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Ecological
Indicators
63
(2016)
249–257
Contents
lists
available
at
ScienceDirect
Ecological
Indicators
j
o
ur
na
l
ho
me
page:
www.elsevier.com/locate/ecolind
Perspectives
on
the
link
between
ecosystem
services
and
biodiversity:
The
assessment
of
the
nursery
function
Camino
Liquete∗,
Núria
Cid,
Denis
Lanzanova,
Bruna
Grizzetti,
Arnaud
Reynaud
European
Commission,
Joint
Research
Centre
(JRC),
Institute
for
Environment
and
Sustainability
(IES)
,
Via
Enrico
Fermi
2749,
21027
Ispra,
VA,
Italy
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
30
July
2015
Received
in
revised
form
17
November
2015
Accepted
29
November
2015
Keywords:
Nursery
habitats
Fisheries
Ecosystem
services
Biodiversity
Conservation
Ecosystem
assessments
a
b
s
t
r
a
c
t
The
relationship
between
biodiversity
and
each
ecosystem
service
or
bundle
of
ecosystem
services
(e.g.
win−win,
win−lose
or
win−neutral)
is
an
active
field
of
research
that
requires
structured
and
consistent
information.
The
application
of
that
research
for
conservation
and
decision-making
can
be
hampered
by
the
ambiguity
found
in
the
definition
of
the
nursery
function
under
the
ecosystem
service
perspective.
In
this
paper,
we
review
how
the
role
of
nursery
habitats
is
included
in
the
ecosystem
services
literature,
covering
conceptual,
biophysical
and
economic
reflections.
The
role
of
ecosystems
as
nurseries
is
mostly
analyzed
in
coastal
environments.
The
main
observation
is
that
there
is
no
consensus
on
the
consideration
of
the
nursery
function
as
a
service
(e.g.
which
species
or
habitats)
or
on
how
to
assess
it
(e.g.
which
indicators
or
valuation
methods).
After
that
review,
we
analyze
three
different
interpretations
given
to
the
nursery
function,
namely
the
ecological,
conservationist
and
economic
point
of
view;
and
we
distinguish
between
different
types
of
assessment
that
may
consider
the
nursery
function.
We
conclude
that
the
nursery
function
can
be
considered
an
ecosystem
service
on
its
own
right
when
it
is
linked
to
a
concrete
human
benefit
and
not
when
it
is
represented
with
indicators
of
general
biodiversity
or
ecosystem
condition.
Thus,
the
analysis
of
the
delivery
of
ecosystem
services
should
be
differentiated
from
the
analysis
of
ecological
integrity.
Only
with
this
distinction
science
may
be
able
to
quantify
the
link
between
biodiversity
and
ecosystem
services
and
policy
may
be
effective
in
halting
biodiversity
loss.
Similar
considerations
could
apply
for
other
biodiversity
constituents
that
may
be
treated
as
ecosystem
services.
©
2015
The
Authors.
Published
by
Elsevier
Ltd.
This
is
an
open
access
article
under
the
CC
BY
license
(http://creativecommons.org/licenses/by/4.0/).
1.
Protecting
biodiversity
through
ecosystem
services
Ecosystem
services
became
a
policy
tool
to
protect
biodiver-
sity
mainly
as
a
result
of
the
global
strategic
plan
2011−2020
of
the
Convention
on
Biological
Diversity
(Aichi
biodiversity
tar-
gets),
before
scientific
consensus
about
the
mutual
relationship
between
ecosystem
services
and
biodiversity
was
well
established.
Still
today,
although
there
are
numerous
evidences
supporting
a
positive
relationship
between
biodiversity,
ecosystem
functions,
and
the
delivery
of
particular
ecosystem
services
(Egoh
et
al.,
2009,
Cardinale,
2011,
Isbell
et
al.,
2011,
Mace
et
al.,
2012,
Harrison
et
al.,
2014),
there
is
not
much
consensus
on
what
the
links
are
and
how
they
operate
(Loreau
et
al.,
2001,
Harrison
et
al.,
2014).
Ecosystem
services
have,
by
definition,
an
anthropocentric
focus.
They
are
the
direct
or
indirect
contributions
from
ecosystems
to
human
welfare.
To
consider
something
as
an
ecosystem
service,
∗Corresponding
author.
E-mail
address:
camino.liquete@gmail.com
(C.
Liquete).
this
must
have
human
demand
or
identified
beneficiaries
(Haines-
Young
&
Potschin,
2013).
Nevertheless,
it
does
not
mean
that
ecosystem
services
promote
a
utilitarian
view
of
nature;
they
rather
aim
at
highlighting
the
processes
and
outputs
from
ecosystems
that
contribute
to
human
well-being
and
that
are
usually
over-
looked,
especially
in
sectors
not
related
with
nature
conservation
or
in
areas
where
nature
protection
is
not
the
first
priority.
Biological
diversity
at
species
and
population
levels
is
closely
linked
to
ecosystem
functioning
and
it
is
assumed
to
positively
influence
the
provision
of
particular
ecosystem
services
across
scales
(Naeem
et
al.,
1995,
Worm
et
al.,
2006,
Cardinale
et
al.,
2012).
At
the
same
time,
biodiversity
and
ecosystem
functioning
are
influenced
by
interactions
between
individuals
or
species
(see
Gray
et
al.,
2014
and
references
therein),
which
directly
rely
on
habitat
availability
and
condition.
For
example,
the
ecosystem
ser-
vices
that
improve
water
quality
(i.e.
water
purification)
and
flow
regulation
(i.e.
flood
protection)
are
enhanced
by
increases
in
com-
munity
and
habitat
area
(Harrison
et
al.,
2014).
Biodiversity
is
also
alleged
to
stabilize
the
delivery
of
ecosystem
services
through
time
(Tilman,
1996,
Chapin
et
al.,
2000,
Hooper
et
al.,
2005,
Schindler
http://dx.doi.org/10.1016/j.ecolind.2015.11.058
1470-160X/©
2015
The
Authors.
Published
by
Elsevier
Ltd.
This
is
an
open
access
article
under
the
CC
BY
license
(http://creativecommons.org/licenses/by/4.0/).
