Alder, J., Campbell, B., Karpouzi, V., Kaschner, K. and Pauly, D. (2008) Forage fish: from ecosystems to markets. Annual
Reviews in Environment and Resources 33: 153-166.
ANNUAL
REVIEWS
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Forage Fish: From
Ecosystems to Markets
Jacqueline Alder,1 Brooke Campbell,1
Vasiliki Karpouzi,1 Kristin Kaschner,2
and Daniel Pauly1
1
Sea Around Us Project, University of British Columbia, Vancouver, British Columbia
V6T 1Z4, Canada; email: j.alder@fisheries.ubc.ca, b.campbell@fisheries.ubc.ca,
v.karpouzi@fisheries.ubc.ca, d.pauly@fisheries.ubc.ca
2
Evolutionary Biology and Ecology Laboratory, Institute of Biology (Zoology),
Albert-Ludwigs-University Freiburg, Freiburg 79104, Germany;
email: kristin.kaschner@biologie.uni-freiburg.de
Annu. Rev. Environ. Resour. 2008. 33:153–66
Key Words
First published online as a Review in Advance on
August 1, 2008
aquaculture, fishmeal, small pelagics
The Annual Review of Environment and Resources
is online at environ.annualreviews.org
This article’s doi:
10.1146/annurev.environ.33.020807.143204
c 2008 by Annual Reviews.
Copyright
All rights reserved
1543-5938/08/1121-0153$20.00
Abstract
Fisheries targeting small-to-medium pelagic, so-called forage fish, impact on human food security and marine ecosystems. Because their operations are shrouded by the myth that forage fish are unsuitable for
human consumption, the role of these fisheries in intensive food production is not well understood or appreciated. Thus, although they
account for over 30% of global landings of marine fish annually, our
knowledge of how these levels of removal impact on marine ecosystems
is limited. Nevertheless, there is considerable scope for policy makers to
change the current management of these fisheries and to enhance their
contribution to food security and economic development. Industry and
consumers also have an important role in finding the balance between
these fisheries contributing to human food security and poverty alleviation on the one hand, and sustaining intensive animal food production
systems, especially aquaculture, on the other.
153
Contents
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INTRODUCTION . . . . . . . . . . . . . . . . . .
LANDINGS OF FORAGE FISH
SINCE 1950 . . . . . . . . . . . . . . . . . . . . . .
FORAGE FISH IN A MARINE
ECOSYSTEM CONTEXT . . . . . . .
CONSUMPTION OF FORAGE
FISH BY SEABIRDS . . . . . . . . . . . . . .
CONSUMPTION OF FORAGE
FISH BY MARINE MAMMALS . . .
FOOD SECURITY AND SAFETY . . .
FORAGE FISH CONSUMED
BY HUMANS . . . . . . . . . . . . . . . . . . . . .
FORAGE FISHERIES AND
INTENSIVE FOOD
PRODUCTION . . . . . . . . . . . . . . . . . .
POLICY OPTIONS
AND FUTURES . . . . . . . . . . . . . . . . . .
154
155
156
157
158
159
159
161
162
INTRODUCTION
Forage fish are often described as the prey for
other animals to eat and are composed primarily
of small- and some medium-sized pelagic fish.
Forage fish are used directly for human food
and reduced to fishmeal and fish oil for industrial purposes. The current state of fisheries, the
growth in the aquaculture sector, and impending changes from increasing sea temperature
raises the question of the future of these fisheries because they are a source of food for many
of the world’s poor as well as a critical input
to the current expansion of aquaculture especially for high-value carnivorous species. This
review attempts to examine the interaction of
forage fisheries, ecosystems, and intensive food
production.
Forage fishes tend to form large dense
schools, which make them easy to catch using little fuel energy, especially in comparison with demersal fish, typically caught by bottom trawling. Forage fishes (e.g., anchovies,1
1
In this article, we use common names, standardized by the
American Fisheries Society; for the corresponding scientific
names, see http://www.fishbase.org.
154
Alder et al.
sardines, and mackerels) school and are easy
to catch in large numbers, and hence inexpensive. The fisheries that rely on forage fish
are found throughout the world’s oceans, except in Antarctica (1). Presently the annual
catch is about 31.5 million tonnes, a staggering
37% of global marine landings (2). However,
the largest catches occur in three areas of the
world, the west coast of South America (southeast Pacific), which sustains the world’s largest
(by volume) fisheries; northern Europe; and
the United States (the East Coast and Alaska).
These fisheries are not only important to human well-being, but also as food for marine
mammals and seabirds (1).
Small pelagics play a crucial role in most
ecosystems because they are the group that
transfers energy from the plankton to the
larger fishes and marine mammals. Along with
their short life span, the direct dependence of
these fishes on plankton, which are impacted
by environmental fluctuations, often causes
the biomass of these fishes to fluctuate more
strongly than other commercial fish species (3).
This has led many fisheries scientists to conclude that fisheries have little impact on small
pelagics, as their abundance seems determined
mainly by environmental factors. Yet, intense
fishing pressure on small pelagics does result
in, among other things, depleting the food base
of seabirds (4) and marine mammals (5).
Historically, humans in all areas of the world
consumed small pelagics, and in many countries, these fish contribute significantly to human diets, particularly among people with low
incomes. However, their low prices, owing in
part to their schooling behavior, which implies
low fuel and other fishing costs, and their high
nutritional value, also make them an important input of animal feeds for poultry and pigs,
and more recently for farmed fish. The economics of fisheries for small pelagics are thus
impacted by factors, such as the price of soymeal
and other inputs to animal feeds, which are
well beyond the control of fishers and fishmeal
producers.
The growing practice of fish farming, especially of high-value, carnivorous fish, requires
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increasing amounts of fishmeal and fish oil.
This demand is met, in part, by increasing
the fraction of fishmeal diverted away from
animal husbandry, by increasing the pressure
on small pelagics (including previously unexploited species), and by improving the efficiency
of the use of fishmeal and fish oil (6).
The extraordinary responsiveness of small
pelagic fishes to environmental fluctuations,
and their apparent resilience to fishing, has been
the focus of much research, which has yielded
powerful generalizations (7). However, ensuring sustainable catch levels in the face of environmental variability and growing industry demand has remained a challenge. In addition,
their potential role in contributing to human
food security, in sustaining and potentially constraining the aquaculture sector, and their ability to transport persistent organic pollutants
through the international trade in aquafeed are
hardly explored, as argued below.
LANDINGS OF FORAGE FISH
SINCE 1950
Although small pelagic fishes have been exploited for millennia, it was not until the 1950s
that these fisheries became industrialized. Today, small pelagic fish make up 37% of the total
capture fish landings, and 90% of these landings (or 27% of total landings) are processed
into fishmeal and fish oil with the remaining
10% of these landings used directly for feed for
animals (2).
