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Fishes
and
the
Forest
Expanding perspectives
on
fish
-
wildlife interactions
Mary
F.
Willson, Scott
M.
Gende, and Brian
H.
Marston
E
very year, millions upon mil
-
lions of anadromous fish come
from the oceans to spawn in
freshwater streams. In Southeast
Alaska alone, these fish spawn in
over
5000
streams (Halupka et al. in
press). The best
-
known anadromous
fishes on the Pacific coast are the
seven species of Pacific salmon
of
the
genus
Oncorhynchus
(including
steelhead,
Oncorhynchus mykiss,
and sea
-
run cutthroat trout,
Oncor
-
hynchus clarki).
Other, less
-
publi
-
cized and less well studied anadro
-
mous species include the chars
(Salvelinus
spp.) and smelt, such as
the eulachon
(Thaleichthys pacifi
-
cus).
In addition to anadromous spe
-
cies, several species of fully marine
“forage fishes” use inter
-
and subtidal
zones. For example, along the north
Pacific coast, Pacific herring
(Clupea
harengus pallasi)
spawn on rocky
coastlines, and Pacific sand lance
(Ammodytes hexapterus)
can be
found buried in soft sands, often
near the mouths
of
streams.
These teeming hordes of fish fall
prey not only to marine hunters,
such as other fish, whales, and sea
lions, but also to numerous terres
-
trial predators and scavengers. His
-
torically, the predators were seen as
competing with human harvesters of
fish, and predator
-
control programs
aimed at reducing the number of
Mary
F.
Willson (e
-
mail: willsonm@ptialaska.
net), Scott M. Gende (sgende@ptialaska.
net), and Brian
H.
Marston are ecologists
at the Forestry Sciences Laboratory, Ju
-
neau,
AK
99801.
They study ecological
interactions intemperate rainforests.
©
1998
American Institute of Biological Sciences.
June
2
998
Anadromous and inshore
-
spawning fishes constitute
such
an important prey
base
for
terrestrial wildlife
that conventional
ecological dogmas need
to
be revised
nonhuman consumers were a typical
management tool. For example, in
the first half
of
the twentieth century
a bounty was placed on the bald
eagles
(Haliaeetus leucocephalus)
in
Alaska. Although this predator con
-
trol program program resulted in the
killing of over
100,000
eagles, its
effect on fish populations was never
assessed (Willson and Halupka
1995).
Proposals for predator control are
still occasionally popular, but the
view that predators simply reduce
the availability
of
fish for humans
is
quite one
-
sided, and recent studies
show that it is far too limited. In
-
stead, the developing picture is one
of critical and reciprocal interactions
between aquatic and terrestrial sys
-
tems. Many wildlife species, both
aquatic and terrestrial, depend on
fish as a food resource; population
declines
of
many marine mammals
and seabirds have been linked to
diminishing populations of high
-
quality fish prey (e.g., Ainley et al.
1994,
Merrick
1995)
and to declines
in prey diversity (Merrick et al.
1997).
In this article, we argue that
anadromous and inshore
-
spawning
marine fish provide a rich, seasonal
food resource that directly affects
the biology of both aquatic and ter
-
restrial consumers and indirectly af
-
fects the entire food web that knits
the water and land together. In addi
-
tion, we suggest that the presence of
a seasonally abundant food resource
has helped to shape the evolution of
aquatic and terrestrial consumers and
that predators have probably exerted
reciprocal evolutionary pressures on
their prey, potentially influencing the
life history and morphology
of
these
fishes. Finally, we suggest that
anadromous and inshore
-
spawning
fishes constitute such an important
prey base for terrestrial wildlife that
conventional ecological and manage
-
ment dogmas need to be revised.
Interactions between anadromous
fishes and wildlife have been recog
-
nized as having some general eco
-
logical importance (e.g., Brown
1982),
but only recently have the
ramifications
of
these interactions
and their potential magnitude begun
to be explored. Because many of the
nuts and bolts of the ecological links
still need to be described and quan
-
tified, we concentrate on sketching
an outline
of
the interactions, docu
-
menting the effects where possible
but also noting effects that seem prob
-
able, subject to future research.