250
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
et
al.,
2010)
and
this
is
even
more
demanded
in
ecosystems
that
are
expected
to
provide
multiple
functions
(Hector
&
Bagchi,
2007).
Consequently,
there
is
a
big
concern
about
the
effects
of
biodiversity
loss,
not
only
for
the
ecosystems,
but
also
for
human
well-being
and
livelihood
(Hoekstra
et
al.,
2005,
Duffy,
2009,
Schindler
et
al.,
2010,
Treml
et
al.,
2015).
In
this
context
where
biodiversity
is
being
linked
to
human
well-being,
several
initiatives
promote
the
ecosystem
service
approach
(e.g.
MA,
2005,
UNEP,
2007,
TEEB,
2010,
IPBES
in
Díaz
et
al.,
2015),
which
aims
at
integrating
both
natural
and
social
systems
providing
a
more
comprehensive
approach
for
decision-
making.
A
major
challenge
to
apply
the
concepts
of
ecosystem
services
in
management
and
decision-making
is
to
have
clear
assessment
frameworks
that
allow
measuring
each
service
and
linking
them
to
human
well-being.
During
our
involvement
in
some
initiatives
that
try
to
operationalize
ecosystem
services
(e.g.
MAES,
2014,
OpenNESS,
2014,
MARS,
2015),
several
conceptual
discrepancies
and
empirical
challenges
have
arisen
when
trying
to
quantify
par-
ticular
ecosystem
services.
One
of
the
most
controversial
services
is
the
so-called
“maintenance
of
nursery
populations
and
habitats”
in
the
Common
International
Classification
of
Ecosystem
Services
(CICES,
2015)
or
“habitats
for
species”
in
The
Economics
of
Ecosys-
tems
and
Biodiversity
(TEEB)
(see
Appendix).
The
main
reasons
behind
are
that,
on
the
one
hand,
this
ecosystem
service
could
be
interlinked
or
correlated
with
other
services
that
directly
rely
on
it
(e.g.
fisheries)
and,
on
the
other
hand,
it
refers
to
biodiversity
components
and
ecosystem
functions
(i.e.
nursery
function).
In
this
context,
our
main
questions
were:
Can
the
nursery
function
be
con-
sidered
an
ecosystem
service?
If
so,
how
should
it
be
adequately
assessed?
What
are
the
different
options?
This
paper
presents,
first,
a
short
review
of
existing
approaches
that
analyze
the
nursery
function
as
an
ecosystem
service
(Section
2);
then,
a
critical
analysis
of
these
approaches
discussing
differ-
ent
perspectives
in
considering
biodiversity
components
(Section
3);
and
finally
a
proposal
of
specific
options
to
tackle
the
nursery
function
in
ecosystem
service
assessments
(Section
4).The
analysis
is
especially
important
when
aiming
to
assess
the
links
between
biodiversity
and
the
delivery
of
ecosystem
services.
2.
Nursery
habitats
and
the
ecosystem
service
approach
2.1.
Definitions
and
classifications
A
nursery
can
be
defined
as
a
habitat
that
contributes
more
than
the
average,
compared
with
other
habitats,
to
the
production
of
individuals
of
a
particular
species
that
recruit
to
adult
populations
(Beck
et
al.,
2001).
The
main
factors
that
facilitate
the
reproduc-
tion
and
recruitment
are
density,
growth
and
survival
of
juveniles,
movement
to
adult
habitats,
or
a
combination
of
those
(Beck
et
al.,
2001).
In
this
sense,
experimental
studies
have
demonstrated
how
the
nursery
function
(i.e.
the
production
of
individuals
that
recruit
to
adult
populations
per
unit
area
of
juvenile
habitat
sensu
Beck
et
al.,
2001)
decreased
with
nursery
habitat
loss
(Cheminée
et
al.,
2013).
In
an
ecosystem
service
context,
it
is
unclear
whether
the
nurs-
ery
habitats
and
function
could
be
regarded
as
a
distinct
ecosystem
service
or
as
a
biodiversity
component.
For
example,
The
Economics
of
Ecosystems
&
Biodiversity
foundations
(TEEB,
2010)
proposed
“maintenance
of
life
cycles
of
migratory
species”
as
an
ecosystem
service,
postulating
that
when
the
migratory
species
have
commer-
cial
value
and
reproduce
in
a
certain
habitat,
that
nursery
function
should
be
valued
by
itself
(e.g.
mangroves
used
as
spawning
and
nursery
areas
of
fish
and
crustaceans
harvested
far
away)
(Table
1).
Still,
both
TEEB
(2010)
and
MA
(2005)
state
that
the
so-called
habitat
or
supporting
services
(such
as
“habitats
for
species”
or
“photosynthesis”,
see
Appendix)
are
necessary
for
the
production
of
most
of
the
other
ecosystem
services
and,
thus,
have
only
indi-
rect
impacts
on
people.
Similarly,
even
if
not
so
explicit,
the
CICES
description
of
the
“lifecycle
maintenance,
habitat
and
gene
pool
protection”
class
(which
includes
pollination
and
the
maintenance
of
nursery
populations
and
habitats,
see
Appendix)
seems
to
be
restricted
to
the
reproduction
and
nursery
functions
that
support
provisioning
services
(e.g.
pollination
as
a
support
to
commercial
crops)
(Haines-Young
&
Potschin,
2013).
Within
this
classifica-
tion,
the
“maintenance
of
nursery
populations
and
habitats”
is
an
independent
service
defined
as
habitats
for
plant
and
animal
nursery
and
reproduction.
In
contrast,
the
UK
National
Ecosystem
Assessment
Follow-on
(Turner
et
al.,
2014)
states
that
the
nursery
function
is
already
valued
through
the
fish
that
is
caught
and
sold
on
markets
(i.e.
through
its
contribution
to
fisheries)
and,
thus,
it
is
not
included
in
the
list
of
final
ecosystem
services.
Instead,
it
is
split
between
two
intermediate
services
named
“larval
and
gamete
supply”
and
“formation
of
species
habitat”.
Other
authors
include
the
maintenance
of
all
vegetal
and
animal
populations
as
well
as
their
resilience
among
regulating
or
suppor-
ting
services
(Beaumont
et
al.,
2007,
Rönnbäck
et
al.,
2007)
which
is
difficult
to
detach
from
biodiversity
or
ecological
integrity.