Although herring, sardines, and menhaden
were the main species targeted for reduction
(i.e., processed/reduced into fishmeal and fish
oil) early in the twentieth century, the range of
species targeted has expanded (Table 1). Landings destined for reduction also increased very
slowly until 1958, when large industrial-scale
fishing for Peruvian anchovy began (Figure 1).
This fishery is the world’s largest with landings
of 10.7 million tonnes in 2004, virtually all of
it already destined for reduction (2). Landings
of fish are highly variable as seen in total global
landings of these fish in the three major fishing
areas (Figure 1).
Table 1
Species that made up 75% of the fishmeal produced globally in
1950, 1976, and 2001a,b
1950
1976
2001
Atlantic herring
Peruvian anchoveta
Peruvian anchoveta
Atlantic menhaden∗
Capelin
Inca scad∗
Japanese
pilchard∗
South American pilchard
Capelin
Gulf menhaden
Chub mackerel
Blue whiting
Chub mackerel
Atlantic herring
Japanese anchovy∗
pilchard∗
European sprat
European
Capelin
European sprat
Chub mackerel
South American pilchard
Blue whiting
Norway pout∗
Atlantic herring
Pacific menhaden∗
Atlantic mackerel
Threadfin breams∗
Peruvian anchoveta
Gulf menhaden
Sand lances
Chilean jack mackerel
Sand lances
Gulf menhaden
a
An asterisk shows species present in only that year.
Data from 1950 are based on Grainger & Garcia (48); other data are from the Sea
Around Us database (49).
b
The expansion of the industry surrounding
reduction fisheries from the late 1950s saw a
dramatic global change in the species composition of fishmeal (Table 1 and Figure 2). In
1950, Peruvian anchovy made up a very small
proportion of the global production of fishmeal.
However, by the late 1960s, it was the major
species used for fishmeal (Figure 2a), and in
2003, Peruvian anchovy contributed 57% of
global landings used for fishmeal production
(8). Other important species used for fishmeal
are South Pacific hake and Inca scad, caught
mainly off Chile.
In northern Europe, a major forage fish is
capelin, which makes up to 10% of fish landings globally used for fishmeal; other species
include European sprat, Norway pout, and haddock (9). European sprat declined, beginning in
the 1960s, as a major component of fishmeal;
Norway pout followed a similar pattern, with
landings peaking in the mid-1970s and then declining steadily, with current catches of less than
100,000 tonnes.
Initially, blue whiting was caught as bycatch,
but as other fish species traditionally used for
fishmeal were depleted, a targeted fishery developed in the late 1960s (9). Thus, blue whiting,
in 2007, contributed over 73% of fish destined
for reduction in Norway (10).
www.annualreviews.org • Forage Fish
Capture fish
landings: fish caught
using a variety of gear,
such as nets and hooks;
not farmed fish
Reduction fisheries:
generally small pelagic
species that are
processed into
fishmeal and fish oil
155
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In the United States, Atlantic and Gulf menhaden have been used, since the early 1900s,
for producing fishmeal and fish oil, and this use
continues amid controversy, especially because
Atlantic menhaden is food for recreational
species of fish. Japan has an even longer history
of fishmeal production, using Pacific saury, Pacific herring, and sardines. In southwest Africa,
landings of fish used for reduction have declined
since peaking in the 1960s, with catches annually fluctuating around 850,000 tonnes.
In recent years, the use of Antarctic krill for
fishmeal and fish oil has increased. In the 2005–
2006 fishing season, landings totaled 106,000
tonnes; in spite of predicted increases, catches
remain well below the catch limit of 6.5 million
tonnes (11).
Many forage fish are highly sensitive to
oceanographic changes and landings are highly
variable from year to year. For example, in
strong El Niño years, the abundance of Peruvian anchovy declines, and that of South
American pilchard increases (12), which is reflected in the catch, and ultimately in the composition of the fishmeal. This variability affects
the quality of the product as anchovy meal is
preferred. Globally, there is a tendency, since
the mid-1980s, toward increasing the proportion of carnivorous fish used for fishmeal, as indicated by the increased trend in mean trophic
levels in Figure 3, which shows only Africa as a
region where this trend did not occur until the
mid-1990s.
These high fluctuations in the abundance of
small pelagic fishes also led to questions regarding sustainability. For fisheries where assessments are available, each one’s status has been
assessed as sustainable by various organizations
(8, 13). However, not all stocks are within safe
limits (Table 2). North Sea herring, for example, were used for reduction until 1997, when
the stock collapsed and the European Union
(EU) banned its use for reduction (14).
Most fisheries are under some form of management, and given their sensitivity to changing oceanographic conditions, a precautionary
approach to management, including setting of
quotas and effort limits, is needed within an
156
Alder et al.
ecosystem-based management approach (15).
Blue whiting is noteworthy because it is one
of the major inputs of fishmeal and fish oil in
Europe. The stocks in the North Atlantic are
exploited by a number of countries within and
outside of the EU, which, until 2006, could not
agree on quotas for the fishery. In 2006, landings totaled over 1.97 million tonnes, close to
the recommended quota of 1.9 million tonnes
by the International Council for the Exploration of the Sea (ICES) (16).
The upward trend in the average trophic
level of landings destined for reduction
(Figure 3) contrasts with the downward trend
in the average trophic level of fish for human
consumption, i.e., “fishing down the food web”
(17). This indicates that an increasing amount
of fish suitable for human consumption is being diverted to make fishmeal. The demand for
fishmeal and fish oil is driven by intensive animal production systems, seeking inexpensive,
yet valuable, components to animal feeds. This
increasing demand has expanded the number
of species of fish targeted for reduction, which
now has grown to include higher trophic level
species; this expansion increasingly results in
competition with human needs.
FORAGE FISH IN A MARINE
ECOSYSTEM CONTEXT
Forage fish play a crucial role in marine ecosystems, mainly because they are the group that
transfers energy from the plankton to the larger
fishes and marine mammals. Hereby, they operate at the crucial “wasp-waist” trophic level,
where one or more small plankton-consuming
nektonic species tend to dominate the trophic
transfers, as opposed to the many species involved in transfers at lower and higher trophic
levels (3, 12).