The seasonal
food
resource
The potential number of fish return
-
ing to spawning areas along shore
-
lines and in freshwater streams
is
455
prodigious. The best indicators of
abundance are found in the records
of commercial harvests, For example,
in 1985 approximately 147 million
salmon were harvested commercially
in Alaska; this catch included 52
million pink salmon
(Oncorhynchus
gorbuscha)
in Southeast Alaska and
24
million sockeye salmon
(Oncor
-
hynchus nerka)
in western Alaska’s
Bristol Bay (Kruse 1988). In 1995,
the Alaskan salmon harvest soared
to over 217 million fish (Savikko
1996). Historically, the herring har
-
vest in Alaska has fluctuated dra
-
matically, with peaks (in the 1930s
and around 1970) of over
140,000
tons (Funk 1993). Herring harvests
in Southeast Alaska between 1980
and 1990 ranged from 6000 to
13,000 tons of fish (Funk 1993), or
roughly
50
-
100
million herring. To
these catch estimates must be added
the sometimes substantial numbers
of fish caught in other fisheries (“by
-
catch”) and those remaining fish that
actually arrived on the spawning
grounds. Eulachon and sand lance
are not commonly harvested com
-
mercially along the Pacific coast, and
no estimates of their abundance are
available.
Even allowing for annual varia
-
tion in abundance and the contribu
-
tion of salmon hatcheries to the total
catch, potential numbers of return
-
ing fish are huge. Before the late
1800s,
returns of great magnitude
actually reached spawning streams
and shores, except where localized
heavy subsistence use decimated cer
-
tain stocks (Karl C. Halupka, For
-
estry Sciences Lab, Juneau, AK, un
-
published reports) or where natural
disturbances (e.g., landslides
or
gla
-
ciers) blocked access to streams.
However, by the end of the nine
-
teenth century, commercial harvests
began to regularly intercept the re
-
turning hordes. Early harvests were
often
so
massive that entire popula
-
tions of salmon were threatened with
extinction (Grinnell 1902, Halupka
et al. in press). Recent commercial
harvests are still large. For example,
it is not uncommon for more than
60
-
70% of a returning population
of salmon to be taken before they
reach fresh water (Karl C. Halupka,
Forestry Sciences Lab, Juneau, AK,
unpublished reports). Furthermore,
habitat degradation associated with
logging, farming, dam building, and
urbanization has severely impaired
salmon reproduction in many areas
(NRC 1996, Slaney et al. 1996).
Thus, far fewer wild salmon are
probably arriving at spawning
grounds now than before the advent
of commercial harvesting and wide
-
spread habitat degradation. Numer
-
ous salmon stocks in Washington,
Oregon, Idaho, and Northern Cali
-
fornia are extinct or nearly
so
(Nehlsen et al. 1991). Estimates of
extinct
or
at
-
risk stocks farther north
range from 20% for British Colum
-
bia and Yukon (Slaney et al. 1996) to
less than 2% for Southeast Alaska
(Baker et al. 1996), but these esti
-
mates are probably on the low side,
because they exclude many stocks
that may have been affected before
systematic records were kept, as well
as small stocks that contribute little
to commercial harvests. The harvest
levels for herring appear to be lower
(i.e.,
10
-
20%
of the estimated num
-
bers present in Southeast Alaska;
Funk 1993). However, even for her
-
ring, local lore and sketchy records
indicate declines in the amount of
shoreline that is used by spawning
herring.
Despite the high harvest levels,
many fish escape the harvest haz
-
ards. Average “escapements” of pink
and chum
(Oncorhynchus keta)
salmon sometimes number over
10,000
fish per stream in Southeast
Alaska, and runs of several thousand
fish are common (Karl
C.
Halupka,
Forestry Sciences Lab, Juneau, AK,
unpublished reports). Spawning
groups of herring and eulachon com
-
monly contain hundreds of thou
-
sands, and often millions, of fish and
are often concentrated in certain lo
-
cations. For example, in Prince Wil
-
liam Sound the 1992 herring escape
-
ment was estimated at
1.1
billion
fish (Funk 1993), and herring
spawned along 106
-
273 km of shore
-
line in Prince William Sound each
year from
198
3 to 1988 (Paine et al.
1996). Thus, large numbers
of
fish
are potentially available for wildlife
predators.