In
other
cases,
the
definition
of
nurseries
as
ecosystem
service
remains
ambiguous
and
can
be
used
with
different
connotations.
For
exam-
ple,
the
service
habitat/refugia
analyzed
by
Costanza
et
al.
(1997)
included
nursery
areas
for
commercial
species
as
well
as
resting
areas
for
migratory
species.
It
was
valued
with
fish/shrimp
market
prices,
endangered
species
conservation
value
and
general
conser-
vation
value.
In
Salomidi
et
al.
(2012)
the
service
“reproduction
&
nursery
areas”
seems
to
cover
by
definition
all
marine
species
(i.e.
the
viability
of
populations),
but
the
examples
are
mostly
linked
to
commercial
species.
Some
other
names
referring
to
the
nursery
function
as
an
ecosystem
service
in
the
literature
are:
breeding
and
feeding
ground,
nursery
habitat,
habitat
provision,
refuge
or
shelter
(see
Table
S2
in
Liquete
et
al.,
2013).
Given
this
variety
of
opinions
about
how
the
nursery
function
should
be
defined
and
classified
in
an
ecosystem
services’
context,
we
propose
to
follow
a
simplified
representation
of
the
ecosys-
tem
services’
cascade
framework
(derived
from
Haines-Young
&
Potschin,
2010)
(Fig.
1).
More
complete
schemes
have
been
devel-
oped,
for
instance,
in
international
initiatives
such
as
Müller
et
al.
(2010),
TEEB
(2010)
or
Maes
et
al.
(2013)
or
other
proposals
such
as
Villamagna
et
al.
(2013).
Applying
this
kind
of
conceptual
frame-
work
clarifies
which
compartment
of
the
socio-ecological
systems
is
being
analyzed
and
what
is
missing
to
fully
characterized,
for
instance,
one
ecosystem
service.
In
Fig.
1,
ecosystem
functions
and
processes
comprise
all
the
biophysical
roles
that
sustain
the
pro-
vision
of
a
specific
ecosystem
service,
thus
indicating
the
natural
capacity
to
provide
that
service.
Ecosystem
services
(also
noted
as
ecosystem
service
flows)
are
the
actual
contribution
of
ecosys-
tem
components
(as
goods
or
services)
to
human
well-being.
The
benefits
and
values
designate
the
perception
or
valuation
that
human-beings
attribute
to
a
specific
service.
The
management
and
social
responses
reflect
how
the
political
and
personal
decisions
act
as
drivers
of
change
of
the
environment,
affecting
the
ecosystems’
condition.
Biodiversity
is
the
variety
of
life,
including
variation
among
genes,
species,
ecosystems
and
habitats.
To
move
from
this
conceptual
framework
to
real-world
assess-
ments
researchers
generally
use
indicators
or
proxies.
Indicators
are
variables
that
provide
aggregated
information
on
certain
phenomena,
acting
as
communication
tools
that
facilitate
a
sim-
plification
of
complex
processes
(Müller
&
Burkhard,
2012).
Proxies
are
here
assumed
to
be
approximations
of
ecosystem
services’
indi-
cators
when
the
entire
phenomena
cannot
be
quantified;
a
proxy
is
thus
a
figure
that
can
represent
the
value
of
an
ecosystem
service
indicator.
Depending
on
the
objective
of
each
case
study,
the
prox-
ies
or
indicators
may
refer
to
ecosystem
functions
and
processes,
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
251
Table
1
Summary
of
definitions
and
interpretations
aiming
to
classify
the
nursery
function
as
an
ecosystem
service.
Ecosystem
service
Service
category
Definition
Application
Reference
Habitats
for
species
Habitat
or
supporting
service
Habitats
provide
everything
that
an
individual
plant
or
animal
needs
to
survive:
food;
water;
and
shelter.
Each
ecosystem
provides
different
habitats
that
can
be
essential
for
a
species’
lifecycle.
Migratory
species
including
birds,
fish,
mammals
and
insects
all
depend
upon
different
ecosystems
during
their
movements.
It
seems
to
cover
all
habitat
function
for
all
species
TEEB
(2015)
Maintenance
of
nursery
populations
and
habitats
Regulation
and
maintenance
service
Habitats
for
plant
and
animal
nursery
and
reproduction
Reproduction
and
nursery
functions
that
support
provisioning
services
CICES
(2015)
Larval
and
gamete
supply/Formation
of
species
habitat
Supporting
intermediate
services
For
instance,
the
quantity
of
larvae
&
gametes
supplied
to
a
particular
location/For
instance,
change
in
area
or
quality
of
habitat
The
nursery
function
is
already
valued
through
the
fish
provision
Turner
et
al.
(2014),
UK
NEA
Follow-on
Life
cycle
maintenance
Regulating
and
maintenance
services
Biological
and
physical
support
to
facilitate
the
healthy
and
diverse
reproduction
of
species
The
maintenance
of
key
habitats
that
act
as
nurseries,
spawning
areas
or
migratory
routes
for
all
species
Liquete
et
al.
(2013)
Reproduction
and
nursery
areas
The
provision
of
the
appropriate
environmental
conditions
for
reproduction
and
growing
during
the
early
stages
of
marine
species.
The
definition
seems
to
coverall
marine
species,
but
the
examples
are
mostly
linked
to
commercial
species
Salomidi
et
al.
(2012)
Maintenance
of
life
cycles
of
migratory
species
Habitat
or
supporting
service
Habitats
that
sustain
migratory
species
with
commercial
value
The
focus
is
on
temporal
habitats
and
commercial
species
TEEB
(2010)
Biologically
mediated
habitat
Support
services
Habitat
which
is
provided
by
living
marine
organisms
It
refers
to
“essential
breeding
and
nursery
space
for
plants
and
animals
[.
.
.]
commercial
and/or
subsistence
species”
Beaumont
et
al.
(2007)
Maintenance
of
plant,
algal
and
animal
populations
Regulating
services
Reproduction
It
refers
to
the
maintenance
of
all
vegetal
and
animal
populations
Rönnbäck
et
al.
(2007)
Refugia/habitat
Habitat
for
resident
and
transient
populations
Nursery
areas
for
commercial
species
as
well
as
resting
areas
for
migratory
species.
