Download Keystone Interactions: Salmon and Bear in Riparian Forests of Alaska

Keystone Interactions: Salmon and Bear in Riparian Forests of Alaska
Author(s): James M. Helfield and Robert J. Naiman
Source: Ecosystems, Vol. 9, No. 2 (Mar., 2006), pp. 167-180
Published by: Springer
Stable URL: http://www.jstor.org/stable/25470328 .
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(2006) 9: 167-180
Ecosystems
DOI: 10.1007/sl0021-004-0063-5
ES*S\C\/CTEAAC
E VA/3 T O 1 EfVlD
? 2006Springer
Science+Business
Media,Inc.
Keystone
in
Bear
Interactions:
Forests
Riparian
James M. Helfield,1,3*1
of Forest
College
Sciences,
of Alaska
and Robert
Box 352100,
Seattle,
University
of Washington,
Box 355020,
98195,
Seattle, Washington
of Washington,
Umed
and Environmental
Science,
University,
Resources,
University
and
Salmon
J.Naiman2
98195,
Washington
USA;2
School
of Aquatic
USA;3 Landscape
Ecology
Group,
SE-901
Sweden
87, Umed,
and Fishery
Department
of Ecology
Abstract
in the presence
of
increased
forest is significantly
not
both salmon and bear, but
by either species
of salmon and bear
The interactions
individually.
to
of
24%
may provide up
riparian N budgets, but
varies in time and space according
this percentage
is used to describe
species"
"keystone
that exert a disproportionately
organisms
impor
on the ecosystems
tant influence
in which
they
as "keystone
such
live. Analogous
concepts
The
term
in
and "mobile
links" illustrate how,
of two or more
cases, the interactions
species
an effect greater
than that of any one
produce
Because
in
of their
role
species
individually.
ocean
to
river
nutrients
from the
and
transporting
mutualism"
to variations
many
ties, rather
animals
than
are equal,
but some animals
Orwell
are more
(1945)
Received 25 May 2004; accepted 16 December
2004; published online
15March 2006.
*
Corresponding author; e-mail: [email protected]
^Current address: Department of Environmental
Sciences, Huxley College
Western
of the Enviroment,
Bellinaham,
University,
Washington
98225-9181,
mor
than
their
specific
component
parts.
that control
the integrity
describe
those animals
Since then, the
and stability of their communities.
used in ecology and con
concept has been widely
has been
and the keystone
servation,
designation
range of taxa at various
trophic
applied to a wide
levels in various ecosystems
(see Bond 1993; Mills
and others 1993; Power and others 1996).
there is no universally
accepted oper
Although
a keystone
of what
constitutes
ational definition
Ecological
theory holds that certain animals exert
a disproportionately
on the
influence
important
in
Paine
which
live.
ecosystems
(1966) first
they
a
in reporting
described
this phenomenon
how
starfish
influences
the
(Pisaster ochraceus)
predatory
and population
of an
species composition
density
Washington
channel
of barnacles,
intertidal ecosystem.
By eating masses
Pisaster prevents
exclusion
competitive
by domi
nant organisms,
thereby creating open space for a
Paine
of species.
subse
greater number
(1969)
the term "keystone
introduced
species" to
quently
others."
George
escapement,
salmon; bear; riparian forest; marine
Key words:
derived nutrients;
nitrogen;
species.
keystone
Introduction
equal
salmon
characteristics,
vegetation
phology
and functional
redun
suggesting
interdependence
sources.
These
illustrate
N
findings
dancy among
of interspecific
the
the complexity
interactions,
across
bound
of
ecosystem
linkages
importance
of examining
aries and the necessity
the processes
communi
and interactions
that shape ecological
Pacific salmon
riparian ecosystems,
(Oncorhynchus
and
bear
brown
(Ursus arctos) have been de
spp.)
scribed as keystone
links, al
species and mobile
are
to
few
data
the
available
though
quantify
to
of
this
interaction
relative
other
importance
vectors.
nutrient
of a mass
balance
Application
to data from a southwestern
stream
model
Alaskan
to
that
influx
the
suggests
nitrogen
(N)
riparian
"All
in
and watershed
species, certain requisite traits have been identified.
are generally
so designated
native
Animals
species
their activities
and abun
that regulate,
through
USA
167
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All use subject to JSTOR Terms and Conditions
168
J. M. Helfield
and R. J. Naiman
or physical
productivity,
diversity
their communities,
with
influences
those organisms
extending
beyond
directly affected
through
trophic interactions
(Paine 1966, 1969).
is that keystone
Implicit in the concept
species are
in their importance
relative to the rest
exceptional
dances,
structure
the
of
of
the community
(Mills and others
1993), that
in their functioning
within
the
they are unique
and that their impacts
community
(Kotliar 2000),
are disproportionately
large relative to their abun
dances
(Power and others 1996). Loss of a keystone
in the struc
species results in significant
changes
ture
or
of
organization
a
ecosystem,
given
pre
with
adverse
for the
consequences
sumably
survival of other native
species or populations.
Most
of the keystone
descriptions
phenomenon
focus on a single species, although
it is understood
cases keystone
that in many
effects arise through
the interactions
of two or more
species. For exam
the "key
ple, studies of mutualism
(for example,
sensu Gilbert
stone mutualist
1980;
hypothesis"
and
Christian
2001)
Bertness and Shumway
facilitation
(for example,
1993; Bertness and Leonard
and others 2001) demonstrate
how
1997; Mulder
interactions
among different
positive
species help
maintain
the structure and diversity of various plant
and animal
under
ad
communities,
particularly
verse environmental
conditions.
There has been
some debate as to whether
such positive
interac
tions exert amore widespread
influence
than do the
in
forces of competition
and predation
described
Paine's
definitive
(Bruno and
keystone
example
are dependent
on
others 2003), but both paradigms
interspecific
tion
strength"
interactions.
as
a measure
Use
of the term "interac
of
the
importance
of
most
of their
life histories
and
(see Lundberg
2003).
Moberg
Another
of this sort of interspecific,
example
interaction
is the transfer of nutri
trans-boundary
ents from the Pacific Ocean
to river and riparian
ecosystems
by sockeye salmon (Oncorhynchus nerka)
and brown bear (Ursus arctos). Pacific salmon have
as keystone
been described
species in coastal eco
as a food re
because
of their importance
for vertebrate
and scavengers
predators
and others
1995; Willson
(Willson and Halupka
salmon and bear have been de
1998). Similarly,
scribed as interacting mobile
link organisms because
of their role in transporting marine-derived
nutri
ents to forest ecosystems
in Alaska
(Lundberg and
systems
source
marine-derived
nutrients
2003). Although
Moberg
to influence
have been
shown
riparian structure
and dynamics
2001, 2002;
(Helfield and Naiman
Bartz and Naiman
to
few data are available
2005),
of the salmon-bear
the importance
inter
quantify
to other nutrient
action relative
vectors. Here we
for nitrogen
present a mass balance model
(N) flux
in the riparian forest adjacent
to a boreal Alaskan
stream. The objectives
of this study are to quantify
in N contributions
variations
via
spatiotemporal
salmon and bear relative to other N sources, and to
elucidate
the potential
effects of salmon
long-term
on the productivity
bear interactions
and species
of riparian ecosystems.
