Content uploaded by Damian Lidgard
Author content
All content in this area was uploaded by Damian Lidgard on Apr 05, 2018
Content may be subject to copyright.
REVIEW
Marine mammal culling programs: review of effects on
predator and prey populations
W. D. BOWEN* Population Ecology Division, Bedford Institute of Oceanography, Dartmouth, NS B2Y
4A2, Canada. E-mail: don.bowen@dfo-mpo.gc.ca
Damian LIDGARD Biology Department, Dalhousie University, Halifax, NS B3H 4JI, Canada.
E-mail: damian.lidgard@dal.ca
Keywords
cetaceans, pinnipeds, predator control, seals
*Correspondence author.
Submitted: 3 August 2011
Returned for revision: 20 October 2012
Revision accepted: 26 April 2012
Editor: KH
doi:10.1111/j.1365-2907.2012.00217.x
ABSTRACT
1. Culling is widely practised as a means to reduce predation effects of terrestrial
carnivores, birds and marine mammals in many parts of the world. Of marine
mammals, coastal pinniped species have usually been the target of culling pro-
grams, but dolphins and a large odontocete have also been culled.
2. We reviewed the published literature on marine mammal culling programs to
evaluate the extent of their efficacy as a fisheries management measure.
3. Changes in species’ distributions and abundance demonstrate that culling pro-
grams can be very effective at reducing predator density.
4. Several conclusions from experimental studies of terrestrial mammals and
birds may also apply to marine mammal control. Firstly, predator removal gener-
ally increases productivity and population size of target prey populations, but not
always. Secondly, culling programs typically involve a large proportional reduction
(>50%) in predator populations.
5. Thirdly, the effects of culling are typically dependent on continued control, and
in the absence of control the population rapidly returns to pre-culling density.
This underscores the need for predator removal to be a long-term management
strategy. Fourthly, culling predators often has non-intuitive and unintended con-
sequences for target species and for other predator and prey species.
6. Marine mammal culling programs rarely have measurable objectives with
respect to prey populations, and their success has not been evaluated. Culling
marine mammals is controversial because of the following: (i) they are high-
profile charismatic megafauna; (ii) many populations are recovering from a
period of over-exploitation while others remain threatened or endangered; and
(iii) the scientific evidence needed to justify a cull is usually highly uncertain.
7. Marine mammal culling programs should be based on scientific analysis with
stated and measurable objectives to be evaluated during planned follow-up
monitoring.
INTRODUCTION
Some 270 species comprise the Carnivora, a diverse group
of terrestrial and aquatic species representing 11 families of
mammals. Many of these species limit or regulate prey
species populations and their top-down effects alter the
structure and functioning of ecosystems, either through
control of herbivore populations or of medium-sized
predators when predation pressure from top predators is
reduced (Crooks & Soule 1999, Terborgh et al. 1999,
2001, Berger et al. 2001, Johnson et al. 2007). Because of
these effects and the prey species consumed (which are
often commercially valuable), carnivore–human conflicts
are common and widespread (Treves & Karanth 2003).
Although these conflicts have a long history (wolf Canis
lupus control to protect livestock dates back 2500 years in
bs_bs_banner
Mammal Review ISSN 0305-1838
1Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
Greece; Reynolds & Tapper 1996), expansion of human
activities combined with the recovery of over-exploited
animal populations has led to an increase in contact and
conflict between people and predators in many parts of the
world (Woodroffe & MacDonald 1995, Berger 2006).
Predation by marine mammals on fish and shellfish species
of commercial importance also has been a source of conflict
with fisheries for centuries (e.g. Merriam 1901, Worthington
1964, Fiscus 1979, Gulland 1987, Bearzi et al. 2004). Increas-
ing pressure on fisheries (Anonymous 2010) coupled with an
increase in the perception of conflict with marine mammals,
particularly pinnipeds, has renewed an interest in the use of
culling as a management tool to alleviate conflicts (e.g.
Anonymous 2011). The perceived conflict between harvesters
and marine mammals underlies recent calls for increased
whaling in the context of ecosystem management and the
‘whales eat fish’ argument (Gerber et al. 2009).
The objectives of this review are fourfold. The first is
briefly to review predator effects on prey populations. The
second is to evaluate the efficacy of marine mammal preda-
tor control (i.e. culling – killing animals for a specific
purpose, e.g. to reduce the perceived negative effects of a
predator on prey species of interest to humans) on prey
populations. In most cases, this amounts to determining if
culling predators increases the productivity and population
size of the target prey species. Although culling has been
used widely to control marine mammal species, the results
of those programs have not been comprehensively reviewed.
The third is to draw some lessons about predator control as
a management tool. Here, we draw on experimental studies
from the terrestrial and freshwater literature, as there are
few experimental studies of the efficacy of culling in marine
ecosystems. The fourth is to provide recommendations with
respect to culling marine mammals.
METHODS
We reviewed the literature by querying the Web of Science
for articles containing the following topic expressions, pub-
lished during the period 1900–2010: vertebrate predator
control, vertebrate predator removal, predator–human con-
flict, predator–prey conflict, seal-fishery, cull* and seal pre-
dation. Additional primary literature and government
reports referenced in papers identified in the Web of Science
queries were also consulted.
RESULTS
Predator–prey background
Predator control is based on the assumption that predators
limit prey abundance and that a decrease in predators will
increase prey productivity or abundance. Many consider that
removing predators should increase prey populations, but
predator–prey interactions usually are far too complex to
assume this. For example, if prey are limited by habitat, then
removal of predators has little impact. The success of preda-
tor removal depends on what fraction of natural mortality is
caused by the predator and how other sources of natural
mortality interact. Thus, to manage predator and prey popu-
lations successfully, it is important to know if there is indeed
an impact of predators on prey and then to quantify this
impact (Graham et al. 2005). Sinclair et al. (1998) attempted
to predict the size of the prey population needed to overcome
predation effects and the degree of predator reduction
needed to allow prey populations to increase. Assuming that
predation was known to be the cause of the decline, Sinclair
et al. (1998) observed that to counteract predation effects
requires knowledge not only of the degree of predation but
also of the nature of the functional response, because the
stability of the interaction differs depending on the type of
functional response. Thus, three types of evidence from a
predator–prey interaction are relevant to management and
the decision to cull. Firstly, do per capita rates of change for
prey increase or decrease with declining prey densities?
Secondly, is predation depensatory or density dependent?
Thirdly, what is the magnitude of predation?
The view that predators can limit prey populations has
been a source of debate dating back to the middle of the last
century (Nicholson 1933, Andrewartha & Birch 1954).
Population limitation occurs when factors, such as preda-
tion, reduce the rate of population growth to limit the
population below its carrying capacity (Sinclair & Pech
1996). There are two schools of thought on the effects of
predation. The ‘compensatory hypothesis’ states that preda-
tors consume the proportion of the prey population that
would have suffered natural mortality in the absence of
predation (Errington 1946, Jenkins et al. 1963). Under this
hypothesis, control of predators would not be expected to
result in larger or more productive prey populations. By
contrast, the ‘additive hypothesis’ states that predation
causes mortality above the level that would have occurred in
the absence of predation and thus can limit prey population
numbers (Valkama et al. 2005). Under this hypothesis,
predator removal can be expected to result in either
increased productivity or abundance of prey. Both hypoth-
eses have received support in studies of wild populations
(see, e.g. references in Holt et al. 2008). There is almost cer-
tainly a continuum of responses, with the compensatory
mortality hypothesis at one end of the continuum and the
additive mortality hypothesis at the other. Nevertheless, Sin-
clair and Pech (1996) have argued that completely additive
mortality and exact compensation are unlikely conditions.
Predators can exert density dependent, inverse density
dependent and more complex effects on prey populations
(Sinclair & Pech 1996). The total response of predators to
Marine mammal predator control W. D. Bowen and D. Lidgard
2Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
changes in prey density is the product of two components –
the functional response and the numerical response – and
represents the total proportional mortality imposed by the
predator on its prey. At high prey density, both functional
and numerical responses reach an asymptote because of
handling time and satiation in the former and interference
in the latter. This means that the prey will experience
decreasing proportional mortality, i.e. predation is depensa-
tory at high prey density.