The capture of these fish rewards
a predator well. The amount of lip
-
ids in a prey item is usually a rough
indicator of energy yield to a preda
-
tor, although the kind
of
lipid also
influences the predator’s ability to
use
it. One sample of whole sockeye
salmon averaged
8
%
lipids (Sidwell
1981), a Pacific herring may contain
an average of approximately 8
-
1
8
%
lipids (e.g., Sidwell
1981, Krzynowek
and Murphy 1987), and a eulachon
is estimated to contain up to 22%
lipids (Payne et al. 1997). In terms of
energy, herring and eulachon may
contain as much as 8
-
11 kJ/g wet
mass (e.g., Perez 1994). The energy
value of these fishes is considerably
higher than that of most other ma
-
rine fishes commonly eaten by sea
-
birds and sea mammals. For example,
the lipid content of Pacific cod
(Ga-
dus macrocephalus)
and walleye pol
-
lock
(Theragra
chalcogramma)
is re
-
ported to be 3% or less (Sidwell
1981, Krzynowek and Murphy
1987), and their energy density is
less than 6 kJ/g (e.g., Perez 1994).
The lipid content of
a
fish commonly
varies with location and the length
of the migratory pathway, as well as
with spawning status, age, season,
temperature, and diet, but no com
-
prehensive picture
of
lipid variation
is yet available.
Thus, the influx
of
spawning fish,
measured in terms of numbers, bio
-
mass,
or
energy content, provides a
large food resource for consumers.
Although we have emphasized the
return of adult fish to the spawning
areas, the eggs and young of these
fishes are also important food re
-
sources for wildlife species. The po
-
tential ecological importance
of
these
fishes is
so
great that we have ven
-
tured to call them “keystone spe
-
cie~~~ (Willson and Halupka 1995).
However, a better architectural anal
-
ogy might be “cornerstone species,”
because we think that these fish pro
-
vide a resource base that supports
much of the coastal ecosystem.
Direct effects
of
fish
on
predators
A wide array of consumers use
anadromous and inshore fishes as
prey. Over 40 species of mammals
and birds in Southeast Alaska forage
on salmon in freshwater habitats;
some feed on adult salmon and car
-
casses, others on eggs
or
juveniles
(Willson and Halupka 1995). At one
location in Southeast Alaska, we have
recorded over
30
species of birds and
mammals feasting on eulachon dur
-
ing their spawning run; gulls, sea
ducks, eagles, seals, and sea lions are
most numerous, but the list also in
-
cludes shorebirds and passerines
(Brian H. Marston, Mary F. Willson,
and Scott M. Gende, unpublished
manuscript).
The numerical response of preda
-
tors to runs
of
spawning fish is often
prodigious. Crowds
of
gulls and
eagles gather along shallow streams
when salmon are running in late sum
-
mer and fall. Brown and black bears
(
Ursus
arctos
and
Ursus
americanus,
respectively) commonly congregate
along salmon streams, sometimes in
sufficient numbers to provide a popu
-
lar tourist attraction. When the eula
-
chon run in the spring, the number
of
gulls present along the spawning riv
-
ers soars rapidly, from several dozen
to 50,000
-
100,000, and the number
of bald eagles also rises, from just a
few to 1000 or more (Drew 1996;
Brian
H.
Marston, Mary F. Willson,
and Scott M. Gende, unpublished
manuscript). The sheer magnitude
of the numerical response suggests
that the availability of spawning fish
is important to predators.
The specific ecological importance
of the seasonal exploitation
of
fish
runs to consumer species has just
begun to be documented. For ex
-
ample, bears consume vast amounts
of food in late summer and fall, lay
-
ing down the fat stores needed for
hibernation; anadromous fishes are
a major source
of
high
-
energy food
for many bears at this time of year.
Bears give birth during hibernation,
and production of milk for the cubs
is supported by the energy laid down
as fat before the female enters hiber
-
nation; indeed, well
-
fed, fat female
bears may reproduce more success
-
fully than thin ones (Blanchard 1987,
Stringham 1989, Miller 1994, Sam
-
son and Huot 1995). Coastal brown
bears have also been reported to
mature earlier than interior bears
(Spraker et al. 1981), perhaps be
-
cause they have access
to
better food
resources. Large bears require high
-
energy, abundant food, such as salmon,
to maintain body weight (Welch et al.
1997); the large body size attained by
coastal brown bears may thus be
possible because
of
the seasonal
abundance of anadromous fish.
