Sacrificing patches for linear habitat elements enhances metapopulation performance of woodland...

RESEARCH ARTICLE

Sacrificing patches for linear habitat elements enhancesmetapopulation performance of woodland birdsin fragmented landscapes

Peter Schippers AElig Carla J Grashof-Bokdam AElig Jana Verboom AElig Johannes M Baveco AEligRene Jochem AElig Henk A M Meeuwsen AElig Marjolein H C Van Adrichem

Received 23 July 2008 Accepted 29 November 2008 Published online 19 December 2008

Springer Science+Business Media BV 2008

Abstract It is generally assumed that large patches

of natural habitat are better for the survival of

species than the same amount of habitat in smaller

fragments or linear elements like hedges and tree

rows We use a spatially explicit individual-based

model of a woodland bird to explore this hypothesis

We specifically ask whether mixtures of large small

and linear habitat elements are better for population

performance than landscapes that consist of only

large elements With equal carrying capacity meta-

populations perform equally or better in heterogeneous

landscape types that are a mix of linear large and

small habitat elements We call this increased

metapopulation performance of large and small

elements lsquolsquosynergyrsquorsquo These mixed conditions are

superior because the small linear elements facilitate

dispersal while patches secure the population in

the long run because they have a lower extinction

risk The linear elements are able to catch and

guide dispersing animals which results in higher

connectivity between patches leading to higher

metapopulation survival Our results suggest that

landscape designers should not always seek to

conserve and create larger units but might better

strive for more variable landscapes with mixtures of

patch sizes and shapes This is especially important

when smaller units play a key role in connecting

patches and dispersal through the matrix is poor

Keywords SLOSS Woodland birds Linear elements Hedgerows Patch size Metapopulation Dispersal Synergy Landscape design

Introduction

Habitat patches in fragmented and intensively used

landscapes can be considered as islands in a sea of

non habitat (Bender et al 2003 Wiens 1995) In

these landscapes the amount of habitat size of habitat

patches inter-patch distance and habitat configura-

tion can be regarded as key factors determining

species survival and diversity (Ricketts 2001

Thomas and Kunin 1999 Verboom et al 2001

Tischendorf et al 2003 Schultz and Crone 2005)

Since in many countries space is scarce there is an

increasing need for knowledge of how to optimize the

design of landscapes and nature reserves from a

biodiversity conservation perspective (Lomolino

1994 Kingsland 2002 McCarthy et al 2005 2006)

P Schippers (amp) C J Grashof-Bokdam J Verboom J M Baveco R Jochem H A M Meeuwsen M H C Van Adrichem

Alterra Landscape Centre Wageningen University and

Research Centre PO Box 47 NL-6700AA Wageningen

The Netherlands

e-mail peterschipperswurnl

123

Landscape Ecol (2009) 241123ndash1133

DOI 101007s10980-008-9313-9

Already since 1986 a debate is going on that is

commonly known as the SLOSS debate (Single

Large Or Several Small Patterson and Atmar 1986)

