Web site 1: http://www.clivar.ucar.edu/vol2/pdl.html –
The North Atlantic Oscillation (NAO)
ICES Coop. Res. Rep. No. 232
7
A review of the causes, and consequences at the population level, of mass
mortalities of seabirds
C. J. Camphuysen1, P. J. Wright2, M. Leopold, O. Hüppop2 and J. B. Reid3
1
Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands.
Fisheries Research Services, Marine Laboratory, P.O. Box 101 Victoria Road, Aberdeen AB11 9DB, United Kingdom.
3
IBN-DLO, P.O. Box 167, 1790 AD Den Burg, Texel Netherlands.
4
Vogelwarte Helgoland, PO Box 1220, D–27494 Helgoland, Germany.
5
Joint Nature Conservation Committee, 7 Thistle Place, Aberdeen AB10 1UZ, U.K.
2
7.1
Introduction
Of the millions of seabirds that die of natural causes each
year only a small proportion come ashore. However,
public attention and concern is often drawn to the
frequent large strandings of dead or moribund birds
washed up on beaches. These “wrecks” may reflect mass
mortalities of seabirds at sea, but are in fact defined as
any much larger than usual concentration of seabird
corpses washed ashore over a short period. The
definition must be applied relative to the population sizes
of the species concerned (perhaps considering only that
part of the population within a local area from which the
wrecked birds probably originate). ‘Large’ numbers of
an uncommon species may qualify as a wreck whereas
‘large’ numbers of a very common species might not.
There is rarely any indication from the size of wrecks of
the total mortality of birds at sea. Mass mortalities that
do not result in wrecks are, by their very nature, difficult
to study. The numbers and even species of bird involved
may only be ascertained by the subsequent effect on the
size of breeding populations. However, wrecks of
seabirds are recorded sufficiently frequently to enable
some, usually qualitative, consideration of their likely
causes, seasonality and possible effects on population
levels. This section reviews the major causes of seabird
wrecks, their seasonal occurrence and the relative
vulnerability of various species to different causal
agents.
7.2
Presumed causes
Wrecks can be explained by several factors. These
include those related to weather (for example storms,
calm conditions, severe cold), food, pollution (for
example oil spills, chronic oil pollution, chemical
polllution), fishing activities (for example bycatch) and
parasites. The most frequent causes are those due to
storms, oil, severe cold weather, and food. Other, less
commonly cited, causes include chemical pollution,
toxins, calm weather, diseases and parasites. In many
cases wrecks cannot be identified as being due to one
single cause. For example, adverse weather conditions
may affect foraging behaviour and success and may be
indirectly responsible for a wreck of emaciated birds.
However, in the following treatment we distinguish
between the above categories and food related causes per
se.
ICES Coop. Res. Rep. No. 232
Storm-related wrecks are those in which mortality has
been linked with birds being blown away from favoured
feeding areas or being prevented from feeding by wind.
Calm weather in summer has been associated with
wrecks of fulmars Fulmarus glacialis (Anonymous,
1982; Camphuysen, 1989a), possibly as a result of
increased energetic costs associated with flapping flight
in these birds which are adapted for gliding in the wind
(Furness and Bryant, 1996). Oil-related wrecks may be
divided into those related to major oil pollution incidents
or to chronic oil pollution. Effects on birds of both types
tend to be physical, disabling the birds through plumage
saturation and subsequent hypothermia and also
physiological through the toxic effects of oil. Major oil
incidents are widely reported because the events
engender public awareness (major ship-wreck, blowout), from which stranded birds are easily detected.
Chronic oil pollution is a constant process, a more severe
threat to seabirds because of a mosaic of larger and
smaller oil slicks which reduces the quality of the areas
where seabirds live, most notably around busy shipping
lanes and near larger harbours. Oil-related wrecks are
relatively well studied, because the effects of oil
pollution on seabirds has attracted attention of the
ornithological community since the end of the 19th
century (Bourne, 1969; Camphuysen, 1989a). Beached
bird surveys are an appropriate method of identifying
trends in oil contamination of stranded birds, but not
(necessarily) in identifying trends in mortality patterns of
seabirds (Heldt, 1969; Joensen, 1972; Kuyken, 1978;
Vauk, 1978; Becker and Schuster, 1980; Commecy,
1982; Stowe, 1982; Heubeck, 1987; Vauk et al., 1990,
1991; Camphuysen and van Franeker, 1992;
Camphuysen, 1995a; Heubeck, 1995).
