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ICES Journal of Marine Science, 54: 726–737. 1997
Seabirds as monitors of the marine environment
R. W. Furness and Kees (C. J.) Camphuysen
Furness, R. W. and Camphuysen, C. J. 1997. Seabirds as monitors of the marine
environment. – ICES Journal of Marine Science, 54: 726–737.
Many studies have shown that seabirds are sensitive to changes in food supply, and
therefore have potential as monitors of fish stocks. For most seabird species
breeding parameters suitable for biomonitoring have yet to be measured over a wide
range of prey densities. However, it is clear that responses vary among species and
care must be taken when interpreting seabird data as a proxy for fish abundance.
For many years seabirds have also been used as monitors of pollution, especially oil
pollution. Beached bird surveys provide important evidence of geographical and
temporal patterns, and, for example, show consistent declines in oil release into the
southern North Sea over the last 15 years. Analysis of oil on birds can now permit
fingerprinting of sources, allowing prosecution of polluters. As predators high in
marine food webs, seabirds also have potential as monitors of pollutants that
accumulate at trophic levels. Recent work on mercury in seabirds has permitted an
analysis of spatial patterns and of the rates of increase in mercury contamination of
ecosystems over the last 150 years, since mercury concentrations in feathers of
museum specimens can be used to assess contamination in the birds when they were
alive. Surprisingly, pelagic seabirds show higher increases than most coastal ones,
and increases have been greatest in seabirds feeding on mesopelagic prey. This seems
to relate to patterns of methylation of mercury in low-oxygen, deeper water.
Accurate measurement of long-term trends in mercury contamination depend on the
assumption that seabird diet composition has not changed. This can be assessed by
analysis of stable isotopes of N and C from the same feathers used for mercury
measurement, a technique that also permits the monitoring of trophic status over
time or between regions. While high mercury contamination of seabirds in the
southern North Sea is unsurprising, we cannot yet explain certain unexpected
results, such as high levels in seabirds from north Iceland compared with those from
south Iceland or Scotland.
?1997 International Council for the Exploration of the Sea
Key words: biomonitors, fish stocks, mercury, oil pollution, pollution, seabirds, stable
isotopes.
R. W. Furness: Applied Ornithology Unit, Graham Kerr Building, Glasgow University,
Glasgow G12 8QQ, Scotland, UK. C. J. Camphuysen: Netherlands Institute for
Sea Research, Postbus 59, 1790 AB den Burg, Texel, The Netherlands. Correspon-
dence to R. W. Furness: tel: +441413303560; fax: +441413305971; email:
r.furness@bio.gla.ac.uk
Introduction
The world’s oceans and seas have long been under
pressure from human exploitation of renewable
resources and from pollution (Cushing, 1988;Clark,
1992). There are many examples of collapses of fish
stocks as a result of a combination of excessive human
harvesting and environmental changes. Often it is diffi-
cult to assess the relative contributions of these two
factors in determining fish stock collapse, but there is a
clear message that monitoring of marine resources is
essential if such problems are to be avoided through
reductions in fishing mortality imposed on stocks that
have become vulnerable (Cushing, 1988). The complex
ecological interactions that can occur between fish
stocks through competitive and through predator–prey
relationships make the prediction of changes in stocks
extremely difficult (May et al., 1979;Daan et al., 1990;
Hamre, 1994), further increasing the need for empirical
monitoring of change.
In addition, the oceans are the ultimate sink in the
biogeochemical cycles of many pollutants (Bourne,
1976a,b;Clark, 1992), while shallow seas, often the
most important areas for commercial fisheries, have
often been used as a dumping ground for a wide range of
pollutants, as well as being particularly affected by
accidental pollution through their relatively enclosed
and shallow nature. The long-term consequences of
1054–3139/97/040726+12 $25.00/0/jm970243 ?1997 International Council for the Exploration of the Sea
polluting shallow seas have become more evident in
recent decades, and many pollution problems of the past
are now being given greater attention. Controls on
industrial emissions of chemicals, discharge of oily
wastes, ballast water, garbage, plastics, sewage and
dredging sludges have all been reduced in Europe and
North America, though such problems may be increas-
ing in less developed parts of the world. For example,
mercury loss from rivers in which gold mining is being
carried out has greatly increased in parts of South
America and Asia (Nriagu, 1994). Monitoring of all of
the forms of pollution, and of effects of harvest-
ing renewable resources on ecosystem structure and
stability, is well beyond present capabilities and budget-
ary limits. Much effort is put into the monitoring of
commercially important fish stocks and into the
measurement of pollutant concentrations in marine
foods, but many fish stocks are not amenable to stock
assessment through collection of catch and effort data
(Cairns, 1992), while pollutant levels and effects that do
not constitute direct toxic risks to humans or influence
the profitability of fisheries, generally receive little atten-
tion. For example, sandeels (Ammodytes marinus)inthe
North Sea are a key prey species of many commercially
important predatory fish, of most seabirds during sum-
mer and of many marine mammals (Furness, 1990;
Bailey et al., 1991), as well as the target of the largest
single species fishery in the North Sea (Monaghan,
1992). Yet due to their short lifespan, high natural
mortality rate and poorly known distribution and
ecology, which make it impossible to carry out reliable
Virtual Population Analysis, and the difficulty of using
acoustic survey for sandeels, there are no accurate data
either on the size or trends in sandeel stock biomass in
the North Sea (ICES, 1991). Such a lack of information
casts considerable doubt on whether it is satisfactory to
allow unregulated fishing on sandeels in the North Sea
and indicates the need for assessment of possible eco-
logical effects of fish stock changes on other components
of this ecosystem.