This debate is concentrating on the question whether

many small habitats elements are better than a

single large patch for species conservation pur-

poses given the same total amount of habitat area

(Patterson and Atmar 1986 Baz and GarciaBoyero

1996 Etienne and Heesterbeek 2000 Kingsland

2002 Ovaskainen 2002) It is generally assumed

that a single large patch is superior when a single

species is considered because in a large patch the

overall population is less prone to dispersal mortal-

ity Allee-effects and demographic stochasticity

(MacArthur and Wilson 1967 Verboom et al

2001 Vos et al 2001 Ovaskainen 2002) Compared

to this the lsquoSeveral Smallrsquo configuration is inferior

because of the larger loss of animals during

dispersal the relatively high extinction probability

of small populations due to demographic stochas-

ticity and Allee-effects The situation becomes more

complicated when we compare landscapes that have

Few Large patches with landscapes that have Many

Small (FLOMS) patches (Etienne and Heesterbeek

2000 Ovaskainen 2002) because in the landscape

that consists of a few large patches dispersal

limitation might play a key role

In many intensively used landscapes however

landscapes consist of mixtures of large and small of

habitat patches and of linear habitat Because land is

scarce a design of a sustainable habitat configuration

is essential to improve the conservation potential of

the landscape (Van Apeldoorn et al 1998) Existing

theory favors large patches (eg key patches

Verboom et al 2001) suggesting that all effort

should be put into conservation enlargement

and improvement of large nature areas in a habitat

network We challenge this viewpoint here by

exploring the hypothesis that synergy is possible

between large and small patches Therefore a logical

next step is to evaluate mixtures of large and small

habitat patches and compare their performance with

landscapes that consist of only small or large patches

Here we might expect advantage synergy from

mixed landscape configurations because these land-

scapes might have the best of both (Grashof-Bokdam

et al 2008) In many landscapes linear elements like

hedges and tree rows are important small elements

(Haddad 1999 Chardon et al 2003) Moreover these

elements which are often considered as part of the

matrix may play a key role in the dispersal survival

and reproduction in many species (VanDorp et al

1997 Ricketts 2001 Grashof-Bokdam and van

Langevelde 2005) Knowledge about how these

linear elements function and under what conditions

they facilitate population survival will provide insight

in the use of these elements in landscape planning

and their role in the ecology of species

To investigate the possible added value of mixed

landscapes we explore the population dynamics of a

woodland bird in artificial landscapes in which the

landscape configuration is defined as the percentage

of landscape coverage of large small and linear

elements We specifically ask is there an ecological

advantage (synergy) possible in landscapes which

consist of a mix of small patches linear elements and

large habitat patches compared to landscapes that

consist of only one type Furthermore we want to

understand the mechanisms and prerequisites that

make this lsquosynergyrsquo possible To answer these

questions we adapt the individual-based model

METAPHOR (Verboom et al 2001 Vos et al

2001) and use the model to evaluate the survival

and populations dynamics in different artificial land-

scapes that have the same total amount of habitat

using a woodland bird in open landscapes as an

example

Materials and methods

We use a detailed spatially explicit individual-based

model (METAPHOR) that simulates the dynamics of

a metapopulation (Verboom et al 2001 Vos et al

2001) The model keeps track of every individual in

space and time We use the model to simulate the

population dynamics of a territorial bird (parameter-

ized as the middle spotted woodpecker) living in

patchy landscapes with hedgerows having 25 ha

territories Six kinds of individuals were distin-

guished juveniles territory owners and floaters

(non territorial adults) of both sexes The model

simulates a number of life cycle events every year

reproduction dispersal survival (mortality) aging

and completing pairs (Fig 1) To model the dynamics

in linear elements the habitat area is explicitly

divided into territories that have a sufficient amount

of habitat to support a pair and their offspring

1124 Landscape Ecol (2009) 241123ndash1133

123

Population dynamics of the model

At the start of a year there are only floaters and adults

present in a territory (Fig 1) The adults may

reproduce if paired The offspring the number of

juveniles per female surviving their nesting and

fledging period is drawn from a Poisson distribution

with the parameter k representing the expected

number of surviving offspring and its variance Only

juveniles are allowed to disperse to other territories

The next step in the model is the survival of the

different stages The survival probability in a territory

(i) is made up by a background survival affected by

environmental variability Here the environment is

the same for all territories in any year the environ-

mental variation is perfectly correlated for all

territories and both sexes The survival probability

for a specific territory (Psi) is a Normal distributed

random variable with mean Ps and standard devia-

tion SDs

Psifrac14 Ps thorn et SDs

The standard deviation SDs corresponds to the

natural variation in the survival rate (environmental

stochasticity) It is obtained from a random variable

et with a standard normal distribution We assume

that floaters and juveniles have a lower survival than

the territorial adults (Table 1) Subsequently the

juveniles become adult floaters Floaters may become

territorial adults when a residential adult of the same

sex dies and a territory becomes available (Fig 1)

Artificial landscape configurations

In this paper we focus on Western-European agricul-

tural landscapes where the coverage of woody

elements is typically in the order of magnitude of

10 (Tellerıa et al 2003) Therefore we choose our

artificial landscapes with 10 of woody habitat

Definitions of large and small woodland elements are

based on Dutch nature policy where nature areas

should be larger than 5 ha whereas smaller units were

A A

J

F

S

RD

D

S FC

1 year

Counting

R Reproduction

Dispersal

S SurvivalCJ

Completing pairs

S J

F

A = adults (having a territory)J = juvenilesF = floaters (adults without territory)

AA Aging

Fig 1 Simulation scheme

of stages and life cycle

events of a woodland bird

during a year Life stages Aterritorial adult F floater

adult that does not

reproduce J juvenile

Events R reproduction Ddispersal S survival Aaging C completing pairs

floater replace an adult of

his own sex that has died

Table 1 Parameters of a woodpecker type bird used in the

model

Description Symbol Value Unit

Population dynamics

Survival of territorial adults Psa 078 Year-1

Standard dev aldult survival SDsa 01 Year-1

Survival of juviniles and floaters Psj 065 Year-1

Standard dev Juv and floaters SDsj 02 Year-1

Number of offspring k 3 Year-1

Territorial area requirement T 25 ha

Dispersal

Number of steps N 1000 Year-1

Standard deviation walking angle SDD 5 8

Step size St 10 m

Catchment radius of territory R 89 m

Probability of reflexion

Habitat- [ non habitat Ph 095

Non habitat- [ habitat Pn 0

Landscape Ecol (2009) 241123ndash1133 1125

123

considered to be part of the matrix (Grashof-Bokdam

et al 2008) Therefore we define three landscape

elements small patches of one territory that are

25 ha and linear elements that are 25 ha but have a

width of 25 m and large patches of four territories

that are 10 ha So here we simulate the matrix

structure explicitly To avoid confusion however we

will use the term matrix to describe the non habitat

part of the landscape The total area of the artificial

landscapes is 6 9 6 km

We use a replacement approach to construct

different landscapes We start with a landscape with

only large elements subsequently we replace large

elements by small patches andor linear elements

keeping the same total amount of habitat This results

in seven landscape types all having 10 of habitat

area but differing with respect to the total abundance

of the different landscape elements (Table 2) We

choose the maximal connection version of linear

elements and patches of the landscape as our default

landscape Here linear elements are as much as

possible physically connected to the patches (Fig 2)