In so doing, we
composition
to build on the existing body of theoretical
hope
related to the keystone
and
species concept
our understanding
in which
enhance
of the ways
are shaped by interspecific
communities
ecological
across
and
interactions
ecosystem
linkages
work
boundaries.
Macarthur
1972;
(for example,
keystone
predators
Paine 1992) implies that this importance
is derived
through the reactions of other species. Accordingly,
some authors
com
have
that ecological
argued
more
and
be
community
plexity
stability may
on synergistic
from
effects
dependent
resulting
on
or
actions
interactions
the
than
interspecific
of any one species (Naiman and Rogers
and Jones
and others
1993; Lawton
1995; Soule and others 2003).
In some cases these keystone
interactions
involve
across
boundaries.
that
ecosystem
migrate
species
abundances
1997; Mills
link" pollinators
and
include the "mobile
Examples
and
the
seed dispersers described by Gilbert
(1980),
and
Polis
others
subsidies
described
by
spatial
or
that carry nutrients,
energy
(1997). Animals
food
material
otherwise
among
separate
genetic
on the
exert a significant
influence
webs may
structure and dynamics
of receiving
communities,
even if they are extrinsic
to those communities
for
of Salmon,
Interactions
Vegetation
Riparian
Bear
and
Having
spent most of their lives feeding and grow
at
Pacific salmon returning to spawn and die
sea,
ing
in their natal streams carry marine-derived
nutri
ents in their body tissues. Returning
salmon are
eaten
mammal
and bird species
by numerous
and others
and others
1989; Willson
(Cederholm
car
from
nutrients
salmon
and
1998),
decaying
casses support the production
of periphyton,
aqua
resident
freshwater
fishes
tic macroinvertebrates,
streams (Mathis
salmon in spawning
and juvenile
en and others
1990, 1993;
1988; Kline and others
Schuldt and Hershey
1995; Michael
1995; Bilby and
and others 1998). These
others
1996, 1998; Wipfli
are also delivered
to terrestrial vegetation.
nutrients
stable isotopes
indi
Studies of naturally-occurring
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All use subject to JSTOR Terms and Conditions
Keystone
Interactions
169
to spawning
cate that riparian
plants
adjacent
as
as
streams may
much
derive
18-26% of their
N
from
salmon
and
others
foliar
1996; Ben
(Bilby
and
Hilderbrand
others
David
and others
1998;
and midge
(Diptera:
Chironomidae)
feed
directly on salmon carcasses in streams,
species
whereas
blackflies
mayflies
(Ephemeroptera),
on
and
fine par
feed
(Diptera: Simuliidae)
midges
2001, 2002).
1999a; Helfield and Naiman
from
nutrients
Transfer
of marine-derived
streams
to
is
medi
ecosystems
spawning
riparian
are an important
ated largely by bears. Salmon
downstream
from decomposing
ticles immediately
carcasses
and others 1998;
1997; Wipfli
(Minakawa
nutri
and Gara 1999). Salmon-derived
Minakawa
ents are also incorporated
into the body tissues of
stoneflies
and dragonflies
(Odonata)
predatory
interactions
(Kline and others
trophic
through
are
1990; Bilby and others
1996). These materials
to
transferred
terrestrial
subsequently
adjacent
source for coastal bear populations
and
others
1996, 1999b), and bears
(Hilderbrand
a
consume
of total
large proportion
frequently
or
either
biomass,
spawner
through
predation
seasonal
food
carcasses
of post-spawn
(Quinn and
scavenging
Kinnison
and
Buck
1999; Quinn
2000; Reimchen
and
others
and
2000; Gende
2000; Ruggerone
others 2001; Quinn and others 2001). Marine-de
are then made
to riparian
rived nutrients
available
vegetation
through
carcasses
salmon
dissemination
and
of partially-eaten
salmon-enriched
wastes.
Hilderbrand
and others
(1999a) report that brown
bears on the Kenai Peninsula,
deliver 83
Alaska,
in white
N detected
84% of marine-derived
spruce
500 m of spawning
(Picea glauca)
foliage within
streams. These findings are consistent
with
other
studies demonstrating
between
spatial correlations
N in riparian fo
bear activity and marine-derived
and others
and
1998; Helfield
liage (Ben-David
Naiman
2002).
bears are the most visible consumers
of
Although
are
use
not
to
the
make
salmon, they
only species
of this anadromous
food source. River otter (Lontra
canadensis) and mink
(Mustela vision) feed regularly
on salmon
and
others
1998; Ben-David
(Blundell
marten
and others
whereas
1997a),
(Martes ameri
into
salmon
their
diets during
cana) incorporate
of
low
abundance
of
years
prey species
principal
and
others
Bald
(Ben-David
1997b).
eagle
(Haliaeetus leucocephalus) and gulls (Larus spp.) also
and occasionally
kill salmon
in Alaskan
scavenge
streams
and
others
and
1998;
Quinn
(Ben-David
Buck 2000). On the Olympic
Peninsula
of Wash
bear are absent and black
brown
ington, where
bear
(U.
Cederholm
mammals
carcasses.
americanus)
are
relatively
scarce,
and others
list 22 species of
(1989)
to consume
and birds known
salmon
These
animals
all
transport
marine-de
rived
to terrestrial
nutrients
and organic matter
with amounts
and spatial distributions
ecosystems,
to the abundance,
varying
according
longevity,
and per capita salmon
of
mobility
consumption
each species.
At finer spatial scales, insects play an important
role
in mediating
(Jackson
numerous
nutrient
transfer
stream-riparian
and Fisher
larvae of
1986). Aquatic
stonefly
(Plecoptera),
(Tri
caddisfly
choptera)
of the adult insects
the emergence
or
death
subsequent
consumption
by
terrestrial insectivores.