Similar issues arise in many other areas where natural
predators and commercially important predatory fish
depend on stocks of small pelagic fish or crustaceans as
a basis for the food web, as with capelin (Mallotus
villosus) in the Barents Sea (Krasnov and Barrett, 1995)
or Canada (Diamond et al., 1993), krill (Euphausia
superba) in the Southern Ocean (Croxall et al., 1988),
sardines or anchovies in upwelling areas such as
Peru (Duffy, 1983) or southern Africa (Berruti and
Colclough, 1987). A small part of the gap in our
knowledge of marine ecosystems under stress from
exploitation or pollution can be filled by studies of
seabirds, which as top predators may provide a means of
monitoring changes in lower trophic levels of the marine
food chain (Bourne, 1976b;Furness and Monaghan,
1987).
Seabirds as biomonitors
Because seabirds are conspicuous animals they are a
suitable choice to play a role as sentinel organisms;
unexpected changes in their numbers, health or breeding
success provide an alarm that may indicate an unknown
pollution or food supply problem. This kind of ‘‘bio-
indicator’’ role has included the detection of serious
pollution in the southern North Sea from drins (com-
pounds such as dieldrin, aldrin, etc.) production, which
was first noticed as a result of the effect on local seabird
populations (see below). Biomonitoring, as distinct from
bioindication, requires long-term data sets, and most
ecological research is short-term, being funded for per-
haps 2 or 3 years. However, seabirds are relatively easily
counted, as well as being a group with considerable
public and scientific interest, as evidenced by the exist-
ence of various regional Seabird Groups devoted to their
study. The extensive availability of manpower, to carry
out designed fieldwork and so provide monitoring data,
is one major advantage of choosing seabirds as bio-
monitors. Volunteers provide an enormous free input of
time and effort that would be extremely expensive if run
as a professional research programme.
The detailed knowledge of general seabird ecology
and of the numbers and productivity of many popula-
tions also makes them particularly appropriate as a
choice of biomonitor or bioindicator. The colonial
nature of breeding seabirds has several benefits. It allows
numbers to be tracked for less effort than if the breeding
populations were dispersed, and it allows large quan-
tities of data to be collected from a particular site in a
relatively short period of time. However, to be useful, a
biomonitor must respond in a sensitive way to changes
in the variable for which it is a proxy measure (Furness
and Greenwood, 1993). Preferably the response should
also display a high signal-to-noise ratio, and the
response must be predictable. The causal mechanism
should preferably be understood, and similar responses
should not be caused by a variety of other factors. The
speed of response is also an important issue. A response
that is delayed by a lag of many years, for example
changes in breeding numbers of a bird with several years
deferred maturity, would be an inappropriate bio-
monitor, as such a delay in providing information on a
fish stock decline would be of little practical value. Thus,
we can expect to select as a biomonitoring tool such
rapid and sensitive responses as parameters of breeding
success, diet composition or the activity budgets of
breeding adults, all of which are likely to respond
immediately and markedly to changes in food supply.
Similarly, pollutants are likely to cause toxic effects in
seabird populations that are most evident in terms of
embryo or chick development, hatching success or chick
behaviour. The fact that seabirds are close to the top of
marine food chains means that they will be particularly
727Seabirds as monitors of the marine environment
appropriate as biomonitors of pollutants that are
amplified in concentration through food chains. This is
especially a characteristic of pollutants that are lipid-
soluble but have low water solubility, such as organo-
chlorines and organo-metals. Thus, seabirds may be
more appropriate as monitors of food chain exposure to
lipid-soluble pollutants than are, for example, benthic
invertebrates (Furness, 1993). Furthermore, the mobility
of seabirds, perhaps at first appearing to be a drawback
for a biomonitor, can be an advantage if the aim is to
monitor over a broad scale and the ranging behaviour
of the birds is known. Individual seabirds can then
integrate the signal over defined space and/or time,
providing a lower analytical cost than if frequent or
spatially finer scale sampling was required to average
out local variations in exposures of sedentary organisms
(Noble and Elliott, 1986;Walsh, 1990).