Other animals also benefit from
the spawning fish. Mink
(Mustela
June
1998
vison)
in coastal Southeast Alaska
feed extensively on salmon during
the spawning season (Ben
-
David et
al. 1997) and have apparently de
-
layed the timing of their breeding
cycle such that lactation, which has a
high energy cost, occurs when salmon
carcasses are available (Ben
-
David
1997). Bald eagles that had access
to
overwintered salmon carcasses along
the Chilkat River in Southeast Alaska
were more likely to breed and laid
eggs earlier than eagles that lacked
access (Hansen 1987). Fledgling
eagles in Southeast Alaska leave their
nests at about the same time as pink
salmon return to spawn in August.
Immature eagles are poorer foragers
than the more experienced adults (e.g.,
Bennetts and McClelland 1997), and
the mortality
of
young birds is often
high as they become independent of
their parents. Juvenile eagles may
survive better by fledging at a time of
high fish abundance because the
salmon provide an easily acquired
and energetically valuable food re
-
source for young eagles learning to
forage for themselves.
In addition, spring runs
of
fish are
probably important to migratory
birds (Brian
H.
Marston, Mary F.
Willson, and Scott M. Gende, un
-
published manuscript). For example,
many thousands of Thayer’s gulls
(Larus thayeri)
feed intensively on
eulachon in Southeast Alaska in May,
as they migrate to breeding grounds
in the Canadian Arctic. Migrating
red
-
breasted mergansers
(Mergus
ser
-
rator)
throng the river mouths, feast
-
ing on eulachon as they move into
fresh water.
Anadromous fishes have also been
a staple food
of
many indigenous
people in northwestern North
America. Settlement patterns
of
Na
-
tive Americans along the northwest
coasts were often determined by the
location
of
fish runs (Maxwell 1995),
and the yearly cycle
of
food harvest
commonly centered on times of fish
runs (de Laguna 1972). Eulachon
oil,
which was used as both a food
and a preservative, was an item of
trade between coastal and interior
tribes (Betts 1994). Far in the inte
-
rior, along the upstream reaches of
the transmontane Taku River and
the Yukon River system, salmon runs
were central to the economy
of
the
First Nations in Canada (Seigel and
McEwen 1984). Even today, many
groups of indigenous people in
Alaska and northwestern Canada
move seasonally to traditional fish
camps.
Effects
of
fish
on
food
webs
The influx of anadromous fishes dra
-
matically affects the freshwater com
-
munity (Juday et al. 1932, Hartman
and Burgner 1972, Richey et al. 1975,
Durbin et al. 1979, Koenings and
Burkett 1987, Kline et al. 1993,
Schuldt and Hershey 1995, Bilby et
al. 1996, Larkin and Slaney 1996).
Most salmon die after they spawn.
Their carcasses accumulate in
streams, where they are stranded in
the shallows or caught on logs and
rocks (Cederholm and Peterson
1985), or along lakeshores (Hartman
and Burgner 1972). A rich commu
-
nity of algae, fungi, and bacteria
develops on the carcasses, and popu
-
lations
of
invertebrates increase
(Wipfli et al. in press). These inverte
-
brates then serve as food for fish in
the stream, including juvenile
salmon. Juvenile salmonids contain
more marine
-
derived nitrogen (Kline
et al. 1993) and grow faster in streams
with salmon carcasses than in those
without (Bilby et al. 1996). The re
-
productive success of coho salmon
(Oncorhynchus kisutch)
in the Skagit
River in Washington was found to
be correlated with the biomass of
pink salmon spawners in the system,
in part because of the nutrient sub
-
sidy provided by the carcasses
(Michael 1995).
More surprising are the potential
fertilizer effects of salmon carcasses
on land. Bears and other carnivores
commonly haul salmon, living or
dead, onto stream banks and tens of
meters back into the forest (Shuman
1950, Cederholm et al. 1989; Mary
F. Willson and Scott M. Gende, un
-
published data). Eagles sometimes
move carcasses to the streamside,
and ravens and crows cache salmon
bits in trees and under grass and
rocks. Decomposers then break down
incompletely consumed carcasses and
digested remains
of
fish in feces of
vertebrate consumers. Marine
-
de
-
rived nutrients, which are identifi
-
able by isotopic markers, pass from
the bodies
of
salmon into the soil
and then into the riparian vegetation
457
Figure 1. A complex
food web based on
anadromous fishes,
with numerous links
between the aquatic
and the terrestrial sys
-
tems. Fish enter the
stream, spawn, and die.