Still, a study of the impact of reduction
fisheries on EU marine ecosystems concluded
that “the impact of industrial fisheries we were
able to identify is relatively limited compared
to the effects of fisheries for species destined
for human consumption” (18). The researchers
concluded that the overall impact of industrial
Table 2
Stock status for fish destined for reduction in 2002 (56)
Target stock
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Atlantic menhaden
FAO areaa
State of exploitation in 2002b
NW Atlantic FAO21
F
WC Atlantic FAO31
F
Gulf menhaden
WC Atlantic FAO31
F
Atlantic mackerel
NE Atlantic FAO27
F
Blue whiting
NE Atlantic FAO27
O
Norway pout
NE Atlantic FAO27
F
Sand eels/sand lances
NE Atlantic FAO27
F
Atlantic herring
NW Atlantic FAO21
U, F, R
NE Atlantic FAO27
F
European sprat
NE Atlantic FAO27
F
Mediterranean and Black Sea FAO37
D
Capelin
NE Atlantic FAO27
F
Chub mackerel
EC Atlantic FAO34
F
South African anchovy
SE Atlantic FAO47
F
Horse mackerel
SE Atlantic FAO47
M, F
Pilchard
SE Atlantic FAO47
F
Pacific herring
NW Pacific FAO61
?
Pacific saury
NW Pacific FAO61
F
Japanese sardine (anchovy)
NW Pacific FAO61
Peruvian anchoveta
SE Pacific FAO87
R, O
South American pilchard
SE Pacific FAO87
F, O
Chilean jack mackerel
SE Pacific FAO87
F, O
Hake
SE Pacific FAO87
F, O, D
F
a
Multiple values of exploitation are due to multiple stocks within the UN Food and Agriculture Organization (FAO) area
being in different states of exploitation.
b
D, deleted; F, fully exploited; O, overexploited; U, underexploited; R, recovering; M, moderately exploited; ?, unknown.
fisheries is relatively limited on predators, but
interactions with certain populations of predators can be locally significant. Most incidental
catches are also species used for fishmeal, and
where edible species are caught incidentally,
they generally represent a low proportion of the
catch, which is considered acceptable by the EU
(14). However, concern in the United Kingdom
over the role of sand eels as food of seabirds resulted in the EU banning catches of sand eel in
an area of 20,000 km2 in the North Sea (14).
Strong interactions are also documented in
South America, especially in El Niño years,
where significant mortalities of seabirds and
marine mammals occur, owing in large part to
a reduction in prey abundance (4). Changes in
the Benguela upwelling system also result in
substantial mortalities of seabirds and marine
mammals (19). In the United States as well,
there is growing concern over the landings of
menhaden impacting the catch of striped bass
in the Chesapeake Bay (20).
Our understanding of the forage fish role in
supporting seabirds and marine mammals is still
limited. However, recent research (21, 22) provides considerable insight into the consumption
of these fish by seabirds and marine mammals,
as presented below.
CONSUMPTION OF FORAGE
FISH BY SEABIRDS
A database of 351 species of seabirds was combined with a seabird food consumption model
to estimate the global consumption of small
pelagic fishes by all seabird species combined
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157
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(21). This led to the result that this consumption was, in the 1990s, at least eight times lower
than the fisheries catches of these same fishes
today (22). Small pelagics are about 12.5%
of the overall food consumed annually by the
world’s seabirds. Alcids (puffins and murres) and
larids (gulls) are responsible for about 75% of
small pelagic fish consumption by all seabird
species combined.
The work predicted that more than 52%
of the forage fish that seabirds consume is
extracted over the continental shelves of the
northeast Atlantic Ocean (Figure 4). In this
area, sand lance and capelin accounted for
>54% of the food taken annually by seabirds.
The eastern Central Pacific Ocean (Figure 4)
was the second most important area, where
small pelagics taken by seabirds are 21% of the
overall forage fish consumption. In this area,
forage fish groups in seabirds’ diets were dominated (up to 92%) by fish species of the family
Exocoetidae. Areas of highest forage fish consumption were closely linked with the distribution of those seabird species that are limited to
waters above continental shelves when foraging
(23).
Furthermore, predicted maximum food
consumption rates exceeded 10 t·km−2 ·year−1
along the continental shelves of the northeast
Atlantic Ocean and around islands of the western Central Pacific Ocean. However, seabird
consumption still remains several orders of
magnitude lower than the highest fisheries
catch rates.
Direct competition between fishing operations and seabirds is not a significant threat to
species with large foraging ranges on the basis of the small size of predicted hot spots. In
contrast, our findings support a previously proposed hypothesis that the most common type
of harmful competitive interaction will be one
in which fisheries adversely impact species with
restricted distributional ranges (24, 25) (indicating that local depletions of food resources
through intensive fishing, as for example, in the
North Sea populations of Black-legged kittiwakes) and also localized populations of other
species.
158
Alder et al.
Resource overlap does not automatically imply competition and vice versa; however, it is reassuring that the hot spots of potential conflict,
highlighted by their approach, coincide with
many areas that have been the focal points of
much previous debate about seabird-fisheries
interactions. Several areas of potential conflict
for seabirds were identified, for instance in the
Norwegian and Barents Seas, where rapid decline in the numbers of Common murres has
been attributed to the development of industrial fisheries, which target mainly sand eel for
industrial raw materials, fish oil, and fishmeal
(26).
By contrast, there is a growing literature
on seabirds being starved by depletion of small
pelagics by fishing. For example, the development of an anchovy fishery offshore of Chubut,
Argentina, has raised concerns over Magellanic
penguins and other wildlife (27).
CONSUMPTION OF FORAGE
FISH BY MARINE MAMMALS
Maps of the distribution of 115 species of marine mammals (22) were combined with population, diet composition, and food consumption estimates to obtain a model of the fish consumption of marine mammal (28), subsequently
used to estimate forage fish consumption by all
marine mammal species (22). The key result
was that marine mammals consume about two
thirds of the fisheries’ catch of small pelagics
in the 1990s. Although small pelagics represent
the single most important prey type targeted
by fisheries, contributing over 50% of the total
catch, this food type makes up—at the most—
20% of the diet of any marine mammal species
group. Baleen whales and pinnipeds (seals, sea
lions, and their relatives) consume the bulk of
small pelagics consumed by marine mammals.
Toothed whales, in contrast, are much less dependent on forage fish, and this prey type eats
less than 10% of the total amount consumed by
both small and large species.
The food consumption models predicted
that much of the forage fish that marine mammals consume occur at high latitudes, with high
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consumption rates on continental shelves in
the North Atlantic (Figure 5). Owing to the
sheer size of the distributional ranges of many
of the baleen and larger toothed whales, consumption densities (annual food intake per km2 )
are comparatively low and homogenous across
large areas (Figure 5). Areas of highest forage fish consumption are closely linked with
pinniped occurrence because of their coastal
ranges and their frequently high local abundances. However, predicted maximum food
consumption densities did not exceed 0.75
t·km−2 ·year−1 anywhere in the world, i.e., maximum food intake of small pelagic prey by
marine mammals is several orders of magnitude lower than the highest fisheries catch
rates.