Different species of seabirds feed at a variety of
trophic levels and in all of the zones from littoral to
pelagic (Furness and Monaghan, 1987). Thus, for
example, islands in the south of the North Atlantic may
hold a range of breeding species that sample a wide
range of the local habitats and food chains (Monteiro,
1996). These include species that feed extensively
in mesopelagic food chains, such as Bulwer’s petrel
(Bulweria bulweria) and Madeiran storm petrel
(Oceanodroma castro), as well as species occurring in the
same breeding sites that feed in epipelagic food chains,
such as Cory’s shearwater (Calonectris diomedea) and
common tern (Sterna hirundo), and the generalist feed-
ing yellow-legged gull (Larus cachinnans), which feeds
on the coast, inshore and offshore. Similar differences in
foraging niches of seabirds that share breeding sites are
common in other regions, and thus permit targeting of
particular food chains by sampling from appropriate
bird species.
Biomonitoring fish stocks and fisheries
It is a natural feature of most marine invertebrates and
fish that recruitment is highly variable from year-to-
year. Thus, for short-lived, or heavily fished, organisms,
total population size will fluctuate considerably over
years, resulting in a large variation in food supply for
seabirds. Among birds, seabirds have some of the
highest adult survival rates, low reproductive rates and
several years of deferred maturity, so that their popu-
lation sizes generally vary very little from one year to
the next. Given the lack of direct tracking of prey
abundance by seabird abundance, seabirds must clearly
be buffered to some extent from the fluctuations in
abundance of organisms lower in the food chain. This
buffering can occur through adults refraining from
breeding when food is scarce, as in shags (Phalacrocorax
aristotelis; see Aebischer and Wanless, 1992), Arctic
skuas (Stercorarius parasiticus; see Phillips et al., 1996),
and Peruvian guano birds (Duffy, 1983), or from re-
location of breeding sites by species that depend on
locally abundant food for successful breeding, as in
Arctic terns (Sterna paradisaea) and pomarine skuas
(Stercorarius pomarinus) or from diet switching. Thus,
the information to be gained about changes in fish
stocks from responses of seabirds requires a detailed
knowledge of the biology of the seabird species and how
it responds to changes in food supply.
Differences in response can be quite dramatic and
unexpected (Furness and Barrett, 1991;Barrett and
Krasnov, 1996). For example, when sandeel availability
decreased at Foula, Shetland in the mid-1980s (Bailey
et al., 1991) the Arctic tern breeding numbers immedi-
ately fell dramatically and their breeding success fell to
zero (Phillips et al., 1996). Arctic tern breeding success
correlated closely with estimates of sandeel stock size
(Monaghan, 1992). At the same time, breeding success
of common guillemots (Uria aalge) at Shetland remained
high, and adults continued to feed their chicks on
sandeels, but the breeding numbers of guillemots fell.
When sandeel abundance recovered after 1991, Arctic
tern breeding numbers recovered as a consequence of the
recruitment of birds that apparently had refrained from
breeding for about 7 years of food shortage. However,
guillemot numbers apparently did not recover in this
way, perhaps reflecting an increased winter mortality of
guillemots during the period of food shortage, even
though their breeding success was unaffected (Heubeck
et al., 1991). Detailed investigation of guillemot foraging
behaviour showed that breeding guillemots were able to
increase foraging effort to compensate for reduced food
density (Monaghan et al., 1996) and hence the breeding
numbers of guillemots (Monaghan, 1992) or adult
activity budgets provided an index of sandeel abundance
while breeding success did not. Great skuas (Catharacta
skua) showed changes in diet, chick growth, breeding
success, adult survival, numbers of non-breeders and
adult activity budget in response to reduced sandeel
abundance (Hamer et al., 1991;Klomp and Furness,
1992), while Arctic skuas also showed several responses.