Food-related wrecks are those where mortality results
from starvation due to the birds' not being able to forage
successfully, either through low food availability or
abundance. Seabird mass strandings (and also large scale
fluctuations in wintering distribution of seabirds) may be
indicative of changes in prey stock abundance,
distribution or availability. In the early 1980s, a major
south and eastward shift in the wintering distribution of
common guillemots Uria aalge, kittiwakes Rissa
tridactyla and razorbills Alca torda occurred in the North
Sea. This was consistent with a decline in sprat Sprattus
sprattus availability in the northern North Sea (Corten,
1990), sprats being a major prey species of these birds in
winter. The change in the pattern of sprat distribution
together with poor weather was implicated in a wreck of
51
auks along the east coast of Britain in February 1983
(Blake, 1984), and multiple wrecks in the southern North
Sea (Camphuysen, 1981, 1989b, 1990a,b,c,d, 1992,
1995a,b; Camphuysen and Keijl, 1994).
The rapid decline in Barent Sea capelin Mallotus villosus
during the 1980s provides an even more dramatic
example of a starvation induced wreck. Thousands of
emaciated common guillemots were washed ashore
along the coasts of Finnmark during the winter 1986/87,
and breeding populations in the Barents Sea collapsed,
coincident with the decline of this important prey (Vader
et al., 1987).
Fishing has often been alleged to be a contributory factor
in wrecks of emaciated birds, due to the common
utilisation of many small fish species by seabirds and
fisheries. For example, concern was expressed that the
sandeel Ammodytes marinus fishery off the east coast of
Scotland may have been involved in the large wreck of
auks and shags Phalacrocorax aristotelis along the east
coast of British in February, 1994. The wreck occurred
over a far more extensive region than the area where the
fishery operated, but it is typical of wrecks that seabirds
affected disperse beyond their normal distribution. There
are inadequate data to attribute a cause, beyond
starvation, to this particular wreck. Wrecks due to
bycatch in fishing nets of various sorts (set nets, gill nets)
are locally important (e.g., Robins, 1991).
Other, apparently less common, causes of seabird wrecks
include mortality due to natural toxins (for example
botulism, red tides, paralytic shellfish poisoning).
Botulism may hit coastal seabirds that utilize freshwater
bodies for drinking or bathing in summer, but as yet
there is little evidence that this is a major problems for
seabirds except at a local scale (Sutcliffe, 1986).
Epizootics, involving e.g., Noctiluca in red-tides have
been reported to kill a variety of seabirds (Coulson et al.,
1968; Armstrong et al., 1968; Wrånes, 1988). Toxins
inducing paralytic shellfish poisoning are known to
affect gulls in the USA that take contaminated shellfish
(Kvitek, 1991) and there are suggestions that such
poisoning might be responsible for recent die-offs of
common guillemots in the Baltic (Hario, 1994).
Occasionally, other less common factors may cause
wrecks. For example, the production of an oily substance
by a plankton bloom of Coscinodiscus concinnus in the
southern German Bight in spring 1996 resulted in
strandings of red-throated divers Gavia stellata, due to
plumage contamination (Camphuysen, 1997).
7.3
Frequency and seasonal occurrence
of wrecks
An initial literature search led to identification of over
100 wrecks, or events, in European waters, and a very
incomplete list of events elsewhere in the world. Wrecks
were roughly classified as:
52
•
pollution related wrecks (e.g., oil, chemicals,
netting)
•
weather related wrecks (e.g., storm, calm or cold
weather)
•
food related wrecks
•
other types.
It needs emphasizing that the effect of severe winters on
marine and estuarine birds is not fully addressed here,
although it is an important factor behind mass mortality.