In the simulations and results section we will evaluate

what the effect is of this choice Additionally we

define the precise location of the territories To do

this we first overlay the landscape with a large cloud

of random points and check around every point

whether there is enough habitat (25 ha) to support a

territory We continue this procedure until we have

144 territories in all the landscape types As a result

we get landscapes havening all 10 of habitat and

90 non-habitat with scattered territories located in

the 10 habitat Animals are allocated to a territory

when they do not disperse Dispersing animals are

allowed to move freely in all directions in this

landscape in both habitat and non-habitat according

to the rules described in the next section until they are

within a critical radius from a new territory and are

allocated to this territory

Random walk dispersal

We simulate the dispersal between territories using

SmallSteps a separate movement module (Baveco

2006) This module simulates the dispersal of the

juveniles from a territory in which they were born to

a territory in which they settle The animal movement

in the model is in fact a correlated random walk

(Schippers et al 1996 Tischendorf and Wissel 1997

Tischendorf et al 1998 Haddad 1999) In this model

a dispersing animal has a coordinate in a continuous

xndashy space and a walking direction between 0 and

360 Each time step a new direction (Dt) relative to

the old direction (Dt-1) is calculated

Dt frac14 modethDt1 thorn et SDD 2pTHORN

where et is a number drawn from a standard normal

distribution SDD is the standard deviation of the

walking direction lsquolsquomodrsquorsquo is a modulus function with

2p (rad) as the basis number Next the dispersing

animal takes a step in this new direction with a step

size (St) of 10 m subsequently the new position is

calculated A dispersing animal is allowed to take

1000 steps during dispersal If during dispersal in

habitat an animal meets non habitat it has a proba-

bility to be reflected Ph of 95 (Table 1) Reflecting

means that the walking direction is mirrored against

the habitat edge When a dispersing animal however

enter habitat the animal continues its path Animals

continue dispersing until they find a new territory that

is not occupied by a territorial adult of the same sex

If an animal has not found another suitable patch after

Table 2 Habitat cover

( of total) of different

landscapes

Landscape

description

Habitat large

patches

Habitat small

patches

Habitat linear

elements

Matrix

Large 10 0 0 90

Mix-P 5 5 0 90

Mix-L 5 0 5 90

Mixed-LP 5 25 25 90

Small-P 0 10 0 90

Small-L 0 0 10 90

Small-LP 0 5 5 90


123

1000 steps and is not located in habitat the dispersing

animal dies Animals that arrive in habitat after 1000

steps but not in a vacant territory are allocated to the

nearest territory Animals that arrive in a new

territory become floaters and may reproduce when

the territorial adult of the same sex dies Animals that

encounter the landscape edge are reflected These

rules cause that dispersing animals first disperse in

the habitat patch of their territory checking neighbor

territories before they start dispersing through the

matrix and might find another habitat patch and

territories in there

Parameterization and calibration

We use demographic parameters of the middle

spotted woodpecker (Pettersson 1985 Kosenko and

Kaigorodova 2001 Kosinski and Ksit 2006) whereas

the dispersal distance is based on the work of Muller

(1982 Table 1) Demographic parameters were cal-

ibrated to meet criteria published by Verboom et al

(2001) for medium sized birds

Evaluating synergy

Synergy occurs when mixtures of large and small

habitat patches perform better with respect to survival

than landscapes with patches of the same type In this

study we did 250 simulations in the default land-

scapes each run starting with one reproductive unit

ie an adult male and female in every territory We

evaluated metapopulation survival and the mean

number of adult individuals between year 50 and

150 to avoid transient behavior due to the initiali-

zation state (lsquolsquoburn-inrsquorsquo) Since there is a strong

correlation between the mean number of individuals

and survival we present only the survival results in

our graphs Of every survival fraction the 95

confidence interval is calculated using a v-test We

present our results as a replacement series in which

we replace large patches by smaller elements keeping

the same amount of habitat ultimately resulting in the

landscape with small elements only (Fig 3) Monot-

onously increasing relations (small- [ mixed- [large) support the more traditional hypothesis that

