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Habitat Loss, Trophic Collapse, and the Decline of Ecosystem Services
Author(s): Andrew Dobson, David Lodge, Jackie Alder, Graeme S. Cumming, Juan Keymer,
Jacquie McGlade, Hal Mooney, James A. Rusak, Osvaldo Sala, Volkmar Wolters, Diana Wall,
Rachel Winfree, Marguerite A. Xenopoulos
Source: Ecology, Vol. 87, No. 8 (Aug., 2006), pp. 1915-1924
Published by: Ecological Society of America
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Ecology, 87(8), 2006, pp. 1915-1924
? 2006 by the the Ecological Society of America
HABITAT LOSS, TROPHIC COLLAPSE, AND THE DECLINE OF
ECOSYSTEM SERVICES
Andrew
Hal
David
Dobson,1'10
Jackie
Lodge,2
A.
James
Mooney,6
Graeme
Alder,3
Osvaldo
Rusak,2'11
S. Cumming,4
Volkmar
Sala,7
and Marguerite
A.
Wolters,8
Juan
Keymer,1
Diana
Wall,9
Jacquie
McGlade,5
Rachel
Winfree,1
Xenopoulos2'12
1
Department
Princeton
New Jersey 08544-1003
and Evolutionary
USA
Princeton,
University,
of Ecology
Biology,
Sciences,
of Biological
University
of Notre Dame, P.O. Box 369, Juniper and Krause Streets,
Notre Dame,
Indiana 46556-0369
USA
V6T 1Z4 Canada
The University
British Columbia
3Fisheries Centre, 2204 Main Mall,
Vancouver,
of British Columbia,
Institute of African Ornithology,
7701, Cape Town, South Africa
of Cape Town, P. Bag Rondebosch
University
4[Percy FitzPatrick
5
10 The Coach House,
University
College
Compton
Verney CV35 9HJ UK
of London,
94305-5020
USA
Sciences,
Stanford
University, Herrin Labs, Room 459, Stanford,
California
of Biological
6Department
Brown University,
and Evolutionary
Rhode Island 02912 USA
Providence,
of Ecology
Biology,
7Department
Giessen, Germany
of Animal Ecology,
Justus-Liebig-University
of Giessen, Heinrich-Buff
Ring 26-32 (IFZ), D-35392
8Department
State University,
Fort Collins, Colorado
USA
Colorado
80523-1499
9Natural Resource Ecology
Laboratory,
2Department
Abstract.
of sustaining
and services
that we
provisioning
goods
for the conservation
of
economic
strong
justification
these
the relationship
between
and
services
and
goods
The
is a
ecosystems
Understanding
and
arrangement,
In
management.
habitats
of natural
is a fundamental
quality
we describe
a new
this paper,
approach
changes
of natural
challenge
to
from
obtain
biological
the
assessing
natural
diversity.
in the size,
resource
of
implications
loss for loss of ecosystem services by examining how the provision of different
ecosystem services is dominated by species from different trophic levels. We then develop a
mathematical model that illustrates how declines in habitat quality and quantity lead to
sequential losses of trophic diversity. The model suggests that declines in the provisioning of
services will initially be slow but will then accelerate as species from higher trophic levels are
habitat
lost
at
rates.
faster
collapse
(and
these
patterns
similar
suggest
In general,
change.
anthropogenic
of
Comparison
assembly)
ecosystem
with
empirical
in natural
occur
patterns
and
goods
services
of
examples
systems
by
provided
ecosystem
impacted
species
by
in the
upper trophic levels will be lost before those provided by species lower in the food chain. The
decrease in terrestrial food chain length predicted by the model parallels that observed in the
oceans
following
as
them
susceptible
Whereas
exploited.
extinct
by
on
the
this
trophic
as
traditional
order-of-magnitude
loss of an entire
the
represent
species
an
The
overexploitation.
to extinction
area
large
are
they
species-area
in habitat
decline
trophic
level
and
conservation;
ecosystem
Key
biodiversity;
Lake; species-area;
species loss; trophic collapse.
Introduction
The
study of
of
goods
and
from
theoreticians
predict
the effects
ecosystems
services
has
and
that decreases
and
attracted
all
this magnitude
of
services
performed
abundance,
the ecosystem
loss may
by the
level.
words:
functioning
of higher
levels make
trophic
where
they are systematically
are driven
that 50% of species
requirements
in marine
systems
curve
suggests
in ecosystem
reductions
of biodiversity
their
much
experimentalists.
in biodiversity
on
the
to provide
ability
recent
attention
Ecologists
will
lead to
received 31 December
13 January
2004; revised
Manuscript
16 January 2006. Corresponding
Editor: R. B.
2006; accepted
see footnote
Jackson. For reprints of this Special Feature,
1, p.
1875.
10
E-mail:
[email protected]
11
Present
Center
for Limnology,
address:
of
University
Trout Lake Station,
Wisconsin-Madison,
Boulder-Junction,
Wisconsin
54512 USA.
12
Present
address: Department
of Biology,
Trent Univer
K91 7B8 Canada.