Effects of predators on prey populations depend on the
form of the functional response (Sinclair & Pech 1996). If
the predator functional response is type II, the proportional
mortality on prey is dispensatory at all prey densities. If the
functional response is type III, then the accelerating part of
the curve at low prey density has a density-dependent effect
on prey, whereas the decelerating part at high prey density is
depensatory. If prey density is low and the predation rate is
greater than recruitment, predators can drive prey extinct.
For this to happen, predators must have a type II functional
response, no density dependence in numerical response,
and predators must depend primarily on another prey.
Examples of this are reported for wolves driving caribou
Rangifer tarandus extinct while depending on moose Alces
alces (Seip 1992), and for small carnivores driving passerine
bird populations extinct (Terborgh 1992).
Culling marine mammals
Culling marine mammals ostensibly to protect fish stocks
has a long history (Smith 1995, Lavigne 2003, Bearzi et al.
2004) and has been undertaken in many parts of the world.
This history involves culls on eight species of pinnipeds and
a similar number of odontocete species in 14 countries
(Table 1). In Canada and the USA, culling programs were
conducted on both the east and west coasts, including in
Alaska, USA. With the exception of the selective cull of
Cape fur seals Arctocephalus pusillus pusillus in South Africa
to reduce predation on Cape gannets Morus capensis
(Makhado et al. 2009), conflicts with marine mammals are
about perceived economic loss and the belief that consump-
tion by marine mammals represents losses that would
otherwise be available to fisheries.
PINNIPEDS
Three of 15 phocids and five of 17 otariid species have been
culled (Fig. 1). Grey seals Halichoerus grypus, harbour seals
Phoca vitulina and ringed seals Histriophoca fasciata have
been the targets of control of phocid species (Table 1).
These species and the five otariid species have coastal distri-
butions for at least part of the year, making them accessible
to hunters. The sole member of the Odobenidae, the walrus
Odobenus rosmarus, apparently has not been culled.
One of the first large-scale control programs was under-
taken in the Baltic Sea against grey and ringed seals
(Table 1) which were considered competitors with fisher-
men. Several bounty systems were introduced to reduce the
seal stocks and protect stocks of Atlantic cod Gadus morhua,
herring Clupea harengus and sprat Sprattus sprattus.Grey
seals were culled for 38 years beginning in 1889. This was
followed by decades of culls of ringed seals beginning in
1889 in Denmark (36 years), 1903 in Sweden (64 years) and
1909 in Finland (60 years; Harding & Harkonen 1999).
Bounties dramatically reduced the seals’ populations, by
perhaps 80% in the 1950s. This decrease was followed by a
second decline in the 1960s because of reduced reproductive
success caused by pollutants (Harding & Harkonen 1999).
There appears to have been no evaluation of the impacts of
the culls on prey populations.
During the same period, seals and sea lions were consid-
ered competitors with fisheries in western North America
(Table 1). In 1899, the California State Board of Fish
Commissioners authorized a two-year cull of California
sea lions Zalophus californianus on the grounds that sea
lions were ‘highly destructive of the salmon fishery’
(Oncorhynchus spp.; Merriam 1901). In British Columbia,
Canada, harbour seals were culled for almost 50 years,
beginning in 1914, despite the fact that the harbour seal
population had been decimated by a long period of com-
mercial harvesting that ended in 1914 (Olesiuk 2009).
Although more than 2900 harbour seals per year were
reported killed for bounty in most years between 1914 and
1963, at least as many kills probably went unreported (Bigg
1969). The cull held the population roughly stable, at
perhaps 40% of historical abundance, until another period
of commercial harvesting dramatically reduced the popula-
tion to about 10% of the estimated historical population
size (Olesiuk 2009). Steller sea lion Eumetopias jubatus
numbers were also controlled along the British Columbia
coast until their protection in 1970 (Table 1). The control
programs and commercial harvests reduced the population
to about one-quarter to one-third of historic levels (Bigg
1984, 1985). In order to protect coastal fisheries in Oregon,
USA, control programs were conducted against harbour
seals, northern sea lions Callorhinus ursinus and California
sea lions for seven years, beginning in 1925 and again
for a period of three decades ending in 1967. These culls
were thought to have reduced harbour seal numbers by
about 50%. Sea lions declined by an unknown amount.
Further north in Alaska, control of harbour seals and
Steller sea lions began in 1927 to attempt to protect Pacific
salmon Oncorhynchus spp. fisheries (Table 1). For almost
50 years, both culls and bounties were employed, but little
effort was given to determining by how much the seal
populations were reduced or how salmon populations
responded.
W. D. Bowen and D. Lidgard Marine mammal predator control
3Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
Table 1. Culls conducted to reduce numbers of marine mammal predators to protect fisheries. From a Web of Science search for papers published in 1900–2010
Species Dates Location Target prey Predator reduction Prey response Source
Pinnipeds
Phocidae
Grey and ringed seal 1889–1927, 1941–77
Denmark; 1903–67
Sweden; 1909–18,
1924–75 Finland
Baltic Sea Cod, herring, sprat Populations reduced by
c. 80%
None at time, recent
evaluation using
ecosystem model
simulations
Harding & Harkonen
1999, Hansson et al.
2007
Harbour seal 1891–1905; 1937–45
Maine; 1888–1962
Massachusetts
Eastern USA Cod, mackerel Scomber
scombrus, other fishes,
salmon, lobster
Homarus americanus
Population was reduced
greatly; estimate
72000–136000
claimed for bounty
Unknown Lelli & Harris 2006, Lelli
et al. 2009
Harbour seal 1914–63 British Columbia, Canada Herring, salmon Population reduced 60%
from historical level
Unknown Olesiuk 2009
Harbour seal 1927–67 Alaska, USA Salmon in gill net fishery Bounty and cull, not clear
how much populations
were reduced
Unknown Lensink 1958
Harbour seal 1924–33; 1936–67 Columbia River, North
America
Salmon c. 50% reduction in
harbour seals
Unknown Pearson & Verts 1970
Harbour seal 1927–76 Nova Scotia, Canada Inshore fisheries Population was
substantially reduced
Unknown Boulva & McLaren 1979
Grey seal 1934; 1962–65 – pup
culls; 1978 – pups and
adult females
UK Salmon Population continued to
increase
Unknown Harwood & Greenwood
1985, Bonner 1989
Grey seal 1967–83 Eastern Canada,
excluding Sable Island
Inshore fishing gear
and/or catch: cod,
salmon, mackerel,
herring, lobster
Population continued to
increase
Unknown Mansfield & Beck 1977,
Zwanenburg et al.
1985
Grey seal 1978–90 Gulf of St. Lawrence,
Canada
Not specified Culling pups – population
briefly stabilized
Unknown Lavigueur & Hammill
1993
Grey seal 1980–90; 2003– Norway Coastal fisheries Bounty seems to have
stabilized population
Unknown Nilssen & Haug 2007
Grey and harbour
seal
1982– Iceland Cod Grey seal reduced by c.