Salmon carcasses deposited
on exposed gravel bars and in the riparian zone are
and consumed
quickly colonized
by larval forms of
flies
terrestrial
and
(Diptera:
Calliphoridae
carrion
and
beetles
Scathophagidae)
(Coleoptera:
which
be an important
factor
may
Silphidae),
ecosystems
and their
with
and distribution
of sal
decomposition
controlling
mon-derived
nutrients
(Meehan 2000).
are also transferred
to
nutrients
Marine-derived
In
habitats
abiotic
lar
processes.
riparian
through
carcasses on
salmon
ger rivers, flooding deposits
stream banks
and
others
1989; Ben
(Cederholm
David and others 1998). In streams with hydrauli
conductive
cally
from decomposing
riparian ecosystems
dissolved
nutrients
substrates,
carcasses may be transferred
to
via shallow subsurface
(that is,
Studies
of non-salmon
flowpaths.
hyporheic)
streams have demonstrated
that the hyp
bearing
orheic
zone
can
as
serve
as
a transient
solutes
storage
area
for
from
surface
nutrients,
downwelling
zone can be rapidly atten
water
to the hyporheic
uated
and uptake
through
sorption
physical
by
communities
microbial
and
Walters
1983;
(Bencala
zones
Triska and others
1994). Where
hyporheic
are shallow and extend
the
active
laterally beyond
the roots of riparian plants may extend
floodplain,
zone and take up transiently
into this saturated
stored nutrients.
and Edwards
O'Keefe
(2003)
concentrations
that
of ammonium
reported
(NH4)
and soluble reactive phosphorus
increased
signifi
stream following
Alaskan
cantly in a southwestern
of spawning
and
that
salmon,
entry
sockeye
water
nutrient-enriched
surface
subsequently
zone beneath
entered
the hyporheic
the riparian
forest. The importance
as a
of hyporheic
exchange
vector
for marine
nutrients
is controlled
by the
physical
hyporheic
salmon
extent
zone,
carcasses
and hydraulic
of the
conductivity
as well
as by the abundance
of
within
the
stream.
This marine
nutrient
subsidy has a potentially
important influence on riparian plant communities.
This content downloaded from 128.163.8.62 on Wed, 5 Nov 2014 10:44:57 AM
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170
and R. J. Naiman
J. M. Helfield
Recent
found that foliar N content,
studies have
and stem densities
of riparian
basal area growth
streams
trees are enhanced
at sites near spawning
and
Bartz
and
Naiman
2002;
2001,
(Helfield
and
richness
whereas
2005),
species
are
relative
of
decreased,
understory
plants
density
to comparable
sites without
salmon
(Bartz and
It
marine
N influx
is
that
Naiman
2005).
possible
of N
also
decrease
the
may
advantage
competitive
as
in
such
alder
(Alnus spp.), resulting
fixing plants
of these species near spawn
decreased
abundance
2002). Because
ing streams
(Helfield and Naiman
are generally
contents
foliar
N
with
plants
higher
more nutritious
to browsers
such as
and palatable
Naiman
moose
hare
snowshoe
(Lepus
(Alces dices) and
and
others
Pastor
1987;
americanus; Bryant
1988),
of
marine
also influence
N inputs may
patterns
turn
nutrient
in
affects
which
cycling,
browsing,
and plant species composi
successional
processes
and
and Bryant
tion (Kielland
1998; Suominen
to -6?C. Annual
-15
ranges from 250
precipitation
cm falls as snow
to 340 cm, of which
200-250
and Johnson
Creek
is
1984).
Lynx
(Hartman
at
2.3
km
Lynx
long, originating
approximately
into Lake Nerka.
Mean
Lake and discharging
summer
500
is approximately
1 s-1
discharge
Including Lynx Lake
(O'Keefe and Edwards 2003).
cov
the Lynx Creek watershed
and its tributaries,
ers approximately
2760
ha
The
(USGS
1979).
a
is
association
of
boreal
forest
riparian vegetation
and paper birch
(Betula papyrifera)
stands of balsam poplar
with
(Populus
interspersed
willow
(Salix spp.) and cottongrass
balsamifera),
are dominated
(Eriophorum spp.). Upland hillslopes
alder
stands
of
dense
green
(Alnus crispa).
by
of sockeye
sal
Since 1947, annual
escapement
mon
to Lynx Creek has ranged from 464 to 17,023
=
from
with
spawning
occurring
3,084),
(mean
and
late July
(Rogers
Rogers
August
through
that the average adult sockeye con
1998). Given
white
spruce
others 1999).
The consequences
82 g of N in its body tissues
runs
1997), annual
spawning
=
38
N
-1,397
(mean
253)
kg
bring approximately
to the Lynx Creek watershed
during the growing
of approx
season. The area supports a population
stream, potentially
increasing
aquatic productivity.
trees en
Increased growth and density of riparian
fil
sediment
bank
hances
stabilization,
shading,
debris
of large woody
tration
and production
enhance
spawning and rearing
(LWD), all of which
and others
fishes
for salmonid
habitat
(Meehan
and
Naiman
Harmon
and
others
1986;
1977;
imately 2.8 bears per 100 km2 (Van Daele 1998), all
the spawning
feed on salmon throughout
of whom
season. Recent
studies have characterized
patterns
on sockeye
of bear predation
(Quinn and Buck
and
and others
2000; Gende
2000; Ruggerone
as well
as
and others 2001),
others 2001; Quinn
tains
nutrient
subsidies to
of marine
also
affect
ecosystems
aquatic ecosystems.
riparian
in
in riparian
Increased N content
foliage entails
to
the
of
litter
delivered
creased nutritional
quality
1997; Bilby
Decamps
others
1998). Because
element
retaining
and Bisson
LWD
and
1998; Naiman
is a key
structural
carcasses
salmon
in
streams
and Peterson
1985), increased riparian
(Cederholm
of
the availability
enhances
further
production
effects in
nutritive
salmon carcasses and associated
As a result of these
lotic ecosystems.
linkages,
nutrients
carried upstream
by adult salmon help to
of subsequent
the productivity
enhance
genera
fishes.
tions of salmon and other stream-dwelling
A Mass Balance
at Lynx Creek
Model
for Riparian
N
estimates N flux at Lynx
The mass balance model
River Lakes system
Creek, a tributary of the Wood
in the Bristol Bay region of southwestern
Alaska,
a tran
area
in
is
The
158?55'
USA
N,
W).
(59?29'
as
as well
climatic
sitional
zone, with maritime
influences
continental
patterns.
affecting weather
summer
range from 6 to
temperatures
Average
20?C, and average winter
temperatures
range
from
approximately
(Larkin and Slaney
2003)
(O'Keefe and Edwards
of riparian veg
N enrichment
and
and Naiman
etation
2002; Bartz
(Helfield
in
River
the
Wood
Naiman
system.