Overall, a low overlap in resource exploitation between all marine mammals and fisheries was inferred (Figure 6). High overlaps
appeared to be restricted to small geographical areas, mostly on high-latitude continental
shelf areas of the Northern Hemisphere and
on highly productive upwelling systems in the
Southern Hemisphere. The highest overlap occurred in areas where high fishing effort coincided with high densities of seals, such as
the North Atlantic shelves (containing harp,
hooded, harbor, and gray seals), the Benguela
upwelling ecosystem (containing South African
fur seals), or along the coast of western South
America, where upwellings support a wide
range of marine mammals and fisheries. Although only a few pinniped species occur in
the waters around Japan, high overlap in this
region can be attributed to the large number of
dolphins and some baleen whale species feeding on small pelagic fishes, combined with very
high fishing rates.
FOOD SECURITY AND SAFETY
In many areas of the world, especially developing countries, forage fish are important for
food security. Their importance contrasts with
the notion that the reduction of such fishes to
fishmeal and fish oil has no impact or only a
positive impact on human food security. Almost
all the small fish dominating reduction fisheries
are (or were) eaten by people, for example:
The Peruvian anchovy, was consumed in
Peru until reduction fisheries were introduced in 1953, and there are new efforts
to turn it into an upscale food (29);
Some capelin is frozen for specific markets in Japan and Europe, and the market
appears to be increasing (30) with predictions of increased share of landings going
for human consumption (30a);
Approximately 33% of Japanese pilchard
landings are destined for human consumption;
Chilean jack mackerel was historically
used for human consumption as a frozen
or canned product sold in Latin America,
Africa, and Oceania, although it is now
used mainly for fishmeal;
Round sardinella are frozen and exported
to Africa, Asia, and Eastern Europe for
human consumption (31); and
European anchovy is consumed as a fresh,
dried, smoked, canned, or frozen product
(31a).
Current regional patterns of small pelagic
consumption suggest that the use of forage fish
for animal (including fish) husbandry competes
directly with human consumption in some areas
of the world. Overall, there is a declining human
consumption of relatively cheap pelagic fish,
and in richer countries, an increased consumption of expensive seafood, some of it farmed
with aquafeeds derived from small pelagics.
FORAGE FISH CONSUMED
BY HUMANS
The small pelagic fish species that are eaten
vary between geographic regions and reflect
historical and current taste preferences. These
fish, owing to their schooling habits, are easy to
catch using small mesh nets with low operating
costs and are relatively easy to preserve. Consequently, for low-income groups, the fish are
often much cheaper and more accessible than
demersal fish. Where the demand for animal
www.annualreviews.org • Forage Fish
159
Small food fish landed as a percentage of global landings (%)
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20
15
10
5
0
1965
1970
1975
1980
1985
Year
1990
1995
2000
Figure 7
Forage fish landed and consumed directly by humans as a percentage of global landings (49, 50).
protein (or for cheap protein) is not met domestically, such as in West Africa, the Caribbean,
Oceania, and Latin America, imports of small
pelagics, such as herrings, sardines, and mackerel, are often used to meet that demand
(31, 32).
The percentage of forage fish catch that
is landed and consumed directly as food has
fluctuated between 10% and 20% of global
landings since 1961 (Figure 7). Much of the
variation is a reflection of the environmentally
induced variation in landings of small pelagic
fish.
The trend in per capita consumption of forage fish varies with each continent (Figure 8)
and represents between 10% and 25% of per
capita consumption of fish globally. In Africa
and Oceania, where these fish play an important role in food security, per capita consumption has declined since the mid-1980s in Ocea160
Alder et al.
nia and late 1990s in Africa. Consumption has
declined since the late 1970s in South America
and since the late 1980s in North and Central
America. In Asia, where these fish are also important for food security, per capita consumption has remained steady, and in Europe it has
increased since the late 1980s (Figure 8).
A recent study (33) examined trends in “lowvalue food fish” and noted that low-value food
fish as a proportion of total fish consumed by
humans in developing countries dropped by
11% from 76% in 1973 to 65% in 1997. However, if China is excluded, the decline (5%) is
much less, from 77% in 1973 to 72% in 1997.
Globally, low-value food fish increased from
41% to 47% of food fish consumed for the same
time period (33). However, it was noted that the
rise in consumption was due, in part, to the poor
in Asia (especially in China) increasing their
consumption of farmed freshwater fish (33).
There are a number of reasons for this, beyond prices and supplies, which account for the
spatial differences and fluctuations in human
consumption of small pelagic food fish. They
are:
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Increasing wealth in some countries, resulting in a switch to higher-valued fish,
such as cods and haddock, and large
pelagics, such as tuna and billfish;
Substitution of small pelagic fish when
there is limited availability of demersal
and large pelagic fish;
Increasing competition for small pelagic
fish for fishmeal and for human consumption, driving the price of these pelagic
fish up and making it difficult for poorer
countries to purchase the fish; and
Soybean price fluctuations, owing to the
use of soymeal as a substitute for fishmeal
in some industries.
Soymeal can be used as a substitute for fishmeal in intensive animal production, especially
in the pig and poultry sectors. Soymeal can also
substitute for fishmeal in aquaculture, although
the fish cultured do not achieve the same high
growth rates (34), and thus, it is the total supply and demand for protein meals that determine its price (35). If the total demand for protein meals increases, the price for protein meals
will increase, including the price of fishmeal.
This will also increase the likelihood that small
pelagic fish, destined for human consumption,
will be diverted to the reduction sector.
The trade that occurs in fishmeal and fish
oil gives merit to the recent warnings of toxins in farmed salmon (36). The reduction process concentrates toxins, such as dioxins in fishmeal and oil. In northern Europe, where there
are a high concentration of dioxins and large
catches of forage fish, fishmeal and oil are likely
to have high levels of dioxins. When these processed products are exported to other areas,
dioxins and other toxins are also transported
and enter the intensive animal food production
system and ultimately the human food system.
Recent concerns over fishmeal and fish oil toxicity have resulted in many companies develop-
ing the technology to filter out toxins such as
dioxins (37).
FORAGE FISHERIES AND
INTENSIVE FOOD PRODUCTION
Although fishmeal and fish oil are beneficial in
the intensive production of poultry, pigs, and
ruminants, they are essential to most farmed
fish. Thus, the growth of aquaculture has led
to a decline in the use of fishmeal in poultry
and livestock. The demand for fishmeal in animal feeds is determined by the least cost of
meals, especially soy, with the upper limit set by
the taste imparted into the meat (38). Although
soymeal can be substituted for fishmeal, the
essential fatty acids in fishmeal and fish oil are
superior to other meals, with several benefits
such as increased disease resistance. Changes
in consumption of fishmeal have led to increasing prices, which have had limited impact on
livestock production because substitutes such
as corn have been affordable. However, the increased demand for biofuels has changed the
pricing structure of many inputs into animal
feeds, and how this will change demand for fishmeal is uncertain.