50% and eliminated
from northeast coast;
harbour seal reduced
by 66%
No formal evaluation, cod
biomass fluctuated
without trend
Hauksson & Bogason
1997, Anonymous
2008
Marine mammal predator control W. D. Bowen and D. Lidgard
4Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
Grey and harbour
seal
1993–2004; 2005– Scotland Salmon Harbour seal population
reduced by 25–55%,
grey seal no trend
Management plan to
evaluate success with
respect to objectives
agreed in 2005
Thompson et al. 2007,
Butler et al. 2008,
2011
Otariidae
California sea lion c. 1897–99 California, USA Salmon Unknown Unknown Merriam 1901
California sea lion 2005– Oregon, Columbia River,
USA
Salmon Selective on few
individuals
Increasing http://www.dfw.state.or.us/
fish/sealion/index.asp
Steller sea lion 1913–16; 1923–39 British Columbia, Canada Salmon Local extinction Salmon stock went
extinct some time after
sea lions exterminated
Bigg 1985, McKinnell
et al. 2001, Olesiuk
pers. comm. 2010
Steller sea lion 1927–67 Alaska, USA Salmon in gill net fishery Bounty and cull, not clear
how much populations
were reduced
Unknown Lensink 1958
Cape fur seal 1921; 1928–29;
1948–49
Tasmania, Australia Taken from seriously
depleted population
Unknown R. Kirkwood pers.
comm., Ling 1999
Northern and
California sea lion
1925–31 Oregon, USA Coastal commercial
fishes
Sea lions declined by
unknown amount
Unknown Pearson & Verts 1970
Cape fur seal 1993– Namibia Commercial fishes Mainly pups killed,
population declining
Unknown http://www.mfmr.gov.na
Cape fur seal 1993–2001; 2007 South Africa Cape gannet Targeted removal of 153
selected individuals
Seal predation mortality
reduced by c. 7%;
effects short term
David et al. 2003;
Makhado et al. 2009
Cetaceans
Dolphins c. 1910–82 Japan Yellowtail, damage to
gear and catch
No evaluation of success
of culling; unknown
effects on dolphin
numbers
No evidence that cull had
any positive impact on
yellowtail
Kasuya 1985
Short-beaked common
dolphin, bottlenose
dolphin Tursiops
truncatus
Historical times;
1940–60 (Croatia);
1930–60 (Italy)
Adriatic Sea Fisheries in general Dolphin populations
declined by unknown
amount
No evaluation of effects
on fisheries
Bearzi et al. 2004
Killer whale 1969–80 Norway Herring 700 whales Stock failed to recover
until mid-1980s
Oien 1988, Dragesund
et al. 1997
W. D. Bowen and D. Lidgard Marine mammal predator control
5Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
On the east coast of North America, bounties for harbour
seals began in the late 1880s in Maine and Massachusetts,
USA, and in about 1927 in Nova Scotia, Canada, to reduce
the number of seals ‘harassing’ and competing with fisher-
men (Table 1, Boulva 1973). What appears to be the longest
control program (74 years) took place in Massachusetts
from 1888 to 1962. In Massachusetts and Maine together,
beginning in 1891, it is estimated that between 72000 and
136000 seals were killed for the bounty (Lelli et al. 2009).
Although the extent of reduction is not known, it was clear
that the populations were greatly reduced. Further north in
Nova Scotia, culling did not commence until some 40 years
later, but continued for 50 years, ending in 1976. Although
aimed at harbour seals, the bounty included an unknown
proportion of grey seals until 1949 when the submission of
a jaw was required to claim a bounty. This long period of
hunting greatly reduced the harbour seal population,
although again quantitative estimates of the reduction are
not available. In each of the above jurisdictions, there
appears to have been no analysis of the benefit of these
long-standing culls on fish stocks.
In Norway, grey seals have been hunted along the coast
for centuries. Between 1980 and 1990, a culling program
was instigated along southern and central coastal areas
(Nilssen & Haug 2007). Additional grey seals were shot by
local hunters during this period, but the numbers are
unknown. Since 2003, in areas of particular conflict with
grey seals, Norwegian management authorities have used
hunting to control the grey seal population size by permit-
ting a quota of 20–30% of the estimated population,
assessed every 5 years. Although a time series of estimates is
not available, there was probably no significant difference in
population estimates in 1996–98 and in 2001–03; both
suggest a population of 4000–6000 seals. There seems to
have been no evaluation of the effects of controlling seals on
fisheries.
Grey seals have also been hunted for centuries in Iceland
(Hauksson 2007). The shooting of grey seals is allowed in all
areas except the west coast and a bounty program was initi-
ated in 1982 to address conflicts with fisheries. Grey seals
and harbour seals are thought to compete with fisheries and
to show a preference for cod (Hauksson & Bogason 1997),
although the authors of the study provide no evidence for
either conclusion other than that cod are eaten by seals.
Increased hunting beginning in 1990 resulted in a reduction
in the distribution of grey seals and their disappearance
along the northeast coast. Abundance estimates indicated
that the size of the grey seal population had declined by
about 3% per year from 1982 to 1990 and by 6% per year
from 1990 to 2002, due to the increased hunting effort. By
comparison, the harbour seal population was reduced by
66%. During this period of culling, cod spawning stock
biomass fluctuated without trend and average recruit-
ment declined slightly, suggesting no obvious population
response to the seal culls (Anonymous 2008).
Complaints about the effects of seals on fisheries in the
UK are thought to have begun in the 1920s, in connection
with damage done to Atlantic salmon Salmo salar popula-
tions by grey seals (Rae 1960). As a result, predator control
programs against grey seals were undertaken in the 1930s to
protect salmon (reviewed by Harwood & Greenwood 1985,
Bonner 1989). In the early 1960s, the grey seal population
1Arctocephalus pusillus doriferus
1880 20201920 1960 200019801900 1940
Grey and
Ringed seal
Harbour seal
Steller sea lion
California and
Northern sea lion
Cape fur seal
Maine, USA
Massachusetts, USA
British Columbia, Canada
Alaska, USA
Nova Scotia, Canada
Iceland
UK
Denmark
Sweden
Finland
Eastern Canada
UK
Norway
Iceland
California, USA
British Columbia, Canada
Alaska,
USA Oregon, USA
Oregon, USA
Namibia
South Africa
Australian fur seal1
Tasmania, Australia
Fig. 1. Timeline and locations of pinniped cull programs.
Marine mammal predator control W. D. Bowen and D. Lidgard
6Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
had increased to the point where control in Orkney (Scot-
land) and the Farne Islands (England) was proposed to
reduce the population to three-quarters of its current size
by killing moulted pups. Although culling began in 1963, by
1965 on the Farne Islands the National Trust, owner of the
Islands, decided that culling seals was not consistent with
the goals of the reserve and did not permit further killing.
Further complaints of damage to fisheries led to a new
control program, which would have reduced the Orkney
and the Outer Hebrides (Scotland) populations from 50000
in 1976 to 35000 in the end of 1982, through killing both
adult females and pups. However, public protest after the
first cull in 1978 on the Orkneys resulted in a return to pup
culling only, which had already proved inadequate to limit
population growth and had the further undesirable feature
that the effects of culling were not evident in pup produc-
tion figures until about 6 years after culling began
(Harwood & Prime 1978). Side effects from the adult female
cull were also evident. Firstly, some females failed to return
to breed and, secondly, some females that came ashore to
breed abandoned their pups when the colony was disturbed
(Summers & Harwood 1979). While these unintended
effects could be seen as increasing the effectiveness of the
cull, they also raise ethical issues in terms of responsible
management. There seems to have been no evaluation of
the effectiveness of this limited control program on fish
stocks.
The largest sustained cull of a pinniped occurs in
Namibia, where since 1993 large numbers of Cape fur seal
pups have been killed during the breeding season. The cull
began during a period of declining fish stocks thought to be
partly caused by poor environmental conditions. Justified to
protect fish stocks, the number of fur seal pups culled
increased from c. 50000 in 1993 to 85000 in 2009. Annually
since 2006, an additional 6000 adult males have been culled.
There appears to be no published scientific analysis of the
predation mortality caused by fur seals or how this mortal-
ity compares with other sources of natural mortality on
target fish stocks. Again, there appears to have been little
effort to evaluate the impact of the seal culls on fish stock
productivity, although productivity did increase with the
return of favourable environmental conditions in the late
1990s (http://www.mfmr.gov.na).
Pinniped culls have typically been non-selective and have
resulted in the killing of large numbers of animals.
However, recently several selective culls have been used to
reduce predation mortality caused by seals (Table 2). Cape
fur seals prey upon young Cape gannets. Between 1993 and
2001 and again in 2007, the targeted removal of individual
fur seals known to have eaten gannets successfully reduced
mortality. Selective removal of small numbers of individuals
has also been used since 2005 to reduce predation by
Californian sea lions on endangered populations of Pacific
salmon, including steelhead Oncorhynchus mykiss, on the
Columbia River, Oregon (Stansell et al. 2010).
Based on the published literature, it appears that in about
46% of the populations culled (often in multiple time
periods, see Table 1) the extent of the resulting population
decline is unknown (Table 2). Overall, 79% of culled popu-
lations declined, whereas the remainder are thought or
known to have increased or remained stable (Table 2).