2005)
calculates N influx to a
The mass balance model
corridor (45.2 ha) of riparian forest on
200 m-wide
processes
hyporheic
and marine-derived
the model
either side of Lynx Creek. Specifically,
N
of marine-derived
estimates annual contributions
for com
via bear activity and hyporheic
exchange
sources
from non-marine
parison with contributions
soils
and
leaching from upland
(that is, precipitation,
defines
For each N source, the model
N fixation).
and identifies variables
environmental
parameters
then be ad
N fluxes. Parameters may
controlling
justed to estimate N fluxes under different scenarios.
from empirical observa
Input data were derived
not
data
from Lynx Creek were
tions. Where
sites
we
from comparable
data
used
available,
or
River
the Wood
within
ranges of pub
system
Mini
for boreal Alaskan
lished values
ecosystems.
were
mean
identified
values
and
mum, maximum
calculations were then
for all input variables. Model
combina
using all possible
repeatedly,
performed
as
so
to
full
the
tions of input data
range of
generate
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All use subject to JSTOR Terms and Conditions
Keystone
values for
possible results for each N source. Mean
values for all in
results were obtained using mean
of salmon
put variables. To assess the importance
total annual N in
bear interactions, we calculated
all possible
flux under 1,296 scenarios representing
maximum
and mean
combinations
of minimum,
the
from each N source, assuming
contributions
of both salmon and bear (729 scenarios),
presence
salmon but not
bear but not salmon (243 scenarios),
salmon nor bear
bear (243 scenarios),
and neither
scenarios were
Differences
among
(81 scenarios).
evaluated with Kruskal-Wallis
analyses of variance
contrast
using ranks, followed by Dunn's multiple
test. Calculations,
and in
assumptions
hypothesis
put data are described below.
Sample calculations
A
in Appendix
using mean
input data are provided
Interactions
171
to export N to the riparian zone via
potential
(USGS 1979). In a study of
downslope
leaching
at
much
forest sites encompassing
nutrient
cycling
in boreal
encountered
of the range of conditions
Alaska, Van Cleve and others
(1983) report mean
to 1.9 kg N ha"1
0.4
from
annual
fluxes ranging
mean
via
This
range
=1.2)
(all-site
leaching.
with
values reported in subsequent
encompasses
(Kaye and others 2003). Using these data,
at Lynx Creek are calculated
contributions
NL
=
JL
'
AL
studies
leaching
as
(2)
via
NL is the mass of N delivered
annually
from upland
soils, JL is the per unit area
leaching
annual flux of N via leaching, and AL is the upland
where
leaching
area.
(http://www.springerlink.com).
N Fixation
Precipitation
source of N
is a variable
but continuous
data are available
describing
of N within
the Wood River
atmospheric
deposition
system, but the US National Atmospheric
Deposition
(NADP 2003) reports amean annual flux of
Program
0.19 kg ha"1 (range = 0.02-0.63)
for the years 1980
at each of its two closest monitoring
sites
-2001
AK03
Poker
Denali
National
Creek;
(AK01
Park).
these sites are in the interior of Alaska and
Although
Precipitation
in boreal forests. No
receive
less annual
rainfall than does the Bristol Bay
and Johnson
1984),
region (NADP 2003; Hartman
studies of global patterns of N cycling indicate that
or
receive
greater,
they
comparable,
slightly
amounts
of reactive N via atmospheric
deposition
(Galloway and Cowling 2002). Using these data, the
as
model
calculates N influx via precipitation
NF=JF'AR
(1)
via
NF is the mass of N delivered
annually
area
is
the
unit
flux
of
annual
JP
per
precipitation,
N via precipitation,
and AR is the area of the
where
riparian
Leaching
zone.
from Upland
Soils
accumu
forests are areas of net nutrient
Riparian
lation within
the watershed
(Van Cleve and Yarie
1986) and typically derive
proportions
significant
of their total nutrient
from upland
soils.
budgets
Whereas
in the
surface runoff is likely negligible
forested
Creek
undisturbed,
watershed,
Lynx
of soil solution
leaching and downslope movement
the lake
may be important vectors for N. Excluding
its tributaries,
and
the Lynx
Creek watershed
area
273 ha of upland
comprises
approximately
Biological N fixation may be an important source of
N in northern
forests. Through
the
symbiosis with
Frankia actinomycete,
alders fix atmospheric
N2,
to ammonium
is converted
and transferred
which
to surrounding
secretions
soils via root and nodule
of N-rich
leaf litter (Binkley
and production
1986;
in
Wurtz
This
results
accelerated
N
process
2000).
as
in
N
and
increased
forest
soils,
availability
cycling
as in increased growth and foliar N content
in
and
conifers
sympatric
understory
plants
(Binkley
1983; Binkley and others 1985, 1992; Wurtz
1995;
and
Gower
Rhoades
and
others
1998;
2001).
Vogel
Shrub alders of boreal ecosystems
(for example, A.
well
forests
crispa;A. tenuifolia) inhabit early-successional
Van
and
others
Cleve
and
Viereck
Cleve
1971;
(Van
stable
1981; Wurtz
1995), but also form long-term,
Wurtz
communities
and
others
1985;
(Wilson
influence
soil N dynamics
which
may
2000),
the
later
of
succession.
stages
throughout
at
No data are available
N fixation
describing
Lynx Creek, but other studies have characterized
rates of N fixation
in boreal Alaskan
forests. Van
Cleve and others
annual N
(1971) report a mean
fixation rate of 156 kg ha-1 (range = 72 -362)
for
alder stands of various
the Tanana
ages within
River floodplain.
These values are similar to those
area
in subsequent
in the
studies
reported
and Van Cleve
(Klingensmith
1993) and at other
boreal
and Alaskan
sites (Lawrence
1958; Daly
that N fixation rates are compa
1966). Assuming
rable at Lynx Creek and proportionate
with
alder
as
N fixation may be calculated
abundance,
h
where
fixation,
= a
(Jaref / tfref) (3)
Ja is the per unit area annual flux of N via N
a is alder abundance
of
(that is, proportion
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172
J. M. Helfield
and R. J. Naiman
cover or aboveground
forest biomass),
Jaref is the
per unit area annual flux of N via N fixation at the
site (for example,
reference
Van Cleve and others
at the reference
1971), and aTci is alder abundance
site. Alder comprises 83 - 89% (mean = 86) of total
at the Tanana River
aboveground
plant biomass
sites (Van Cleve and others
1971). As alder abun
dance data for Lynx Creek are reported in terms of
uses percent cover as
percent cover, this calculation
a surrogate
for percent biomass
and
(see Mynemi
others 2001; Fensham
and others 2002).
covers approximately
Alder
44% of the Lynx
Creek watershed
(O'Keefe and Edwards 2003), but
zone is negligible
alder abundance
in the riparian
and
Naiman
The
of alder
(Helfield
2002).