These allowed investigation of the detailed relationship
between breeding data and sandeel stock size, generally
confirming theoretical predictions (Cairns, 1987) that
behaviour and diet respond to reduced food supply at a
higher level of resource than breeding success, while
adult survival is most strongly buffered against effects of
food shortage. The relationship between food supply
and breeding response is clearly non-linear in the case of
the Arctic skua (Fig. 1), as also predicted from theor-
etical considerations, although relationships between
sandeel abundance and breeding success of Arctic terns
or breeding numbers of guillemots are adequately
described by linear models over the range of variation
observed (Monaghan, 1992). On a theoretical basis,
Furness and Ainley (1984) predicted that small seabirds
728 R. W. Furness and C. J. Camphuysen
would respond more severely to food shortage than
would large species of similar ecology, since there is a
tendency for the proportion of available time spent in
foraging to decrease with body size. Thus, larger birds
such as shags and gannets (Morus bassanus) are better
buffered in terms of time budget flexibility. Further-
more, species with short foraging ranges and narrow or
specialized diets and feeding behaviours, such as terns,
can be predicted to be more vulnerable, and so also
potentially more sensitive indicator species. Furness and
Ainley (1984) identified terns as particularly likely to act
as sensitive indicators of food shortage, and this predic-
tion has been supported by evidence from effects of
sandeel shortage in Shetland.
While the breeding success, activity budgets or, in
some cases, breeding numbers of seabirds that are
specialist fish predators may all be useful as monitors of
changes in prey abundance, an alternative approach is to
use diet composition of generalist seabirds as an index of
the relative abundance of prey stocks. Since diet compo-
sition can often be sampled rather easily, this has proved
an attractive approach to using seabirds as monitors
of prey stocks (Hislop and Harris, 1985;Berruti and
Colclough, 1987;Montevecchi et al., 1987;Martin,
1989). The relative merits of monitoring diets of prey
generalists or monitoring breeding parameters of prey
specialists are reviewed in detail by Montevecchi (1993).
However, even where relationships between fish stock
biomass and seabird breeding parameters have been
established, it is important to appreciate that other,
confounding, factors may confuse interpretations. For
example, northern fulmar (Fulmarus glacialis) foraging
costs may be very sensitive to windspeed (Furness and
Bryant, 1996), so that changes in weather may affect
behaviour and breeding success that could be interpreted
as due to reductions in food supplies.
Seabird mass strandings and large-scale fluctuations
in wintering distribution of seabirds may be indicative of
changes in prey stock abundance or prey availability
in winter. In the early 1980s, a major southward
and eastward shift in the wintering distribution of
guillemots, kittiwakes (Rissa tridactyla) and razorbills
(Alca torda) occurred in the North Sea, which was
apparently related to a retreat of the sprat (Sprattus
sprattus) stock from the northern North Sea
(Camphuysen, 1990). Large numbers of these birds
shifted to wintering in areas where exposure to oil
pollution was higher (southern North Sea) or where the
chances of drowning in gillnets were much greater
(Skagerrak) and where food supply was apparently quite
poor. A long series of wrecks (large numbers of dead
birds) from 1980–1991 led to stabilization or even slight
declines in breeding populations of these species in the
British Isles (Harris and Wanless, 1988;Swann et al.,
1989). Long-term changes in the relative abundance of
little auks (Alle alle) wintering in the North Sea, which
were quite rare in the 1970s and early 1980s but increas-
ingly common since 1984, may be indicative of changes
in the availability and stock of particular prey relevant
to these birds (Camphuysen and Leopold, 1996).
Although few studies have been performed so far, and
although the patterns found may be very difficult to
interpret, these variations in ‘‘wintering performance’’ of
seabirds might provide valuable insight into temporal
and spatial fluctuations in prey stocks.
In addition to acting as monitors of fish stocks,
seabirds may sometimes be used as a monitor of fisheries
activities. Trawl fisheries in the North Sea, for gadids,
flatfish or crustaceans, generate very large amounts of
unwanted catch, including undersized fish, which results
in the discarding of dead and moribund fish from boats.
These are consumed in large quantities by scavenging
seabirds (Hudson and Furness, 1988;Camphuysen
et al., 1995;Garthe et al., 1996). Sampling of regurgi-
tated pellets at colonies or at roost sites provides otoliths
from these fish which can be identified to species,
measured to give fish size and sectioned to count annual
layers to determine fish age. Thus, the species and sizes
of fish being discarded can be assessed from sampling at
seabird colonies providing the extent of discard selection
practised by the birds is known. In the North Sea,
gannets and great black-backed gulls (Larus marinus)
are able to swallow most sizes of discards and show little
selection among roundfish discards, although they tend
to reject discarded flatfish (Hudson and Furness, 1988;
Camphuysen et al., 1995). Discarding is extensively
practised in fisheries such as in the Mediterranean (Oro
and Ruiz, 1997), southern Africa (Abrams, 1983,1985),
and in Australia (Blaber and Wassenberg, 1989), but
in these areas data on quantities and composition of
discards from on-vessel studies are even more limited
than for the North Sea.