Estimates of fishmeal consumption by the
aquaculture sector on a national basis are lacking. The amount of fishmeal (as feed) consumed
in the aquaculture sector was therefore estimated for countries with major fishmeal supplies (see Referenc 39 for details). China, India, Indonesia, the Philippines, Thailand, and
Vietnam have large supplies of fishmeal. They
also use fisheries bycatch as direct feed in aquaculture, which is often not recorded in official
production statistics. This makes it difficult to
reliably estimate the use of fishmeal in the aquaculture sector for these countries (40). Nevertheless, China’s increasing fish and meat consumption makes it a major fishmeal consumer
for farmed fish and pork production, and this
contributes to rising fishmeal prices. China currently consumes more than 1.3 million tonnes
of fishmeal each year and is investing in fishmeal companies in Peru and Chile to secure
supplies.
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In 2002, fishmeal and fish oil were primarily used throughout the world for intensive food
production, with 24% for pigs, 22% for poultry,
and 46% for aquaculture (40a). The farming of
carnivorous species as well as changes in feeding practices for omnivorous fish species, such
as shrimp and tilapia, have shifted fishmeal use
patterns. Since 1981, the proportion of fishmeal
used in aquaculture has been increasing, especially for high-value species (Figure 9).
The use of fishmeal by the aquaculture sector in 2002 was estimated to be 46%, with projections to 2012 of 60% (6) and with significant
declines in the use of fishmeal in the poultry
sector by 2012. In 2002, 81% of fish oil production was used in aquaculture, with projections
of 88% in use by 2012 (6).
The aquaculture sector has increased its use
of fishmeal in feeds since the early 1990s, but
there is still considerable scope for the sector
to increase its use of fishmeal. Currently, only
half of global production is used in aquaculture, with the other half primarily used by the
pig and poultry sector. How much more fishmeal can be diverted from pig and poultry consumption will depend, in part, on the price of
fishmeal and soy meal. It also depends on the
price increase consumers will pay for poultry
and pigs. Clearly, as fishmeal demand increases
in the aquaculture sector, fishmeal prices will
increase, forcing pig and poultry producers to
consider the trade-off between the unit cost of
production and the increased risk of disease and
lower meat quality if they substitute soymeal for
fishmeal.
There is a trade-off in replacing fishmeal and
oil with plant-derived products; studies have
shown that, for young poultry and piglets, using
fishmeal and fish oil in the diet increases disease
resistance, decreases the impact of the disease
if contracted, decreases the severity of inflammatory diseases, and improves the nutritional
status of animals, leading to better quality and
leaner meat. This reduces the overall unit cost
of production compared to diets of exclusively
plant-based meals (41).
The situation for fish oil, however, is different, with 87% of global fish oil production
162
Alder et al.
consumed by the aquaculture sector in 2003
(42). This is in spite of the industry developing feeds and improving feed conversion efficiency to reduce the amount of oil required, as
well as searching for alternatives. A study (42)
indicated that, by 2010, feed conversion efficiency should decrease, so that the use of fish
oil in feeds should be reduced by 8% for salmon,
implying that the scope for expansion will increase. However, considering how fast aquaculture has expanded in the past decades, a saving
of 8% when the industry is already consuming over 87% will not be sufficient to allow for
much more industry expansion of salmon and
other carnivorous species.
Asia is the exception in this because fisheries bycatch is often fed directly to high-valued
species, e.g., in China (43), Japan (44), Thailand, and Vietnam (40). The benefits of decreasing the amount of bycatch disposed of at sea
are debatable. Some argue that it is better to
use the fish than to return them to the ecosystem, whereas others argue that the biomass
returned to the sea is beneficial in that it is recycled by other organisms (45). In some countries, fish bycatch is also a cheap source of food,
e.g., Ghana, and therefore diverting bycatch
can threaten local food security (46). There has
been a trend in some countries to feed omnivorous and herbivorous fish aquafeeds containing
fishmeal and fish oil to promote faster growth
for a better return on investment, as seen in
China (47). This is only possible if fishmeal and
fish oil prices are low.
The expansion of aquaculture will continue
to influence the production, trade, and consumption trends. How these trends will change
depends on a number of international factors,
including the international price of soymeal and
fuel, as well as food quality and safety standards,
all of which are currently in a state of flux.
POLICY OPTIONS AND FUTURES
Concern over forage fish sustainability, including the impacts of fishing on marine ecosystems,
is increasing. The International Fishmeal and
Fish Oil Organization explored the feasibility
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of Marine Stewardship Council (MSC) certification but opted to develop their own Code of
Responsible Practice. The intention of the code
is to reassure users that the products are responsibly and carefully produced, and this code does
not compete with ecolabels.
The industry will face significant challenges
in meeting MSC certification because information on the effects of fishing is limited for
most fisheries. This is seen in the UN Food
and Agriculture Organization’s (FAO’s) State
of Fisheries and Aquaculture reports, where
reporting of fisheries on large geographic
scales masks the status of small and locally
important stocks. Managers and policy makers
should take a precautionary approach that
includes ecosystem-based management for
forage fish fisheries because of the influence
of oceanographic conditions and the unknown
consequences of climate change and associated
warming sea temperatures.
In a future of expanding aquaculture without fishmeal and oil alternatives, the price of
fishmeal and fish oil will likely rise, and the
meals and oils will be increasingly consumed
in the aquaculture sector at the expense of first
the poultry sector and second the pig sector.
Increasing prices will ultimately increase production costs, with consumers paying more for
farmed fish, and will affect the food security of
developing countries by pricing forage fish and
farmed fish out of their price range.
A world of expanding aquaculture and pricecompetitive alternatives to fishmeal and fish
oil will likely result in the forage fish fisheries continuing at current levels, but the price
of fishmeal and fish oil decreasing as demand
is lowered. However, if fuel costs continue to
rise, some fleets may decrease, so that only the
most economically efficient vessels operate. In
such a scenario, it is possible that other uses
of fishmeal and fish oil in higher-value products, such as human food and pet food, will be
expanded.
Similar to an expanding aquaculture sector if
production of soymeal slows or stalls, the price
of fishmeal and fish oil will rise with declining
supplies. Pressure to find new sources of fishmeal as well as initiatives to improve the food
conversion ratios will increase. Such a scenario
has significant implications for food security
because high prices could see low-value fish destined to developing countries diverted to reduction plants instead. This scenario also has
implications for the use of bycatch, with an
even greater incentive to use it in the aquaculture sector either as direct feed or as inputs to
fishmeal and fish oil.
SUMMARY POINTS
1. The composition of landings of forage fish fisheries have changed over the past 50 years
with the trophic level of fish used in fishmeal increasing over the past 20 years.