majority
fixed N affecting
the Lynx Creek riparian
forest is
an
therefore
leached
from upland
stands. Mean
nual
losses described
leaching
by Van Cleve and
others
0.2%
of
(1983)
represent
approximately
a similar rate of
forest floor soil N pools. Assuming
leaching at Lynx Creek, total riparian N influx via N
as
fixation is calculated
Na
=
'
'
(JaU PL AL) -r (JaR AR)
(4)
via N
Na is the mass of N delivered
annually
fixation, JaU is the per unit area annual flux of N via
as in Eq. (3), pL is the
upland N fixation, calculated
to
of
soil
N
lost
proportion
leaching, AL is the up
where
land leaching area, JaR is the per unit area annual
as in Eq.
flux of N via riparian N fixation, calculated
area
zone.
is
and
the
of
the
This
AR
(3),
riparian
assumes upland alder distribution
to be
calculation
relatively homogenous
(that is, non-patchy).
alder
is
the
primary N-fixing
Although
species in
Alaska's boreal forests (Wurtz 1995), there are other
the
capable of fixing N. For example,
organisms
Schreber's
feather moss
(Pleurozium
ubiquitous
(Nos
schreberi) forms symbioses with cyanobacteria
as 1.5 - 2 kg N ha-1
toc spp.) and may fix as much
in mid- to late-successional
boreal forests,
annually
on abundance
and the length of the
depending
season
Simi
(DeLuca and others 2002).
growing
form symbioses with
larly, some lichen mycobionts
fix N
and
(Rai 1988; Honegger
cyanobacteria
rates of N fixation by lichens and
1991). However,
are 1-2
lower
orders of magnitude
bryophytes
Alex
for alder (for example,
than those reported
and Billington
1986; Van Cleve and others
may
1971), and N fixed by lichens and bryophytes
to soil N pools. Previous
be less likely to be exported
fix barely enough N
studies suggest that bryophytes
own metabolic
to satisfy
their
requirements
and
that N
and Billington
1981),
(Alexander
trees or
transfer from feather moss to neighbouring
ander
tortuous
and Alexander
(Van Cleve
a
of N
1981). Similarly,
large proportion
relatively
fixed by lichens
is retained
for cyanobacterial
metabolism
it
(Rai and others
1983). Nonetheless,
should be recognized
that the mass balance model
underestimates
total biological
N fixation by con
shrubs
is
sidering
only
Hyporheic
alder-mediated
N fixation.
Exchange
O'Keefe
and Edwards
the exis
(2003) confirmed
tence of an extensive
zone
parafluvial
hyporheic
to Lynx Creek and demonstrated
that
adjacent
is a feasible mechanism
for
hyporheic
exchange
to riparian
nutrients
marine-derived
transporting
a spawning
run of 9460
vegetation.
Following
sockeye in 2000 (T. P. Quinn, unpublished
data), a
flux of 4.3 kg N ha-1 yr"1 was observed moving
through a 100-cm deep column of hyporheic water
to Lynx Creek
and T. C.
adjacent
(R. T. Edwards
a propor
O'Keefe,
unpublished
data). Assuming
tional relationship
between
escapement
sockeye
of N downwelling
and the mass
into hyporheic
as
annual
flux may be calculated
flowpaths,
JH = E
where
JH is the per unit
100 cm deep column
JHref is the
escapement,
100 cm deep column of
(JHref/ ?ref) (5)
area annual
flux of N per
of hyporheic
E is
water,
per unit area flux of N per
water
observed
hyporheic
during the reference year (for example,
2000), and
the
reference
ETei is escapement
year.
during
zone
to the parafluvial
The depth
hyporheic
cm
to
to
30
150
Creek
from
ranges
Lynx
adjacent
below the soil surface (O'Keefe and Edwards 2003).
Because
of white
the maximum
rooting
depth
120 cm (Nienstaedt
and
spruce is approximately
Zasada 1990), only the upper portion
of the hyp
is accessible
orheic water column
for uptake, and in
some
cases none
of it is accessible.
Accessible
as
flux is therefore
calculated
hyporheic
JHacc
= JH
[(Zrt
-
ZH) / 100]
(6)
N
where
Jnacc is the per unit area flux of hyporheic
to riparian plants, JH is the flux of hypor
accessible
heic N as in Eq. (5), Zrt is the rooting depth of riparian
zone. On
plants, and ZH is the depth to the hyporheic
zone
35
extends
the parafluvial
average,
hyporheic
m (range = 0 -100)
at
the active channel
beyond
and T. C. O'Keefe,
(R. T. Edwards
Lynx Creek
data). As the spatial extent and con
unpublished
zone varies according
to
figuration of the hyporheic
in
and
variations
channel morphology
reach-scale
substrate permeability
(Edwards 1998), the riparian
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Interactions
Keystone
area underlaid
flows at Lynx Creek
by hyporheic
to
45.2
N contri
0
ha.
from
may range
Hyporheic
butions are therefore calculated as
Nh
=
*
^Hacc ^H
(7)
to
is the mass of N delivered
annually
is
via
the
JHaCc
exchange,
hyporheic
riparian plants
flux of accessible hyporheic N as in Eq. (6), and AH
is the area of the parafluvial
zone, cal
hyporheic
as
stream
twice
and
the product of
culated
length
where
the
NH
extent
lateral
active
of hyporheic
flow
beyond
173
to salmon
and
abundance
also varies according
a greater proportion
ease of capture, with
eaten
or harder to capture
when
fish are less abundant
and others (2001)
and
others
Gende
2001).
(Gende
that
per fish killed
percent
report
consumption
=
mean
4
to
80
from
the
ranges
25) within
(all-site
the uneaten
Wood River system. Assuming
portion
is left on the riparian
of each bear-killed
salmon
forest floor, N influx via discarded
as
may be calculated
the
Ncarc
channel.
= E
PBK
'
(1
~
Peat)
salmon
carcasses
'
^Nsock
(10)
via
ATcarc is the mass of N delivered
annually
E
is
salmon
of
carcasses,
deposition
partially-eaten
is
the
of
salmon
killed
pBK
escapement,
proportion
of
by bears as in Eq. (9), peai is the proportion
biomass eaten per fish, and mNsock is the mass of N
in the body tissues of each adult sockeye
contained
where
Bear Activity
in the northern
Bristol Bay region is
density
2.8
individuals
per 100 km2 (Van
approximately
from 0.53 to
Daele
with
densities
1998),
ranging
100
interior
30.4 individuals
km2
per
throughout
Local
densities
Alaska
Daele
and
others
(Van
2001).
near streams are typically greater during
salmon
Bear
For example,
and others
Hilderbrand
spawning.
on
43
of
-57%
bear
observations
(1999a) reported
as being within
500 m of
Peninsula
the Kenai
a similar degree of
streams. Assuming
spawning
at
be
bear
Creek,
Lynx
aggregation
density may
as
calculated
?agg
= B
(pbf / Paf) (8)
spawning
Bagg is local bear density during
season, B is regional bear density, pB? is the pro
500 m of spawn
portion of bears observed within
is
and
of the total
the proportion
pAF
ing streams,
m
area observed
is
500
of
that
within
spawning
where
streams
In the
and others
1999a).