Ontario,
sity, Peterborough,
of
provisioning
web; Little
services; food
ecosystem
function;
Rock
in the
and hence
functioning
et al. 1994,
1995, Daily
et al. 2000, Loreau
2000, Chapin
services
(Naeem
et al. 1997,
1997, Daily
et al. 2001). The exact
shape of this relationship
depends
on the ecosystem
as well as the order
and service
process
in which
species
are
lost
or potentially
from,
added
to,
the ecosystem (Mikkelson 1993, Sala et al. 1996, Petchey
et al. 1999, Petchey and Gaston 2002, Duffy 2003). A
number
of
possible
functional
have
forms
been
sug
that couple biological
gested for the relationships
diversity to the rate and resilience with which different
types
of
are undertaken
processes
ecosystem
1996, Tilman et al. 1996, Kinzig
all of
these
maximum
declines
1915
is the argument
rate
to zero
at which
as
species
that
the
(Sala
et al.
et al. 2001). Central to
there
activity
diversity
is some
asymptotic
is undertaken
that
and
abundance
are
1916
ANDREW
ET AL.
DOBSON
40
in
Primary
producers
20
these
be
may
almost
under
land
1986
The
1987
earliest
linearly
each
of
stage
8
water
and
the
upon
dependent
habitat
conversion
diversity-functioning
-40
Large-scale
ground
the
explicitly
investigate
on
focused
above
relationship
and plant
production
species
diversity.
primary
manipulative
species in different
-60
pattern,
with
decreases
in
similar
Tertiary consumers
small
-80
?CO
20
no
discernible
-60
services
and
-80
becoming
a!
-120
habitats
et al. (1993)
and
reduced (Mikkelson
et al.
Crawley
one
only
for (B) in Schindler
1993, Tilman
1999,
or a few
Loreau
species
Examples
studies
show
lost
ecosystem
levels
different
trophic
are
studies
from
the
species
more
rapidly
of
services
as
uses.
marine
levels
higher
trophic
from
than
species
are
lower
loss of habitat quality or quantity
and
services
are
in a predictable
ecosystem
ecosystem
sequence
and
terrestrial,
at
slowly
et al.
Larsen
2002,
on
other
is
types
needed
freshwater,
that
These
levels
species,
or
on
loss
biodiversity
ecosystem
et al.
(Kremen
habitat particularly
relating
algal
production
other
trophic levels with
\-$).
of
of ecosystem
replacement
or converted
for other
disrupted
are
Stres
specific
loss
in primary
of
effects
for
-100
(Figs.
examine
in
rates (Schindler et al. 1985). Empirical
available
typically
that
in little
changes
the
but more
2005),
or
the collapse
Brezonik
further
in decreases
resulted
diversity
experiments
resulted
acidification
of
carnivorous
(initial N =9
(B)
primarily
Zooplankton
species).
consumers
in Lake 223, Ontario,
Canada
Quaternary
(initial N
= 7 fish
=
=
5.59, final pH
4.75; for
species). For (A), initial pH
=
= 5.13.
fish data were
6.49, final pH
(B) initial pH
Complete
taxa were
unavailable
for (A), and complete
data for other
unavailable
for (B). For
of recruitment
(B), the cessation
was treated as species extirpa
(absence of young-of-the-year)
are available
tion. Additional
details
for (A) in
experimental
production
in
resulting
while
(Tilman et al. 1996, 1997, Hector et al. 1999).
evidence
loss (as a percentage
of pre
species
to gradual
in response
number)
experi
in two north
lakes. (A) Four
temperate
in Little Rock
USA:
Lake, Wisconsin,
= 51
primary
(initial N
producers
phytoplankton
species);
consumers
TV=
36 primarily
herbivorous
primary
(initial
= 9
consumers
secondary
(initial N
Zooplankton
species);
consumers
omnivorous
and
tertiary
Zooplankton
species);
losses
species
primary
species
decomposition
1. Annual
acidification
species
mental
acidification
levels
lower-trophic
all showed a
production
and
Fig.
the first
grassland
using
in
sors,
1977
CD -20
O)
cc
i??
c -40
CD
experiments
regions of the world
reductions
In whole-lake
0
to
experiments
-20
where
nutrients
of
87, No.
(Dobson 2005).
0
1998,
amount
the
cases,
processed
area
of
Vol.
Ecology,
other
examples
dominated
way.
services
A
by
logical
respond
that
suggest
specific
inference
some
trophic
is that
to loss of
differently
if the spectrum of functional forms
services
(producers
to biodiversity
onto
maps
to consumers).
Thus we might
et al. (1985).
et al. 1997, Loreau
et al.
undertake
In cases
2001).
the ecosystem
function then decline may be rapid as the abundance of
the activity declines
the species undertaking
(for
of herbivores
top
by
regulation
are
functions
of
this
ecosystem
type
as brittle.