Several case studies indicated that very large numbers of
seabirds can suffer from cold stress and starvation in
association with severe winter weather (Crisp, 1964;
Schoennagel, 1980; van Gompel, 1987; Meininger et al.,
1991; Suter and van Eerden, 1992; Beukema, 1994;
Camphuysen et al., 1996). The literature search of this
subject was not completed for this review. The very long
lists of smaller and larger scale oil-related wrecks which
have been published in association with accounts dealing
with marine oil pollution are not repeated in Appendix
7.1 (Bourne, 1969; Vermeer and Vermeer, 1974; Stowe
and Underwood, 1984; Hooper et al., 1987;
Camphuysen, 1989a; Camphuysen and van Franeker,
1992; Camphuysen, 1995b). Large numbers of recently
fledged birds occasionally wash up dead near their
colonies. These post-fledging incidents appear to be
relatively common,, but are not often reported (Jones,
1980). Post-fledging wrecks can only be studied after
having set clear criteria from which 'wrecks' (as
unusually large numbers of birds which died) may be
separated from the background noise.
Wrecks, as described earlier, were identified in the first
place through stranded birds and influxes of birds in
areas where they do not normally occur in large
numbers. Some of these birds showed clear symptoms of
the cause of the event. However, the mass mortalities as
a result from drowning and entanglements in fishing gear
are not easily attributed if the cause of death was not
found (i.e. the net in which the birds had drowned). In
the literature, or more commonly before the stage on
which things get written up, there is frequently
considerable speculation as to why such birds had died
(good condition, non-oiled, no adverse weather, but still
dead in large numbers). Although such events were
possibly caused by netting incidents, a firm conclusion as
to the cause cannot be reached. While we are aware of
several areas in which potential 'conflicts' between
seabirds and fishermen in terms of unwanted bycatch of
birds exist, there is very little factual evidence available,
and several wrecks in such areas may have been misinterpreted. Post-mortem analysis might help in
confirming drowning as the cause of death.
It is important to stress that an analysis of wrecks such as
this is inherently biased towards scarce species, and in
other words to the relatively rare ‘more interesting’
events. Strandings of common birds are often taken for
granted and do not become subject of further study or be
ICES Coop. Res. Rep. No. 232
published in the ornithological literature. As a result, a
thorough literature search will lead to a relatively
complete picture of little auk wrecks (Camphuysen and
Leopold, 1996; Stenhouse and Montevecchi, 1996), but a
very incomplete idea of e.g., post-fledging mortality in
herring gulls Larus argentatus. Phalarope strandings will
be reported even if only very few individuals were
found, whereas common guillemot strandings get noticed
only when many hundreds wash ashore over short
lengths of coast.
A conclusion which might be drawn is that some (causes
of) wrecks get more attention than others because the
underlying factors are more obvious. In the absence of
adequate data relating to the underlying factors of most
(reported) mass-strandings of seabirds, this analysis
should only be considered as a first attempt to discuss
wrecks. It is not possible at present to reach firm
conclusions as to which species are more vulnerable than
others and as to what type of wrecks most affect seabird
populations.
A final aspect which needs to be addressed before the
frequency of wrecks is discussed is the possible overlap
of cause of wrecks, or the accumulating effect of a
number of factors which lead to mass mortality. Where
we refer to storm-driven or food-related wrecks,
starvation of the birds found dead is a key point, while
strong winds were more obvious in the first type. It is
easy to understand that while wind may have been an
important factor in reducing the availability of food for
certain species, a wind-driven event may be also foodrelated. It has been suggested that starving birds are also
more susceptible to the effects of oil pollution, while
netting as a factor behind mass mortality of auks in the
Skaggerak region had increased after a displacement of
wintering auks due to poor feeding conditions in their
more usual wintering areas (Peterz and Oldén, 1987).
From our first analysis, oil-related and storm driven
wrecks occur very frequently. A preliminary search of
the literature revealed 30 events of the former type and
41 of the latter in a list which only took account of major
events (Appendix 7.1). On the scale of the north-east
Atlantic, both types of wrecks probably occur annually,
but many have a local or regional character. Oil-related
wrecks include those caused by shipping accidents and
blow-outs, but very many more small wrecks occur as a
result of chronic oil pollution due to deliberate,
operational discharges of oil. Storm-driven events
overlap with 17 wrecks that were temporarily labelled as
'food-related', because both types comprise stranded
birds that were seriously emaciated and apparently died
as a result of starvation (see above). Fewer wrecks
appeared to have been related to bycatch of seabirds in
fishing nets (7), parasites (3), chemical pollution (2),
exceptionally calm weather (2), plankton bloom (1).