(Hilderbrand
no
assumes
absence
of salmon,
model
bear
the
=
(that is, Bagg
B).
aggregation
On average,
bears kill approximately
37% of
in the Wood
River
system
spawning
sockeye
rates vary
(Quinn and others 2001), but predation
to bear density
from year to year according
and
salmon
abundance
Kinnison
and
1999;
(Quinn
and others
and others
2000; Quinn
Ruggerone
Creek, another
2001). At Hansen
tributary of the
River system that is comparable
Wood
in length
to Lynx Creek (Rogers and
and average escapement
and others
Rogers
1998), Ruggerone
(2000) report
an inverse relationship
between
and
escapement
the proportion
of salmon
killed by bears. This
as
is quantified
relationship
pBK=
where
bears
(2493 E-0531) j 100
salmon
1997).
(Larkin and Slaney
The other means
bear contribute N to
by which
waste
is
via
forests
excretion.
riparian
Among Kenai
500 m of spawning
Peninsula bears observed within
and others (1999a) report that
streams, Hilderbrand
each adult female passes 0.046 -0.051
kg ha"1 of
N annually via urine and, to a lesser
salmon-derived
feces and decomposition
of body
tissues
extent,
after death. On average,
salmon represent 62% of
carbon and N for Kenai Peninsula
bears,
dietary
with values for coastal, salmon-eating
populations
in Alaska ranging from 33 to 79% (Hilderbrand and
others
1999b). Using these
excretion may be calculated
^excr
^Mexcr
/
influx
/?Ndiet
via bear
/
V11
of N per
JexCr is the per unit area excretion
area
is
unit
excretion
the
of
salmon
bear, JMexcr
per
derived N per bear, and /?Ndiet is the proportion
of
where
bear
of
dietary
salmon,
N
from
derived
the model
between
tributions
via bear excretion
Nexcr
Jexcr
=
salmon.
calculates
difference
and
(#agg
'
^F
JMexcr-
In
this
the
flux
Annual
absence
as
N
are then calculated
*
)* ^excr ^R
the
con
as
(12)
where
via
iVexcr is the mass of N delivered
annually
as
bear excretion,
is
local
bear
in
density
Eq.
Bagg
500 m of the stream, Jexcr
(8), AF is the area within
is the per unit area excretion
of N per bear as in Eq.
and
is
the
this
AR
(11),
riparian area over which
flux is deposited.
Total bear-mediated
N contribu
as
tions are calculated
(9)
of salmon killed by
pBK is the proportion
and E is escapement
and others
(Ruggerone
of biomass
eaten per fish
2000). The proportion
=
data, N
as
NB
=
NCarc + NeXcr (13)
where NB is the mass of N delivered
annually
bear activity, NcaTC is the mass
of N delivered
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via
via
J. M. Helfield
174
and R. J. Naiman
D escapement
* 464
escapement*
annual
nitrogen
contributions
(kg N yr"1) and percentage of
total annual nitrogen influx (%) to the riparian
zone of Lynx Creek via precipitation
(P),
leaching from upland soils (L), alder-mediated
nitrogen fixation (A), hyporheic exchange (H),
0 escapement*17023
1200
1. Estimated
Figure
3084
|
and
bear
800*4^-1
(B), as a function
are mean
values,
activity
Data
of
salmon
calculated
escapement.
balance
model
values
using mean
by the mass
within
of
for all input variables
the parameters
Error
scenario.
bars represent
each
escapement
the full range of results obtained
z
400-?-fm*mm
P
possible
L
A
H
B
discarded salmon carcasses as in Eq. (10), and Nexcr is
as in Eq. (12).
via excretion
the mass of N delivered
Model
Results
and Discussion
is the
Model
calculations
indicate
that leaching
source of N in the riparian zone at Lynx
dominant
from
contributions
Creek
(Figure 1). Annual
sources
and other non-marine
(that is,
leaching
are not influenced
and N-fixation)
by
precipitation
in salmon abundance,
but these decrease
changes
sources
as contributions
in importance
from marine
in
and bear activity)
(that is, hyporheic
exchange
crease with
At
levels of escapement.
increasing
minimum
accounts
marine-derived
N
levels of escapement,
for approximately
7% of total annual
levels of escape
riparian N influx. At maximum
to 39%.
increases
this percentage
ment,
bear activity
When
salmon are abundant,
rep
source
resents
of
the
second most
important
for an average
of 15% of
riparian N, accounting
and
total N influx at mean
levels of escapement
at maximum
levels of escapement
(Figure 1).
24%
of
combinations
input
using all
values.
Total
Model
spawning
calculations
season
indicate
there
are,
that
on
average,
during
8.4
the
bears
the vicinity of Lynx Creek, and
per 100 km2 within
that bears kill approximately
35% of returning
in years of mean
This cor
spawners
escapement.
mean
roborates the
value (37%) reported forWood
streams by Quinn
River
and others
(2001). The
via par
N is distributed
of bear-mediated
majority
salmon carcasses
(that is, ort). In years
tially-eaten
of mean
bears discard an average of 66
escapement,
as
in
0.7 kg N yr"1
ort,
compared with
kg N yr-1
a
in
urine and feces. Although
greater mass
passed
via ort, N distributed
via excre
of N is distributed
more
tion is
Carcass scraps are found
widespread.
the immediate
within
vicinity of
exclusively
streams
and Naiman
2002),
spawning
(Helfield
whereas
bear excretion may be detected more
than
500 m from the stream
and others
(Hilderbrand
because
the majority
of excreted
1999a). Moreover,
converts
to
in
is
which
N
delivered
urine,
rapidly
ex
ammonium
and
others
1999a),
(Hilderbrand
to riparian
creted N may be more
readily available
almost
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Interactions
Keystone
trees than organic forms of N bound in carcass tis
sues (Schulze and others 1994).
It should be recognized
is not
that bear activity
zone.
in the riparian
distributed
homogenously
streams are
Certain locations adjacent to spawning
for fishing and feeding on salmon, and
preferred
these are characterized
elevated
by significantly
rates of excretion
and carcass deposition
(Hilder
600
500
zone
riparian
interactions
salmon-bear
source of marine-derived
at
Lynx
Creek,
there
are generally
N in the
are
?'?