60 000
1.0
0
Total number (millions) of 0-group plus 1-group
sandeels in Shetland waters
Arctic skua chicks fledged per pair
50 000
0.6
0.8
0.4
0.2
10 000 20 000 30 000 40 000
1987
1988
1989
1986
1992
1993 1991
1990
Figure 1. The relationship between Arctic skua breeding success
at Foula, Shetland and sandeel abundance at Shetland. Data
from Phillips et al. (1996).
729Seabirds as monitors of the marine environment
Biomonitoring oil pollution
Stranded, oiled (‘‘beached’’) seabirds have been used for
nearly a century to demonstrate the effects of oil pollu-
tion on the marine environment (Bourne, 1976a,b;
Camphuysen, 1989). It has been recognized that the
effect on seabirds of chronic oil pollution (i.e. the sum of
operational discharges of oil by ships at sea, small
accidents at sea, natural seeps, river run-off, and the
leakage of oil during drilling operations on offshore
installations) can be assessed by means of beached bird
surveys (Camphuysen and Van Franeker, 1992). Busy
shipping lanes and areas with extensive offshore oper-
ations lead to very high oiling rates (i.e. the proportion
of all dead birds found that have oil in their feathers)
among stranded birds on nearby coasts. Beached bird
surveys (BBS), if coupled with the chemical analysis of
feather samples, can be effective indicators of pollution
of the seas by other lipophilic substances (Dahlmann
et al., 1994;Camphuysen, 1995).
The use of beached bird surveys as a monitoring
instrument has been hotly debated. Although it is
obvious that a dead oiled bird is a clear demonstration
of the effect of mineral oil contamination on such
organisms, it is not quite clear what beached bird survey
results actually tell us. Firstly, what can be expected
from these surveys? As a tool for monitoring seabird
mortality rates, or population trends, beached bird
surveys are certainly inadequate. Similarly, attempts
to estimate total mortality among seabirds due to oil
contamination have been inconclusive. Chronic oil
pollution is, as the name suggests, a constant process in
which variable numbers of seabirds under variable con-
ditions are killed. The difference between a tideline
covered with corpses and a clean beach means very little
in terms of offshore seabird mortality.
However, some other aspects of beached bird surveys
have led to consistent results. Where the numbers of
seabirds washing ashore are subject to massive fluctu-
ations from year-to-year and month-to-month, variation
in oil rates may, in fact, be minimal. Regular beached
bird surveys provide insight into consistent patterns in
oiling rates of different species of birds (interpreted as
differences in the risk of oil contamination), seasons and
areas. For example, while in stranded guillemots in The
Netherlands typically 88% were contaminated by oil
(1979–1991) the oil rate in Shetland was only 18%
(Camphuysen and Van Franeker, 1992). Oiling rates are
particularly high in the vicinity of large harbours and
near shipping lanes (e.g. the Channel, southern North
Sea), and comparatively low in cleaner sea areas, such as
the north-western North Sea and along the Atlantic
coast (Fig. 2). These patterns reflect the risk for indi-
vidual seabirds in different sea areas of encountering
oil slicks and, hence, beached bird surveys are a useful
tool for recording and measuring these differences.
Compared to aerial surveillance for oil slicks at sea,
beached bird surveys are a very cost-effective method,
with a proven efficacy and application on a very wide
scale.
Seabirds are vulnerable to a wide range of lipophilic
substances, many of which are legally dumped into
the North Sea without restrictions. BBS results are a
powerful means by which to demonstrate the adverse
effects of these substances, if systematic sampling of
contaminants is performed in combination with these
surveys (e.g. Dahlmann et al., 1994). Fingerprinting
techniques, in which an enormous range of mineral oils
and other (chemical) compounds can be identified from
feather or beach samples, have been shown to be an
effective tool in the prosecution of polluters. Besides,
they provide essential information on (changes in) the
sources of pollution at sea. While most governmental
action is aiming at a reduction in the visibility of oil
pollution (i.e. mainly to prevent oil strandings), beached
bird surveys are a very effective way of demonstrating
ongoing pollution offshore.
A power analysis, used to determine if the programme
had a high probability of detecting trends, has shown the
sensitivity of this sort of survey. In most situations, BBS
can lead to statistically significant results over a span of
10–15 years of collecting data. The main European BBS
schemes have now been running for 20–30 years
(Camphuysen and Van Franeker, 1992;Heubeck, 1995),
so valuable conclusions may be drawn with respect to
trends in the pollution of European seas with mineral
oil. An analysis of oil rates in stranded North Sea
seabirds has demonstrated gradual, but significant
declines over the last 15 years (Fig. 3).