Wrecks did not occur evenly over the year, and different
types of wrecks appeared associated with different
seasons (Tables 7.1, 7.2). Obviously, post-fledging
wrecks of young birds and wrecks due to cold-stress
ICES Coop. Res. Rep. No. 232
occurred in one season only, being late summer and
winter respectively. Food-related and storm-driven
wrecks were basically autumn and winter phenomena.
Oil-related wrecks occurred through the year, but
incidents due to chronic oil pollution were concentrated
in the half year spanning winter (Bourne, 1969; Stowe
and Underwood, 1984; Camphuysen, 1989a). An overall
conclusion of this first inventory of wrecks is that the
types of mass-mortality events which are considered here
occur seldom in summer, and most frequently in autumn
and winter.
Little auk Plautus alle wrecks and influxes, which were
studied in considerable detail, occurred rather frequently,
but not randomly during the last odd 150 years
(Camphuysen and Leopold, 1996). In Europe, over 60
influxes/wrecks were recorded since 1840, but these
events appeared to occur in clusters (Runs test, ts = –
2.30, n1 = 62, n2 = 94, P< 0.05). A detailed analysis of
the most recent influxes demonstrated that the events
were in fact related to major shifts in wintering
distribution of little auks. Hence, wrecks may occur if the
North Sea is used as a wintering area and not, or not be
recorded, when the birds were wintering elsewhere.
These wrecks were often wind-related, and stormy
weather usually suggested as the cause of the wreck,
however several little auk influxes and wrecks took place
under calm conditions.
7.4
Vulnerability of seabird species to
wrecks
Most species of seabird are subject to wrecking (Tables
7.2, 7.3) but some are more vulnerable than others. For
example, auks tend to be wrecked more often than
Procellariiformes while grebes are rarely wrecked. Of
course there is variation in the degree to which different
species and groups of species are vulnerable to different
types of wreck, their preferred food (fish/plankton) being
one component of this variability.
Species have different vulnerabilities towards the
different causes of wrecks (Table 7.3). Birds spending
long time swimming such as divers, grebes, duck and
auks are especially vulnerable towards oil pollution
(Stowe, 1982; Averbeck et al., 1993; Camphuysen,
1989a, 1995b, 1997, Williams et al., 1994), whereas
small species that spend a higher proportion of their time
flying may be wrecked as a consequence of severe
storms, e.g., storm petrels, fulmar, kittiwake, little auk
(Pashby and Cudworth, 1969; Threlfall et al., 1974;
Doumeret, 1979, 1980; Nakamura, 1983; Teixeira, 1987;
Camphuysen and Leopold, 1996). For species that rely
on gliding rather than flapping,, the energy expenditure
at sea increases with decreasing wind speed (Furness and
Bryant, 1996), hence they may run into energetic
bottlenecks during periods of calm weather which may in
time end in a wreck. Diving birds are especially
vulnerable to entanglement and drowning in fishing gear
(Brewka et al., 1978, 1985, 1989; Barrett and Vader,
1984; van Eerden and Bij de Vaate, 1984; Peterz and
Oldén, 1987; Kies and Tomek, 1990; Hüppop, 1996).
53
Table 7.1. Frequency distribution of different types of North Atlantic wrecks in different seasons (see Appendix 7.1 for a list of
wrecks).
Category
Type
Pollution
oil
summer
Autumn
9
1
5
winter
30
chemicals
2
2
bycatch
7
7
1
1
storm
24
cold
calm
1
Other
food’adults’
1
post-fledging
1
parasites
2
unknown
Totals
17
41
4
4
1
2
winddrift
Food
Totals
15
plankton
Weather
spring
2
1
1
14
17
1
1
2
1
1
13
7
32
3
4
61
113
Table 7.2. Frequency distribution of wrecks in the North Atlantic for different groups and species of birds (see Appendix 7.1 for a
list of the wrecks; review papers and non-European wrecks were excluded for this analysis).