Costanza
et
al.
(1997)
the
actual
flow
of
ecosystem
services,
or
the
human
benefit
or
value.
Thus,
selecting
adequate
indicators
to
measure
each
ecosystem
service
is
a
crucial
step
of
any
ecosystem
service
assessment.
2.2.
Assessments
of
nursery
habitats
After
the
overview
of
the
conceptual
approaches
in
Section
2.1,
sections
2.2
and
2.3
review
the
practical
assessments
about
the
nursery
function
and
nurseries
and
ecosystem
services
found
in
the
literature.
The
majority
of
the
articles
that
analyze
the
nursery
function
deals
with
the
role
that
coastal
environments
play
for
the
main-
tenance
of
prosperous
fisheries.
These
assessments
explore
and
quantify
the
role
of
habitats
such
as
salt
marshes
(Boesch
and
Turner,
1984),
mangroves
(Mumby
et
al.,
2004,
Aburto-Oropeza
et
al.,
2008,
Zavalloni
et
al.,
2014),
macroalgae
and
seagrasses
(Cheminée
et
al.,
2013,
Blandon
and
zu
Ermgassen,
2014,
Tuya
et
al.,
2014),
maerl
(Kamenos
et
al.,
2004)
or
their
combinations
(Meynecke
et
al.,
2008,
McMahon
et
al.,
2012)
for
protecting
larvae
and
juveniles,
especially
of
fish
and
shrimp
populations.
The
main
reasons
for
the
loss
of
this
ecological
function
are
the
disruption
of
Fig.
1.
General
diagram
of
the
concepts
linking
natural
and
social
systems
through
ecosystem
services.
See
the
definitions
of
the
five
boxes
in
Section
2.1.
252
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
connectivity
between
spawning,
nursery
and
adult-stage
habitats
(McMahon
et
al.,
2012,
Lee
et
al.,
2014)
and
the
rapid
destruction
of
essential
habitats
due
to
anthropogenic
disturbances
like
land
use
change
or
intensive
exploitation
(Mangialajo
et
al.,
2008,
Walters
et
al.,
2008,
Zavalloni
et
al.,
2014).
Generally
without
establishing
links
to
specific
species,
some
studies
on
terrestrial
ecosystems
highlight
the
importance
of
maintaining
habitats’
diversity
(either
for
their
nursery
or
shelter
functions)
for
agricultural
production
(Firbank
et
al.,
2008,
Cong
et
al.,
2014).
Others
focus
on
the
importance
of
maintaining
habitats
and
populations
for
recreational
purposes
like
recreational
fish-
eries,
diving
or
other
activities
related
with
ecotourism
(Rees
et
al.,
2010).
The
problem
arises
when
trying
to
quantify
nursery
as
an
ecosystem
service
with
the
help
of
appropriate
indicators
or
prox-
ies.
Most
of
the
examples
found
in
the
literature
link
the
nursery
function
of
certain
habitats
with
the
delivery
of
food
provision
or
recreation
(Table
2),
either
quantifying
nurseries
independently
or
as
a
supporting
service.
In
contrast,
other
publications
consider
the
nursery
function
as
a
service
but
they
suggest
using
the
same
indicators
as
for
biodiversity
or
ecosystem
condition
(see
Fig.
1).
For
instance,
Maes
et
al.
(2014)
compiles
a
series
of
indicators
to
measure
ecosystem
services
under
the
EU
Biodiversity
Strategy.
They
propose
to
quantify
the
“maintenance
of
nursery
popula-
tions
and
habitats”
with
proxies
such
as
conservation
investments,
habitat−landscape
protection,
biodiversity
value,
ecological
status
or
habitats
diversity
that
can
be
considered
as
indicators
of
ecosys-
tem
condition
(Table
2).
This
may
hamper
the
analyses
that
try
to
assess
the
relationships
between
biodiversity,
ecosystem
functions,
and
the
delivery
of
particular
ecosystem
services;
as
introduced
in
Section
1.
The
same
authors,
though,
acknowledge
that
these
indicators
can
be
surrogates
of
ecosystem
services
(Maes
et
al.,
2016).
The
proxies
of
ecosystem
service
capacity
(i.e.
ecosystem
func-
tions
and
processes)
usually
relate
to
the
condition
of
the
nursery
habitats
(extent,
density,
etc.)
or
to
the
diversity
found
on
them,
without
necessarily
focusing
on
species
with
direct
human
inter-
est.
The
majority
of
proxies
of
ecosystem
service
flow
propose
measuring
the
presence
or
increase
of
juveniles
with
commer-
cial
or
recreational
interest
within
nursery
habitats;
while
a
few
proxies
require
the
comparison
of
fish
production
with
other
char-
acteristics
of
the
nursery
habitats
(e.g.
Aburto-Oropeza
et
al.,
2008,
Meynecke
et
al.,
2008).
Most
of
the
proxies
of
benefits
and
value
try
to
estimate
the
proportion
of
commercial
fisheries
that
depends
on
the
existence
and
functioning
of
a
certain
nursery
habitat.
The
input
for
recreational
fishing
is
less
studied
but
can
be
estimated
in
a
similar
way.
Only
a
few
proxies
involve
the
opinion
of
local
residents
or
users.
The
methodologies
used
to
estimate
the
bene-
fits
and
values
have
a
great
variety,
which
is
dealt
with
in
the
next
section.
It
must
be
noticed
that
the
classification
of
indicators
in
Table
2
Examples
of
indicators
and
proxies
related
to
the
nursery
function
extracted
from
peer-reviewed
literature.
We
organized
and
reclassified
those
indicators
and
proxies
following
the
framework
proposed
in
Fig.
1.
Sources: 1Aburto-Oropeza
et
al.,
2008,2Barbier
et
al.,
2002,3Blandon
and
zu
Ermgassen,
2014,4Cheminée
et
al.,
2013,5Jackson
et
al.,
2015,6Kamenos
et
al.,
2004,7Knowler
et
al.,
2003,8Maes
et
al.,
2014,9Meynecke
et
al.,
2008,10Mumby
et
al.,
2004,11Stone
et
al.,
2008,12Tuya
et
al.,
2014,13Zavalloni
et
al.,
2014.