Large

Large

Large

Small-P Mix-P

Small-L

Small-PL

Mix-L

Mix-PL

only small mixed only largereplacing

Small toLarge

Small andLinear toLarge

Linear tolarge

Fig 2 Default landscapes

of 6 9 6 km lines are

linear elements of

6000 9 25 m smallsquares are small forest

patches of 25 ha that can

contain one territory Largesquares are large patches of

10 ha that contain four

territories


123

larger patches are always better an optimum rela-

tionship supports our alternative hypothesis that

synergy occurs

Simulations and results

Reference simulations

We evaluate metapopulation survival in the seven

default landscapes for the species parameterized

according to Table 1 When we replace half of the

large patches by small elements these mixed land-

scapes performe best if these small elements were all

linear elements (L Fig 4) Here metapopulation

survival in mixed landscapes was higher than in the

landscape with only large patches indicating syn-

ergy If half of the large patches is replaced by a mix

of small patches and linear elements (LP) metapop-

ulation survival is the same as in the landscapes with

only large patches This indicates that mixed land-

scapes with linear elements perform equally or better

than the landscape with only large patches Mixed

landscapes without linear elements (P) or landscapes

with only small elements however always performe

worse compared to the other landscapes Furthermore

we see that a landscape with only small elements that

contained both linear elements and small patches

(LP) performed much better than landscapes with

only small elements that contained only linear

elements (L) or only small patches (P) These results

suggest that replacing a part of the small patches by

linear elements also enhances population survival

Effects of physical connections

The results suggest that linear elements are respon-

sible for the synergy due to the fact that they connect

patches with each other and guide dispersers To

investigate this effect we create three alternative

landscapes in which the linear elements are not

connected to the patches

If linear elements are not connected to the large

patches number of individuals and survival decrease

in the mixed landscapes with linear elements (L and

LP) (compare Figs 4 5) This indicates that linear

connections are responsible for the synergy found in

the reference conditions Survival in landschapes

Large

Mix-L

Mix-LP

Mix-P

Small-L

Small-LP

Small-P

S

urvi

val o

f met

apop

ulat

ion

Only Mix Onlysmall largeelements patches

L-line

P-line

LP-line

Fig 3 Explanatory graph that relates individual simulation

results to synergy If mixed landscapes perform better than

landscapes with only small and large elements there is synergy

L linear elements present as small elements P small patches

present as small elements LP both linear elements and small

patches present as small elements

0

02

04

06

08

1

only small mix only large

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

Fig 4 Fraction of surviving metapopulations of default

simulations of seven different landscapes that differ with

respect to the percentage of large and small habitat patches or

linear habitat elements error bars represent the 95 confi-

dence inteval Only small landscapes that only consist of small

elements mix landscape that are a mix of large and small

elements only large is a landscape that has only large patches





123

with only small elements however is still higher in

landscapes with small patches and linear elements

(LP) than in landscapes with only small patches

Effects of decreasing the dispersal through

the matrix

To investigate whether linear elements are indeed

crucial for synergy we decrease the dispersal effi-

ciency through the matrix by increasing the standard

deviation of the turning angle (SDD) from 5 to 20 and

40 This change results in a decrease of the realized

dispersal distance As a result 90 of the animals

move less than resp 29 and 15 km in the matrix

whereas in the reference situation this was 84 km In

these simulations we use the seven default landscapes

again

As a result of the decreased dispersal efficiency

through the matrix the metapopulation survival in

landscapes without linear elements (P) decrease

strongly (Fig 6a b) resulting in a clear synergy

pattern for the linear replacement lines (L) and

linear combined with small patches replacement

lines (LP Fig 6) Replacing large patches by

smaller patches does not help to compensate for

the loss of dispersal efficiency through the matrix

The landscapes containing only small patches the

decreased dispersal efficiency even caused extinc-

tion in a simualtion for the most inefficient dispersal

class These results indicate that if dispersal through

the matrix is difficult or avoided by a species linear

elements are crucial

Discussion

Main results

It is generally assumed that larger patches of natural

habitat are better for the survival of species than the

same amount of habitat in smaller fragments

(MacArthur and Wilson 1967 Verboom et al 2001

Vos et al 2001) Our results suggest that replacing a

part of the larger units by smaller linear elements

enhance population performance with respect to

population level and survival Without any large

patches however we see a serious decrease in

performance of the population indicating that large

patches are still very important The explanation for

this synergy is that the large patches secure survival

of the population whereas the linear units enhance

inter-patch dispersal by serving as corridors Addi-

tionally we see that populations in landscapes with

small patches also benefit from the availability of

linear elements Also here we see synergy to the

extent that a mixture of linear elements and small

patches performs better than landscapes consisting of

solely linear elements or small patches

In this study linear elements have a double

function they can serve as a corridor but also as

habitat In real landscapes corridors may not be wide

or qualitatively good enough to support both func-

tions Small patches may serve as stepping stones

because the mean inter-patch distance decreases with

increasing number of patches (Etienne and Heester-

beek 2000) However if we reduce the area of the

patches with a certain factor the average inter-patch

distance (centre to centre) is reduced with only the

square root of this factor Consequently replacing

large patches by smaller patches is inferior to

replacing large patches by linear elements

0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP

Fig 5 Fraction of surviving metapopulations of simulations

in which the linear elements were not connected to the large

patches of five different landscapes that differ with respect to

the percentage of large and small habitat patches or linear

habitat elements error bars represent the 95 confidence

inteval Only small landscapes that only consist of small



L linear elements present as small elements LP both linear

elements and small patches present as small elements


123

Mechanisms favoring large or small patches

Seven processes are put forward in literature that

determines metapopulation performance in response

to the subdivision of habitat

1 Population extinction larger patches have a

higher carrying capacity and therefore a lower

extinction risk due to Allee-effects and demo-

graphic stochasticity than smaller patches

(Shaffer 1981 Soule 1987)

2 Colonization When dispersal potential is weak

and the dispersal mortality in the matrix is high

however the lsquoSeveral Smallrsquo approach might be

superior (Etienne and Heesterbeek 2000) The

extreme case is when the inter-patch distances of

the large patches are too large for recolonization

whereas the species is able to bridge the smaller

inter-patch distance between the small patches

Here the landscape configuration with few large

patches is actually more fragmented than the

landscape with many small patches (Flather and

Bevers 2002)

3 Finding a mate it seems likely that especially

monogamous animals that live in a landscape

with many small patches have a higher risk to

stay single This lowers the reproduction (Engen

et al 2003)