Species/group
spring
divers
1
grebes
1
summer
Autumn
1
storm petrels
7
shearwaters
winter
Totals
2
4
2
3
1
8
1
1
2
2
2
3
11
Fulmar
4
Gannet
1
1
2
4
cormorants
1
1
5
7
seaduck
5
1
16
25
3
phalaropes
1
1
smaller skuas
7
7
Great skua
Larus gulls
0
2
1
Sabine’s gull
1
1
Kittiwake
2
4
terns
1
1
Common guillemot
4
1
2
Razorbill
1
Puffin
1
Little auk
54
1
1
9
1
7
15
2
5
24
34
2
2
2
17
21
1
8
10
9
11
20
3
4
Brunnich’s guillemot
Black guillemot
5
ICES Coop. Res. Rep. No. 232
7.5
Consequences to populations
Possible consequences of wrecks are hard to detect.
Further, the number of birds wrecked is not a good
indicator of the true number of birds affected. As has
been shown, wrecks often occur outside the breeding
season. This means that birds from different
populations and colonies may be affected.
Consequently, due to the large numbers of most
seabird species, severe effects affecting populations or
even on single colonies are rare. With regards to oil
contamination, there is no evidence that chronic
pollution has had a long-term effect on populations, but
this lack of apparent effect may be confounded by the
effect of long-term increases in seabird numbers in
many areas. Major effects of wrecks caused by oil
contamination could be detected only after a small
proportion of major oil spills and only at the colony
level. Examples are only a few big accidents near the
breeding season and close to the breeding colonies,
such as the wreckages of the Torrey Canyon
(Cornwall), Amoco Cadiz (Brittany), Sea Empress
(Wales), Braer (Shetland), and Exxon Valdez (Alaska)
(Bourne et al., 1967; Bourne, 1970; Jones et al., 1978;
Anonymous, 1993; Heubeck et al., 1995; Paine et al.,
1996).
However, there are cases where effects at a population
level have been detected following a wreck. For
example, severe and long lasting effects were observed
during and following a period of pollution involving
chlorinated hydrocarbon insecticides in the Wadden
Sea. Sandwich terns Sterna sandvicensis and common
eiders Somateria mollissima were the most affected
birds although declines in populations of all coastal
birds of the Wadden Sea were recorded (Koeman et al.,
1968, 1969, 1972; Swennen, 1972). The Sandwich tern
colony at Vlieland collapsed from 20,000 pairs to less
than 1,000 pairs within a few years. At the main eider
colony on the island of Vlieland numbers of breeding
females dropped from c. 4000 to 800 pairs (Swennen
1972, Furness and Camphuysen, 1997).
Table 7.3. Frequency distribution of different types of wrecks in the North Atlantic for different groups and species of birds (see
Appendix 7.1 for a list of the wrecks; review papers and non-European wrecks were excluded for this analysis).
Species/group
oil
storm
Food
other
Totals
divers
4
4
grebes
3
3
storm petrels
8
shearwaters
1
8
1
2
Fulmar
4
2
5
11
Gannet
2
1
1
4
cormorants
4
2
1
7
15
2
8
25
seaduck
phalaropes
1
smaller skuas
6
1
1
7
Great skua
0
Larus gulls
5
Sabine’s gull
1
1
1
Kittiwake
5
terns
1
Common guillemot
2
17
6
1
1
3
1
1
9
10
15
2
7
35
Brunnich’s guillemot
2
Razorbill
9
1
7
Puffin
5
1
4
10
Little auk
4
12
3
19
Black guillemot
4
ICES Coop. Res. Rep. No. 232
2
5
22
4
55
7.6
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63
APPENDIX 7.1
LIST OF WRECKS
Shown are authors, year of publication, type of wreck (e.g., storm, oil incident, severe winter, food shortage), region of
occurrence, season and species.
Author
Year
Wreck
Region
Season
Species
Europe
Andersen
Anker-Nilssen et al.
Anker-Nilssen and Røstad
Anonymous
Anonymous
Anonymous
Anonymous
Anonymous
Barrett
Barrett
Bibby and Bourne
Blake
Bodenstein
Bourne
Bourne
Boyd
Brewka et al.
Byrkjeland
Campbell et al.
Camphuysen
Camphuysen
Camphuysen
Camphuysen
Camphuysen
Camphuysen
Camphuysen
Camphuysen
Camphuysen et al.
Camphuysen and Derks
Camphuysen and IJzendoorn
Camphuysen and Keijl
Camphuysen and Leopold
Clarke
Cobb
Craik
Debout
Doumeret
Dreckhahn
Durinck et al.
Eber
Engelen
Evans
Furphy et al.