X
a
*
400
a _L
-T-3
'
I
ci
cp
300J_
B
N
2. Estimated
Figure
to
yr"1)
the
presence
of
salmon
(B),
and
bear
intervals,
scenarios
imum,
riparian
neither
S
total annual nitrogen
zone
SB
influx
of Lynx
Creek,
assuming
nor bear
salmon
but
(N), bear
(kg N
the
not
salmon
bear
but not
salmon
(S), and both
are mean
? 95%
values
confidence
(SB). Data
on mass
based
balance
for 1,296
calculations
all possible
combinations
of min
representing
maximum
and mean
from each N
N contributions
source.
letters
denote
subsets.
homogenous
Superscript
ranks
indicates
Kruskal-Wallis
of variance
analysis
by
=
means
P <
differences
89.86,
among
significant
(x23
tests indicate
contrast
Dunn's
0.001).
multiple
significant
differences between SB and N (Q4 = 5.42, P < 0.001), but
not between B and N (Q4 = 0.20, P > 0.5) or S and N
(Q4
=
2.26,
0.2
> P>
0.1).
circum
stances under which
contributions
may
hyporheic
be equally if not more
of
important. The magnitude
N flux via hyporheic
is controlled
exchange
largely
to and lateral extent
of hyporheic
by the depth
are in turn controlled
flowpaths, which
by topog
soil texture and
raphy, channel
geomorphology,
all of
hydraulic
1998),
conductivity
(Edwards
which
within
the
At
the
watershed.
vary spatially
maximum
extents
and
minimum
lateral
depths
observed at Lynx Creek, hyporheic
flows are below
to the area
the reach of riparian roots or confined
so
beneath
active
the
that N in
channel,
directly
is nonexistent.
In
exchange
hyporheic
as
as
annual
contributions
be
N
contrast,
may
high
316 kg, or 65% of total influx
in areas where
are at minimum
hyporheic
flowpaths
depth and
ex
maximum
lateral extent
(Figure 1). Hyporheic
a
source
of
therefore
be
dominant
N
change might
some reaches of Lynx
in other systems or within
flux
'
*L
and others
and Naiman
1999a; Helfield
for localized
effects in
2002). By not accounting
the mass balance model may
these bear middens,
underestimate
the importance
of bear-mediated
N
at smaller (for example, patch-level)
spatial scales.
The importance
of bear activity as a source of N is
individually.
Although
the greatest
"j
_b
brand
Con
derived
interactions
with
salmon.
through
the importance
of salmon-derived
N to
versely,
on facilitation by bear.
riparian forests is dependent
Model
simulations
indicate
that total N influx to
zone at Lynx Creek
is significantly
the riparian
in the presence
increased
of both salmon and bear,
but not in the presence
of either salmon or bear
alone
suggest that the
(Figure 2). These
findings
interactions
of salmon and bear are more
important
to riparian N budgets,
to riparian
and by extension
than are the actions of either species
ecosystems,
175
via
Creek.
in hyporheic
Temporal
variability
exchange
also
be
than
indicated by the mass
greater
might
balance model.
The mass
of dissolved
nutrients
to
increases
with
downwelling
hyporheic
flowpaths
not
but
this
be
escapement,
might
relationship
a
is
When
escapement
proportionate.
high,
large
of spawner
biomass
will
proportion
decompose
instream and potentially
into the hyp
down well
is low, however,
orheic zone. When
escapement
a
consume
bears and other terrestrial piscivores
of
biomass
spawner
greater proportion
(Ruggerone
and others 2000; Gende and others 2001), leaving a
small amount of carcass material
disproportionately
to decompose
instream. Accordingly,
the impor
tance of hyporheic
be
overestimated
exchange may
and underestimated
for years of low escapement
for years of high escapement.
alder-mediated
N fixation contributes
Although
a relatively
of total riparian N
small proportion
influx at Lynx Creek
(Figure 1), this process may
source of N at other sites. Among
be the dominant
other sub-basins within
the Wood
River
system,
alder coverage ranges from 5 to 82% in the uplands
and R. T. Edwards,
(T. C. O'Keefe
unpublished
0
to 19% in riparian zones (Helfield
and
from
data)
are
and Naiman
these parameters
2002). When
results indicate
applied to the Lynx Creek model,
that annual N contributions
from alder could the
be as high as 3,800 kg, accounting
for
oretically
97% of total influx, or as little as 2 kg, accounting
for less than 1% of total influx (Figure 3). Riparian
This content downloaded from 128.163.8.62 on Wed, 5 Nov 2014 10:44:57 AM
All use subject to JSTOR Terms and Conditions
J. M. Helfield
176
and R. J. Naiman
tance of marine-derived
N and the relative impor
tance of different N vectors vary from year to year
to variations
in escapement
and other
according
climatic
and
parameters
(for example,
ecological
bear abundance,
Seasonal
patterns
precipitation).
might also be important. For example, precipitation
and leaching occur throughout
the year, and a large
OtcgNyr1
0%
10000i
1000-1
o.i
I |
in winter may be lost to
of N deposited
proportion
In contrast,
the system during
the spring thaw.
N is deposited
marine-derived
primarily
during the
a
and
of annual
season,
greater proportion
growing
H?
J?I-Hi?,?I-HH?,?ILynx Creek
Wood
Minimum
Wood Rtver
Maximum
River
influx may
(kg N
Figure 3. Estimated annual nitrogen contributions
of
influx
and
total
annual
percentage
(%)
nitrogen
y"1)
zones
riparian
are presented
tershed
area, 0%
to
via
Data
alder-mediated
for Lynx
Creek
of riparian
area)
fixation.
nitrogen
= 50% of wa
(alder
and for theoretical
sites
(5% watershed, 0% riparian)
representing the minimum
and maximum
19% riparian) alder
(82% watershed,
abundances
observed within
the Wood River system
(Helfield and Naiman 2002; R. T. Edwards and T. C.
O'Keefe,
culated
by
unpublished
the mass
all
variables
input
Error
nario.
bars
tained
using
are mean
Data
data).
balance
model
within
the
parameters
the
full
represent
all possible
combinations
values,
mean
using
range
of
values
for
each
sce
results
ob
of
of
cal
input
values.
is the most
abundance
factor
important
N contributions,
alder-related
with
each
affecting
1% increase in riparian alder abundance
resulting
in an increase of approximately
80 kg in annual N
contributions.
alder
Keystone
Interactions:
versus Parts
Processes
and bear meet
the basic criteria of keystone
in
that
their
loss
entails significant
species
changes
in the N budget and, by extension,
the productivity
and structure of the riparian forest. Organisms
af
fected
include
terrestrial
scavengers,
plants,
as well
as stream
and browsers,
decomposers
fishes (Figure 4). To the extent
that bear
dwelling
food source, and to
rely on salmon as an essential
the extent
that bear-mediated
fertilization
of
Salmon
habitat
for juve
helps to enhance
are
salmon and bear populations
not only
in their role as
mutually
dependent
nutrient
vectors, but also for their long-term
per
sistence. These findings illustrate the complexity
of
interspecific
linkages and interactions
structuring
river and riparian ecosystems.
riparian forests
nile salmonids,
Yet
varies
of this keystone
the significance
both temporally
and spatially.
interaction
The
impor
therefore
be retained and assimilated
by
bear excretion
and dis
riparian plants.
