source: https://doi.org/10.7892/boris.89326 | downloaded: 6.1.2020 View metadata,citationandsimilarpapersatcore.ac.uk This article isThis article by protected copyright. All rightsreserved. 10.1111/1365 differences thisbetween andVersion version the ofRecord.cite Please this asdoi article the through copyediting, typesetting, pagination and proofreading process, to whichmay lead This article a has been 1085,1081HVBoelelaan Amsterdam, The Netherlands 6 25,F, Senckenberganlage Germany 60325Frankfurt, 5 4 Groningen, The Netherlands 3 BritainOxford M139PT,Manchester, Great Road, 2 1 SchramaMaarten marsh Decoupled Section heading: Sanders Nate Editor: Paper :Standard Article type : 23 Accepted Date : 22 Revised Date : Received Date 26
Dept Senckenberg Gesellschaft fürNaturforschung, Biodiversity and ClimateCentre BIK Research Institute Ecology,Community ofGroningen, andConservation University P.O. Box11103,9700CC andEcosystemSoil of EcologyGroup,University Smith Manchester, Michael Building, AcceptedInstitute for EnvironmentalScience, Article of
Ecological Sciences, Ecological
of Sciences, Plant Universityof Bern,Altenbergrain 21,3013 Bern, Switzerland diversity dynamics ingreen and dynamics websdiversity brown primary succession during inasalt - 2656.12602 - - - 1 Sep Jun Sep ,2 Community EcologyCommunity
,3 * - - - 2016 , 2016 ccepted forpublication andundergone full peer review buthasnotbeen 2016 Fons van der Fons vander Plas
s
Section Animal Ecology,
University University of 4 , 5 , Matty P.Berg
Leiden, 2333CCLeiden, Netherlands Leiden,The .
. V
3, rije 6 , Han Olff Universit 3
eit provided byBernOpenRepositoryandInformationSystem(BORIS) , Amsterdam, De : .
brought toyouby . - CORE This article isThis article by protected copyright. All rightsreserved. Accepted Article SUMMARY Running head: 071 [email protected] * Corresponding author 4. 3. 2. 1. - 5277581
groups) both peaked at bothat groups) peaked intermediate productivity and successional age, the of diversity while Wespecies richness foundthat, and herbivores(green for invertebrate web plants di groups assembly trophic groups covary diversity twohypothesesWe between onthe relationship contrast green food andbrown web inasaltmarshsuccession ecosystem,a using ofinvertebraterange green trophicgroups ofprimary andbrown during 100 years Here, we studiedrarely andbrowngreen food web web (plant green ecosystemsTerrestrial characterisedbyastrong are functional connection the between , which
Decoupled diversity dynamicsDecoupled diversity succession over
across succession versity respond to different drivers demonstrate demonstrate versus versus
- both herbivore .
:
ii develop successional over time ) the ; - changes species richness in similarly
based) brown and (detritus ‘ decoupled diversity decoupled
: diversity patterns diversity i ) ‘ coupled
with main the of drivers
diversity hypothesis’,diversity which thatall predicts
hypothesis’, during succession in relation tokeyecosystem processesare well . However, the interlinked. However, the change ,
- -
detritivore diversity diversity calibrated chronosequence.
successional where and evenness and evenness - based) partsbased) of food the .
green and browntrophic ecosystem over awideover
s in
This article isThis article by protected copyright. All rightsreserved. is unfortunate groups how othertrophic such plant (herbivores, decomposers)predators, longbeen have ( alongchanges succession,aemphasis butwith strong on the Since earliest days of research, successional isSuccession recognized processes oneoftheoldest ecology in INTRODUCTION food web, KEY WORDS AcceptedClements 1916 Article 5.