Furtado and LeGrant
Géroudet
Gill et al.
1996
1988
1983
1869–75
1982
1912
1979
1985
1979
1982
1971
1983
1956
1979
1990
1954
1978
1989
1978
1989b
1990b
1996a
1987
1989c
1990b
1995a
1996b
1988
1989
1988
1994
1996
1895
1976
1992
1982
79 / 80
1969
1993
1958
1987
1892
1971
1979
1991
1967
storm
oil
oil
storm?
calm
storm
oil
food
oil
oil
bycatch
oil
storm
oil
food
storm
bycatch
oil
oil
food
oil
food
calm
postfiled
food
oil
food
oil
cold
food
oil
storm
storm
bycatch
food
storm
storm
oil
bycatch
storm
oil
storm
?
storm
food
oil
Scandinavia
Skagerrak
Norway
UK–Clyde
Netherlands
UK
Atlantic Spain
Netherlands
Norway
Norway–north
UK?
Skaggerak
German Bight
Norway
UK–northeast
Europe
Poland
Norway
UK–east
Netherlands
Netherlands
Netherlands
Netherlands
North Sea
Netherlands
Netherlands
Netherlands
Netherlands
Netherlands
Europe
Netherlands
Europe
UK–northeast
UK?
UK–west
France–west
France–west
German Bight
Denmark
German Bight
Wadden
UK–north
Irish Sea
Azores
Europe
UK–southwest
autumn
winter
autumn
winter
spring
autumn
winter
winter
Auks
Auks
guillemot
auks
fulmars
auks
64
winter
winter
winter
winter
winter
autumn
winter
winter
winter
spring
autumn
summer
summer
winter
autumn
winter
winter
winter
autumn
autumn
aut/winter
winter
summer
winter
autumn
autumn
winter
winter
winter
autumn
autumn
winter
auks
auks
auks
auks
auks
kittiwake
seaduck, auks
auks
storm petrels
seaduck, auks
auks
grebes
auks
auks
auks
fulmars
kittiwake
auks
auks
seaduck
grebes, auks
grebes
skuas
auks
auks
auks
divers, auks
mixture
mixture
Mixture
Seaduck
Seaduck
Gulls
Seaduck
storm petrels
Auks
Auks
Seaduck
Mixture
ICES Coop. Res. Rep. No. 232
Author
Year
Wreck
Region
Goethe
Greenwood et al.
Grenquist
Haila
Ham
Ham et al.
Hanssen
Harris et al.
Harris and Wanless
Haverschmidt
Hesse
Heubeck
Heubeck
Heubeck and Richardson
Heubeck and Suddaby
Holdgate
Joensen
Jones et al.
Jones et al.
Jones et al.
Jouanin
Kennedy et al.
Kies and Tomek
Larsson
Leopold et al.
Leopold and Camphuysen
Lloyd et al.
Lönnberg
Louzis et al.
MacPherson
Mathiasson
McCartan
Mead
Meek
Mehlum
Meininger et al.
Mudge et al.
Nelson
Nelson
Oldén et al.
O’Donovan and Regan
Parrack
Partridge
Pashby and Cudworth
Poulsen
Proger and Paterson
Rittinghaus
Robinson
Sage
Sage and King
Seilkopf
Sergeant
Soikkeli and Virtanen
1978
1971
1970
1970
1989
1991
1982
1991
1996
1930
1912
1991
1994
1980
1991
1971
1961
1970
1978
1984
1953
1954
1990
1960
1986
1992
1974
1927
1984
1892
1963
1957
1974
1985
1980
1991
1992
1880
1911
1986
1950
1967
1993
1969
1957
1913
1956
1909
1979
1959
1955
1952
1972
oil
oil
parasite
oil
storm
storm
oil
food
food
storm
storm
food
oil
oil
food
food
?
oil
oil
food
?
storm
bycatch
?
cold
oil
food
storm
storm
storm
?
storm
storm
oil
oil
cold
food
storm
storm
bycatch
storm
oil
oil
storm
storm
storm
oil
storm
oil
storm?