Some carcasses wash
downstream and are
consumed by the es
-
tuarine community.
Others are fed on by
aquatic organisms,
which also feed on each
other, and marine
-
de
-
rived nutrients pass up
the aquatic food web.
Carcasses and living
fish, as well as aquatic
invertebrates and other
stream fishes, are car
-
ried to land by terres
-
trial consumers; ma
-
rine
-
derived nutrients.
from undigested and
digested material enter
the terrestrial food
web. The relative mag
-
nitudes of nutrient flow
along different path
-
ways have yet to be
determined. For pur
-
poses of clarity, the food web is illustrated
in a simplified form, showing only the links
that are central to our argument.
(Bilby
et al. 1996, Ben
-
David et al. in
press). The nutrients passed to the
terrestrial system probably move up
the food chain (Figure
1)
and may
affect not only vegetation but also
animal consumers. Avian popula
-
tions in northern forests have the
capacity to respond to experimental
nitrogen fertilization (Folkard and
Smith 1995); the response of ripar
-
ian consumer communities to ana
-
dromous fish fertilization has not
yet been measured, but our prelimi
-
nary results suggest that bird popu
-
lations are denser
on
streams with
salmon runs.
The magnitude of nutrient input
from salmon varies from tiny to tre
-
mendous. We will show some ex
-
amples in terms of phosphorus, which
is often limiting in nutrient
-
poor
freshwater systems (e.g., Koenings
and Burkett 1987) and perhaps also
in rainforests like those of the north
-
west Pacific coast (Sidle and Shaw
1983), where much phosphorus is
leached away
or
bound
to
soil
par
-
ticles in forms inaccessible to plants;
similar examples could be shown for
1
nitrogen (e.g., Kline et al. 1990). For
example, a good run of 24 million
sockeye salmon to Lake Iliamna in
western Alaska adds 170 t of phos
-
phorus to the lake per year, but a
poor run of less than
0.5
million
yields less than
7
t
of phosphorus
(Hartman and Burgner 1972). In the
Karluk Lake system in south
-
central
Alaska,
1
million sockeye and 4 mil
-
lion pink salmon added
27
t
of phos
-
phorus to the annual nutrient budget
of
the
lake system (Koenings and
Burkett 1987). The Karluk Lake fig
-
ures are equivalent to approximately
0.7
g
of phosphorus per square meter
of lake surface, which is equal to the
recommended application of a stan
-
dard commercial fertilizer to ever
-
greens and trees of 0.7 g/m
2
but sub
-
stantially lower than that of
commercial fertilizers for gardens in
high
-
rainfall areas, such as South
-
east Alaska (up to approximately
50
g/m
2
; University of Alaska
-
Fairbanks
Cooperative Extension Service rec
-
ommendations). Anadromous fishes
have been reported to add up to 29
of phosphorus per liter of water
to freshwater streams (Schuldt and
Hershey 1995.)
Historical runs of coho salmon
might have occurred at a density of
125
-
300/km of stream in Washing
-
ton,
but
present levels are less than
one
-
tenth of that density (Cederholm
et al. 1989). Runs of pink and chum
salmon in Alaska are far larger than
runs of coho in Washington. Assum
-
ing that a prespawning fish contains
an average of 13.3 g of phosphorus
and a postspawning fish an average
of
9.4
g
(these values were calculated
for sockeye salmon, which is inter
-
mediate in size between pink salmon
and chum salmon; Mathisen et al.
1988), that the concentration of fish
in a small Alaska stream is 1000/km,
and that all of the fish die in situ
without predation and are not
washed downstream, then an esti
-
mated 9.4 kg of phosphorus is added
to
that length of the freshwater sys
-
tem from senescent fish carcasses.
(Many runs of fish are much larger
than 1000/km, with correspondingly
larger nutrient input.)