In contrast,
classified
there will be other
types
a
function
where
between
of ecosystem
competition
example,
population
carnivores);
diversity
so that
by
of
species may
loss of one
the
in
increase
the
create
species
abundance
considerable
may
be
and
0.08
redundancy,
for
compensated
activities
of
a similar
that occupies
niche
(Naeem
competing
species
rate at which
In
these
the
relative
and Li
cases,
1997).
as species
slow
will
be relatively
the process
declines
we would
For example,
decline.
and abundance
diversity
argue
cleansing
compete
that
this
where
with
is the case
for nutrient
and water
cycling
a huge
of microbial
diversity
species
each other while
the function;
undertaking
a
0.06
Perimeter-to-area
0.04
0.02
ratio
2.
Fig.
of
landscape
simplification
(decreasing
Impact
of
loss (as percentage
ratio) on the species
perimeter-to-area
of herbaceous
species number)
(line a)
pre-acidification
plants
and carabid
fields
trophic groups
(lines b-d)
inhabiting wheat
=
located in central Germany
groups of carabids
35). Trophic
(n
include (b) mixophagous,
and (d) predaceous
(c) phytophagous,
are (c) 40.3 (P < 0.05) and
coefficients
species. The regression
the slopes
of (a) and
(P <
0.005);
(d) 66.3
(b) are not
different
from zero (Purtauf et al. 2005.).
significantly
DETERMINANTS OF BIODIVERSITY CHANGE 1917
August 2006
100
few
Primary producers
o Primary consumers
Secondary consumers
Q.
O
TO
10
T 6>
O T
.C
pattern
O
"cO
C/)
with
V
10
on each
no. species
Total
100
3.
scatter to the data, the rate of
there is considerable
Although
decline of plant species (solid circles) has a shallower
slope than
consumers
the rate of decline
of primary
(open circles). The
consumers
et al.
show no clear pattern, but Terborgh
secondary
on the smaller
in ant abundance
(2001) record huge increases
islands in terminal
stages of collapse,
on ants has essentially
disappeared.
brittle
such
as carbon
services;
of
provisioning
that depend
are
chains
also
aim
is consider
under
the
diversity
thus
levels,
we
that
also
may
these
quantity;
recreation,
the
services
services
collapse by assuming
We
recognize
that
in habitat
to
relationships
loss. Second, we
on
2000),
forms
key
but
explicitly
ecosystem
assumes
that
predominantly
then model
ecosystem
is lost.
trophic
that their
such
the
similarly
services
associated
activity
of
(Bunker
et
empirical
many
provided
al.
example
2005).
The
would
Naeem
processes
predominantly
located at specific
species
most
be
that most
Such
services
levels,
loss
an
be
drugs,
and
genetic
on
readily
these
"type C"
as each
from
species
characteristics
unique
for
compensated
loss
the
essence,
of
each
in the loss of a "unit" of
of
Examples
the provisioning
include
in service
depend
with
In
species results
the biodiversity
intermediate,
may
cannot
they prey.
are
responses
fall between
decrease
each
species.
of
would
example,
a linear
E
type
service.
ecosystem
of
resources,
C
type
fruits,
ecosystem
pharmaceut
supporting
CO
.<D 500
?
CD
?" 400
services
J
3001
-
?All species
-o- Plants
- Plants and herbivores
200i
100
result
processes
regulation;
ecosystem
result
and
trophic
include
species
the abundance
regulation
levels on which
A
we
diversity-service
such
by
relationships
remaining
individual
species
lower
levels.
ecosystem
of population
species.
services,
at
of
trophic
and
show
would
species
by
and
brittle
brittle
very
type
For
multiple
these more
provided
lower
service
extremes.
1880
from the interaction between trophic levels (particularly
many
services
of
mapping
trophic
most
are
fragile
600
that higher trophic levels decline
lower
than
rapidly
We
levels.
trophic
specific
are
in
in the
First,
between
and reduction
species-area
or
the
700
explored
manuscript).
to biodiversity
decline
ecosystem
specific
more
use
be
are
changes
These
rare
keystone
ecotourism,
species
response
ical
trophic
when
relationship
a simple,
but plausible,
onto
which
biodiversity,
propose
explicitly
will
unpublished
possible
we
essentially
link habitat
model
complications
in species diversity
decline
by
is no
lost,
the
on
have
Services
relationships.
services
on different
species
increase
in prey abundance
(A. P. Dobson,
the simplest
assume
and
between
there
are
predators
elsewhere
The
is a
there
trophic diversity
services.
ecosystem
interactions
ignores
of biodiver
that
assumption
between
simple mapping
of
the consequences
na?ve
services.
to supply
likely
acknowledge
levels
two
habitat
further
the relationships
evaluate
between
we have
and ecosystem
services,
trophic
collapse,
a three
of
built
model
component
phenomenological
loss
decline
of
Our
and
services.
ecosystem
biodiversity
small
in large changes
ecosystem
or
and
control,
responses
services,
fuel
While many species located in the upper levels of trophic
ecosystem
To
E
type
these
result
that
recognize
conditions
boundary
loss of ecosystem
erosion
storage,
predominantly
loss,
principal
loss
sity
for
services;
of
provisioning
with
total
biomass
In contrast,
protection.