Biomonitoring heavy metal pollution
Because they allow non-destructive sampling and permit
retrospective study, seabird feathers are particularly
convenient for monitoring heavy metal pollution in
marine food webs (Monteiro and Furness, 1995).
Feathers can be sampled for analysis of lead, cadmium,
and many other elements (Burger, 1993). Since metals
may be deposited from the atmosphere onto the surfaces
of feathers (Hahn, 1991) as well as incorporated into
growing feathers from the blood, use of feathers to
monitor may be confounded by a combination of these
two processes. In some instances, as with cadmium and
lead, most appears to originate from direct atmospheric
deposition onto feather surfaces, whereas ingested
cadmium and lead become firmly bound in kidney and
bone, respectively, and only enter feathers in trace
amounts (Walsh, 1990;Furness, 1993;Stewart et al.,
1994). In these cases, monitoring of atmospheric con-
tamination by feathers is possible but the results say
little or nothing about food chain contamination (Hahn,
1991). Mercury presents a quite different situation.
730 R. W. Furness and C. J. Camphuysen
Mercury occurs in the environment in several forms,
with quite different biological properties. Inorganic
mercury is much less toxic than organic mercury. Most
organic mercury is in the form of methylmercury and
this is almost all assimilated by animals from ingested
foods, whereas most inorganic mercury passes through
the alimentary system to be voided in faeces. Methyl-
mercury is lipid-soluble, and thus shows accumulation
patterns similar to those of organochlorine compounds
such as DDT. It is stored in lipid-rich tissues and tends
to be accumulated to higher concentrations at each step
up the food chain; i.e. methylmercury is biomagnified
through food chains. All of the mercury entering
feathers is methylmercury (Thompson and Furness,
1989a), even in birds storing inorganic mercury in the
liver (Thompson and Furness, 1989b). Thus, when
analysing feathers, a biochemical separation can be
made to obtain measures of methylmercury derived
from the diet and inorganic mercury (if any) that is a
surface contaminant of the feather, since surface
contamination with methylmercury is unlikely.
Experimental laboratory (Lewis and Furness, 1991,
1993) and field (Monteiro, 1996) studies have shown
that concentrations of mercury in feathers reflect the
mercury levels in the blood at the time of feather growth
and that mercury level in the growing feather is directly
linearly related to the dietary intake of methylmercury
by chicks. Correlational studies have also shown feather
Oil rate
25%
50%
75%
North Sea
Figure 2. Differences in oil rates of common guillemots in western Europe. Data from Camphuysen (1995).
731Seabirds as monitors of the marine environment
mercury levels to relate closely to levels in liver
(Thompson et al., 1991). Levels in chick down correlate
with those in the egg (Becker et al., 1993a,b; Stewart
et al., 1997) and are a good measure of local food chain
contamination with mercury in the area around the
colony in which the birds fed during egg formation
(Barrett et al., 1985;Becker, 1989). Levels in chick
feathers do not correlate closely with levels in their
down, suggesting that down levels reflect egg content
whereas feather levels reflect mercury in food given to
chicks during their development. Thus chick feathers
provide a good way to monitor local mercury levels in
the diet and foraging area used during chick rearing
(Becker et al., 1994;Stewart et al., 1997). By contrast,
mercury levels vary more widely between adult feathers.
The concentration in feathers depends in part on the sex
of the bird, tending to be higher in males (Braune and
Gaskin, 1987;Lewis et al., 1993;Stewart et al., 1994),
since females can excrete about 20% of their soft tissue
methylmercury burden into eggs (Lewis et al., 1993).
Feather mercury concentrations in adult birds are
usually higher than in chicks, though there are excep-
tions to this (Stewart et al., 1997), but feather mercury
concentrations do not vary with adult age (Furness
et al., 1990;Thompson et al., 1991) as methylmercury
accumulated in soft tissues since the end of the previous
moult is excreted into the newly growing plumage
(Braune, 1987). For this reason, mercury concentrations
tend to increase in soft tissues up to the start of the main
autumn moult (Stewart et al., 1994) and are higher in the
feathers first regrown (Furness et al., 1986). Levels in
first moulted feathers indicate a combination of current
dietary intake plus stored organic mercury accumulated
between moults, whereas feathers grown at the end of
moult indicate only current intake. For a general
measure of exposure, a pooled sample of several small
body feathers (avoiding brood patch areas) give the
best measure of the mercury contamination of a bird
(Furness, 1993). Burger et al. (1992) suggest that
mercury concentrations in flight feathers grown in the
wintering area reflect winter site contamination, whereas
those grown in the breeding area reflect contamination
there, but higher mercury levels in feathers grown in
the breeding area may simply reflect accumulation of
mercury prior to moult.