Spatially,
carcasses
occur at varying
semination
of salmon
rates
of
whereas
of hyporheic
degrees
aggregation,
to reach
and
vary according
exchange
leaching
in topography,
soil texture
scale differences
and
In general,
N processing.
microbial
the influence
of
to the
N increases with proximity
marine-derived
stream
channel
and others
1998;
(Ben David
and others 1999a; Helfield and Naiman
Hilderbrand
differences
2001, 2002), but at broader resolutions,
in climatic and biogeographic
factors (for example,
alder abundance,
bear density)
entail
significant
in the relative importance
differences
of N sources.
their
the
Moreover,
despite
interdependence,
are
some
in
to
involved
this
interaction
species
extent
Marine
nutrients
may be
interchangeable.
various
carried upstream
of
salmon,
species
by
those with
low spawning
den
including
typically
sities
Schuldt
and
1995;
(for example,
Hershey
1996), or by other anadromous
Bilby and others
such as char
fishes,
(Salvelinus
spp.) or smelt
Willson
and
others
spp.;
1998). Simi
(Thaleichthys
vectors
be
bears
the
dominant
for
may
larly,
of
marine
in
transfer
nutrients
stream-riparian
but this function may
many Alaskan watersheds,
be supplemented
and others
1997a, b;
(Ben-David
and Buck 2000; Blundell
and others 2003)
Quinn
bears are scarce, replaced by
or, in regions where
and others
other species
1989; Bilby
(Cederholm
in
and others
nutrient
1996). Long-term
cycling
watersheds
therefore
de
salmon-bearing
might
of different
pend on a combination
species and
ex
abiotic
processes
(for example,
hyporheic
alternate over time in their relative
change), which
none of these is
functional
importance.
Although
in its function,
loss of any one will
entirely unique
if not immediate
consequences.
long-term
reason why
is not easily
Another
this interaction
in terms of the keystone
characterized
species
is its reliance on linkages across ecosystem
concept
boundaries.
the impact of a given species
Assessing
or guild relative to its abundance
within
the com
munity
implies an ability to discern the boundaries
have
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All use subject to JSTOR Terms and Conditions
Keystone
4.
Figure
of marine-derived
Cycling
MDN
transport
salmon-enriched
upstream;
wastes
(B) Bears
and
nitrogen
and other
partially-eaten
(MDN)
and
on
effects
consume
piscivores
carcasses
salmon
in
river
and
salmon;
the
riparian
salmon carcasses, enhancing decomposition
and MDN diffusion;
beneath
is
the
forest
and
taken
up by tree roots; (F)MDN
flowpaths
riparian
colonize
rates
of riparian
trees;
(G) Riparian
trees
provide
shade,
bank
riparian
(C) Bears
forest;
ecosystems;
and
plants,
potentially
altering
patterns
of browsing,
which
in turn
affects
cause
of
salmon
(A) Spawning
other
into hyporheic
(E) Dissolved N downwells
content
enhance
foliar
N
and growth
inputs
organic
matter
debris (LWD), enhancing the quality of instream habitat for salmonid fishes; (H) LWD retains post-spawn
in streams, further enhancing MDN availability; (/) Increased foliar N content enhances palatability
riparian
177
disseminate
piscivores
and
insects
(D) Terrestrial
aquatic
allochthonous
stabilization,
Interactions
patterns
of
riparian
and
large woody
salmon carcasses
and nutrition of
productivity
and
species
composition.
of that community
Paine
1992;
(for example,
Power
and others
is
This
1996; Hurlbert
1997).
easier to accomplish
in an
for sessile organisms
intertidal
Paine
community
(for example,
1966)
than for animals
like salmon and bear that migrate
over long distances
freshwater
spanning marine,
and
terrestrial habitats. As with
functional
impor
to
of a community
is sensitive
tance, the definition
the spatial and temporal
scales of observation.
are especially
Riverine
characterized
ecosystems
by
connectivity
and others
with
(Naiman
surrounding
landscapes
even
1987; Ward
1989),
although
are
discrete
af
ecosystems
seemingly
invariably
fected to some degree by external
influences.
or possibly because of, its importance
as
Despite,
a theoretical
con
the keystone
construct,
species
cept has
Whereas
been the subject of considerable
debate.
some authors
have
recommended
that
the focus of environ
species be made
keystone
mental management
and conservation
efforts
(for
1989; Woodruff
1989; Rohlf
Conway
example,
the
1991; Carroll
1992), others have questioned
of the keystone
be
species concept
applicability
in quantifying
inherent
the difficulties
and
effects
which
keystone
distinguishing
species
merit
such distinction
1993;
(Mills and others
Hurlbert
Our
illus
1997; Kotliar
2000).
findings
trate the extent to which
keystone
species rely on
interactions
and
linkages across eco
interspecific
extent
to which
and
the
their
boundaries,
system
in
varies
time
functional
and
space.
importance
Losses of species identified as keystones may have
adverse
for other members
of their
consequences
but protection
of these species does
communities,
not guarantee
the avoidance
of such consequences.
more
to con
it
be
constructive
may
Accordingly,
the interactions
and processes
that structure
communities
rather than their specific com
for and protection
of
ponent
parts. The search
a
to
tacit
species
keystone
implies
permission
more
obscure
but
other,
ignore
impor
potentially
tant taxa, along with
and
interactions
interspecific
abiotic processes
any
ecosystems,
linking multiple
of which may be essential
combination
for main
the
taining
long-term
productivity,
diversity,
or viability
structure
of a given commu
physical
sider
those
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All use subject to JSTOR Terms and Conditions
J. M. Helfield
178
and R. J. Naiman
is to
nity. If the first rule of intelligent
tinkering
save all the parts (Leopold
1953), the second rule
how they fit together.
should be to understand
ACKNOWLEDGEMENTS
thank M.
We
C.
R. T. Ed
R.
T.
D.
E.
T. C. O'Keefe,
Liermann,
T. P. Quinn,
L. Peterson,
D.
Paine,
R. E. Bilby,
C. A.
two anonymous
reviewers
for their
to this paper. We also thank
contributions
valuable
L. Strom for illustrating Figure 4 and the University
for logistic
Alaska Salmon Program
of Washington
was
in
Financial
Alaska.
support
support
provided
and
Schindler
Science
Foundation
National
(DEB
by
Service's Pa
States
Forest
the
United
98-06575),
Station and the University
Research
cific Northwest
the
of Washington.
Ecol
Bond WJ.
Bruno
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