brown web trophic groups are mostly groups are brown webtrophic by driven amountas the so ofbare suggest continuouslygroups) increased towards thelatest stages. successional macro components ecosystem inour to differently responded other speciesall groups thatdriveecosystem functioning,as diversitybrown andgreen O organic ur results show plantur results diversity that simplycannot usedasa be - green web, green driven succession - ,
detritivores, micdetritivores,
because thebecause biodiversity crisis current : material andsoil development. that webtrophicgreen mainly groups are byvegetation parameters, driven such ; brown web,chronosequence Miles Miles & Walton 1993
salt marsh, , especially below those ground, ( Connell &Slatyer 19 roarthropod roarthropod microbivores web andsecondaryconsumers (brown il, vegetationil, and biomass vegetation production, while height, succession ) . Compositional changesCompositional connected in trophic
,
ecosystem assembly rules, m any studies have have any studies 77
urges ustodevelop (implicitly) ) .
the We lack of anunderstanding therefore
aboveground taxa,especially
change
production andstanding ofdead stock successional gradients
(
Clements 1916 assumed derivative bethe to of across investigated proxy for diversity the of
succession
basic understandingbasic of ecosystem functioning, These results
; how Elton 1958 al al . diversity diversity
axes. levels plants
This )
. This article isThis article by protected copyright. All rightsreserved. ( intheirdiversity enemies diversity more resource for herbivores ( andbrowngreen food compartments web (bottom hypot disturbance arealsothese locations intermediate the with ofwherebothearlysuccessional levels disturbance, ( 2015 intermediate of levels wewouldexpectunimodalcase forall trophic groups patterns in coupled “Uncoupled hypothesis”.diversity trophic Two main can hypotheses beformulated Crutsinger detritivore web green for calls ofthe the study joint changes in how diversity along changes environmental as such gradients Brown &Southwood1983 sensu Grime 197
Accepted creases in biomass succession)plant a during Article ) hesis hesis .
Hooper One of mainfor the explanations patternis the this green andbrown if
, i.e. plant -
they simultaneously covary main with the drivers et al. based might - 3 tolerating andtolerating disturbance late successional intolerantspecies ) , which et al.et
2014 ) be
along
, 2000 - particularly
herbivores predicts that plantdiversity is ) succession .
successional groups ( ) Srivastava .
; For example,would this more occur when diversity plant Edwards -
based and succession. important
of biomassplant D iversity oftheiversity and green brown web
gradients et al. et - )
Jones Jones & Brown 1993 and and below ground(thebrownweb on diversity
decomposers if plant diversity 2009
the generalthe relationship nd (
Schrama, Berg2012 & Olff ) i) . /
- : or respond other´s toeach diversity. Inthis Experimental evidence of this of different trophicgroups, above both (the ( up regulation of diversity) up regulation Grime 1977 the highest in intermediate successional stagesas “Coupled diversity hypothesis” (
Hutchinson 1959Hutchinson intermediate disturbance hypothesis ; drives of Knops those driventhose by , as plant diversity usually, asplant diversity peaksat
ecosystem ; Rosenzweig 1995
consumer diversity ofboth
et al.et between
trophic groups trophic
, i.e. , i.e. 1999 can assembly )
; and in and in turn more to
, or
diversity in change Mulder
succession. occur. detritus ; Siemann, has beenfound vice versa ;
Fraser (e.g. with (e.g.
This et al. leads to -
and the can be
This
et al. 2013
ii)
;
This article isThis article by protected copyright. All rightsreserved. dynamics dominant groups of greenand brown wasstudiedto trophic the species level. This theseWe ideasin a tested succession, or whether the aredifferent patterns diversity of belowunderstand whether aboveand ground organismssimilarly increase over maymay linkednot be with biomass(Adler or groundorganisms throughoutand below inthisstudy increase succession system, biodiversity Although earlierwork(Schrama the spiders 1998 diversity, much onplant but rather Manning different groups ofarthropod diversity example, s observational whichhavestudied studies otherenvironmental gradients than succession groundorganisms.and below hypothesis assumes rolefor which conditions, larger abiotic a havedifferenteffects on above above groundimportantin websare uncoupledexplaining diversitypatterns,the diversity diversityhypothesisassumesSo whilethethattrophicin coupled or might describing in be best patternswhen diversity by All Haarstad & Tilman 1999
Accepted Articleenvironmental conditions main driverof ; Mittelbach a , n & Crawley (20
below
et al. everal studieseveral have
ground 2015
et al.et their speciestheir richness ) . In addition, invertebrates 2001 11 ) . salt marsh chronosequence, primary inwhichthe succession di ) Examples driving ofanimaldiversity have plant diversity been
and Hooper(2000) ; determine diversity the ofeachgroup oforganisms independently.