2. Our understanding of the role of forage fish in marine ecosystem and the impact of
fishing is still limited.
3. Landing of forage fish peaked by the 1970s, and these high levels are highly unlikely in
the future, even if fisheries are managed sustainably.
4. The consumption of forage fish by seabirds and marine mammals is not likely to be
onerous to fisheries, except in a few localized areas. By contrast, fisheries, by reducing
the biomass of small pelagics, might pose a threat to these predators, particularly to those
species for which stocks have been heavily depleted by human exploitation in the past.
5. Some forage fish species are consumed by many people with consumption patterns changing over the last 20 years.
6. Aquaculture continues to increase its consumption of fishmeal and fish oil.
www.annualreviews.org • Forage Fish
163
FUTURE ISSUES
1. The demand for fishmeal and fish oil may not be met, constraining the expansion of
aquaculture until alternative feeds are found.
2. Our lack of understanding of how forage fish will respond to climate change will limit
industry’s ability to plan or adapt to these changes.
3. Certifying forage fisheries to MSC standards (or similar) will be difficult because information on the impacts of these fisheries on marine ecosystems is poor.
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DISCLOSURE STATEMENT
The authors are not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
The work upon which this is based was performed within the framework of the Sea Around Us
Project, initiated and funded by the Pew Charitable Trusts. We also acknowledge a supplementary
grant through the Pew Institute for Ocean Science and funding (to K. Kaschner) by the Humane
Society. The support of M. Bowman and E. Pikitch are also gratefully acknowledged.
LITERATURE CITED
1. Fréon P, Cury P, Shannon L, Roy C. 2005. Sustainable exploitation of small pelagic fish stocks challenged
by environmental and ecosystem changes: a review. Bull. Mar. Sci. 76:385–462
2. UN Food Agric. Organ. (FAO). 2006. State of World Fisheries and Aquaculture. Rome: FAO
3. Cury P, Bakun A, Crawford RJM, Jarre-Teichmann A, Quiñones RA, et al. 2000. Small pelagics in
upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J.
Mar. Sci. 57:603–18
4. Jahncke J, Checkley DMJ, Hunt GLJ. 2004. Trends in carbon flux to seabirds in the Peruvian upwelling
system: effects of wind and fisheries on population regulation. Fish. Oceanogr. 13:208–23
5. Bearzi G, Politi E, Agazzi S, Bruno S, Costa M, Bonizzoni S. 2005. Occurrence and present status of
coastal dolphins (Delphinus delphi and Tursiops truncatus) in the eastern Ionian Sea. Aquat. Conserv.: Mar.
Freshw. Ecosyst. 15:243–57
6. Jackson A. 2007. Challenges and opportunity for the fishmeal and fish oil industry. Feed Technol. Update
2:3–11
7. Bakun A. 1996. Patterns in the Ocean: Ocean Processes and Marine Population Dynamics. San Diego, CA/La
Paz, Baja Calif. Sur, Mex.: Univ. Calif. Sea Grant/Cent. Investig. Biol. 323 pp.
8. Huntington TC. 2004. Feeding the fish: sustainable fish feed and scottish aquaculture, Poseidon Aquatic
Resour. Manag. Rep. 199/R/01/B to Jt. Mar. Programme (Scott. Wildl. Trust/World Wildl. Fund Scotl.)/R.
Soc. Prot. Birds Scotl., Hampshire, UK
9. Macer CT. 1974. Industrial fisheries. In Sea Fisheries Research, ed. FR Harden-Jones, pp. 193–221.
London: Elek Sci.
10. Fish. Inf. Services (FIS). 2007. Fishmeal report. http://www.fis.com/fis/reports/report.asp?l=e&mm=
no&specie=512
11. Comm. Conserv. Antarct. Mar. Living Resour. (CCAMLR). 2007. Commission Report XXVI. Hobart,
Aust.: CCMALR. http://www.ccamlr.org/pu/e/e pubs/cr/07/all.pdf
12. Bakun A, Broad K. 2003. Environmental ‘loopholes’ and fish population dynamics: comparative pattern
recognition with focus on El Niño effects in the Pacific. Fish. Oceanogr. 12:458–73
164
Alder et al.
Annu. Rev. Environ. Resourc. 2008.33:153-166. Downloaded from arjournals.annualreviews.org
by University of British Columbia Library on 11/22/08. For personal use only.
13. Sustain. Environ. Aquac. Feeds (SEAfeeds). 2003. A background overview document highlighting key issues
and research needs. http://www.nautilus-consultants.co.uk/seafeeds/Files/SEAfeedsBackground.pdf
14. Eur. Union. 2004. The Fish Meal and Fish Oil Industry: Its Role in the Common Fisheries Policy. Luxembourg:
Eur. Parliam.
15. Pikitch EK, Santora C, Babcock EA, Bakun A, Bonfil R, et al. 2004. ECOLOGY: Ecosystem-Based
Fishery Management. Science 305:346–47
16. Int. Counc. Explor. Sea (ICES). 2007. ICES report of the working group on northern pelagic and blue
whiting fisheries (WGNPBW). ICES Rep. Cm 2007/ACFM:29, Copenhagen
17. Pauly D, Watson R. 2005. Background and interpretation of the ‘Marine Trophic Index’ as a measure of
biodiversity. Philos. Trans. R. Soc. Lond. Ser. B 360:415–23
18. Anonymous. 2004. Industrial fishing in nine questions and answers. Fish. Eur. 22:5–7
19. Crawford RJM, Underhill LG, Raubenheimer CM, Dyer BM, Martin J. 1992. Top predators in the
Benguela ecosystem: implications of their trophic position. S. Afr. J. Mar. Sci. 12:675–87
20. Pauly D. 2007. Tales of a small, but crucial fish: review of ‘The Most Important Fish’ by H. Bruce
Franklin. Science 318:750–51
21. Karpouzi VS, Watson RA, Pauly D. 2007. Modelling and mapping resource overlap between seabirds
and fisheries on a global scale: a preliminary assessment. Mar. Ecol. Prog. Ser. 343:87–99
22. Kaschner K, Karpouzi VS, Watson R, Pauly D. 2006. Forage fish consumption by marine mammals and
seabirds. See Ref. 57, pp. 33–46
23. Karpouzi VS. 2005. Modelling and mapping trophic overlap between fisheries and the world’s seabirds. MSc
thesis. Univ. Br. Columbia, Vancouver BC, Can.
24. DeMaster DP, Fowler CW, Perry SL, Richlin MF. 2001. Predation and competition: the impact of
fisheries on marine-mammal populations over the next one hundred years. J. Mammal. 82:641–51
25. Frederiksen M, Wanless S, Harris MP, Rothery P, Wilson LJ. 2004. The role of industrial fisheries and
oceanographic change in the decline of North Sea black-legged kittiwakes. J. Appl. Ecol. 41:1129–39
26. Anker-Nilssen T, Barrett RT, Krasnov JV. 1997. Long- and short-term responses of seabirds in the
Norwegian and Barents Seas to changes in stocks of prey fish. In Forage Fishes in Marine Ecosystems. Proc.