4 Density dependent population growth in a more

fragmented landscape animals encounter more

density dependent effects because some patches

are at or above carrying capacity while others are

empty Here individuals are not optimally utiliz-

ing the resources This lowers the growth rate of

fragmented populations

5 Patch edge effects if a species utilizes patch

edges more than the patch core several small

patches might be superior over a few large

patches because the amount of edges and

ecotones is larger when the landscape is more

fragmented On the other hand if core habitat is

preferred eg because the influence of the

Fig 6 The effect of increasing the turning angle of dispersing

birds from 5 to 20 and 40 degrees resulting in lower matrix

permeability The figure depict the fraction of surviving

metapopulations in the default landscape and the error bars

represent the 95 confidence interval Only small landscapes

that only consist of small elements mix landscape that are a

mix of large and small elements only large is a landscape that

has only large patches L linear elements present as small

elements P small patches present as small elements LP both

linear elements and small patches present as small elements

c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123

matrix makes the edges suboptimal larger ele-

ments are better

6 Spreading of risk if populations fluctuate due to

local environmental factors subdivision may

save parts of the metapopulation from events

such as fire or other adverse conditions When

species like a predator or a disease are taken into

account a fragmented landscape may be superior

Here predator or disease might also suffers from

isolation leaving their prey or host untouched in

patches that are not yet colonized by the predator

or disease (Baz and GarciaBoyero 1996 Lang-

lois et al 2001 Tscharntke et al 2002) Another

special case is habitat heterogeneity among

patches which makes eg wet patches more

suitable in dry years and dry patches in wet years

(Boer 1981) Although the spreading of risk

might also occur in larger elements it generally

favors population subdivision

7 Round off effects in fragmented landscapes

specific patch carrying capacity might not be

whole even numbers For instance if we sub-

stitute a patch with a carrying capacity of ten by

four fragments with carrying capacities of 25

these patches together can only support eight

breeding pairs

In our simulation study we do not incorporate all

these seven processes We take extinction (due to

demographic stochasticity and Allee-effects) coloni-

zation (dispersal success) pair formation and density

dependent population growth into account We do not

incorporate patch edge effects (when habitat quality

differs between patch core and patch edge) spreading

of risk (local disturbances patch heterogeneity and

antagonistic species) and round off effects These

three missing factors have an evident effect while

round off effects will favor large patch landscapes

and spreading of risk will favor fragmented land-

scapes the effect of taking into account edge effects

will depend on a preference for patch core or edge

habitat but in either case a straightforward relation is

expected Therefore our results may be slightly

modulated by taking into account these aspects but

our conclusions should be robust since some factors

are in favor of small patches and others are in favor of

large patches an optimum configuration is expected

somewhere between the two extreme cases with only

large or only small patches

Climate change

In the face of climate change there might be a few

extra considerations the habitat of species in climatic

terms is no longer stationary so species should be

able to track their climatic window Consequently the

global survival of a species is no longer only

dependent on the survival locally but also on the

ability of species to move and follow the climate

suitability window (Tischendorf et al 2003 Travis

2003 Saether et al 2004 Thomas et al 2004) This

underpins the idea that under climate change condi-

tions heterogeneous landscapes with many linear

elements might be even more superior for species

survival because they both facilitate animal movement

en survival Whereas large patches are necessary to

buffer the population against increasingly stochastic

weather events and provide dispersers connectivity by

linear elements should allow populations to shift

Generality of the results

We did a series of simulations with a spatially

explicit individual-based population model simulat-

ing the population dynamics of a territorial woodland

birds in open agricultural landscapes Our results

indicate that replacing patches by linear elements that

can serve as habitat enhances metapopulation perfor-

mance Clearly we can not extrapolate these results to

conclusions for other species and spatial configura-

tions We think however that our conclusions are

likely to be valid for other species and conditions if

(1) the carrying capacity of the habitat is not affected

by the replacement (2) the dispersal trough habitat is

more efficient and less risky than dispersal through

matrix and (3) if spatial configurations are such that

patches are relatively isolated so that dispersal

limitation is an important factor

Implications for sustainable landscape design

and nature conservation


increasing need for knowledge about how to optimize

the design of landscapes nature reserves and habitat

networks from a biodiversity conservation perspec-

tive (Lomolino 1994 Kingsland 2002 McCarthy


123

et al 2005 McCarthy et al 2006) Our results

indicate that landscape designers and nature conser-

vationists should reconsider the value of small linear

elements that often are considered as part of the

matrix and not always seek to create larger units but

may better create more variable landscapes with

mixtures of patch sizes and shapes This is especially

important when smaller units play a key role in

physically connecting large patches when dispersal

through the matrix is poor or dispersal distances are

smaller than inter-patch distances On the other hand

the smaller units should be large enough to have a

habitat function for the species considered ie

reproduction should be possible there

Acknowledgments This research was financed by the

program lsquolsquoVernieuwend Ruimtegebruikrsquorsquo of Habiforum and

co-financed by the Dutch Ministry of Agriculture Nature and

Food Quality

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26820

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Chardon JP Adriaensen F Matthysen E (2003) Incorporating

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study for the Speckled wood butterfly (Pararge aegeria L)