Hawkins &Porter2003 Evidence forEvidence t shown that grasslandshown that biodiversity canbea poor predictor of , Berg & Olff , Berg& studies have studies have reported on plant
and bird
( Kruess &Tscharntke 2002 ( Greenstone 1984 productivity andvegetationstructure he uncoupled diversity hypothesis s , vertical , 2012) has shown has the biomass that above , 2012) ofboth et al . .
In contrast, t
different ecosystem . , 2011). ) . vegetation
Also f
that that
; Langellotto & Denno Therefore weinsufficientlyTherefore herbivore diversity dependherbivore he uncoupled diversity hypothesis he uncoupled diversity or secondary consumerssecondary as such teractions between and below structure ; van Klink properties or properties
has been arguedhas been as
et al. is foundin
( 2004 Olff &Ritchie
2014 processes ) . s .
For not so not so ; versity versity
shown
This article isThis article by protected copyright. All rightsreserved. onehundredspans years of succession KNMI atwww.knmi.nl). On 824mmrainfall is SD149.1 (± yearlytemperature2008. Theaverage island10.2 onthe is marsh ofthe The species ofthediversity different trophic werebrown andgreen groups marshDescription chronosequenceof salt and todrivers, other.in response each species to study interpretation in ofobservedpatterns species richness easier. therefore an It provides ideal setting dispersal limitation apossible as ecosystemcause ofchangesin making the structure, bydispersed asthe water, frequently area logistically feasible;study 3)most and and plantspecies, to a extentlesser invertebrates, are arespatiallyclosetogether(within1 stages This speciesvertebrate composition Olsen corresponding inplantspecies changes diversity Berg 2012 hasbeentochronosequence calibrated of aperiod 100years AcceptedMETHODS Article particular successional sequence
et al.et ) . Primaryleads succession
2011
barrier
richness for patterns different trophicgroups to and in response biotic abiotic ; Schrama,Olf
island ofSchiermonnikoog(53°30' N,6°10' Netherlands, E),the inJuly this this
( f &Berg 2012 mm Edwards Sugg & 1993 saltmarsh awell ) (data from(data RoyalN the )
is highly suitable for testing our is highly suitablefortesting ideas as to (directional) build
(Figure 1;(Figure
floods
- 3 km); 2) the rather lowspeciesmakes the richness ) , as as well to in changes invertebrate and
with sea ( Olff Clements 1916 - described present, is chronosequence which
et al. et ; Chapin water
- °C
up ofplant 1997 etherlands Meteorologicaletherlands Institut ( Olff
(± SD 0.72 (± . Therefore, wecanexclude
et al.et ; ;
Tilman 1982 et al. et Schrama,Olff &Berg2012
1994 biomass
1997
°C ; studied Kaufmann 2001 ), average annual ), averageannual ; Schrama, Olff &
; 1) the different and Olff
on the salt
et al. et
1997 ) . ) e .