There appear to have been two local extinctions: Steller sea
lions at a site in British Columbia and grey seals along the
northeast coast of Iceland.
CETACEANS
Culling dolphins has an equally long or perhaps even
longer history than culling pinnipeds, having occurred in
the Adriatic Sea (Bearzi et al. 2004) and the Black Sea
(Mitchell 1975, Birkun 2002) in historical times. A culling
campaign against dolphins, mainly short-beaked common
dolphins Delphinus delphis, was launched in 1949 in
Croatia with the intent of eradicating them from the
Adriatic Sea (Table 1). Bounties to promote the killing
of dolphins were also paid in Italy from the early 1930s.
Although the number of animals killed is poorly docu-
mented, dolphin populations are thought to have declined
by an unknown amount.
Dolphins were viewed as competitors in the yellowtail
Seriola quinqueradiata fishery in Japan, so fishermen were
paid to cull five species from about 1910 to 1982 (Table 1).
As there were no species-specific estimates of the size of
these dolphin populations, it was not possible to determine
the impact of culls on the dolphin species, or their effect on
fishery interactions, with any confidence (Kasuya 1985).
Apparently, the only large odontocete species to have
been culled is the killer whale Orcinus orca (Table 1). When
the Norwegian spring-spawning herring population col-
lapsed in the late 1960s, mainly as a result of massive over-
fishing, the government organized a hunt of resident killer
whales which were known to eat herring. Over 700 whales
Table 2. Pinniped population trends at the end of culling programs
listed in Table 1
Population status at end of cull Number of populations
Increasing 2
Stable 3
Decline >75% 3
Decline >25% <75% 3
Decline of unknown extent 11
Local extinction 2
Total* 24
*Excluding two selective culls involving small numbers of Cape fur seals
and California sea lions.
W. D. Bowen and D. Lidgard Marine mammal predator control
7Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
were killed between 1969 and 1980 (Oien 1988). During this
period, the herring stock remained at very low levels and
showed no signs of recovery until the mid-1980s (Drage-
sund et al. 1997). Killer whale predation appears not to have
been considered further as a limiting factor on herring stock
dynamics, although northern minke whale Balaenoptera
acutorostrata predation has been investigated (Tjelmelan &
Lindstrøm 2005).
Predicting the effects of predator removal
on prey populations and ecosystems
Although predators have frequently been culled to alleviate
conflict with terrestrial and marine mammals, little atten-
tion has been given to evaluating the success of culls. Deter-
mining the benefit to a fishery or hunt of having reduced a
predator population is confounded by several aspects of
predator–prey ecology (DeMaster & Sisson 1992). Prey
species usually have more than one predator and thus gains
from culling may be offset by changes in the functional,
aggregative or numerical responses of other predators.
Predators are rarely dependent on a single prey and this
could result in either greater or lesser impact depending on
the functional response of the predator. In the marine envi-
ronment, recruitment to fish populations is highly variable
and difficult to predict but has a large impact on prey abun-
dance. This last point led participants of the Benguela
Ecology Programme Workshop to conclude that compari-
son of fishery yields before and after a seal cull ‘would
almost certainly not provide a reliable indication of its
effect’ (Butterworth & Harwood 1991). Fish usually are the
dominant predator in aquatic ecosystems that have been
studied (e.g. Bax 1991, Trites et al. 1997) and so reducing
populations of marine mammals is likely to produce only
marginal increases in yield that could be difficult to detect
(Gulland 1987, DeMaster & Sisson 1992). Finally, because
of the inherent indeterminacy of outcomes of multispecies
manipulations (Yodzis 1988), an experimental approach to
evaluating the benefit of a cull is often impracticable.
As indicated above, the magnitude of declines is often not
known for marine mammal populations that have been
culled. Thus, it should not be surprising to learn that the
more difficult goal of evaluating the benefit to prey popula-
tions has rarely been attempted. When an evaluation was
done, it was generally not part of the control program itself.
For example, despite the long history of non-sustainable
harvesting and culling of both harbour seals and Steller sea
lions in British Columbia, only recently have analyses shed
light on the probable impacts of previous harbour seal
culls on target prey populations (P. Olesuik pers. comm.).
Harbour seals in the Strait of Georgia, British Columbia,
feed mainly on Pacific hake Meluccius productus and Pacific
herring Clupea pallasii. Herring stock assessments indicate
that herring survival rates declined as harbour seal preda-
tion increased. Selective predation by seals may also explain
an observed decline in the mean weight at age of herring
and size at age of hake, as seal populations increased. In the
1980s, hake consumed mainly juvenile hake and juvenile
herring; however, the smaller hake now feed on euphausiids.
It has been hypothesized that reduced cannibalism by older
hake has led to improved recruitment and higher numerical
abundance of young hake. Thus, hake biomass has
remained stable. Overall predation on herring appears not
to have changed much, but seals have displaced hake as the
primary herring predator. Recruitment rates of herring have
also increased, and there is a positive relationship between
seal abundance and herring recruitment (presumably
because seals are removing large hake which feed on juve-
nile herring). Given these interactions, the previous culling
of harbour seals from this system may have had complex
consequences for prey population dynamics, but those con-
sequences were not explicitly evaluated.
The potential consequences of seal culling in the Baltic
Sea on target fish populations over the last century have
been recently evaluated using ecosystem models to compare
the effects of different scenarios of seal abundance, fishing
pressure and nutrient loads on fish production (Hansson
et al. 2007). Hansson and Rudstam (1990) hypothesized
that the increase in Baltic Sea fish catches during the past
century has been made possible by the increased productiv-
ity resulting from eutrophication. Thus, fish production has
been influenced by a combination of eutrophication (which
has both positive and negative effects), decreased seal preda-
tion and increased fishing. To account for these interacting
factors, an ecosystem model was constructed. Status quo
scenarios of c. 9000 seals were compared with a historical
population of 100000 seals, which authors considered con-
servative as estimated historical abundances in the Baltic
ranged from c. 200000 ringed seals and 100000 grey seals
(Harding & Harkonen 1999) to upwards of 450000 ringed
seals and 200000 grey seals (Kokko et al. 1999). Increasing
seal abundance in the model predicted a 30% drop in
Atlantic cod abundance, a lesser decline in herring and an
increase in Baltic sprat Sprattus sprattus balticus abundance.
However, if the fishery was managed according to a precau-
tionary approach, the model predicted that seal populations
could be as large as they were a century ago, and the stocks
of cod and herring would still be as high as or higher than
they were in the reference period of 1996–2000. Hansson
et al. (2007) concluded that a decrease in benthic produc-
tion had greater negative effects on cod than an increase
in seals.
The most thoroughly analysed example of a proposed
marine mammal cull is in the Benguela ecosystem off the
southwest coast of South Africa (Butterworth & Harwood
1991). Here, interactions between Cape fur seals and hake
Marine mammal predator control W. D. Bowen and D. Lidgard
8Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
fisheries have been well studied with respect to the probable
benefits of culling. Two species of hake are involved, one
inhabiting shallow water (Merluccius capensis) and the other
inhabiting deep water (Merluccius paradoxus); the former
predates on small individuals of the latter. Multispecies
modelling results showed that a reduction in numbers of
fur seals is likely to reduce the abundance of hake, since
fewer seals would result in more shallow-water hake, a main
food of fur seals, and thus more predation on deep-water
hake (Punt & Butterworth 1995). Using a 29-species
food-web model of the same seal-hake system, Yodzis (1998)
concluded also that seal culling may have non-intuitive
consequences, whereby the removal of an upper-trophic
level predator may lead to increases in another species, and
that culling was more likely to be detrimental to total yield
from all exploited species than it was to be beneficial.