Using pooled samples of body feathers, clear geo-
graphical patterns in mercury contamination can be
shown in a variety of seabirds. Although mercury levels
are considerably elevated in southern North Sea seabirds
(Furness et al., 1995;Thompson et al., 1993), levels are
lower in populations in the northern North Sea than in
the west of Britain and Ireland (Thompson et al.,
1992a,b). Surprisingly, mercury levels are high in sea-
birds in north-west Iceland (Table 1) relative to levels in
the same species from the British Isles and Norway
(Thompson et al., 1992b;Furness et al., 1994). The high
95
5
–2
1979
Logit (percentage oiled)
85
0
4
3
2
1
–1
81 83 87 89 91 93
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
Razorbill (a)
Guillemot (z)
Kittiwake (d)
Gulls (m)
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
a
z
d
m
Figure 3. Trends in oil rates in razorbills, common guillemots, kittiwakes, and Larus gulls stranded at the mainland coast in The
Netherlands, 1979–1995. Data from Camphuysen (1995).
732 R. W. Furness and C. J. Camphuysen
levels from north-west Iceland cannot yet be explained;
they are certainly not a result of local pollution, so may
reflect atmospheric transport and deposition.
Comparison of mercury concentrations in feathers
from skins collected up to 150 years ago shows that
mercury concentrations have increased about four-fold
(Fig. 4) in seabirds from Britain and Ireland (Thompson
et al., 1992a), the German North Sea coast (Thompson
et al., 1993) and the Azores (Monteiro, 1996). These
increases agree closely with predictions from general
models of mercury cycling in the atmosphere and oceans
(Mason et al., 1995a,b). Increases have been greatest in
species feeding on mesopelagic prey (Monteiro, 1996)
and this has suggested that methylation of mercury by
bacteria in deeper low-oxygen water may be a key step in
bringing mercury pollution into the food web. This is in
agreement with recent observations that mercury con-
centrations in mesopelagic fish are much higher than in
epipelagic fish (Monteiro et al., 1996), a finding indicat-
ing that many deep-water fish may be too contaminated
with mercury to be safe for human consumption.
Accurate determination of long-term trends in mer-
cury pollution assumes that the diet of the seabirds being
monitored has remained constant over decades. This is
more likely to be true of dietary specialists. Generalists
such as gulls may be less suitable monitors. However, it
is possible to look for evidence of dietary change or
constancy by measuring stable isotope ratios. The
15
N:
14
N ratio increases with trophic level while the
13
C:
12
C ratio differs between marine and non-marine
Table 1. Mercury concentrations (ìgg
"1
fresh weight) in body feathers of some seabirds
from various sites in the north-east Atlantic. Data from Thompson et al. (1992a) and
Furness et al. (1994). Figures presented are arithmetic means&1 standard deviation and
sample size in parentheses. Concentrations in seabirds from NW Iceland are statistically
significantly (p<0.05) higher than those of the same species from most other sites, and in all
cases higher than in NE Norway.
Species NW Iceland Shetland E Scotland NE Norway
Northern fulmar 3.8&1.5 (25) 1.6&0.6 (32) 2.3&0.8 (12) —
Kittiwake 5.5&1.7 (36) 2.9&0.9 (42) 3.8&1.7 (46) 3.1&1.2 (60)
Razorbill 2.7&1.1 (37) 1.9&1.1 (52) 2.2&0.8 (33) 1.7&0.6 (30)
Bru¨nnich’s guillemot 2.1&0.7 (38) — — 1.2&0.2 (25)
Common guillemot 1.6&0.6 (45) 1.2&0.4 (56) 3.8&3.2 (44) 1.2&0.3 (45)
Atlantic puffin 4.8&1.4 (37) 3.7&1.8 (46) 3.2&2.1 (30) 1.0&0.4 (31)
1990
12
0
1850
Mercury concentration (µg g–1)
1930
2
10
8
6
4
1870 1890 1910 1950 1970
Figure 4. Mercury concentrations in body feathers of Atlantic puffins from south-west and west Britain and Ireland. Data from
Thompson et al. (1992b).
733Seabirds as monitors of the marine environment
foods. Isotopes of S, O and H may also be informative
but have received less attention. The use of N and C as
indicators of diet/trophic status is well established
(Rau et al., 1992;Hobson and Welch, 1992;Hobson,
1993;Hobson et al., 1994). Comparisons between
feathers moulted at different times of year can indicate
seasonal dietary shifts (Thompson and Furness, 1995).