; This article isThis article by protected copyright. All rightsreserved. 100yearsover o sediment trappingincreases bythe vegetation ofthesoilsurfaceelevation with16cm clay of characteristicvegetationits succession haveDifferent elevations base will different inundation regimes, therefore and each a elevationflats with base m (±SE2.2cm of1.16 Level aboveAmsterdam (NAP). Ordnance tohavea selected underlying maps, thicknessphotographs, andthe of aerial sediment layeraccumulated on top of the Appendix onvegetation compositiondetails inthedifferent stagescan successional befoundin 35, 45,55and100yearsof We focusedondiversity ats patterns Sampling design by Limonium vulgare species sparse very (dominatedvegetation by A during stages successional last20 the years validated k The earliest areformedstages sideofthe late east onthe island, succession aresituated 8 stages m Accepted Article gradient of long this Elytrigia Elytrigia atherica
to the west. Thejustification west. ofto the space the - rich invegetation intermediate succession stages (dominated by
bymonitoring perm , , fixed T able able
f
S n sand layer sand layer salt marshsalt succession, reducing inundationfrequencybyfloods the 1
and equal . Salt ) in ) in late succession stages. succession
Plan - base elevationbase (position the at on initial gradient elevation the sand bare marsh successional ateach age succession succession tago maritima ( Olff anent vegetation plotsandkeysoilparameters vegetation indifferent anent al stagesal
et et al. even Salicornia europaea al stage al age in 2008age in
1997 , vegetation composition changes from with astate ) and a finally tall, species successional stages ( Olff ; - for Schrama, Berg2012 & Olff ( Olff
-
et al. et time replacement ofthissuccession hasbeen
(Electronic Appendix, Figure S1) Appendix,Figure (Electronic et et
al. 1997
stage wasestimated from topographic 1997
and ; Schrama, Berg2012 & Olff , which
) Puccinellia . As
- the
poor were estimated as
salt marsh matures, Festuca rubra,Festuca ) vegetation . Thesites were maritima elevat )
. More
(dominated Electronic Electronic at towards a towards
0, 10,25, spring ) . ion has This article isThis article by protected copyright. All rightsreserved. Accepted moisture. height,vegetation soil temperature, succession, followingwe sampledthe environmentalparameters: h To understand parametersEnvironmental &1982Straalen Rijninks metalwith an auger springtails, mites,oribatid mostcatch specimens ( offleveling towards the period, that end ofthis suggesting the time ofsamplingwassufficient to completely 'empty'Accumulation curvesforinde plot. the common species theused in period 4 flying insects emerging from soil and vegetation the height Articleland quantitative estimates on enclosure,Perspex adapt method including theofbare cover soil collection techniques diversity To assess were tide
hoppers, ( Schrama,Olff &Berg2012 selected
(Fig. 1) ( Londo 1976 Londo We sampled spiders, beetlesspiders, andbugs.
with a minimumwith a distancem of50 between
of which collection bottleof was whichcollection ow environmental underlie variables relationships between diversity and
of - (Ø10 cm,using height) aTullgren method funnel 5cm extraction 22 July were and emptiedday third every )
at of each . the above One e Electronic Electronic ed after Langed after
the diversitythe of ) above and above and below . and
nclosed nclosed ground enchytraeid worms) from wasextracted
was estimated in the ) . A
In each oftheIn each successional seven stages, points fivesampling
35 sampling cover ofbare soil ppendix plant plant pitfall pitfall trap (Ø10cm ( 2000 One c
soil inhabiting soil
biomass arandomly at location assigned ground food web , )
Figure ) losed insect filled with filled with
points one S ( 2x2 musi quadrat , Ausden 2000 2
clay layer thickness, . ). Soil V macro eth -
points ethylene glycol , a emergence trap of50x50 cm,80cm
scular p placed placed anol (70%) , w ,
meso
- for aperiod of18 days invertebrates e employed .
living in lant lant ) - . These methods two were
and larger and larger one ofan corner
species a single a single ng cover the estimation were used were used to collect and
w
ed showed a strong ed showedastrong as soil anoxiasoil five different , dead
such as
used to gain diversity micro soil core
plant biomass, within within fauna (e.g.,
50x50 cm in order to in order ( and soil and soil Van , taken each each
This article isThis article by protected copyright. All rightsreserved. Accepted traps werethe put in the field. moisture ThetaProbe® meter themeasuringperiod, twice during respectively 7and14 daysafter same day estimatereasonable fortherelative differences inanoxiabetweenlocationsmeasured onthe providemeasurement not does absolute values oftheamount itgives a ofoxygeninsitu, for valuewere corrected oftheAgCl the valuespotential atelectrode, of2cm adepth Tostandardize measurements, soil. the inthe out weread redox GB(Graphtec Ltd).Pt reference electrode (Cole ArticleAutumn of al. et point. measurements ofthe measurement period cm assigned 0.1g nearest being (70°C, after dried 48h). soil sampling point ) . .