Biodiversity
and
ecosystem
condition
Ecosystem
functions
and
processes
Ecosystem
service
flow
Benefits
and
values
•
Biodiversity
value
(species
diversity
or
abundance,
endemics
or
red
list
species)8
•
Oxygen
concentration
(%)8
•
Turbidity
(%)8
•
Ecological
status
(high
to
bad)8
•
Hydromorphological
status
(high,
good,
other)8
•
Habitat
nursery
function
(spp/habitat)4
•
Canopy
height
(cm)4
•
Canopy
cover
(%)4
•
Residence
time
in
seagrass
at
each
life
stage
of
the
fishery
species
(yr)5
•
Spawning
and
nursery
areas
(ha)8
•
Submerged
and
intertidal
habitats
diversity8
•
Species
distribution
and
abundance8
•
Extent
of
marine
protected
areas
(ha)8
•
Mangroves
extent
(km
of
coast)10
•
Size
distribution
of
reef
fish
in
different
habitats
(%
indiv/size
class)10
•
Wild
shrimp
density
at
high
tide
(indiv/m2)13
•
Relationship
between
fisheries
landings
(t/yr)
and
mangroves
edge
length
(km)1
•
Carrying
capacity
of
mangroves
(production)
depending
on
changes
in
area
and
market
prices
(demand)2
•
Enhancement
of
juvenile
fish
by
seagrass
habitats
(indiv/m2)3
•
Annual
production
of
each
fish
species
attributable
to
seagrass
(g/m2)3
•
Density
of
reef
fish
juveniles
with
commercial
or
recreational
interest
in
Cystoseira
forests
(indiv/m2)4
•
Juvenile
gadoids
associated
with
maerl
and
other
habitats
(indiv/m3)6
•
Change
in
recruitment
of
adults
(%)7
•
Catch-per-unit-effort
(kg/day)
distribution
against
wetland
connectivity
index
(%)9
•
Catch-per-unit-effort
(kg/day)
distribution
against
wetland
patch
density
(ha)9
•
Structure
of
reef
fish
communities
(multidimensional
scaling
ordination)10
•
Biomass
of
reef
fish
in
mangrove-rich
systems
(kg/km2)10
•
Biomass
of
commercial
fish
in
seagrass
meadows
(kg/ha)12
•
Annual
value
of
the
services
provided
to
the
fishery
(USD/km
of
mangrove)1
•
Economic
production
along
the
productive
mangrove
fringe
(USD/ha/yr)1
•
Marginal
value
of
a
change
in
mangrove
area
(USD/ha)2
•
Estimated
welfare
losses
associated
with
an
annual
mangrove
deforestation
(USD)2
•
Annual
economic
enhancement
of
commercial
fish
by
seagrass
(kg/m2,
AUD/ha)3
•
Commercial
fishery
landings
linked
to
seagrass-associated
species
(EUR/yr,
%)5
•
Expenditure
of
recreational
fishers
pursuing
seagrass-associated
species
(EUR/yr,
%)5
•
Benefit
of
protecting
fish
habitat
testing
changes
in
habitat
quality
(CAD/ha,
CAD/km)7
•
Increase
of
fish
biomass
from
mangrove-scarce
to
mangrove-rich
systems
(%)10
•
Willingness
to
participate
in
mangrove
reforestation
project
for
the
nursery
benefits
(%)11
•
Willingness-to-pay
for
mangrove
reforestation
project
(Rs/yr)11
•
Value
of
commercial
fish
in
seagrass
meadows
(EUR/ha)12
•
Benefits
from
cultivated
shrimp
over
benefits
from
wild
shrimp
(%)13
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
253
Table
2
has
been
done
for
this
paper.
Most
of
the
publications
pro-
pose
individual
measures
and
figures
of
the
‘nursery
function’
or
the
‘maintenance
of
nursery
populations
and
habitats’
service
that
can
be
as
different
in
magnitude
and
interpretation
as
those
shown
in
Table
2.
2.3.
Economic
methods
and
challenges
The
economic
benefits
derived
from
the
nursery
function
con-
stitute
a
typical
example
of
indirect
use
values
that
is
an
example
of
benefits
derived
from
functional
services
that
support
current
production
and
consumption
(Barbier,
2007).
As
a
result,
the
bene-
fits
from
the
nursery
function
reflect
their
support
or
protection
for
all
activities
that
have
a
direct
measurable
effect
on
human
well-being.
Following
this
view,
the
economic
benefits
of
the
nurs-
ery
function
of
coastal
wetlands
should
be,
for
instance,
estimated
by
valuing
the
additional
benefits
for
commercial
and
recreational
fisheries.
In
the
context
of
ecosystem
service
valuation,
a
variety
of
methods
are
applied
to
estimate
the
economic
value
of
the
nursery
function
related
to
the
enhancement
of
fisheries.
They
include
surrogate
market
price
(Curtis,
2004),
specific
integrated
approaches
linking
biologic
with
economic
models
(Knowler
et
al.,
2003,
Zavalloni
et
al.,
2014),
production
functions
(Barbier
et
al.,
2002,
Johnston
et
al.,
2002,
McArthur
and
Boland,
2006,
Barbier,
2007),
contingent
or
conjoint
valuation
(Nunes
et
al.,
2004,
Stone
et
al.,
2008),
value
transfer
of
willingness
to
pay
(Luisetti
et
al.,
2014),
or
direct
monetary
assessment
of
coastal
fisheries
through
the
transformation
of
fish
abundance
into
financial
value
using
standard
market-prices
with
quantitative
estimates
of
juvenile
fishes
(Aburto-Oropeza
et
al.,
2008,
Blandon
and
zu
Ermgassen,
2014,
Tuya
et
al.,
2014,
Jackson
et
al.,
2015).
The
choice
of
the
appropriate
valuation
method
is
very
much
debated
in
the
economic
literature.
For
instance,
one
limita-
tion
when
combining
market
values
with
surface
or
juvenile
counts
is
that
usually
neither
price
effects
(i.e.
changes
in
mar-
ket
price
in
response
to
fish
abundance)
nor
exploitation
effects
(i.e.
changes
in
exploitation
intensity
in
response
to
fish
abun-
dance)
are
accounted
for.