However, if bears carry half
of
the
spawners to shore (as we have ob
-
served in some systems), approxi
-
mately 6.7 kg of phosphorus would
join the terrestrial nutrient cycle,
through either decomposition or fe
-
cal deposition. If that phosphorus
lands within 100 m of the stream
(where most bear
-
killed carcasses are
found), it will be added at a rate of
approximately 6.7 kg/ha, which is
again similar to the phosphorus ap
-
plication rate for commercial fertil
-
izer for evergreens and trees but much
lower than that for garden fertilizers
blended for high
-
rainfall areas, such
as Southeast Alaska. In actuality, of
course, some of the nutrients may
be
carried far away
by
wandering car
-
nivores or
by
insects maturing from
larvae that developed in the carcass.
In some cases, the input of phospho
-
rus from anadromous fishes over
-
whelms that from other sources
(Koenings and Burkett 1987); in
other cases, the input may be very
modest but nevertheless have a large
effect on productivity in nutrient
-
poor systems (Wipfli et al. in press).
Thus, anadromous and inshore
fish form the basis of a complex food
web at the land
-
water interface (Fig-
ure
1).
Biomass and nutrients (nitro
-
gen, phosphorus, carbon, and mi
-
A9
AT,
cronutrients) derived from
the sea are imported to fresh
water and to land. These
nutrient subsidies signifi
-
cantly enhance productivity
of freshwater systems, but
the consequences of this fer
-
tilizer effect for the terres
-
Thus far, we have empha
-
sized the effects of fish on
Figure 2. Sexual dimorphism of pink salmon
(Oncorhynchus
the rest of the ecosystem,
gorbuscha).
Males are shown above, and females are shown
but
there
are
reciprocal
ef
-
below. Males develop large teeth and dorsal humps that are
fects
of
predators
on
the
fish.
used in intermale competition. Such secondary sexual char
-
Although the evolutionary
text for details).
acteristics may facilitate predation by bears and wolves (see
ecology of the life
-
history
patterns of anadromous
fishes remains largely speculative,
these patterns are of both academic
and management interest and need
to be better understood.
Predation
by
terrestrial predators
on spawning salmon can be intense.
For example, along a
200
m stretch
of stream on Chichagof Island in
Southeast Alaska, we observed that
approximately 56% of over
1100
chum salmon carcasses showed signs
of bear predation, and many living
fish bore wounds from bear attacks.
Predation might influence salmon life
history in several ways. According to
life
-
history theory, semelparity (re
-
producing only once in a lifetime)
evolves when the probability of sur
-
viving to reproduce again is low
(Stearns 1992). Five species of Pa
-
cific salmon are regularly semel
-
parous, as are some steelhead and
sea
-
run cutthroats (Groot and
Margolis 1991, Willson 1997).
The
costs of extensive migrations and
intense sexual competition in salmon
(Brett 1995) probably lowered the
probability of survival of post
-
spawning adult salmon, and preda
-
tion may further lower the chances
of survival (Willson 1997).
Terrestrial predation on spawn
-
ers in fresh water also has the poten
-
tial to change the duration and in
-
tensity of sexual selection. Predation
can shorten in
-
stream life (Dangel
and Jones 1988)
and thus the length
of intrasexual competition and nest
defense. Moreover, in response to
sexual
selection,
some
salmon
have
June
1998
strong sexual dimorphism; adult
males commonly develop hooked,
toothy jaws and dorsal humps (Fig
-
ure 2). Although the mating success
of males can be related to the devel
-
opment of such traits (Jarvi 1990,
Fleming and Gross 1994, Quinn and
Foote 1994), conspicuous dorsal
humps might also make males more
vulnerable to bears in shallow fresh
-
water streams. Indeed, predation is
sometimes sex
-
specific (e.g., Frame
1974), which
may alter operational
sex ratios and patterns of sexual se
-
lection. Selective predation on large
adults would favor the evolution of
maturation at smaller sizes, just as
selective commercial harvest may
have done in the past (Healey 1986).
Implications
Anadromous (and inshore) fishes
appear to link the ocean, fresh wa
-
ter, and land in important functional
ways, supporting a complex food
web
that crosses the land
-
water in
-
terface. This role was particularly
strong in the past, when spectacular
migrations of anadromous fish
graced coastal streams around the
Holarctic. Although anadromous
fishes are still a central, critical re
-
source on north Pacific coasts and in
some interior regions, many of the
southern runs of salmon on the Pa
-
cific coast of North America are gone
or nearly
so,
the victims of overfish
-
ing and anthropogenic changes to
the rivers
(NRC
1996,
Slaney et
al.