30600

Engen S Lande R Seather BE (2003) Demographic stochas-

ticity and allee effects in populations with two sexes

Ecology 842378ndash2386 doi10189002-0123

Etienne RS Heesterbeek JAP (2000) On optimal size and

number of reserves for metapopulation persistence

J Theor Biol 20333ndash50 doi101006jtbi19991060

Flather CH Bevers M (2002) Patchy reaction-diffusion

and population abundance the relative importance of

habitat amount and arrangement Am Nat 15940ndash56 doi

101086324120

Grashof-Bokdam CJ Chardon P Vos CC Foppen RPB

Wallisdevries MF VanDerVeen M Meeuwsen HAM

(2008) The synergistic effect of combining woodlands

and green veining for biodiversity Landscape Ecol doi

101007s10980-008-9274-2

Grashof-Bokdam CJ van Langevelde F (2005) Green veining

landscape determinants of biodiversity in European

agricultural landscapes Landscape Ecol 20417ndash439

doi101007s10980-004-5646-1

Haddad NM (1999) Corridor and distance effects on interpatch

movements a landscape experiment with butterflies Ecol

Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2

Kingsland SE (2002) Creating a science of nature reserve

design perspectives from history Environ Model Assess

761ndash69 doi101023A1015633830223

Kosenko SM Kaigorodova EY (2001) Effect of habitat frag-

mentation on distribution density and breeding

performance of the middle spotted woodpecker Dend-

rocopos medius (Alves Picidae) in Nerussa-Desna

Polesye Zool Zh 8071ndash78

Kosinski Z Ksit P (2006) Comparative reproductive biology of

middle spotted woodpeckers Dendrocopos medius and

great spotted woodpeckers D-major in a riverine forest

Bird Study 53237ndash246

Langlois JP Fahrig L Merriam G Artsob H (2001) Landscape

structure influences continental distribution of hantavirus

in deer mice Landscape Ecol 16255ndash266 doi101023

A1011148316537

Lomolino MV (1994) An evaluation of alternative strategies

for building networks of nature-reserves Biol Conserv

69243ndash249 doi1010160006-3207(94)90423-5

MacArthur RH Wilson EO (1967) The theory of island bio-

geography Princeton University Press Princeton

McCarthy MA Thompson CJ Possingham HP (2005) Theory

for designing nature reserves for single species Am Nat

165250ndash257 doi101086427297

McCarthy MA Thompson CJ Williams NSG (2006) Logic for

designing nature reserves for multiple species Am Nat

167717ndash727 doi101086503058

Muller W (1982) Die Besiedlung der Eichenwalder im Kanton

Zurich durch den Mittelspecht Dendrocopus medius Orn

Beob 79105ndash119

Ovaskainen O (2002) Long-term persistence of species and the

SLOSS problem J Theor Biol 218419ndash433

Patterson BD Atmar W (1986) Nested subsets and the structure

of insular mammalian faunas and archipelagoes Biol J

Linn Soc Lond 2865ndash82 doi101111j1095-83121986

tb01749x

Pettersson B (1985) Extinction of an isolated population of the

middle spotted woodpecker Dendrocopos-Medius (L) in

Sweden and its relation to general theories on extinction

Biol Conserv 32335ndash353 doi1010160006-3207(85)

90022-9

Ricketts TH (2001) The matrix matters Effective isolation in

fragmented landscapes Am Nat 15887ndash99 doi101086

320863

Saether BE Sutherland WJ Engen S (2004) Climate influences

on avian population dynamics In Moller AP Fielder W

Berthold P (eds) Birds and climate change pp 185ndash209

Schippers P Verboom J Knaapen JP vanApeldoorn RC

(1996) Dispersal and habitat connectivity in complex

heterogeneous landscapes an analysis with a GIS-based

random walk model Ecography 1997ndash106 doi101111

j1600-05871996tb00160x

Schultz CB Crone EE (2005) Patch size and connectivity

thresholds for butterfly habitat restoration Conserv Biol

19887ndash896 doi101111j1523-1739200500462x


123

Shaffer ML (1981) Minimum population sizes for species con-

servation Bioscience 31131ndash134 doi1023071308256

Soule M (1987) Viable populations for conservation

Cambridge University Press Cambridge

Tellerıa JL Baquero R Santos T (2003) Effects of forest

fragmentation on European birds implications of regional

differences in species richness J Biogeogr 30621ndash628

doi101046j1365-2699200300960x

Thomas CD Cameron A Green RE Bakkenes M Beaumont LJ

Collingham YC Erasmus BFN de Siqueira MF Grainger

A Hannah L Hughes L Huntley B van Jaarsveld AS

Midgley GF Miles L Ortega-Huerta MA Peterson AT

Phillips OL Williams SE (2004) Extinction risk from

climate change Nature 427145ndash148 doi101038nature

02121

Thomas CD Kunin WE (1999) The spatial structure of pop-

ulations J Anim Ecol 68647ndash657 doi101046j1365-

2656199900330x

Tischendorf L Bender DJ Fahrig L (2003) Evaluation of patch

isolation metrics in mosaic landscapes for specialist vs

generalist dispersers Landscape Ecol 1841ndash50 doi

101023A1022908109982

Tischendorf L Irmler U Hingst R (1998) A simulation

experiment on the potential of hedgerows as movement

corridors for forest carabids Ecol Modell 106107ndash118

doi101016S0304-3800(97)00186-5

Tischendorf L Wissel C (1997) Corridors as conduits for small

animals attainable distances depending on movement

pattern boundary reaction and corridor width Oikos

79603ndash611 doi1023073546904

Travis JMJ (2003) Climate change and habitat destruction a

deadly anthropogenic cocktail Proc R Soc Lond B Biol

Sci 270467ndash473 doi101098rspb20022246

Tscharntke T Steffan-Dewenter I Kruess A Thies C (2002)

Contribution of small habitat fragments to conservation of

insect communities of grassland-cropland landscapes

Ecol Appl 12354ndash363

Van Apeldoorn RC Knaapen JP Schippers P Verboom J

Engen van H Meeuwsen H (1998) Landscape planning

and conservation biology simulation models as tools to

evaluate scenarios for badger in the Netherlands Land-

scape Urban Plan 4157ndash69 doi101016S0169-2046(97)