As
a
result,
Knowler
et
al.
(2003)
argue
that
valuation
should
be
based
on
a
bio-economic
model
link-
ing
nursery
and
habitat
quality
to
some
welfare
measures.
In
addition,
since
the
nursery
function
enhances
the
productivity
of
economic
activities
or
protects
them
from
possible
damages,
Barbier
(2007)
suggests
that
an
appropriate
valuation
method
is
a
production
function
in
which
nursery
is
considered
a
production
input.
Moving
away
from
fisheries,
a
few
studies
assessed
the
eco-
nomic
contribution
of
the
nursery
function
to
the
production
of
insects
for
commercial
purposes
inland,
in
dry
environments
(Rodriguez
et
al.,
2006).
When
the
availability
of
the
nursery
func-
tion
depends
on
the
state
of
the
habitat,
its
value
can
be
estimated
applying
the
replacement
cost
method
(Rodriguez
et
al.,
2006).
Also,
in
the
cases
where
certain
species
have
a
recreational
value,
some
authors
assess
the
nursery
function
with
conventional
stated
preference
methods
such
as
choice
experiment
(Cerda
et
al.,
2013)
or
revealed
preferences
approaches
such
as
travel
cost
(Gürlük
&
Rehber,
2008).
3.
Different
perspectives
-
from
ecology
to
economy
In
our
review
of
the
studies
that
analyze
nursery
habitats
in
ecosystem
service
assessments,
we
identified
some
back-
ground
arguments
or
perspectives
shared
by
different
articles.
We
observed
that
these
background
perspectives
mainly
deter-
mine
which
components
of
natural
and
social
systems
shown
in
Fig.
1
are
evaluated
and
which
method
is
used
for
the
assessment.
Hence,
based
on
our
interpretation
of
the
literature,
we
summarize
below
three
main
perspectives,
not
necessarily
independent
from
each
other,
that
we
have
named
ecologi-
cal,
conservationist
and
economical
perspectives.
The
naming
of
these
perspectives
tries
to
be
illustrative
for
the
readers
and
by
no
means
tries
to
define
the
corresponding
scientific
disciplines.
1.
The
ecological
point
of
view:
Species
populations,
community
composition
and
habitats
are
within
the
most
relevant
biodi-
versity
constituents.
Measurements
of
species
populations
(e.g.
abundance
and
distribution)
and
ecosystem
structure
(e.g.
habi-
tat
structure)
are
considered
key
biodiversity
variables
that
can
be
applied
across
taxa
and
across
terrestrial,
freshwater
and
marine
realms
(Pereira
et
al.,
2013).
The
ecological
point
of
view
aims
at
assessing
ecosystem
condition
using
biodi-
versity
constituents
as
indicators
(e.g.
variety
or
presence
of
certain
habitats,
ecological
status).
The
main
issue
is
to
differ-
entiate
between
biodiversity,
as
the
underpinning
characteristic
supporting
most
ecosystem
services,
and
the
outcome
of
a
spe-
cific
service,
which
has
to
be
measured
with
other
metrics
(e.g.
residence
time
of
fish
in
seagrass,
density
of
gadoid
juve-
niles).
Hence
in
practical
assessments,
this
perspective
focuses
on
the
compartments
‘biodiversity
and
ecosystem
condition’,
‘ecosystem
functions
and
processes’
and
sometimes
on
‘ecosys-
tem
service
flow’
of
Fig.
1.
When
it
covers
‘management
and
social
responses’
it
concentrates
on
the
impacts
that
ecologi-
cal
systems
receive
from
natural
or
human-induced
pressures.
In
this
context,
the
“maintenance
of
nursery
populations
and
habitats”
cannot
be
assessed
as
a
stand-alone
ecosystem
service
as
long
as
it
is
not
differentiated
from
biodiversity
and
ecosystem
condition.
Otherwise
the
ecosystem
service
to
be
assed
would
be
for
instance
fisheries
underpinned
by
nursery
habitats.
2.
The
conservationist
point
of
view:
Ecosystem
services
can
be
a
powerful
tool
to
preserve
biodiversity
and
natural
condition,
and
to
engage
multiple
actors
and
sectors
in
this
objective
(e.g.
Maes
et
al.,
2013).
However,
many
stakeholders,
practition-
ers
and
end-users
of
ecosystem
service
assessments
primarily
measure
provisioning
goods
(e.g.
fish)
or
human
experiences
in
nature
(e.g.
recreation)
and
thereby
dismiss
the
indirect
contri-
bution
of
habitats
and
species
to
human
well-being
(e.g.
nursery)
(Villamagna
et
al.,
2013).
The
conservationist
point
of
view
has
the
objective
of
halting
biodiversity
loss
and
preserving
nature,
in
front
of
natural
resources
exploitation,
using
the
arguments
of
ecosystem
services
across
sectors
and
disciplines.
The
risk
of
this
perspective
is
to
assess
the
nursery
function
using
biodi-
versity
constituents
as
indicators,
especially
when
specific
data
about
the
ecological
processes
(ecosystem
service
capacity)
are
not
available.
The
conservationist
point
of
view
may
address
all
the
components
of
Fig.
1
but
it
gives
a
special
emphasis
to
‘biodiversity
and
ecosystem
condition’
and
‘management
and
social
responses’.
From
this
perspective,
the
“maintenance
of
nursery
populations
and
habitats”
should
be
included
in
the
list
of
ecosystem
services
to
make
its
contribution
to
well-being
explicit,
even
if
some
of
its
indicators
may
refer
to
ecosystem
condition.
3.
The
economic
point
of
view:
The
concept
of
ecosystem
services
represents
the
flows
of
value
from
natural
capital
to
human
soci-
eties
(TEEB,
2010).
We
must
give
these
flows
adequate
attention
and
weight
in
the
decision-making
process,
otherwise
human
welfare
will
deteriorate
(Costanza
et
al.,
1997).
The
economic
point
of
view
pursues
assigning
values
to
ecosystem
services
through
the
benefits
that
have
a
direct
effect
on
human
well-
being
rather
than
through
the
services
themselves.