1996). Most historical runs
of salmon on Atlantic coasts
have also declined severely
(Netboy 1968), although
remnant populations of
wildlife species continue to
use the reduced resource
(Carss et al. 1990).
In many of these
places,
deforestation and urbaniza
-
tion, accompanied
by
intense
hunting and trapping, have
reduced the habitats of natu
-
ral consumers of these fishes,
such that the interlocking
food web has been effectively
demolished from both ends.
For example, grizzly bears
historically foraged inten
-
sively on salmon in the Co
-
lumbia River drainage (Hil
-
derbrand et al. 1996), but
many of those salmon stocks are
threatened or extinct (Nehlsen et al.
1991, NRC 1996), and grizzly bears
are now found only in remote sites in
this region. Northwestern North
America now offers one of the few
remaining places to both study and
conserve these rich ecosystems. Al
-
though many spawning stocks are
ancient, dating from before the last
major glaciation, others were estab
-
lished recently, following receding
glaciers (Milner and Bailey 1989).
As predators discover the new runs,
the aquatic
-
terrestrial nutrient link
is forged, and scientists may be able
to observe their development.
The significance of anadromous
fish to riparian ecosystems has ma
-
jor implications for management. A
broad management perspective is
often useful, but nowhere more so
than in regions where interactions of
anadromous fishes and wildlife link
the water and the land. Management
goals and practices that recognize
and account for strong interactions
among ecosystem components (Will
-
son 1996) would reduce risks to eco
-
logical integrity and function (Kor
-
honen 1996). Under the umbrella of
ecosystem management and ecologi
-
cal integrity, there are implications
for specific aspects of
management:
Fisheries. Commercial fishers typi
-
cally take huge numbers of returning
anadromous fish from the ocean,
neglecting the ecological importance
of
fish. Historically, the magnitude
459
of the harvest was often based chiefly
on allowing an “escapement” just
large enough to produce the next
generation. This practice is not dead,
although Larkin (1977) wrote its epi
-
taph 20 years ago. However, the
idea that fish numbers above the
minimum needed to make the next
generation are “excess production”
(and therefore to be freely harvested)
becomes ecologically meaningless
when the cascading effects of anadro
-
mous fishes in the ecosystem are con
-
sidered (Winter and Hughes 1997).
It is possible
to
model the effects
of
stream enrichment by salmon car
-
casses on the density
of
spawning
salmon in subsequent generations
(Robert
E.
Bilby, Brian R. Fransen,
Jason Walters, Weyerhaeuser Com
-
pany, Tacoma, WA, and Peter A.
Bisson, Forestry Sciences Laboratory,
Olympia, WA, personal communi
-
cation), but estimates of the run size
and number of carcasses needed
to
maintain terrestrial nutrient flow are
lacking.
Salmon are usually harvested be
-
fore they reach their spawning
grounds because they can be har
-
vested in huge numbers and their
bodies are in good condition. Com
-
mercial mixed
-
stock fisheries com
-
monly take the fish in salt water
before the stocks separate
to
their
spawning streams. In addition, com
-
mercial and subsistence harvest of
salmon on lower reaches
of
major
rivers such as the Yukon removes
many fish bound for upriver tribu
-
taries (e.g., Brannian 1990). An in
-
eluctable result of intensive mixed
-
stock harvesting is the extirpation of
some stocks, especially smaller ones
(Hilborn 1985), which reduces
or
eliminates the prey base for wildlife
and people in some watersheds.
Harvest timing also has conse
-
quences for wildlife. Selective fish
-
ing on early runs favors delayed run
timing of pink salmon (Alexanders
-
dottir 1987); such temporal shifts
could reduce numbers and impair
the body condition of animals that
depend on anadromous fish for mi
-
gratory stopovers, reproduction, or
winter survival. In addition, size
-
or
sex
-
selective harvests can exert tre
-
mendous selection pressures on body
size
or
shape, sex ratios, and age
distributions, although such consid
-
erations have been slow to enter the
mainstream literature (Ricker 198
1,
Healey 1986).
Given the probable ecological
roles of anadromous fishes in many
coastal, freshwater, and riparian eco
-
systems, it is clear that high harvest
levels and mixed
-
stock fisheries can
potentially damage these systems by
removing
or
greatly diminishing a
“cornerstone” resource. Truly sus
-
tainable harvest levels would account
for the distribution of fish across the
landscape and through the season as
well as for the number of spawners
needed to fertilize the streams and
riparian zones and feed the wildlife.