We
to see a predictable
hierarchical
as habitats
are eroded.
expect
services
most
of
that pr?dation
implying
cover
species biodiversity
island
loss and net species diversity
(log-log
scale)
Species
on different
et al.
islands
in Lago Guri
(after Terborgh
on
is more
advanced
1997a, b, 2001).
Ecological
collapse
lower net
smaller
islands with
species
diversity
(x-axis).
Fig.
plant
storm
this
as
such
primary
production
or associated
and fiber,
wood
0.1
that
be those directly associated
these will be predominantly
-i'
g>
o
CD
Q.
en
et al. 2003.). We
suggest
as type A ecosystem
loss be classified
1999, Vinebrooke
of
in a
result
et al.
(Schindler
et al. 1995, Crawley
1995, Frost
1994,
losses
species
services
of a
losses
the remaining
for by
compensated
et al.
1985, Naeem
where
studies
further
eventually
in ecosystem
decrease
et al.
8
CD
are mostly
species
until
species
drastic
O
in grassland
observed
response
0
the
their
from
the
levels
observed
primary-production
1920
1940
1960
1980
Year
et al.
and
trophic
commonly
1900
on Krakatau
Fig. 4. Recovery
of trophic diversity
follow
that led to the total extinction
of all
ing the volcanic
eruption
life on the island
lowest
line
(after Thornton
1996). The
illustrates
the number of plant species on the island, the middle
line is the number of herbivore
of predatory
species.
number
species,
and
the top
line is the
1918
ANDREW
as
such
pollination
provision
istics play
et
(Kremen
nutrient
2003),
cycling
al.
of habitat
where
a unique
ecological
individual
role
et
Klein
2002,
et al. 2000),
(Schwartz
al.
and
character
species'
as pollinators
or seed
dispersers (Kremen 2005).
We
have
used
the
list of ecosystem
and
goods
services
developed by theMillennium Ecosystem Assessment as
the basis of our list of services provided by different
and
natural
Millennium
from
the
to biodiver
services
consensus
represent
after
in
services
were
services
table
discussions
classified
ently
in the
each
author
each
ecosystem.
to be
Some
consistently
thought
services
ecosystems
(primary
production),
were
more
in some
others
considerably
fragile
tems
in others
As we
than
control).
(biological
took
it became
this exercise,
ecosystem
strongly
to
services
on
dependent
that
changes
in
of
sufficient
the biodiversity-service
ple, provisioning
relationship.
is the dominant
of food
cultivated
lands,
which
is a
production,
and
shows
a type A
forest
the
ecosystems,
dominant
service
but
productivity
response.
of
provisioning
is not directly
and
to
rather
the
the
under
type
further
exam
in
is not
the
of
presence
to primary
a broader
spectrum of species (from fungi to plants and animals);
it has
a type C
the dominant
whereas
service,
response,
to
has a type A response.
of fiber,
Sensitivity
loss was minimal
for services
predominantly
provision
biodiversity
provided by decomposers and primary producers (type
A) and maximal in the case of services provided by top
predators (type E). The general patterns described in
Table
might
services
two
1 identify
construct
as
a
key
that
we
any model
in
changes
habitat
increasing
of
result
for
assumptions
predicts
of
faunal
support
are
collapse
will
ecosystem
Lambert
increase
of
collapse
et al. 2003);
in herbivores
the
(Terborgh
are
these
when
trophic levels go extinct. This
overexploitation
of plant
of events
sequence
species,
et al.
our
predators
by massive
at higher
in turn is followed
so
that
to
lead
1997?, b, 2001,
characterized
the
that
lost
as
pattern
holds
will
50
after
the
restructure
were
years
there
to colonize.
the net
in size,
by
the vegetation
becomes dominated by inedible and thorny species. This
we
here
that
decline
will
in the
at
many
species
area
larger
requirements
rate
at lower
than
those
faster
lake
acidification
and
(Menge
cally more
fewer
resting
1987). For
levels
trophic
they are physiologi
environmental
to survive
stages
higher
same
the
Sutherland
because
to
habitat quality
example,
ecosystems,
susceptible
this
modify
because
have
a
at
in aquatic
example,
unfavorable
stress,
have
periods,
and
are more dispersal limited (Menge and Sutherland 1987,
Bilton et al. 2001, Vinebrooke et al. 2003). An increasing
body of evidence suggests that species at higher trophic
levels
have
steeper
in their
slopes
relation
species-area
ships (Holt et al. 1999), and that food chain length is a
function
of habitat
size
and Newman
(Cohen
Post
1991,
et al. 2000, Post 2002). A combination
of such
theoretical and empirical studies suggest that declines
in either habitat quantity (or quality) leads to decreases
of food
chains
and thus a more
loss
lengths
rapid
at higher
services
levels.
by species
provided
trophic
in the
the
Modeling
These
Ecosystem
us
allow
services
ecosystem
series
of
Decline
observations
of
collapse
hierarchical
of nested
to
will
Services
that
suggest
be
determined
the
a
by
or breakpoints,
thresholds,
whose magnitude will occur at different levels of decline
we
snapshots
that
on Krakatau
ecosystems
only
will
levels
declines,
in overall
trophic
and
relationship;
assume
trophic
be
more rapidly than those at lower trophic levels (Figs. 1
4; Wardle et al. 1997, Terborgh et al. 2001, Kremen
2005, Larsen et al. 2005). The classic studies of John
Terborgh and colleagues on the islands of Lago Gur?