The
main
254
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
issue
is
that
only
provisioning
and
a
few
cultural
services
have
explicit
prices
or
are
traded
in
markets,
while
other
ecosystem
benefits,
especially
regulating
services,
remain
largely
invisi-
ble
because
they
cannot
be
very
precisely
estimated
with
the
available
monetary
methods.
In
terms
of
assessments,
the
eco-
nomic
perspective
focuses
on
the
‘benefit
and
value’
component
of
Fig.
1
and
sometimes
on
‘ecosystem
service
flow’.
“Mainte-
nance
of
nursery
populations
and
habitats”
is
a
combination
of
ecological
phenomena
supporting
the
delivery
of
other
provi-
sioning
or
cultural
services
(e.g.
food
or
recreation),
from
which
humans
obtain
benefits.
Still,
in
some
economic
assessments,
the
nursery
function
is
considered
as
an
ecosystem
service
that
is
linked
to
the
value
humans
give
to
the
presence
of
wildlife,
either
for
direct
use
(e.g.
diving)
or
non-use
(e.g.
bequest
or
existence
value).
Under
the
economic
point
of
view,
including
nurseries
among
other
ecosystem
services
to
be
valued
could
lead
to
dou-
ble
counting
with
the
assessment
of
other
ecosystem
services
or
with
the
assessment
of
biodiversity
itself.
Therefore,
“main-
tenance
of
nursery
populations
and
habitats”
should
preferably
not
be
considered
as
a
service.
4.
Options
and
recommendations
to
assess
the
nursery
function
In
this
section,
we
describe
the
options
that
ecosystem
service
practitioners
may
face
to
assess
the
nursery
function,
we
high-
light
the
main
risk
of
each
option,
and
we
propose
our
preferred
choice.
Finally,
we
discuss
some
lessons
learnt
from
this
paper
that
go
beyond
the
nursery
function.
1.
The
first
option
is
excluding
the
nursery
function
from
the
list
of
ecosystem
services
assuming
that
it
is
already
quantified
through
food
provision,
recreation
or
other
services.
The
rea-
son
behind
this
choice
is
because
assessing
“maintenance
of
nursery
populations
and
habitats”
may
lead
to
double-counting
or
may
overlap
with
general
analyses
of
biodiversity.
How-
ever,
the
risk
of
this
option
is
to
ignore
the
natural
capacity
to
deliver
food
provision
or
recreation,
where
the
nursery
function
may
play
a
key
role
and,
thus,
promote
unsustainable
manage-
ment
if
an
analysis
of
ecosystem
condition
is
not
performed
in
parallel.
For
instance,
when
the
estimation
of
fisheries
Maxi-
mum
Sustainable
Yield
ignores
the
effect
of
nursery
grounds,
it
may
lead
to
fisheries
collapse.
Even
in
relatively
complete
assessments
(e.g.
fish
stocks
assessments),
it
is
difficult
that
an
analysis
of
fisheries
captures
the
relevance
and
value
of
the
nursery
function
if
this
is
not
an
explicit
objective
of
the
study.
2.
The
second
option
is
to
include
“maintenance
of
nursery
popu-
lations
and
habitats”
among
the
ecosystem
services
but
in
practice
use
a
surrogate
assessment,
i.e.
a
substitute
measure
for
the
service
that
usually
comes
from
general
biodiversity
or
ecological
integrity
analyses.
This
choice
is
understandable
under
certain
circumstances
like
the
lack
of
adequate
resources,
data
or
time
for
conducting
full
integrated
assessments.
Typ-
ical
examples
are
local
assessments
based
on
remote
sensing
in
developing
countries
(Liquete
et
al.,
2016)
.
The
main
risk
of
this
option
is
to
create
confusion
between
the
components
‘bio-
diversity
and
ecosystem
condition’,
‘ecosystem
functions
and
processes’
and
‘ecosystem
service
flow’
in
Fig.
1.
This
confu-
sion
will
hide
the
effects
of
biodiversity
on
ecosystem
services
delivery.
In
this
situation,
it
is
advised
to
differentiate
the
biodiversity-related
information
from
the
ecosystem
services
quantification,
and
to
avoid
aggregating
these
two
kinds
of
results.
3.
The
third
option
also
includes
the
nursery
function
as
an
ecosys-
tem
service,
but
this
time
supported
by
an
integrated
ecosystem
assessment
that
comprises
at
least
‘biodiversity
and
ecosys-
tem
condition’
and
some
or
all
the
other
components
of
Fig.
1,
making
a
clear
differentiation
between
components
and
mak-
ing
reference
to
species
of
direct
use
for
humans.
In
this
kind
of
assessments,
the
relevance
of
the
nursery
habitats
for
all
organisms
can
be
analyzed
as
a
biodiversity
constituent,
but
this
cannot
be
considered
an
assessment
of
ecosystem
services.
The
main
risk
of
this
option
is
to
double
count
the
nursery
function
together
with
other
provisioning
or
cultural
services,
particu-
larly
when
only
the
ecosystem
goods
(e.g.
fish)
and
not
the
processes
are
valued.
Taking
into
account
all
the
arguments
presented,
our
preferred
choice
is
the
third
option.
We
conclude
that
the
nursery
function
should
be
considered
an
ecosystem
service
on
its
own
right
when
it
is
linked
to
a
concrete
human
benefit
(e.g.
enhanced
fishing,
increased
recreational
activities)
and
not
when
it
is
represented
as
a
general
biodiversity
constituent.
In
our
opinion,
the
risk
of
double-
counting
can
be
avoided
by
a
good
planning
and
clear
objective
of
the
study.
Nursery
habitats
are
crucial
for
the
maintenance
of
fish-
eries
(e.g.
Jackson
et
al.,
2015),
but
we
have
not
read
a
single
study
adding
the
monetary
value
from
“maintenance
of
nursery
popu-
lations
and
habitats”
and
that
of
“food
provisioning”,
i.e.
counting
twice
the
same
benefit.
Instead,
the
indicators
used
to
character-
ize
the
delivery
and
benefit
from
the
nursery
function
are
different
from
those
of
fisheries
(e.g.
Table
2).
When
it
comes
to
economic
valuation,
the
results
from
“maintenance
of
nursery
populations
and
habitats”
should
be
only
used
to
estimate
what
share
of
the
total
fishing
value
ultimately
depends
on
specific
nursery
habitats.