These samples byhand dead sorted into were andliving
Soil temperature was temperature measuredSoil continuously 2011 Given that sites, twometers each apart, at ofthesamplinga20 points,using grdrop ( ) van Bochove,Beau , we 2009. For this we Forthis used 2009. . S measure 2 min soil tanding biomass was , using
c anoxia utes - lay layer thickness electrodes wereplaced design,in asquare 10cm referencefrom the d -
Palmer®), which were
the the after the wereAveragesafter electrodes placed. one
is animportant driver ofspeciesdistributionsmarshes onsalt
s chemin &Theriault 2002 oil redox potential iButtons (Maxim Corp.) four measuring Platinum clip -
reference electrode (+197mV atpH7). (± 1mm)(± clay was takenusinga ogreat each ped in
Vegetation heightVegetation wasdeterminedthree at
all all
one at eachat ofthe 35samplingonce the points in (to the(to nearest connected toaGraphtecGL200Datalogg 50x50 cm squares, up50x50 cmsquares, to1cm the above )
. per samplingper point
Soil moisture wasmeasured a using - electrodes electrodes (Pt) and oneAgCl biomass, to andweighed the 0.5 °
of thefour Pt Celsius) .
An averageof five during the Although this Although this - - disc electrodes
sampling
randomly ( Ø - 20 ( - Davy
er
This article isThis article by protected copyright. All rightsreserved. marsh groups (‘brown brown webtrophic web richness’) ofgreensummed webtrophicgroups richness web richness(‘green different trophicgroups Relationships analysisStatistical ( carnivores below other snails colonizing mitesoribatid fauna snails (Coleoptera: and leafhoppers (Hemiptera: Auchenorrhyncha) groups al. speciesofeach according invertebrate to according toclassification the in Invertebrates identified were upto ofspecies into Division AcceptedColeoptera: Coccinellidae Article ( 2004
)
<4mm) feeding on <4mm) feeding colonizinglitter (Mollusca) ; age were age were . 5. 1. ) , Below
Herbivores (sap suckers (sapsuckers weevilsHerbivores and chewers: leaf (spiders Krantz & Walter & Krantz microorganisms
ground predatory species,ground predatory fee Chrysomelidae
between between (Acari: Oribatida(Acari: described using
ground carnivores (predatory mites and
( A rove ran the , summed the ofgroups richness together all (‘total richness’), the trophic groups e ae) biodiversity (richness, or diversity evenness) ) beetles ,
) and and such as such as ( 2009 , ground ); four different plant Electronic
4. moths (Lepidoptera)
) (Coleoptera: Staphylinidae the
and Macro D
bugs iptera beetles species level andafterwardsspecies merged into
Caballe
Remmert Remmert ding preferably on ding preferably microbivores microorg -
(Hemiptera: detritivore - A larvae,
ppendix , competing general models.linear These were (Coleoptera: Carabidae) ro , aphids
et al. et and environmentalthe parameters anisms ( the the landhopper 1983 (Acari: (Acari: Prostigmata) Mesostigmata, , s (larger faunafeeding or onlitter litter ) T ;
( Miridae) (Hemiptera: 2. able able 2004 )
, Irmler Heydemann & , Algae consuming species such as such as
S (Coleoptera: (Coleoptera: Curculionidae) ) ) ) . 2
; We distinguished , using feedingpreferencesfor , using 3. ).