levels
webs
and
and
lost
illustrate
at higher
a sequential
lower
levels
note
recovery
trophic levels (Holt et al. 1999). When
(1)
species at different trophic levels perform different
ecosystem services and (2) species at higher trophic
levels will be lost more rapidly than those at lower
levels.
trophic
A number
of examples
contention
that species
higher
of
ecosystem
losses:
a final
decline disproportionately
In contrast,
related
successively
we
example,
for predators
are eroded
habitats
natural
approach
they
service of
food
seen
that has
to
top
resources
species-area
to primary
related
service
food
structure
the
ecosystem
herbivores,
As
is
For
ants.
in species diversity has traditionally been described by a
under
sensitivity
service that they provide
that
then
ecosystem
in decomposing
In marine
systems,
increase
of
surveys
suggest
ecosys
service
each
a change
in food web
from
loss of species
of the food web.
As
while
of
an
by
leaf-cutter
8
fishing has explicitly focused on the removal of species
from higher trophic levels this "fishing down of the food
chain" has led to a shortening of the food chain. In
contrast, in the Little Rock lake food web example
(Locke 1996), acidification of the water supply has led to
across
biodiversity
the ecosystem
species
providing
consideration.
Characteristics
modify
the
location
the trophic
dominant
and the dominant
apparent
is matched
particularly
87, No.
themselves from the bottom up (Thornton et al. 1988,
Thornton 1996); the island was first colonized by plants,
independ
resilient
turn
in
species,
Vol.
Ecology,
long-term
that
all
of
1;
(Table
2003). We have then
of ecosystem
response
Values
change.
emerged
ecosystems
Ecosystem Assessment
the
classified
sity
human-modified
ET AL.
DOBSON
effect,
web
in a way
In
abundance.
species
assume
that we
can
that
the most
such
rank
to model
order
the
species
resilient
this
in a food
species
are
at
the bottom of the food chain, while the least resilient are
at the top of food chain. Itmay be that body size is a key
of
determinant
however,
ity; some
are
much
pathogens
both
there
are
are
tiny,
trophic
position
resilience,
to this general
important
exceptions
such as elephants
and whales
key herbivores
in contrast
than
their
larger
predators,
but
are
key
regulatory
at all trophic levels. Empirical
relationship
and
between
body
components
studies supporting
size,
trophic
level,
the
and
1919
DETERMINANTS OF BIODIVERSITY CHANGE
2006
August
assessment
1. Qualitative
ecosystems.
Table
of
of different
the susceptibility
Urban
service
Provisioning
Fresh water
Fiber
Fuel wood
Food
resources
Genetic
and
Biochem
Cultivated
A
A
A
A
NA
NA
pharmaceuticals
resources
Ornamental
Drylands
of different
type
Ecosystem
Ecosystem
loss for a number
to species
functions
ecosystem
Inland water
Forests
and
woodlands
Coastal
Mountain
Island
systems
Polar
Marine
E
A
E
A
E
A
A
A
A
A
C
C
A
A
A
C
C
c
NA
A
E
A
E
E
C
E
NA
E
C
C
A
A
A
A
C
C
?
A
A
A
C
C
A
E
E
E
C
E
NA
A
E
E
C
E
A
A
A
A
A
A
A
A
A
B
A
A
A
C
B
A
A
E
E
E
A
A
E
C
A
A
A
A
A
C
A
A
A
A
C
A
A
A
A
A
A
A
NA
NA
A
NA
Regulating
Air quality
Climate
regulation
control
Erosion
Storm protection
Water
purification
treatment
and waste
of human
Regulation
diseases
Detoxification
control
Biological
Cultural
Cultural
and
diversity
B
C
C
A
C
D
A
E
C
D
C
D
E
E
A
E
C
c
C
c
E
A
A
E
A
D
D
C
E
E
E
C
C
D
A
D
D
C
E
E
E
C
C
A
A
A
A
A
A
A
A
A
A
A
A
A
A
E
A
A
A
A
A
A
A
A
A
A
A
A
A
A
NA
C
C
D
E
E
E
C
C
C
C
C
c
A
C
E
NA
A
D
C
C
C
C
C
c
E
E
A
NA
A
E
C
D
identity
Recreation
and
ecotourism
Supporting
Primary production
02 production
Soil formation
and
retention
Pollination
Nutrient
cycling
Provision
of habitat
Notes:
losses of a few species are mostly
for by the remaining
services are those for which
Type A ecosystem
compensated
to species loss, with Type E representing
services that depend primarily on rare
susceptible
species. Types B-E are successively more
or fragile species (see Introduction).
"?" indicates not known.
"NA" indicates not applicable;
diversity have been achieved following intense and
painstaking field studies of a limited number of food
webs (Briand and Cohen 1987, Schoener 1989, Cohen et
al.