Int. Symp. Role Forage Fishes Mar. Ecosyst., pp. 683–98. Fairbanks: Univ. Alaska, Alaska Sea Grant Coll.
Program
27. Skewgar E, Boersma P, Harris G, Caille G. 2007. Anchovy fishery threat to Patagonian ecosystem. Science
315:45
28. Kaschner K, Pauly D. 2005. Competition between marine mammals and fisheries: food for thought. In
The State of Animals III: 2005, ed. DJ Salem, AN Rowan, pp. 95–117. Washington, DC: Hum. Soc.
29. Pauly D. 2006. Babette’s feast in Lima. Sea Around Us Proj. Newsl. 38:1–2
30. Nor. Minist. Fish. Coast. Aff. 2008. Marine stocks: Barrents Sea capelin. http://www.fisheries.no/marine
stocks/fish stocks/marine stocks fish capelin/marine stocks fish Capelin barents sea.htm
30a. Norway Pelagic. 2007. Company presentation: Norway Pelagic AS at Glitnir Seafood Conference.
https://www.glitnir.no/wps/wcm/connect/63138e0049667373881ccc74ddd0aaa2/np.pdf?MOD=
AJPERES&CACHEID=63138e0049667373881ccc74ddd0aaa2&CACHEID=eff3590048
e3150481f0fda07acbc6e9&CACHEID=eff3590048e3150481f0fda07acbc6e9
31. Pelagic Freez.-trawl. Assoc. (PFA). 2006. Pelagic fish: healthy and nutritious. http://www.pfa-frozenfish.
com/pfa2/fish1.html#human
31a. Eurostat. 2005. Landings of main species used for human consumption. http://epp.eurostat.ec.europa.
eu/portal/page? pageid=1073,46870091& dad=portal& schema=PORTAL&p product code=
FOOD IN PFISH3A
32. Alder J, Sumaila R. 2005. Western Africa: a fish basket of Europe past and present. J. Environ. Dev.
13:156–78
33. Delgado CL, Wada N, Rosegrant MW, Meijer S, Ahmed M. 2003. Fish to 2020: Supply and Demand in
Changing Global Markets. Washington, DC: Int. Food Policy Res. Inst.
34. Durand HM. 1998. Fishmeal price behaviour: global dynamics and short-term changes. In Global Versus
Local Changes in Upwelling Systems, ed. MH Durand, P Cury, R Mendelssohn, C Roy, A Bakun, D Pauly,
pp. 465–80. Paris: ORSTOM
www.annualreviews.org • Forage Fish
165
Annu. Rev. Environ. Resourc. 2008.33:153-166. Downloaded from arjournals.annualreviews.org
by University of British Columbia Library on 11/22/08. For personal use only.
35. Asche F, Tveterås S. 2005. Market interactions in aquaculture. Presented at 95th Eur. Assoc. Agric. Econ.
Semin., Civitavecchi, Italy
36. Hites RA, Foran JA, Carpenter DO, Hamilton MC, Knutt BA, Schwager SJ. 2004. Global assessment
of organic contaminants in farmed salmon. Science 303:226–29
37. Tacon A. 2005. State of Information on Salmon Aquaculture Feed and the Environment. Washington, DC:
World Wildl. Fund
38. Robinson MA, Crispoldi A. 1971. The Demand for Fish to 1980. Rome: FAO
39. Campbell B, Alder J. 2006. Fishmeal and fish oil: production, trade and consumption. See Ref. 57,
pp. 47–66
40. UN Food Agric. Organ. (FAO). 2005. Report on APFIC regional workshop on low value and “trash fish”
in the Asia-Pacific Region. RAP Publ. 2005/21, FAO, Bangkok
40a. Malherbe S, Int. Fishmeal Fish Oil Organ. (IFFO). 2005. The world market for fishmeal. Proc. World
Pelagic Conf. Capetown, S. Afr. Tunbridge Wells, UK: Agra Informa
41. Int. Fishmeal Fish Oil Organ. (IFFO). 2006. Land animal nutrition and health. London. http://www.iffo.
net/default.asp?fname=1&sWebIdiomas=1&url=22
42. Tacon A. 2004. Use of fish meal and fish oil in aquaculture: a global perspective. Aquat. Res. Cult. Dev.
1:3–14
43. Grainger R, Xie Y, Li S, Guo Z. 2005. Production and utilization of trash fish in selected ports. Presented at
APFIC Reg. Workshop Low Value Trash Fish Asia-Pac. Reg., Hanoi, Viet Nam
44. Huiwe C, Yinglan S. 2007. Management of marine cage aquaculture. Environ. Sci. Pollut. Res. 14:463–69
45. Cushing DH. 1984. Do discards affect the production of shrimps in the Gulf of Mexico? In Penaeid
Shrimps: Their Biology and Management, ed. JA Gulland, BI Rothschild, pp. 254–57. England: Farnham
46. Atta-Mills J, Alder J, Sumaila UR. 2004. The unmaking of a regional fishing nation: the case of Ghana
and West Africa. Nat. Resour. Forum 28:13–21
47. Sorgeloos P. 2000. Technologies for sustainable aquaculture development. Aquaculture in the Third Millennium: Technical Proceedings. Conf. Aquac. 3rd Millenn. Bangkok
48. Grainger RJR, Garcia SM. 1996. Chronicle of Marine Fishery Landing (1950–1994): Trend Analysis and
Fisheries Potential. Rome: FAO. 51 pp.
49. Sea Around Us Proj. 2006. A global database on marine fisheries and ecosystems. http://www.seaaroundus.
org/eez/eez.aspx
50. UN Food Agric. Organ. (FAO). 2006. Commodity balance database. http://faostat.fao.org/site/520/
default.aspx/
51. UN Food Agric. Organ. (FAO). 2006. Food supply database. http://faostat.fao.org/site/502/default.aspx
52. UN Food Agric. Organ. (FAO). 2006. Fishery: processed products database. http://faostat.fao.org/
site/505/default.aspx
53. UN Food Agric. Organ. (FAO). 2008. Aquaculture production: quantities 1950–2006. http://faostat.fao.
org/fishery/topic/16140
54. New M, Wijkstrom W. 2002. Use of Fishmeal and Fish Oil in Aquafeeds: Further Thoughts on the Fishmeal
Trap. Rome: FAO
55. Tacon A. 1997. Global trends in aquaculture and aquafeed production 1984–1995. In International
Aquafeed Directory and Buyers’ Guide 1997/98. Middlesex, UK: Turret RAI
56. UN Food Agric. Organ. (FAO). 2005. Review of the State of World Marine Fishery Resources. Rome: FAO
57. Alder J, Pauly D, eds. 2006. On the multiple uses of forage fish: from ecosystem to markets. Univ. Br.
Columbia, Fish. Cent. Res. Rep. 14( 3), Vancouver, Can.