00058-3

VanDorp D Schippers P Groenendael van JM (1997)

Migration rates of grassland plants along corridors in

fragmented landscapes assessed with a cellular automa-

tion model Landscape Ecol 1239ndash50 doi101007

BF02698206

Verboom J Foppen R Chardon P Opdam P Luttikhuizen P

(2001) Introducing the key patch approach for habitat

networks with persistent populations an example for

marshland birds Biol Conserv 10089ndash101 doi101016

S0006-3207(00)00210-X

Vos CC Verboom J Opdam PFM Ter Braak CJF (2001)

Toward ecologically scaled landscape indices Am Nat

15724ndash41 doi101086317004

Wiens JA (1995) Landscape mosaics and ecological theory In

Hansson L Fahrig L Merriam G (eds) Mosaic landscapes

and ecological processes Chapman and Hall London

pp 1ndash26


123

Already since 1986 a debate is going on that is

commonly known as the SLOSS debate (Single

Large Or Several Small Patterson and Atmar 1986)

This debate is concentrating on the question whether

many small habitats elements are better than a

single large patch for species conservation pur-

poses given the same total amount of habitat area

(Patterson and Atmar 1986 Baz and GarciaBoyero

1996 Etienne and Heesterbeek 2000 Kingsland

2002 Ovaskainen 2002) It is generally assumed

that a single large patch is superior when a single

species is considered because in a large patch the

overall population is less prone to dispersal mortal-

ity Allee-effects and demographic stochasticity

(MacArthur and Wilson 1967 Verboom et al

2001 Vos et al 2001 Ovaskainen 2002) Compared

to this the lsquoSeveral Smallrsquo configuration is inferior

because of the larger loss of animals during

dispersal the relatively high extinction probability

of small populations due to demographic stochas-

ticity and Allee-effects The situation becomes more

complicated when we compare landscapes that have

Few Large patches with landscapes that have Many

Small (FLOMS) patches (Etienne and Heesterbeek

2000 Ovaskainen 2002) because in the landscape

that consists of a few large patches dispersal

limitation might play a key role

In many intensively used landscapes however

landscapes consist of mixtures of large and small of

habitat patches and of linear habitat Because land is

scarce a design of a sustainable habitat configuration

is essential to improve the conservation potential of

the landscape (Van Apeldoorn et al 1998) Existing

theory favors large patches (eg key patches

Verboom et al 2001) suggesting that all effort

should be put into conservation enlargement

and improvement of large nature areas in a habitat

network We challenge this viewpoint here by

exploring the hypothesis that synergy is possible

between large and small patches Therefore a logical

next step is to evaluate mixtures of large and small

habitat patches and compare their performance with

landscapes that consist of only small or large patches

Here we might expect advantage synergy from

mixed landscape configurations because these land-

scapes might have the best of both (Grashof-Bokdam

et al 2008) In many landscapes linear elements like

hedges and tree rows are important small elements

(Haddad 1999 Chardon et al 2003) Moreover these

elements which are often considered as part of the

matrix may play a key role in the dispersal survival

and reproduction in many species (VanDorp et al

1997 Ricketts 2001 Grashof-Bokdam and van

Langevelde 2005) Knowledge about how these

linear elements function and under what conditions

they facilitate population survival will provide insight

in the use of these elements in landscape planning

and their role in the ecology of species

To investigate the possible added value of mixed

landscapes we explore the population dynamics of a

woodland bird in artificial landscapes in which the

landscape configuration is defined as the percentage

of landscape coverage of large small and linear

elements We specifically ask is there an ecological

advantage (synergy) possible in landscapes which

consist of a mix of small patches linear elements and

large habitat patches compared to landscapes that

consist of only one type Furthermore we want to

understand the mechanisms and prerequisites that

make this lsquosynergyrsquo possible To answer these

questions we adapt the individual-based model

METAPHOR (Verboom et al 2001 Vos et al

2001) and use the model to evaluate the survival

and populations dynamics in different artificial land-

scapes that have the same total amount of habitat

using a woodland bird in open landscapes as an

example

Materials and methods

We use a detailed spatially explicit individual-based

model (METAPHOR) that simulates the dynamics of

a metapopulation (Verboom et al 2001 Vos et al

2001) The model keeps track of every individual in

space and time We use the model to simulate the

population dynamics of a territorial bird (parameter-

ized as the middle spotted woodpecker) living in

patchy landscapes with hedgerows having 25 ha

territories Six kinds of individuals were distin-

guished juveniles territory owners and floaters

(non territorial adults) of both sexes The model

simulates a number of life cycle events every year

reproduction dispersal survival (mortality) aging

and completing pairs (Fig 1) To model the dynamics

in linear elements the habitat area is explicitly

divided into territories that have a sufficient amount

of habitat to support a pair and their offspring


123



















tion SDs




















A A

J

F

S

RD

D

S FC

1 year

Counting

R Reproduction

Dispersal

S SurvivalCJ

Completing pairs

S J

F


AA Aging





adult that does not






model


Population dynamics







Dispersal



Step size St 10 m






123








































































landscapes

Landscape

description

Habitat large

patches

Habitat small

patches

Habitat linear

elements

Matrix

Large 10 0 0 90

Mix-P 5 5 0 90

Mix-L 5 0 5 90

Mixed-LP 5 25 25 90

Small-P 0 10 0 90

Small-L 0 0 10 90

Small-LP 0 5 5 90


123





















Evaluating synergy




















Large

Large

Large

Small-P Mix-P