These
2003).
general
insights
of
estimates
Our
to
that we
of
services
the
(A), primary
of
Alternatively,
approximate
of
relative
at which
on
declines
this we need explicit
decomposers
auto
(Z>),
(P), and
secondary
of well-studied
food
webs.
estimates
of
the
relative numbers of each of these species (Briand and
Cohen 1984, Cohen 1989, Schoener 1989). Here, we
have
opted
successive
diversity
conclusions
invariance.
to
assume
a
levels. We
trophic
on successive
are
We
robust
then
constant
have
ratio
of
at 4:3.
levels
trophic
to this na?ve assumption
obtain
an
species
set the ratio
estimate
of
of
species
main
Our
of
total
on
scale
species
of
estimate
exhaustively
will
particularly
at
We
the
diversity
ratio-based
an
obtain
the
total
we explicitly acknowledge
need.
consumers
in a variety
(Q
we
can use
consumers
as
breakdown
numbers
number
initial
the thresholds
level. To achieve
of
sufficient
calibrate
coarsely
magnitude
each trophic
trophs
is
step
hierarchical
estimates
us
the parameters
first
ecosystem
a
provide
to provide
studies
for
diversity by summing the totals for each trophic level to
then
services
total
to
provided
number
set
by
of
trophic
the
by
species
(here
"threshold"
as
either
will
We
species
total
diversity,
levels).
decomposers
species.
between
characterized
to underestimate
lowest
need
relationship
be
lead us
the
of
number
that our inability to sample
for
decline
a fraction
assume
and
the
that
function
diversity
an asymptotic
of
of
or
the
can
S-shaped
function and that this function can be characterized by a
level of diversity at which the function operates at 50%
of
its
theoretical
maximum.
For
any
trophic
level,
we
will assume that this threshol4 level of diversity is
determined when the total number of species has been
reduced to some fraction p of their original diversity.
The
fraction
unity (as p ?
trophic
this
level),
could
take
any
value
between
zero
and
0, the services become more brittle at any
we will
set this value
to 0.1,
and
argue
that
the log-normal
reflects
distri
phenomenologically
of species
bution
abundance
within
each
level
trophic
1920
ANDREW DOBSON ET AL.
0.4
Species
Vol.
Ecology,
0.6
8
87, No.
1.0
composition
Fig. 5. Functional
forms for the relationship
loss of biodiversity
between
and loss of function. Each of the curves represents
the
in both number of species at each trophic level and the ecosystem
decline
services undertaken
by species on different
trophic levels
as the total number of species in the community
declines. The lowest line (alternating
is for predators
dots and dashes)
and services
on the top trophic level, the second lowest line is for herbivores,
the dotted
line is for plants, and the solid line is for decomposers.
The threshold
values occur when each trophic
level passes
the value of species composition
that corresponds
to 50% of
through
maximum
for services
efficiency
a major
to
the commonly
than
90% of the
contribution
that
phenomenon
greater
level.
of relative abundance
1975). This distribution
(May
makes
at that trophic
undertaken
observed
ecosystem
functioning is undertaken by less than 10% of the species
(at any trophic level; Tilman et al. 1997, Loreau 1998,
Petchey and Gaston 2002).
can
We
now
set
sequentially
the breakpoints
for
growth changes with increasing population
density
(Maynard Smith and Slatkin 1973, Bellows 1981). This
simple function builds upon the hierarchical thresholds
and
above
developed
and
the upper
more
levels
brittle.
with
Rx
at p X D.
abundance
left
has
in the
assumes
This
so
declined
that
then
community,
only
services
species
are
species
p X D
performed
the
by
lowest trophic level will have declined by 50%. The
(50%) threshold for the next trophic level (autotrophs) is
set for when species diversity is reduced to D + p X A
assumes
This
species.
that
at
processes
the
second
same
as at
constant
proportionality
(although we could readily modify
even more
levels
trophic
we
data
empirical
will
brittle;
maintain
of constant
p). The
assumption
set thresholds
and
for primary
the
lower
level
this to make upper
of more
in the absence
We
level
now
define
ecosystem
to
community.
was
that
the
net
Here
originally
a
function
parsimonious
same
us
logic allows
consumers
secondary
that
relates
are performed
number
of species
a modified
we
use
developed
the
at each
to
strength with which density dependence
by
on
species
species
ecosystem
level
x, S
trophic
in the degraded
surviving
services
are
is the
total
and
habitat,
Tx is the threshold level of diversity calculated above for
x. Note
level
trophic
assumed
that
species
determined
x
parameter
that
are
by
to
we
here
lost
from
we
RT,
characterize
each
use
the
have
intrinsically
level at a
trophic
the
trophic-level
with
steepness
which
services (and species) are lost as diversity declines, and
we
have
set
arbitrarily,
level. The
trophic
this
way
in species
declines
as
function
with
which
a
square
of
this function
and
diversity
ecosystem
rate
Standard
curves
species-area
may
be
to mimic
used
the net loss of biodiversity as habitat is either lost or
declines in quality (Simberloff 1988, Reid 1992). We
at
note
trophic
in the
remaining
of a function
characterize
performed
number
of
at which
at
form
to
RT
rate
the
function at different trophic levels is illustrated in Fig. 5.