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30
Landings destined for reduction (million t)
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25
20
South America
15
10
Northern Europe
5
North America
0
1960
1965
1970
1975
1980
1985
1990
1995
2000
Year
Figure 1
Trends in landings for reduction fisheries 1960 to 2001, by major regions. Region-specific information is
not available between 1970 and 1976 (48, 49).
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Fishmeal composition by spp. destined
for reduction (%)
a
45
40
South American pilchard
35
30
Anchoveta
25
20
Inca scad
15
Capelin
10
Chub mackerel
5
0
1976
1981
1986
1991
1996
2001
Fishmeal compostion by spp. destined
for reduction (%)
b
8
Japanese anchovy
7
6
5
Blue whiting
4
Atlantic herring Sandlances
3
2
Gulf menhaden
1
0
1976
1981
1986
1991
1996
2001
Fishmeal composition by spp. destined
for reduction (%)
c
4
Threadfin bream
3
European pilchard
Norway pout
2
Atlantic mackerel
1
European sprat
0
1976
1981
1986
1991
Year
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1996
2001
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3.5
Europe
3.4
3.3
Africa
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Ttophic level
3.2
3.1
Asia
3.0
North America
Global
2.9
2.8
Latin America
2.7
2.6
2.5
1976
1981
1986
1991
1996
2001
Year
Figure 3
Trend in weighted mean trophic level of fish destined for reduction from 1976 to 2001 (49). The mean
trophic level was calculated as described in Pauly & Watson (17).
Figure 2
Trends in the composition of fishmeal on the basis of the top species destined for reduction that made up
at least 75% of the fish used by volume for reduction in 1976 and 2001; (a) top five species by volume,
(b) middle five species by volume, and (c) bottom five species by volume (49).
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Catch rate (t · km -² · year -¹)
> 10
5 - 10
4-5
3-4
2-3
1-2
0.5 - 1
0.25 - 0.5
0.02 - 0.25
< 0.02
Figure 4
Map of predicted global small pelagic fish consumption rate by all seabirds combined for an average year in the 1990s.
C-4
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1990s food consumption (t km–2 year –1)
> 0.5
0.100 – 0.250
0.050 – 0.075
0.015 – 0.025
0.005 – 0.010
0.250 – 0.500
0.075 – 0.100
0.025 – 0.050
0.010 – 0.015
0.001 – 0.005
Figure 5
Distribution of estimated marine mammal food consumption rates (t·km–2·year–1) of small pelagics for an average year in the 1990s
(22).
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Resource overlap index
Low
High
Figure 6
Map of estimated overlap in resource exploitation of small pelagics by marine mammals and fisheries for an average year in the 1990s.
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Consumption per capita (kg • person-1 • year-1 )
Europe
5
4
Africa
3
2
Asia
1
0
1965
1970
1975
1980
1985
1990
1995
2000
7
Consumption per capita (kg • person-1 • year-1 )
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6
6
5
4
Oceania
3
North and Central America
2
1
South America
0
1965
1970
1975
1980
1985
Year
1990
1995
2000
Figure 8
Per capita consumption of small fish from 1961 to 2002 (51).
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Fishmeal consumed in aquaculture (%)
100
Norway
90
80
70
Canada
60
50
40
China
30
Japan
20
10
0
1980
1985
1990
1995
2000
Year
Figure 9
Proportion of fishmeal consumed in aquaculture for major aquaculture-producing countries in 1980, 1985,
1990, 1995, and 2001 (52–55).
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Environment
and Resources
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Contents
Volume 33, 2008
Preface ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣v
Who Should Read This Series? ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣vi
I. Earth’s Life Support Systems
Climate Modeling
Leo J. Donner and William G. Large ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 1
Global Carbon Emissions in the Coming Decades: The Case of China
Mark D. Levine and Nathaniel T. Aden ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣19
Restoration Ecology: Interventionist Approaches for Restoring and
Maintaining Ecosystem Function in the Face of Rapid
Environmental Change
Richard J. Hobbs and Viki A. Cramer ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣39
II. Human Use of Environment and Resources
Advanced Passenger Transport Technologies
Daniel Sperling and Deborah Gordon ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣63
Droughts
Giorgos Kallis ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣85
Sanitation for Unserved Populations: Technologies, Implementation
Challenges, and Opportunities
Kara L. Nelson and Ashley Murray ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 119
Forage Fish: From Ecosystems to Markets
Jacqueline Alder, Brooke Campbell, Vasiliki Karpouzi, Kristin Kaschner,
and Daniel Pauly ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 153
Urban Environments: Issues on the Peri-Urban Fringe
David Simon ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 167
Certification Schemes and the Impacts on Forests and Forestry
Graeme Auld, Lars H. Gulbrandsen, and Constance L. McDermott ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 187
vii
III. Management, Guidance, and Governance of Resources and Environment
Decentralization of Natural Resource Governance Regimes
Anne M. Larson and Fernanda Soto ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 213
Enabling Sustainable Production-Consumption Systems
Louis Lebel and Sylvia Lorek ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 241
Global Environmental Governance: Taking Stock, Moving Forward
Frank Biermann and Philipp Pattberg ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 277
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Land-Change Science and Political Ecology: Similarities, Differences,
and Implications for Sustainability Science
B.L. Turner II and Paul Robbins ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 295
Environmental Cost-Benefit Analysis
Giles Atkinson and Susana Mourato ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 317
A New Look at Global Forest Histories of Land Clearing
Michael Williams ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 345
Terrestrial Vegetation in the Coupled Human-Earth System:
Contributions of Remote Sensing
Ruth DeFries ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 369
A Rough Guide to Environmental Art
John E. Thornes ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 391
The New Corporate Social Responsibility
Graeme Auld, Steven Bernstein, and Benjamin Cashore ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 413
IV. Integrative Themes
Environmental Issues in Russia
Laura A. Henry and Vladimir Douhovnikoff ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 437
The Environmental Reach of Asia
James N. Galloway, Frank J. Dentener, Elina Marmer, Zucong Cai,
Yash P. Abrol, V.K. Dadhwal, and A. Vel Murugan ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 461
Indexes
Cumulative Index of Contributing Authors, Volumes 24–33 ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 483
Cumulative Index of Chapter Titles, Volumes 24–33 ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 487
Errata
An online log of corrections to Annual Review of Environment and Resources articles may
be found at http://environ.annualreviews.org
viii
Contents