Small-L

Small-PL

Mix-L

Mix-PL


Small toLarge


Linear tolarge



linear elements of





territories


123



synergy occurs








































Large

Mix-L

Mix-LP

Mix-P

Small-L

Small-LP

Small-P

S

urvi

val o

f met

apop

ulat

ion


L-line

P-line

LP-line







0

02

04

06

08

1


surv

ivin

g m

etap

opul

atio

ns

L

P

LP












123





the matrix










again
















Discussion

Main results


































0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP












123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123



















tion SDs




















A A

J

F

S

RD

D

S FC

1 year

Counting

R Reproduction

Dispersal

S SurvivalCJ

Completing pairs

S J

F


AA Aging





adult that does not






model


Population dynamics







Dispersal



Step size St 10 m






123








































































landscapes

Landscape

description

Habitat large

patches

Habitat small

patches

Habitat linear

elements

Matrix

Large 10 0 0 90

Mix-P 5 5 0 90

Mix-L 5 0 5 90

Mixed-LP 5 25 25 90

Small-P 0 10 0 90

Small-L 0 0 10 90

Small-LP 0 5 5 90


123





















Evaluating synergy




















Large

Large

Large

Small-P Mix-P

Small-L

Small-PL

Mix-L

Mix-PL


Small toLarge


Linear tolarge



linear elements of





territories


123



synergy occurs








































Large

Mix-L

Mix-LP

Mix-P

Small-L

Small-LP

Small-P

S

urvi

val o

f met

apop

ulat

ion


L-line

P-line

LP-line







0

02

04

06

08

1


surv

ivin

g m

etap

opul

atio

ns

L

P

LP












123





the matrix










again
















Discussion

Main results


































0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP












123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123








































































landscapes

Landscape

description

Habitat large

patches

Habitat small

patches

Habitat linear

elements

Matrix

Large 10 0 0 90

Mix-P 5 5 0 90

Mix-L 5 0 5 90

Mixed-LP 5 25 25 90

Small-P 0 10 0 90

Small-L 0 0 10 90

Small-LP 0 5 5 90


123





















Evaluating synergy




















Large

Large

Large

Small-P Mix-P

Small-L

Small-PL

Mix-L

Mix-PL


Small toLarge


Linear tolarge



linear elements of





territories


123



synergy occurs








































Large

Mix-L

Mix-LP

Mix-P

Small-L

Small-LP

Small-P

S

urvi

val o

f met

apop

ulat

ion


L-line

P-line

LP-line







0

02

04

06

08

1


surv

ivin

g m

etap

opul

atio

ns

L

P

LP












123





the matrix










again
















Discussion

Main results


































0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP












123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123





















Evaluating synergy




















Large

Large

Large

Small-P Mix-P

Small-L

Small-PL

Mix-L

Mix-PL


Small toLarge


Linear tolarge



linear elements of





territories


123



synergy occurs








































Large

Mix-L

Mix-LP

Mix-P

Small-L

Small-LP

Small-P

S

urvi

val o

f met

apop

ulat

ion


L-line

P-line

LP-line







0

02

04

06

08

1


surv

ivin

g m

etap

opul

atio

ns

L

P

LP












123





the matrix










again
















Discussion

Main results


































0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP












123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123



synergy occurs








































Large

Mix-L

Mix-LP

Mix-P

Small-L

Small-LP

Small-P

S

urvi

val o

f met

apop

ulat

ion


L-line

P-line

LP-line







0

02

04

06

08

1


surv

ivin

g m

etap

opul

atio

ns

L

P

LP












123





the matrix










again
















Discussion

Main results


































0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP












123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123





the matrix










again
















Discussion

Main results


































0

02

04

06

08

1


surv

ing

met

apop

ulat

ions

L

LP












123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123





















Bevers 2002)





et al 2003)

























c

40 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP

20 degrees

0

02

04

06

08

1




surv

ivin

g m

etap

opul

atio

ns

L

P

LP

5 degrees

0

02

04

06

08

1

surv

ivin

g m

etap

opul

atio

ns

L

P

LP


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123


ments are better
























breeding pairs























Climate change











































123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123


















Food Quality

References





101007BF00056393




26820



doi101007BF00378792





30600










101086324120





101007s10980-008-9274-2




doi101007s10980-004-5646-1



Appl 9612ndash622 doi1018901051-0761(1999)009[0612

CADEOI]20CO2



761ndash69 doi101023A1015633830223













A1011148316537



69243ndash249 doi1010160006-3207(94)90423-5





165250ndash257 doi101086427297



167717ndash727 doi101086503058



Beob 79105ndash119






tb01749x





90022-9



320863








j1600-05871996tb00160x



19887ndash896 doi101111j1523-1739200500462x


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123








doi101046j1365-2699200300960x







02121



2656199900330x




101023A1022908109982




doi101016S0304-3800(97)00186-5




79603ndash611 doi1023073546904













00058-3





BF02698206





S0006-3207(00)00210-X



15724ndash41 doi101086317004




pp 1ndash26


123

Sacrificing patches for linear habitat elements enhances metapopulation performance of woodland...

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Transcript of Sacrificing patches for linear habitat elements enhances metapopulation performance of woodland...