Cetaceans are also seen as competitors with fisheries,
and governments of whaling countries have advocated the
culling of whales to allow over-exploited fish stocks to
recover and to increase fishery yields (e.g. Komatsu &
Misaki 2001). Gerber et al. (2009) examined the potential
increase in biomass of commercially important fish stocks
that might result if the number of whales in Northwest
African and Caribbean ecosystems were reduced as a fisher-
ies management action. Although the authors acknowl-
edged that the data were often scarce, their ecosystem
modelling results suggested that in the tropical ecosystems,
with a wide range of assumptions on whale abundance,
feeding rates and fish biomass, even the complete removal
of baleen whales would not lead to an appreciable increase
in biomass of commercially exploited fish. There appears to
be little overlap between fisheries and whale consumption
in terms of prey types, and fisheries remove far more fish
biomass than whales consume. By contrast, reductions in
fishing mortality were predicted to have large positive
effects on fish biomass in these ecosystems.
Insights from other taxa
As the case studies above indicate, the few evaluations of the
efficacy of culling marine mammals to increase prey popu-
lations that have been done were based on retrospective
modelling. Although modelling is valuable and often the
only possible approach, experimental studies are needed to
understand fully the costs and benefits of culling. We briefly
review experimental studies in selected terrestrial and fresh-
water systems to see what has been learned about the
efficacy of culling in these better-studied systems.
Globally, predator culling continues to be the most com-
monly used tool for increasing game abundance for hunters
(Reynolds & Tapper 1996, Cote & Sutherland 1997). Holt
et al. (2008) used 40 published studies in a meta-analysis to
quantify the effects of predators on the abundance of their
prey. They found that predator removal caused a 1.6-fold
increase in the abundance of prey, but that there was signifi-
cant heterogeneity in the prey response to culling; cases in
which culling was effective tended to involve mammalian
or multiple predators. Fletcher et al. (2010) conducted an
8-year culling experiment in northern England in which a
43% reduction in red fox Vulpes vulpes abundance and a
78% reduction in carrion crow Corvus corone abundance
led to threefold increases in breeding success of all five
ground-nesting bird species studied.
Several meta-analytical studies have been used to
evaluate the effectiveness of predator removal to enhance
bird populations. Cote and Sutherland (1997) found that
predator control was generally effective in increasing
hatching success and post-breeding population size, but
was not reliably effective in increasing the breeding popu-
lation. These authors also noted that predator removal did
not have long-lasting effects, and if it was not maintained
the benefits rapidly disappeared. Updating the work of
Cote and Sutherland (1997), Smith et al. (2010) summa-
rized the results of 83 predator removal studies to conserve
vulnerable bird populations from six continents. In most
(63%) of the studies analysed, predator removal and
control areas were compared; in the remainder, bird popu-
lations before and after predator removal were compared.
Predator control increased hatching and fledging success
but did not have a significant positive effect on post-
breeding population size. Smith et al. (2010) also found
significant heterogeneity in the population response to
predator removal and that larger increases in bird popula-
tions were achieved by culling all predator species rather
than a subset, as removing all predator species excluded
mesopredator release. Once predator removal was discon-
tinued, any positive effects on prey populations soon
disappeared, underscoring the need for a long-term man-
agement strategy (Tapper et al. 1982, Coté & Sutherland
1997, Smith et al. 2010).
Several populations of double-crested cormorants Phala-
crocorax auritus have been experimentally culled, resulting
in an increase in fish stocks (e.g. Dorr et al. 2010, Fielder
2010, Johnson et al. 2010). Schnieder et al. (1999) con-
ducted an intensive field study to determine the impact of
double-crested cormorants on smallmouth bass Micropterus
dolomieu and other fisheries in the eastern basin of Lake
Ontario, North America. The results indicated a high rate of
predation by double-crested cormorants on smallmouth
bass. A five-year control program and further research
showed that predation on target fish species declined as
cormorant numbers also declined (Burnett et al. 2002,
Lantry et al. 2002, Farquhar et al. 2004). On the basis of
these results, the program was continued, and since 2003 the
abundance of cormorants and their predation on fish in Lake
Ontario has continued to decline (Johnson et al. 2010).
W. D. Bowen and D. Lidgard Marine mammal predator control
9Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
Culls are usually conducted on the assumption that all
predators are equally likely to impact prey species, but
there is increasing evidence that this may not be the case
in a variety of taxa (fish – Svanbäck & Persson 2004,
mammals – Estes et al. 2003, and birds – Guillemette &
Brousseau 2001, Oro et al. 2005). Yellow-legged gulls Larus
michahellis prey upon both breeding and immature storm
petrels Oceanites oceanicus and the resulting mortality is
additive to other causes of mortality (e.g. Oro et al. 2005).
Selective culling of only 16 individual gulls led to a mean
reduction of 65% in the number of storm petrel remains
found locally in gull pellets (Sanz-Aguilar et al. 2009).
Experimental results showed that predation by gulls
affected negatively both adult annual survival probability
and breeding success of petrels, and that after removing
specialist gulls, adult survival probabilities and breeding
success of storm petrels greatly and rapidly increased (by
16% and 23%, respectively).
Culling predators may have unintended consequences
for the target prey populations, depending on the nature
and complexity of the interactions among predators and
prey species (e.g. Summers & Harwood 1979, Punt &
Butterworth 1995, Yodzis 1998). Culling upper trophic level
predators can also result in mesopredator release. For
example, the removal of coyotes Canis latrans may result in
increased predation pressure by smaller (meso) predators
such as foxes Urocyon cinereoargenteus, skunks Mephitis
mephitis and domestic cats Felis catus, and the reduction or
local extinction of avian prey (e.g. Crooks & Soule 1999).
Similarly, the removal of dingos Canis lupus dingo ledtoan
increase in red fox numbers on the removal side of a dingo
exclusion fence in Australia (Letnic & Koch 2010). These
and the above examples serve to illustrate that unintended
consequences of culling top predators are perhaps not
uncommon (Paine et al. 1998, Scheffer et al. 2001, Worm &
Myers 2003).
DISCUSSION
Many terrestrial and aquatic ecosystems have been severely
changed by commercial exploitation of living resources,
habitat destruction and the effects of invasive species
(Jackson et al. 2001, Lotze & Worm 2009). A common con-
sequence of those changes is that some species become less
abundant. Where one of the threats is predation, the ques-
tion arises as to whether to control the predator to reverse
the decline in the prey population or to remove anthropo-
genic threats and hope that natural processes will return the
ecosystem towards a more desirable state (Lessard et al.
2005). Implicit in the ‘let nature do it’ approach of no inter-
vention is the concept that if left alone the system will
return to some former more desirable state. However, there
is considerable evidence that ecosystems do not generally
have a single characteristic state (Scheffer et al. 2001) and
therefore we may be misguided in thinking that passive
management actions will be sufficient (Lessard et al. 2005).
Thus, ecosystem management may require active food-web
manipulation when protection from further human threats
appears likely to fail. This underscores the importance of
determining the sources of mortality of the prey species of
concern (Lessard et al. 2005).
Culling has been widely practised to reduce marine
mammal populations. The perceived conflict with fisheries
has as much to do with fisheries practices and economics as
it has to do with the consumption of fish by native marine
mammals. Nevertheless, marine mammals are perceived as
taking too large a fraction of those fish left in the water
by fishermen. Several authors (Jackson et al. 2001, Lavigne
2003, Roberts 2007) have reminded us that the world’s
oceans were home to much larger populations of both fish
and marine mammals than they are today. So it is certainly
not clear that large populations of marine mammals pre-
clude large and productive fish populations.
Although it is widely practised, there is little evidence that
culling marine mammals to increase the abundance of tar-
geted prey species has been effective. A common feature of
marine mammal culls is the lack of explicit and measurable
objectives with respect to target populations and usually
with respect to the reduction in the size of the marine
mammal population to be achieved. Even so, Lavigne
(2003) argued that we should not expect calls for culling
marine mammals to abate in the near future, as there
appears to be little correlation between the overall size of a
marine mammal population and the conflict it generates
with fishermen. For example, although still a small fraction
of historic population size, the recovering grey seal popula-
tion in the Baltic Sea is once again considered a threat, and
the Swedish government has issued licenses to shoot several
hundred grey seals in response to complaints by fishermen
(Königson et al. 2009). Similarly, grey seals were considered
pests in Eastern Canada early in the last century when the
population size was small (Scott 1968). Due perhaps to their
coastal occurrence, it appears that the extent to which grey
and harbour seals are considered pests is largely indepen-
dent of total population size.