our more
services
Here,
is
characterizes
D + A + p X P and D + A + P + p X C, respectively.
which
'<
rate
trophic level will decline at an earlier level of species
loss than that at which the basal level declines. We use
the
(i)
\
set
the net
that when
species
1
=
the threshold (50% efficiency) level for the lowest trophic
level
in which
way
decreasing
each
we
Thus
decline
diversity:
trophic level in a way that will give a hierarchical series
of breakpoints with the lowest trophic levels being most
resilient
a general
describes
services
ecosystem
the
in population
that
X
number,
assumes
brium.
the
=
that
the
A number
species-area
than
function
continental
curves
N
z =
area,
=
cXz
slope,
(where
c =
and
=
N
a
comes
community
rapidly
of studies
that the
have
shown
tends
scales
and
to b?
steeper
on
that
slopes
are
species
constant),
to equili
local
also
slope of
rather
steeper
DETERMINANTS OF BIODIVERSITY CHANGE 1921
August 2006
a more
rate
rapid
lower
those
than
by
provided
at
species
levels.
trophic
It is also possible to use Eq. 1 (and its underlying
trophic thresholds) to calculate food chain length at
different stages of habitat decline (Fig. 6B). This allows
with
comparison
of
studies
marine
freshwater
and
systems where decrease in food chain length in response
to overexploitation is indicative of declines in "ecosys
tem
size
and
an
al.
et
Post
1998,
al.
to a
loss in habitat
leads
of magnitude
only
a
in species
this
number,
represents
to an
structure
in community
equivalent
order
50%
et
(Pauly
quality"
important observation here is that, although
2000). An
reduction
change
average
one
position
of
in the average
level decline
trophic
the species
persisting
in the
trophic
A
community.
second order of magnitude decline in habitat causes the
loss of the top trophic level from the remaining
a
matches
This
community.
exploited marine
causes
overexploitation
Our
positions.
result
in heavily
observed
(Pauly et al.
fisheries
a
decline
in
an
adds
approach
1998), where
average
trophic
important
detail:
trophic collapse would seem to be initiated by first a
thinning of the species throughout the web (which
0.001
0.0001
would
1
0.1
0.01
Proportion of habitat remaining
in abundance
of species from different
(A) Decline
is lost at a constant
levels as habitat
annual rate. The
trophic
solid black
line illustrates
the net loss of species as habitat
lines reflect loss of species and, hence,
declines, while the broken
services from sequentially
lower trophic levels. The
ecosystem
line represents
the alternating
lowest dashed
top consumers,
Fig.
the
produce
in mean
decline
observed
6.
are
to variation
in the slope of the species-area
to significant
in
robust
variations
relatively
of the model:
the two other
ratio
parameters
principal
on
and
of species
levels,
diversity
sequential
trophic
robust
curve
and
at
rates
in
inequality
which
drive
species
the middle dashed line
dotted-dashed
line is primary consumers,
is plants
and the dotted
line is decom
(primary producers),
between
posers
(B) Relationship
(bacteria and soil organisms).
area of habitat remaining
and length of food chain. The dashed
processes (characterized by p). We would
the maximum
possible
length of the food chain in the
the solid line shows the total proportion
of
habitat,
remaining
and the dotted
line illustrates the
original species still persisting,
of the surviving
average
species.
trophic position
by
line shows
see
an
and
initial
a more
rapid
This
services.
for real islands than for habitat islands (Scott et al.
1998).We will assume that loss of diversity on a local
be
may
characterized
a
by
z =
slope
0.33
1967, Connor and McCoy
(MacArthur and Wilson
This
Simberloff
1979,
1992).
slope leads to a 50% decline
in net species diversity for each order of magnitude
decline
area.
in habitat
to normalize
ward
loss
species
level
as
the species
a proportional
be
used
relatively
to
curve
and
express
loss
from
each
trophic
habitat
the
characterize
straightfor-.
area
to proportional
in response
then
It is then
loss
loss.
of
Eq.
1 can
ecosystem
functioning from each trophic level as habitat is either
lost or degrades in quality (Fig. 6). The model illustrates
that
although
the overall
is comparatively
trophic
levels
modest,
are
lost most
loss
of
because
rapidly,
species
species
as area
at
declines
the highest
the economic
goods
and services provided by these species will thus be lost at
implies
are
systems
these
of
of
collapse
sequential
the sequence
that
declines
the relative
Determining
which
services
breakdown
tween
be
may
similar in different
on
different
requires
further
species
thresholds
ecosystem
and that the
and
predictable
of
the
how
(Table
1).
at
thresholds
interactions
be
affect
these
levels
trophic
and
goods
of
ecosystems
position
and
goods
followed
degraded,
service loss is likely to be hierarchical
sequence
ecosystem
thus expect to
in economic
reduction
sequential
as natural
services
potentially
scale
trophic
position), followed by a more rapid shortening of the
food web (the loss of top trophic levels). These results
attention.