Even
if
those
monetary
values
cannot
be
added,
they
are
extremely
important
to
make
the
case
for
the
protection
of
essential
habi-
tats,
to
justify
conservation
investments
or
to
regulate
conflicting
human
activities.
Thus,
we
advocate
for
the
distinction
between
the
analysis
of
biodiversity
and
ecological
integrity
and
ecosystem
service
assess-
ments
(quantification
of
certain
biologically-mediated
processes
that
benefit
human
beings),
and
for
their
integration
when
ecosys-
tem
services
act
as
a
policy
tool
for
protecting
biodiversity
(e.g.
MA,
2005,
IPBES
in
Díaz
et
al.,
2015).
Only
with
this
distinction
science
may
be
able
to
quantify
the
link
between
biodiversity
and
ecosys-
tem
services
(e.g.
Reyers
et
al.,
2012,
Maes
et
al.,
2012)
and
policy
may
be
effective
in
halting
biodiversity
loss.
The
analysis
of
the
nursery
function
in
ecosystem
service
assessments
presented
in
this
paper
suggests
that
similar
con-
siderations
and
conclusions
could
apply
for
other
biodiversity
constituents
that
may
be
treated
as
ecosystem
services
such
as
“biodiversity”
or
“habitat
quality”
(InVEST,
2015,
Nelson
et
al.,
2011),
“nutrient
cycling”
(MA,
2005),
“water
conditions”
(CICES,
2015),
or
“habitats
for
species”
(TEEB,
2015).
Again,
in
all
these
cases,
we
should
clarify
whether
(1)
these
services
can
be
measured
independently
from
the
overall
ecosystem
condition,
(2)
there
is
a
direct
human
benefit
from
these
services,
and
(3)
their
benefit
is
overlapping
with
other
services
or
can
be
differentiated.
Acknowledgments
This
paper
is
the
result
of
ongoing
discussions
within
a
multi-
disciplinary
team,
where
sharing
and
refining
our
points
of
view
enriched
our
understanding
and
our
work.
This
is
fostered
by
the
research
activities
developed
under
the
EU
FP7
projects
MARS
(grant
agreement
no.
603378)
and
OpenNESS
(grant
agreement
no.
308428)
and,
consequently,
by
all
the
partners
and
colleagues
we
have
the
pleasure
to
collaborate
with.
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
255
Appendix
A.
Common
International
Classification
of
Ecosystem
Services
v4.3
(CICES,
2015):
Section
Division
Group
Class
Provisioning
Nutrition
Biomass
Cultivated
crops
Reared
animals
and
their
outputs
Wild
plants,
algae
and
their
outputs
Wild
animals
and
their
outputs
Plants
and
algae
from
in-situ
aquaculture
Animals
from
in-situ
aquaculture
Water
Surface
water
for
drinking
Ground
water
for
drinking
Materials
Biomass
Fibres
and
other
materials
from
plants,
algae
and
animals
for
direct
use
or
processing
Materials
from
plants,
algae
and
animals
for
agricultural
use
Genetic
materials
from
all
biota
Water
Surface
water
for
non-drinking
purposes
Ground
water
for
non-drinking
purposes
Energy
Biomass-based
energy
sources
Plant-based
resources
Animal-based
resources
Mechanical
energy
Animal-based
energy
Regulation
&
Maintenance
Mediation
of
waste,
toxics
and
other
nuisances
Mediation
by
biota
Bio-remediation
by
micro-organisms,
algae,
plants,
and
animals
Filtration/sequestration/storage/accumulation
by
micro-organisms,
algae,
plants,
and
animals
Mediation
by
ecosystems
Filtration/sequestration/storage/accumulation
by
ecosystems
Dilution
by
atmosphere,
freshwater
and
marine
ecosystems
Mediation
of
smell/noise/visual
impacts
Mediation
of
flows
Mass
flows
Mass
stabilisation
and
control
of
erosion
rates
Buffering
and
attenuation
of
mass
flows
Liquid
flows
Hydrological
cycle
and
water
flow
maintenance
Flood
protection
Gaseous/air
flows
Storm
protection
Ventilation
and
transpiration
Maintenance
of
physical,
chemical,
biological
conditions
Lifecycle
maintenance,
habitat
and
gene
pool
protection
Pollination
and
seed
dispersal
Maintenance
of
nursery
populations
and
habitats
Pest
and
disease
control
Pest
control
Disease
control
Soil
formation
and
composition
Weathering
processes
Decomposition
and
fixing
processes
Water
conditions
Chemical
condition
of
freshwaters
Chemical
condition
of
salt
waters
Atmospheric
composition
and
climate
regulation
Global
climate
regulation
by
reduction
of
greenhouse
gas
concentrations
Micro
and
regional
climate
regulation
Cultural
Physical
and
intellectual
interactions
with
biota,
ecosystems,
and
land-/seascapes
Physical
and
experiential
interactions
Experiential
use
of
plants,
animals
and
land-/seascapes
in
different
environmental
settings
Physical
use
of
land-/seascapes
in
different
environmental
settings
Intellectual
and
representative
interactions
Scientific
Educational
Heritage,
cultural
Entertainment
Aesthetic
Spiritual,
symbolic
and
other
interactions
with
biota,
ecosystems,
and
land-/seascapes
Spiritual
and/or
emblematic
Symbolic
Sacred
and/or
religious
Other
cultural
outputs
Existence
Bequest
256
C.
Liquete
et
al.
/
Ecological
Indicators
63
(2016)
249–257
Current
list
of
ecosystem
services
proposed
by
The
Economics
of
Ecosystems
&
Biodiversity
(TEEB,
2015):
Provisioning
Services
Food
Raw
materials
Fresh
water
Medicinal
resources
Regulating
Services
Local
climate
and
air
quality
Carbon
sequestration
and
storage
Moderation
of
extreme
events
Waste-water
treatment
Erosion
prevention
and
maintenance
of
soil
fertility
Pollination
Biological
control
Habitat
or
supporting
services
Habitats
for
species
Maintenance
of
genetic
diversity
Cultural
services
Recreation
and
mental
and
physical
health
Tourism
Aesthetic
appreciation
and
inspiration
for
culture,
art
and
design
Spiritual
experience
and
sense
of
place
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