storm
storm
oil
Wadden Sea
UK–northeast
Finland
Finland
Netherlands
Netherlands
Baltic
Shetland
UK–east
Netherlands
German Bight
Shetland
Shetland
Shetland
Shetland
Irish Sea
Denmark
Irish Sea
Channel
UK–east
France
Ireland
Poland
Sweden
Netherlands
Netherlands
Irish Sea
Sweden
Channel
UK
Sweden
UK
Irish Sea
Orkney
North Sea
Netherlands
UK–northeast
UK
UK–east
Sweden
Ireland–west
UK–northeast
Channel
North Sea
Denmark
UK–west
German Bight
Irish Sea
Shetland
UK
German Bight
UK
Finland
ICES Coop. Res. Rep. No. 232
Season
winter
winter
autumn
winter
winter
winter
winter
autumn
winter
winter
winter
winter
spring
spring
spring
autumn
autumn
winter
spring
winter
winter
winter
winter
autumn
spring
winter
winter
all
autumn
autumn
winter
autumn
winter
winter
winter
aut/win
winter
spring
autumn
autumn
winter
aut/winter
Species
Mixture
Auks
Seaduck
Seaduck
Skuas
Auks
Seaduck
Auks
Cormorant, auks
Auks
Skuas
Auks
Mixture
Mixture
Auks
Auks
Fulmars
Auks
Mixture
Auks
storm petrels
Skuas
grebe, duck, auks
Fulmar
Seaduck
fulmar, gannet, auks
Mixture
Kittiwake
kittiwake
storm petrels
fulmar
kittiwake
seaduck
fulmar, gulls, auks
grebes, seaduck
skuas
skuas, Sabine’s gull
auks
auks
auks
auks
fulmar
auks
auks
seaduck, terns
storm petrels
seaduck
storm petrels
gulls
auks
seaduck
65
Author
Year
Wreck
Region
Season
Species
Swann and Butterfield
Swennen and Smit
Swennen and Spaans
Swennen and van den Broek
Tasker
Teixeira
Teixeira
Teixeira
Underwood and Stowe
Wheeler
Witherby
Wrånes
Wynne-Edwards
Wynne-Edwards
1996
1991
1970
1960
1994
1985a
1985b
1987
1984
1990
1912
1988
1953
1963
food?
parasite
oil
parasite
wind
storm
bycatch
storm
food
storm
storm
cold?
storm
storm
UK–northeast
Netherlands
German Bight
Netherlands
UK–east
Portugal
Portugal
Portugal
UK–east
North Sea
UK–east
Norway
UK–north
UK–east
winter
summer
winter
summer
winter
winter
winter
autumn
winter
autumn
autumn
winter
autumn
autumn
auks
seaduck
seaduck, auks
seaduck
mixture
storm petrels
auks
storm petrels
auks
auks
auks
seaduck
storm petrels
skuas
Zoun
Zoun et al.
1991
1991
chemical
chemical
Netherlands
Netherlands
winter
winter
gannets, auks
seaduck, auks
Brewster
Cramer
Eliot
Murphy and Vogt
Snijder
Sprunt
Stenhouse and Montevecchi
Stone
Stone
1906
1932
1939
1933
1953
1938
1996
1965
1965
storm
storm?
storm
storm
storm
storm
storm
storm
storm
autumn
auks
phalaropes
storm petrels
auks
auks
auks
auks
auks
phalaropes
Other regions:
Bailey and Davenport
Batchelor
Bond
Bourne
Carter
Crochett and Kearns
Crochett and Reed
Gabrielson and Jewett
Jury
Nakamura et al.
Nevhaev
Pelt and Piatt
Piatt and Lensink
Ryan et al.
Vernon
1972
1981
1971
1981
1985
1975
1976
1970
1991
1983
1993
1995
1989
1989
1988
food
?
storm
storm?
?
food?
storm
storm?
storm
storm
?
food?
oil
storm
?
Western North Atlantic
66
winter
winter
autumn
aut/winter
winter
autumn
Alaska
South Africa
NW Pacific
S Pacific
Australia
New Zealand
New Zealand
NW Pacific
South Africa
Japan
Sakhalin
Alaska
Alaska
South Africa
South Africa
winter
spring
spring
inc
winter
autumn
summer
winter
winter
winter
winter
auks
petrels
phalaropes
petrels
diving petrels
penguins
fulmars
phalaropes
storm petrels
fulmars, auks
auks
mixture
petrels
storm petrels
ICES Coop. Res. Rep. No. 232