Thompson et al. (1995) showed that Scottish northern
fulmar diets have shifted to a lower trophic level over the
last 100 years, whereas diets of several other species
show no such change.
Biomonitoring other pollutants
Gilbertson et al. (1987) found that the variance in
organochlorine concentrations in seabirds was less than
in fish or marine mammals, suggesting that sampling
seabirds was more cost-effective for monitoring the
contamination of the food chain by organochlorines.
However, sampling adult seabirds for organochlorine
analysis usually requires killing birds, since analysis is of
internal tissues, usually liver. This presents ethical and
conservation problems, and an alternative often used is
to analyse tissues from birds found dead as in winter
beached bird surveys. The latter approach is rather
unsatisfactory as the concentrations of pollutants may
not reflect those in healthy birds, and starvation will lead
to the mobilization of lipid-soluble pollutants from fat
stores and to reduced mass of internal organs such as the
liver (Bogan and Newton, 1977). Indeed, birds starving
to death may in fact be killed by these high concen-
trations of mobilized lipid-soluble pollutants. Even if
birds were deliberately killed for pollutant measurement
in soft tissues, problems remain. Organochlorine and
other pollutant concentrations vary seasonally because
of seasonal changes in body composition regardless of
any seasonal variation in pollutant exposure, and differ-
ences occur between the sexes and between age groups
(Clark et al., 1987), requiring care in sampling strategy
and large sample sizes (Fryer and Nicholson, 1993). As a
less damaging means of sampling, eggs may be collected
for analysis since concentrations of lipid-soluble
pollutants in eggs closely reflect those in the blood of the
laying female. Several studies have shown seabird eggs
to be good monitors of local pollutant contamination,
since pollutant concentrations in eggs tend to reflect
pollutant uptake by the female foraging close to the
colony in the few days prior to egg laying (Coulson
et al., 1972;Becker, 1989;1991). However, in some
species the concentration of pollutants in eggs may
reflect accumulated body burdens of females more than
recent local uptake, and pollutant concentrations may
vary through the laying sequence as a result of changes
in the relative inputs to eggs from current intake and
from body reserves as the clutch is produced (Mineau,
1982;Becker and Sperveslage, 1989).
A long-term monitoring study of organochlorines in
eggs of gannets by Chapdelaine et al. (1987) provides an
excellent example of the utility of seabirds as monitors
of changes in pollution, and, in that particular case, also
demonstrates the rapid reduction in environmental con-
tamination after action was taken to stop the use of
DDT in North America.
Given the very large numbers of chemical pollutants
that may occur in the environment – some 30 000
different chemical pollutants enter the Great Lakes, for
example (Fox and Weseloh, 1987) – seabirds may have
an important role as bioindicators, or ‘‘sentinel organ-
isms’’. This has been well illustrated by the example of
drins pollution in the southern North Sea. In the mid-
1960s, Sandwich terns (Sterna sandvicensis)ofdifferent
age classes (chicks, fledglings, and adults) in a large
colony in the Dutch Wadden Sea were seen dying in
tremors and convulsions. Both terns (tissues and eggs)
and prey fish (clupeoid fish) were analysed for the
presence of chlorinated hydrocarbon insecticides. Con-
siderable concentrations of dieldrin, endrin, and telodrin
(an insecticide not used in Europe) were found. The
concentrations found were compared to those in hen
chicks poisoned in the laboratory, and the amounts
present in dead or dying terns were high enough to cause
their death (Koeman et al., 1968,1969;Koeman, 1971).
The Sandwich tern colony collapsed from 20 000 pairs to
less than 1000 pairs within the space of a few years time.
High concentrations were also found in mussels (Mytilus
edulis) in the western Wadden Sea. Incubating eiders
(Somateria mollissima) died in large numbers and the
breeding population declined at Vlieland, the main
colony, from ca. 4000 to 800 pairs (Swennen, 1972). The
source of the pollution, a large insecticide-producing
industrial plant near the mouth of the river Rhine, was
identified and measures were taken to stop the routine
discharges of chemicals into the river. This resulted in a
significant decrease in the amounts of telodrin in the
coastal North Sea environment. Both the eider and
the tern populations have largely recovered since
(Koeman et al., 1972;Brenninkmeijer and Stienen, 1992;
Camphuysen, 1996).
Acknowledgements
We thank Dr S. P. R. Greenstreet and an anonymous
referee for helpful comments on a draft of this paper.
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