Several conclusions can be drawn from experimental
studies on other taxa. Firstly, predator removal can increase
the productivity and population size of target prey popula-
tions but does not always do so. Secondly, these studies
typically have involved large proportional reductions in
predator populations, presumably to increase effect size and
the statistical power to detect a significant effect. Thirdly,
the effects of culling are typically dependent on continued
control, and in the absence of control the benefits rapidly
disappear. Based on a review of predator control experi-
ments to enhance ungulate densities in North America, the
Marine mammal predator control W. D. Bowen and D. Lidgard
10 Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
National Research Council concluded that to be effective,
control must be both intense and frequent and that there is
no factual basis for assuming that short-term control will
have long-term effects (Anonymous 1997). Fourthly, culling
predators often has non-intuitive and unintended conse-
quences for target species and for other predator and prey
species. Therefore, follow-up monitoring should be a
planned component of a culling program, to evaluate the
success of culling with respect to objectives and to docu-
ment unintended consequences.
The decision to use predator control is a management
decision and not a scientific one. This decision should be
based on the best available science, but even when the scien-
tific evidence is strong, other factors, such as ethical consid-
erations and the likelihood of unintended consequences,
influence policy decisions (Reynolds & Tapper 1996).
DeMaster and Sisson (1992) argued that control programs
should only be considered if the magnitude of the increased
fishery yield can be estimated with its associated uncertainty
and if the cost of management is likely to be significantly
less than the minimum economic benefit to the fishery.
These and other ideas, such as clearly stated objectives, are
also embodied in criteria for culling marine mammals
developed by the Scientific Advisory Committee of the
Marine Mammal Action Plan (Anonymous 1999).
Although culling has often generated debate, culling
marine mammals is particularly controversial for at least
three reasons. The first is that they are regarded as charis-
matic megafauna and have a high profile in many parts of
the world. The second is that many populations of marine
mammals are still recovering or have only recently recov-
ered from a long period of over-exploitation, while others
remain threatened or endangered, raising conservation con-
cerns. The third is that the scientific evidence needed to
justify a cull is usually highly uncertain (Yodzis 2001).
ACKNOWLEDGEMENTS
The authors are grateful for comments on an earlier draft of
the manuscript by participants of a workshop on Atlantic
cod-seal interactions, Susan Heaslip, and for the helpful
comments of three anonymous reviewers. Financial support
for the work was provided by the Department of Fisheries
and Oceans, Canada.
REFERENCES
Andrewartha HG, Birch LC (1954) The Distribution and
Abundance of Animals. University of Chicago Press, Chicago,
USA.
Anonymous (1997) Wolves, Bears and Their Prey in Alaska.
National Academy Press, Washington DC, USA.
Anonymous (1999) Protocol for the Scientific Evaluation of
Proposals to Cull Marine Mammals. Report of the Scientific
Advisory Committee of the Marine Mammals Action Plan.
United Nations Enironmental Program, Rome, Italy.
Anonymous (2008) Report of the ICES Advisory Committee,
2008. ICES Advice, Copenhagen, Denmark.
Anonymous (2010) The State of the World Fisheries and
Aquaculture. Fisheries and Aquaculture Department, The
Food and Agriculture Oranization of the United Nations,
Rome, Italy.
Anonymous (2011) Towards Recovered and Sustainable
Groundfish Fisheries in Eastern Canada (FRCC.2011.R1).
Minister of Public Works and Government Services Canada,
Ottawa, Canada.
Bax NJ (1991) A comparison of the fish biomass flow to fish,
fisheries, and mammals in six marine ecosystems. ICES
Marine Science Symposia 193: 217–224.
Bearzi G, Holcer D, Notarbartolo di Sciara G (2004) The role of
historical dolphin takes and habitat degradation in shaping
the present status of northern Adriatic cetaceans. Aquatic
Conservation: Marine and Freshwater Ecosystems 14: 363–379.
Berger J, Stacey PB, Bellis L, Johnson MP (2001) A mammalian
predator-prey imbalance: grizzly bear and wolf extinction
affect avian neotropical migrants. Ecological Applications 11:
947–960.
Berger KM (2006) Carnivore-livestock conflicts: effects of
subsidized predator control and economic correlates on the
sheep industry. Conservation Biology 20: 751–761.
Bigg MA (1969) The Harbour Seal in British Columbia. Fisheries
Research Board of Canada Ottawa, Ontario, Canada.
Bigg MA (1984) Sighting and kill data of Steller sea lions
(Eumetopia jubatus) and California sea lions (Zalophus
californianus) from British Columbia during 1892–1982, with
some records from Washington and southeastern Alaska.
Canadian Data Report of Fisheries and Aquatic Sciences 460:
1–191.
Bigg MA (1985) Status of the Steller sea lion (Eumetopias
jubatus) and California sea lion (Zalophus californianus)in
British Columbia. Canadian Special Publication of Fisheries
and Aquatic Sciences 77: 1–20.
Birkun AJ (2002) Interactions between cetaceans and fisheries in
the Black Sea. In: Notarbartolo di Sciara G (ed.) Cetaceans of
the Mediterranean and Black Seas: State of Knowledge and
Conservation Strategies, Section 10, 1–11. Report to the
ACCOBAMS Secretariat, Monaco.
Bonner WN (1989) Seals and man–achanging relationship.
Biological Journal of the Linnean Society 38: 53–60.
Boulva J (1973) The harbor seal, Phoca vitulina concolor,in
Eastern Canada. PhD thesis, Dalhousie University, Halifax,
Canada.
Boulva J, McLaren IA (1979) Biology of the harbour seal, Phoca
vitulina, in eastern Canada. Bulletin of the Fisheries Research
Board of Canada 200: 1–24.
Burnett JAD, Ringler NH, Lantry BF, Johnson JH (2002) Impact
of double-crested cormorant (Phalacrocorax auritus) piscivory
W. D. Bowen and D. Lidgard Marine mammal predator control
11Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
on the yellow perch (Perca flavescens) populations in the
eastern basin of Lake Ontario. Journal of Great Lakes Research
28: 202–211.
Butler JRA, Middlemas SJ, McKelvey SA, McMyn I, Leyshon B,
Walker I et al. (2008) The Moray Firth Seal Management Plan:
an adaptive framework for balancing the conservation of
seals, salmon, fisheries and wildlife tourism in the UK.
Aquatic Conservation: Marine and Freshwater Ecosystems 18:
1025–1038.
Butler JRA, Middlemas SJ, Graham IM, Harris RN (2011)
Perceptions and costs of seal impacts on Atlantic salmon
fisheries in the Moray Firth, Scotland: implications for the
adaptive co-management of seal-fishery conflict. Marine
Policy 35: 317–323.
Butterworth DS, Harwood J (1991) Report on the Benguela
Ecology Programme workshop on seal-fishery biological
interactions. Report of the Benguela Ecology Progamme of
South Africa 22: 1–65.
Cote IM, Sutherland WJ (1997) The effectiveness of removing
predators to protect bird populations. Conservation Biology
11: 395–405.
Crooks KR, Soule ME (1999) Mesopredator release and
avifaunal extinctions in a fragmented landscape. Nature 400:
563–566.
David JHM, Cury P, Crawford RJM, Randall RM, Underhill LG,
Meyer MA (2003) Assessing conservation priorities in the
Benguela ecosystem, South Africa: analysing predation by seals
on threatened seabirds. Biological Conservation 114: 289–292.
DeMaster DP, Sisson JE (1992) Pros and cons of pinniped
management along the North American coast to abet fish
stocks. In: McCullough DR, Barrett RH (eds) Wildlife 2001:
Populations, 321–330. Elsevier Applied Science, London, UK
and New York, USA.
Dorr BS, Aderman T, Butchko PH, Barras SC (2010)
Management effects on breeding and foraging numbers and
movements of double-crested cormorants in the Les
Cheneaux Islands, Lake Huron, Michigan. Journal of Great
Lakes Research 36: 224–231.
Dragesund O, Johannessen A, Ulltang O (1997) Variation in
migration and abundance of Norwegian spring spawning
herring (Clupea harengus L.). Sarsia 82: 97–105.