urgent
Conclusions
model
The
between
therefore
the upper
diversity
levels are
interactions
such
predators
Terborgh
by
plants
ignored
modified
key
are
ignored
thus
prey
release)
as
levels
ecological
abundance
by
(Terborgh
and maintenance
in this
It will
in abun
important
of
regulation
interaction
levels.
changes
intermediate
at
species
removed,
as
1997&),
framework.
of
soil
We
1988,
structure
have
also
the fact that many habitats are explicitly
to create new habitats that directly supply
to
services
agriculture,
of
no
trophic
compensatory
(meso-predator
et al.
assumes
here
at different
underestimate
and
dance
described
species
but
the
also
human
lands
economy,
for
industry,
particularly
homes,
and
ANDREW
1922
ET AL.
DOBSON
87, No.
Vol.
Ecology,
8
If
services as top predators.
1. Both lions and tigers provide
Plate
They also act as a major draw for ecotourists.
ecosystem
such as these, it is likely that they will also
of top predators
reserves can maintain
and nature
healthy populations
ecosystems
of ecosystem
services at lower trophic
of the many
and populations
contain healthy communities
species that perform a diversity
levels. Photo credit: A. P. Dobson.
recreation. Some models
in
that explicitly explore changes
under
services
ecosystems
are
conversion
habitat
described in Dobson
(Dobson 2005). Similarly, the
model ignores the impact that alien species might have
when they replace and compete with those left in a
degraded community. This will be particularly impor
tant
in agricultural
are
habitat
natural
The
service.
ecological
large portions
into monocultures
that
level)
phototrophic
where
areas,
converted
of
relevance
area
curves
to
rates
estimate
of
the
loss
of
biodiversity
Bevers
2002).
biodiversity
for
local
accurate
Consequently,
of
estimation
loss has to take into account the potential
as
extinctions
not
arrangement,
a
as
just
consequence
a
of
function
of
habitat
net
habitat
remaining. The model framework we have developed
could be adapted to consider all of these processes,
the
to a first approximation,
modifying
although
magnitude of the threshold parameters (/?,-)may most
subtle
readily capture the details of these more
processes.
None
because
of this detracts from our principal conclusion;
services
ecosystem
to be
tend
to
top
we
bottom,
hierarchical
predictable
economic
earthworms,
goods
they become
and
would
and
services
expect
sequential
by
natural
fungi,
crucial
the economically
water
but
as nematodes,
such
species
undertake
and bacteria
many
In contrast,
species.
not
also
food
structure
only
and
the energy
chain
and
by
that
nutrients
and
primary
At
attention.
conservation
buffering
air and
that cleanse
processes
limited
receive
(plants) provide
against
are then
secondary
but
erosion,
up
passed
consumers.
the
The empirical examples and phenomenological model
described above suggest that the ecosystem services
undertaken by species at high trophic levels will
disappear before those undertaken by species at the
bottom of the food chain. While the economic effects of
this loss in services have so far been limited, the loss of
species that benefit by simply serving aesthetic and
(see Plate
services
recreational
as an
1), serves
important
alarm bell for the subsequent loss of services to which
human health and economic welfare are more tightly
because
Ironically,
coupled.
the
volume
of
essential
services provided by species at lower trophic levels is
linearly dependent upon the size (and quality) of habitat
the
remaining,
essential
services
viable
best
way
may
for
be
species
to maximize
to ensure
with
larger
return
that
area
the
on
these
ecosystem
requirements
that have less readily quantified economic value.
under
taken by species at different trophic levels and because
trophic webs will tend first to thin and then collapse
from
these
remains
different
carnivores
top
intermediate trophic levels, autotrophs
(Simberloff 1988, Seabloom et al. 2002). Although
habitat amount is of primary importance in determining
the size and ultimately the persistence of populations,
the spatial arrangement of persisting habitat patches
becomes increasingly more important as habitat is lost
(Flather and Bevers 2002). There is a rapid*decline in
connectivity once 30-50% of habitat is lost, which may
have a significant impact on population dynamics and
interactions between species (Cumming 2002, Flather
and
to conserve
time
the present
such as tigers, wolves, and fish (species that provide a
heightened spiritual and recreational quality to ecosys
tems), there is limited economic incentive to conserve
of
in using species
at
pressure
mites,
pattern
spatial
remains one of the central problems
the
(at
as a major
food
supply
of
activities. This apparently simple, but important, insight
has been overlooked in previous studies of ecosystem
there is significant conservation
functioning. While
to
see
loss of
ecosystems
a
the
as
eroded and degraded by anthropogenic
Acknowledgments
us
for bringing
Assessment
during the production
together and for support and stimulation
we acknowledge
In particular,
of this research.
many
helpful
Prabhu Pingali,
with Walt Reid, Steve Carpenter,
discussions
Mercedes
Jon Paul Rodriguez,
Mark Rosegrant,
Joe Alcamo,
We
Pascual,
thank
the Millennium
and particularly
John Terborgh.
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