Forestry.
Deforestation and habi
-
tat degradation reduce populations
of some aquatic and terrestrial wild
-
life species associated with anadro
-
mous fish streams. Because wildlife
species are important agents
of
nu
-
trient transfer within a riparian sys
-
tem, declines in their numbers must
weaken the links in the complex food
web. Road building (e.g., for log
-
ging) often increases access by hunt
-
ers and trappers,
so
wildlife popula
-
tions commonly decline in areas with
roads (Mace et al. 1996, Person et al.
1996). Roads built in riparian zones
of anadromous fish streams might
also threaten critical ecological in
-
teractions in these zones. Moreover,
if
“buffer strips” of remnant forest
along anadromous fish streams are
too
narrow to accommodate the ac
-
tivity of animals that use runs
of
anadromous fishes, the transfer of
nutrients from water
to
land could
be impaired and the survival and
reproduction of some wildlife spe
-
cies reduced. In addition, the impor
-
tance of the forest for fish goes far
beyond conventional consideration
of water temperatures, sedimenta
-
tion, and pool
-
creating woody de
-
bris. Selection pressures from terres
-
trial predators may influence body
size and shape and several aspects
of
life history
-
factors that, in turn, af
-
fect the economics
of
fish harvesting.
Wildlife. Protection of anadromous
fish runs and maintenance of safe
and productive foraging areas
of
the
terrestrial predators and scavengers
would benefit the wildlife species
that depend seasonally on these prey
populations. Human disturbance and
development can force bears to move
away from feeding areas (Barnes
1989, Reinhart and Mattson 1989),
with potential detrimental effects
on
their body condition. Furthermore,
hunting
of
predators
or
scavengers
during spawning runs probably de
-
ters the surviving individuals from
full use of the fish resources, poten
-
tially reducing their reproductive
success. Management goals that do
not maintain the wildlife species that
transport nutrients in the aquatic
-
terrestrial food web risk damaging
that ecological link.
Finally, there is a clear need for
greater unification of aquatic and
terrestrial ecology (Cairns 1992).
Conventional wisdom acknowledges
the movement of terrestrial materi
-
als such as dead leaves,
logs,
and
insects
into
freshwater streams, but
it has seldom
-
if ever
-
dealt seri
-
ously with transport from water to
terrestrial communities. Recognition
of
reciprocal
interchanges of organ
-
isms and nutrients between water
and land has only recently attracted
much attention, although for many
years linkages have been recognized
among the abundance
of
ocean fish;
the abundance, foraging rates, and
reproductive success of shore
-
nest
-
ing seabirds; and the localized nutri
-
ent deposition in seabird colonies on
land (e.g., Crawford and Shelton
1978, Montevecchi 1993). Recently,
however, Polis and Hurd (1995,
1996) and Rose and Polis (in press)
have described how marine input
subsidizes terrestrial communities in
the Gulf
of
California, and other
workers are exploring the effects of
emergent aquatic insects on migra
-
tory birds (Ewert and Hamas 1995)
and other terrestrial animals (Mary
E. Power, University of California
-
Berkeley, personal communication).
The time has come for aquatic
and terrestrial ecologists to interact
in studying the two
-
way coupling of
land and water systems. Ecological
systems based on anadromous fishes
may have special, but as yet un
-
known, properties because the nutri
-
ent input occurs in pulses (e.g., Lodge
et al. 1994, Odum et al. 1995) and
because they are an ecotone between
water and land (e.g., Risser 1990,
Polis and Hurd 1996). If some or
-
ganisms can be seen as “ecosystem
engineers
n
(Jones et al. 1994), then
anadromous fishes and the wildlife
species that transfer nutrients across
Rio,%ience
vel.
48
habitat boundaries probably qualify.
In general, the transfer of organisms
and nutrients among habitats
is
com
-
mon in many biomes and has sub
-
stantial effects
on
populations, com
-
munities, and ecosystems (Polis et al.
1995, 1997).
Acknowledgments
We thank Peter A. Bisson, Fred
H.
Everest, Robert
T.
Paine, Thomas
C.
Shirley, William W. Smoker, and A1
von Finster for helpful discussion or
comments
on
this manuscript and
Ellen Anderson for creating Figure
2.
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