Errington PL (1946) Predtion and vertebrate populations. The
Quarterly Review of Biology 21: 221–245.
Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE
(2003) Individual variation in prey selection by sea otters:
patterns, causes and implications. The Journal of Animal
Ecology 72: 144–155.
Farquhar JF, Mazzocchi IM, McCullough RD (2004)
Management of Double-Crested Cormorants in the Eastern
Basin of Lake Ontario, 1999–2003: a Summary and
Recommendations. New York State, Department of
Environmental Conservation Special Report, Albany,
New York, USA.
Fielder DG (2010) Response of yellow perch in Les Cheneaux
Islands, Lake Huron to declining numbers of double-crested
cormorants stemming from control activities. Journal of Great
Lakes Research 36: 207–214.
Fiscus CH (1979) Interactions of marine mammals and Pacific
hake. Marine Fisheries Review 10: 1–9.
Fletcher K, Aebischer NJ, Baines D, Foster R, Hoodless AN
(2010) Changes in breeding success and abundance of
ground-nesting moorland birds in relation to the
experimental deployment of legal predator control. The
Journal of Applied Ecology 47: 263–272.
Gerber LR, Morissette L, Kaschner K, Pauly D (2009) Should
whales be culled to increase fishery yield? Science 323:
880–881.
Graham K, Beckerman AP, Thirgood S (2005)
Human-predator-prey conflicts: ecological correlates, prey
losses and patterns of management. Biological Conservation
122: 159–171.
Guillemette M, Brousseau P (2001) Does culling predatory gulls
enhance the productivity of breeding common terns? The
Journal of Applied Ecology 38: 1–8.
Gulland JA (1987) Seals and fisheries: a case for predator
control? Trends in Ecology & Evolution 2: 102–103.
Hansson S, Rudstam LG (1990) Eutrophication and Baltic fish
communities. Ambio 19: 123–125.
Hansson S, Hjerne O, Harvey C, Kitchell JF, Cox SP, Essington
TE (2007) Managing Baltic Sea fisheries under contrasting
production and predation regimes: ecosystem model analyses.
Ambio 36: 265–271.
Harding KC, Harkonen TJ (1999) Development in the Baltic
grey seal (Halichoerus grypus) and ringed seal (Phoca
hispida) populations during the 20th century. Ambio 28:
619–627.
Harwood J, Greenwood JD (1985) Competition between British
grey seals and fisheries. In: Beddington JR, Beverton RJH,
Lavigne DM (eds) Marine Mammals and Fisheries, 153–169.
George Allen & Unwin, London, UK.
Harwood J, Prime JH (1978) Some factors affecting the size of
British grey seal populations. The Journal of Applied Ecology
15: 401–411.
Hauksson E (2007) Abundance of grey seals in Icelandic waters,
based on trends of pup-counts from aerial surveys.
NAMMCO Scientific Publications 6: 85–98.
Hauksson E, Bogason V (1997) Comparative feeding of grey
(Halichoerus grypus) and common seals (Phoca vitulina)in
coastal waters of Iceland, with a note on the diet of hooded
(Cystophora cristata) and harp seals (Phoca groenlandica).
Journal of Northwest Atlantic Fishery Science 22: 125–135.
Holt AR, Davies ZG, Tyler C, Staddon S (2008) Meta-analysis of
the effects of predation on animal prey abundance: evidence
from UK vertebrates. PLoS ONE 3: e2400.
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW,
Bourque BJ et al. (2001) Historical overfishing and the recent
collapse of coastal ecosystems. Science 293: 629–637.
Jenkins D, Watson A, Miller GR (1963) Population sudies on red
grouse, Lagopus lagopus scoticus (Lath) in Northeast Scotland.
The Journal of Animal Ecology 32: 317–376.
Marine mammal predator control W. D. Bowen and D. Lidgard
12 Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
Johnson CN, Isaac JL, Fisher DO (2007) Rarity of a top predator
triggers continent-wide collapse of mammal prey: dingoes
and marsupials in Australia. Proceedings of The Royal Society
B: Biological Sciences 274: 341–346.
Johnson JH, McCullough RD, Farquhar JF (2010) Double-Crested
Cormorant Studies at Little Galloo Island, Lake Ontario in
2009: Diet Composition, Fish Consumption and the Efficacy of
Management Activities in Reducing Fish Predation. Annual
Report, Bureau of Fisheries Lake Ontario Unit and St.
Lawrence River Unit, to the Great Lakes Fishery Commission’s
Lake Ontario Committee, Ann Arbor, Michigan, USA.
Kasuya T (1985) Fishery dolphin conflict in the Iki Island area
of Japan. In: Beddington JR, Beverton RJH, Lavigne DM (eds)
Marine Mammals and Fisheries, 253–275. Allen & Unwin,
London, UK.
Kokko H, Helle E, Lindström J, Ranta E, Sipila T, Courchamp F
(1999) Backcasting population sizes of ringed and grey seals
in the Baltic and Lake Saimaa during the 20th century.
Annales Zoologici Fennici 36: 65–73.
Komatsu M, Misaki S (2001) The Truth Behind the Whaling
Dispute. Institute of Cetacean Research, Tokyo, Japan.
Königson S, Lunneryd S-G, Stridh H, Sundqvist F (2009) Grey
seal predation in cod gillnet fisheries in the central Baltic Sea.
Journal of Northwest Atlantic Fishery Science 42: 41–47.
Lantry BF, Eckert TH, Schneider CP, Chrisman JR (2002) The
relationship between the abundance of smallmouth bass and
double-crested cormorants in the eastern basin of Lake
Ontario. Journal of Great Lakes Research 28: 193–201.
Lavigne DM (2003) Marine mammals and fisheries: the role of
science in the culling debate. In: Gales N, Hindell M,
KirkwoodR(eds)Marine Mammals: Fisheries, Tourism, and
Management Issues, 31–47. CSIRO, Collingwood, Australia.
Lavigueur L, Hammill MO (1993) Distribution and seasonal
movements of grey seals, Halichoerus grypus, born in the Gulf
of St. Lawrence and Eastern Nova Scotia. The Canadian
Field-Naturalist 107: 329–340.
Lelli B, Harris DE (2006) Seal bounty and seal protection laws in
Maine, 1872 to 1972: historic perspectives on a current
controversy. Natural Resources Journal 46: 881–924.
Lelli B, Harris DE, Aboueissa A-M (2009) Seal bounties in
Maine and Massachusetts, 1888 to 1962. Northeastern
Naturalist 16: 239–254.
Lensink CJ (1958) Predator Investigation and Control. Alaska
Department of Fish and Game Annual Report No. 10. Juneau,
Alaska. pp. 91–104. (unpublished). Available from Alaska
Department of Fish and Game, Division of Wildlife
Conservation, 525W.67th Avenue, Anchorage, Alaska 99518,
USA.
Lessard RB, Martell S, Walters CJ, Essington TE, Kitchell JFK
(2005) Should ecosystem management involve active control
of species abundances? Ecology and Society 10: 1. online:
http://www.ecologyandsociety.org/vol10/iss2/art1
Letnic M, Koch F (2010) Are dingoes a trophic regulator in arid
Australia? A comparison of mammal communities on either
side of the dingo fence. Austral Ecology 35: 167–175.
Ling JK (1999) Exploitation of fur seals and sea lions from
Australian, New Zealand and adjacent subantarctic islands
during the eighteenth, nineteenth and twentieth centuries.
The Australian Zoologist 31: 323–350.
Lotze HK, Worm B (2009) Historical baselines for large marine
animals. Trends in Ecology & Evolution 24: 254–262.
Makhado AB, Meÿer MA, Crawford RJM, Underhill LG, Wilke C
(2009) The efficacy of culling seals seen preying on seabirds as
a means of reducing seabird mortality. African Journal of
Ecology 47: 335–340.
Mansfield AW, Beck B (1977) The grey seal in eastern Canada.
Fisheries and Marine Service Technical Report 704: 1–81.
McKinnell SM, Wood CC, Rutherford DT, Hyatt KD, Welch DW
(2001) The demise of Owikeno Lake sockeye salmon. North
American Journal of Fisheries Management 21: 774–791.
Merriam CH (1901) Food of sea lions. Science 13: 777–779.
Mitchell E (1975) Porpoise, Dolphin and Small Whale Fisheries of
the World. Status and Problems. IUCN Monograph No 3.,
International Union for the Conservation of Nature and
Natural Resources, Gland, Switzerland and Cambridge, UK.
Nicholson AJ (1933) The balance of animal populations. The
Journal of Animal Ecology 2: 132–178.
Nilssen KT, Haug T (2007) Status of grey seals (Halichoerus
grypus)inNorway.NAMMCO Scientific Publications 6: 23–32.
Oien N (1988) The distribution of killer whales (Orcinus orca)
in the North Atlantic based on Norwegian catches,
1938–1981, and incidental sightings, 1967–1987. Rit
Fiskideildar 11: 65–78.
Olesiuk PF (2009) An Assessment of Population Trends and
Abundance of Harbour Seals (Phoca vitulina)inBritish
Columbia. Research Document 105. Canadian Science
Advisory Secretariat, Ottawa, Canada.
Oro D, de León A, Minguez E, Furness RW (2005) Estimating
predation on breeding European storm-petrels (Hydrobates
pelagicus) by yellow-legged gulls (Larus michahellis). Journal of
Zoology 265: 421–429.
Paine RT, Tegner MJ, Johnson EA (1998) Compounded
perturbations yield ecological surprises. Ecosystems 1:
535–545.
Pearson JP, Verts BJ (1970) Abundance and distribution of
harbor seals and northern fur seals in Oregon. Murrelet 51:
1–5.
Punt AE, Butterworth DS (1995) The effects of future
consumption by the cape fur seal on catches and catch rates
of the cape hakes. 4. Modellng the biological interaction
between Cape fur seals Arctocephalus pusillus pusillus and the
Cape hakes Merluccius capensis and M. paradoxus.South
African Journal of Marine Science 16: 255–285.
Rae BB (1960) Seals and Scottish fisheries. Marine Research 2:
1–39.
Reynolds JC, Tapper SC (1996) Control of mammalian
predators in game management and conservation. Mammal
Review 26: 127–155.
Roberts C (2007) The Unnatural History of the Sea. Island Press,
Washington DC, USA.
W. D. Bowen and D. Lidgard Marine mammal predator control
13Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
Sanz-Aguilar A, Martinez-Abrain A, Tavecchia G, Minguez E,
Oro D (2009) Evidence-based culling of a facultative
predator: efficacy and efficiency components. Biological
Conservation 142: 424–431.
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B
(2001) Catastrophic shifts in ecosystems. Nature 413:
591–596.
Schnieder CP, Schiavone A Jr, Eckert TH, McCullough RD,
Lantry BF, Einhouse DW, Chrisman JR, Adams CM, Johnson
JH, Ross RM (1999) Double-Crested Cormorant Predation on
Smallmouth Bass and Other Fishes of the Eastern Basin of Lake
Ontario: Overview, Summary and Recommendations. Section 1
in Final Report to Assess the Impact of Double-Crested
Cormorant Predation on the Smallmouth Bass and Other Fishes
of the Eastern Basin of Lake Ontario. Special Report, New York
State Department of Environmental Conservation. Albany,
New York, USA.
Scott F (1968) The seals of Nova Scotian waters. Journal of
Education 149: 16–24.
Seip DR (1992) Wolf predation, wolf control and the
management of ungulate populations. In: McCullough DR,
Barrett RH (eds) Wildlife 2001: Populations, 331–340. Elsevier
Applied Science, London, UK.
Sinclair ARE, Pech RP (1996) Density dependence,
stochasticity, compensation and predator regulation.
Oikos 75: 164–173.
Sinclair ARE, Pech R, Dickman CR, Hik D, Mahon P, Newsome
AE (1998) Predicting effects of predation on conservation of
endangered prey. Conservation Biology 12: 564–575.
Smith RK, Pullin AS, Stewart GB, Sutherland WJ (2010)
Effectiveness of predator removal for enhancing bird
populations. Conservation Biology 24: 820–829.
Smith TD (1995) Interactions between marine mammals and
fisheries: an unresolved problem for fisheries research. In: Blix
AS, Walløe L, Ulltang Ø (eds) Whales, Seals, Fish and Man,
527–536. Elsevier Science, Amsterdam, the Netherlands.
Stansell RJ, Gibbons KM, Nagy WT (2010) Evaluation of
Pinniped Predation on Adult Salmonids and Other Fish in the
Bonneville Dam Tailrace, 2008–2010. US Army Corps of
Engineers Report, Portland District, Cascade Locks, Oregon,
USA.
Summers CF, Harwood J (1979) The grey seal ‘problem’ in the
Outer Hebrides. Proceedings of the Royal Society of Edinburgh.
Section B: Biology 77: 495–503.
Svanbäck R, Persson L (2004) Individual diet specialization,
niche width and population dynamics: implications for
trophic polymorphisms. The Journal of Animal Ecology 73:
973–982.
Tapper SC, Green RE, Rands MRW (1982) Effects of
mammalian predators on partridge populations. Mammal
Review 12: 159–167.
Terborgh J (1992) Why American songbirds are vanishing.
Scientific American 266: 98–104.
Terborgh J, Estes JA, Paquet P, Ralls K, Boyd D, Miller B, Noss R
(1999) Role of top carnivores in regulating terrestrial
ecosystems. In: Soule ME, Terborgh J (eds) Continental
Strategies for Conservation, 39–64. Island Press, Washington
DC, USA.
Terborgh J, Lopez L, Nunez P, Rao M, Shahabuddin G, Orihuela
G et al. (2001) Ecological meltdown in predator-free forest
fragments. Science 294: 1923–1926.
Thompson PM, Mackey B, Barton TR, Duck C, Butler RRA
(2007) Assessing the potential impact of salmon fisheries
management on the conservation of harbour seals (Phoca
vitulina) in north-east Scotland. Animal Conservation 10:
48–56.
Tjelmelan S, Lindstrøm U (2005) An ecosystem element added
to the assessment of Norwegian spring-spawning herring:
implementing predation by minke whales. ICES Journal of
Marine Science 62: 285–294.
Treves A, Karanth KU (2003) Human-carnivore conflict and
perspectives on carnivore management worldwide.
Conservation Biology 17: 1491–1499.
Trites AW, Christensen V, Pauly D (1997) Competition between
fisheries and marine mammals for prey and primary
production in the Pacific Ocean. Journal of Northwest Atlantic
Fisheries Science 22: 173–187.
Valkama J, Korpimaki E, Arroyo B, Beja P, Bretagnolle V, Bro E
et al. (2005) Birds of prey as limiting factors of gamebird
populations in Europe: a review. Biological Reviews of the
Cambridge Philosophical Society 80: 171–203.
Woodroffe R, MacDonald DW (1995) Cost of breeding status in
the European badger, Meles meles.Journal of Zoology, London
235: 237–245.
Worm B, Myers RA (2003) Meta-analysis of cod-shrimp
interactions reveals top-down control in oceanic food webs.
Ecology 84: 162–173.
Worthington EB (1964) Grey seals and fisheries. Nature 203:
116–118.
Yodzis P (1988) The indeterminacy of ecological interactions as
perceived through perturbation experiments. Ecology 69:
508–515.
Yodzis P (1998) Local trophodynamics and the interaction of
marine mammals and fisheries in the Benguela ecosystem.
The Journal of Animal Ecology 67: 635–658.
Yodzis P (2001) Must top predators be culled for the sake of
fisheries? Trends in Ecology & Evolution 16: 78–84.
Zwanenburg K, Bowen WD, Sergeant DE (1985) Assessment of
Northwest Atlantic Grey Seal (Halichoerus grypus)Pup
Production for 1977 to 1984. Research document 67. Canadian
Atlantic Fisheries Scientific Advisory Committee, Ottawa,
Canada.
Marine mammal predator control W. D. Bowen and D. Lidgard
14 Mammal Review •• (2012) ••–•• © 2012 The Authors. Mammal Review © 2012 Mammal Society/Blackwell Publishing