Microbivores (small springtails ’ Orchestia gammarellus, Orchestia gammarellus, ) Aphididae) ,
, lady the summed of richness
values of ) ; bird bird
6. (Collembola) A trophic , beetles bove (
leaf beetles six each of 1986
( with trophic
mainly ground )
groups groups , Berg soil and , the the
salt plant and and
( six i ) a ) a et et -
This article isThis article by protected copyright. All rightsreserved. environmental factors. and stage (ii) different whether varied trophicgroups in th (i) whether richness ofdifferent varied trophicgroups in their relationships with successional theenvironmentalgroup and variables first withthe ordination axes,to two inorder investigate we investigatedtheAfter analysis, also NMDS relationships vegan (R function wasused package; Oksanen,2015;R distances species richness andbetween successionalstages.within intheextenttowhichsamplinglocPCA, insights yielded variables and multidimensionalnonmetric scaling (NMDS) analysis stages successional To examine S ( modelthe with age term null Electronic Accepted Article weretatistics carriedout R( in - (ii) (ii) model, amodel i.e. asalt without marsh term, age calculated the correlations of ,
and measured the richness axes among thediversityvar (ii A i whether richnesswhether levelsof different trophicgroups ) a model) a withboth andquadratic saltmara linear ppendix, ppendix,
variables
lowest and other
T able S3 able
within within AIC , succession
, thus correcting for, thus number the ofterms inmodels included ) R . each iables
2011), 12.5and Sigmaplot Statistica 9.0.
first two first trophic
between the This . - related Hence, NMDS the analysis,anonmetricalternative to
analysis
group ordination
environmental factors , was used to determine , wasusedto 35 , (a non (a which was (i sampling points
Core Team, 2014 i
axes ) a ) a model withonly ations differed inrichness patterns eir relationships with other
of eachtrophic richness the -
parametric multivariate anal with the measuredwith the environmental
sh age term.sh age We selected finally responded responded differently to based onbased the , we ,
for whichthe ) .
(i) the Braythe
a linear conducted seven seven - Curtis Curtis different salt marshsalt
metaMDS
, a ysis)
This article isThis article by protected copyright. All rightsreserved. herbivor showed number ofspecies in the latestsuccessional stage. inte at showed apeak withsu decreased in Within web,wefound green different the species the exhibit succession For dynamicsspecific Diversity of 2 (Fig. over (Fig.change succession 2 2 whereas richnessin Species strong richnessforobserved differences between ofspecies patterns We D RESULTS C iversity vertebrate andherbivores above
Accepted Article)
. found a clear optimumclear found a for vascular In contrast, the In contrast, G peak in intermediate peak in stages successional es - the
I dynamics green of andbrown webs ).
(
composition becomes by dominated Fi
brown web species richnessshow brown webspecies plants, speciesplants, richness g .
3 ccession A ed ). the Shannon diversity
a strongdecline rmediate successionstages (
green web al stage al trophic D total - F
showed (Fig ground preda ).
richness at inter
A first increasefirst
in the numberin the ofspecies
groups . lso the
of or either thegreen brownweb notshow did any 3 C
species richness a clear optimumintermediate atsuccession ), whereas species richness forinvertebrate ), whereas herbivores
species evenness ed
tors. Species forrichness algae Elytrigia atherica Elytrigia , thus mirroring, thus pattern the ofinvertebrate
a steady increasetowardsa steady latesuccession (Fig d Fig. S
with successional age with successional pecies richness forpecies m
ediate succession succession (Fig ediate 3 B).
patterns Both (Fig did not show any clear trends show trends did not anyclear trophic groups . . for algae
3 the the ) . above Towards succession, late green andbrown web , buttowardslate
2 consumers
ground A
consumers ). had However, w However,
a
predators predators
very low very (Fig 2 ,
B e s ) , .
This article isThis article by protected copyright. All rightsreserved. Accepted claylayer the ( succession deadstanding biomass d succession, but level the towards l Vegetation height inFurthermore, increase wefoundthe an saturatingWe decrease clear founda Changes inimportantenvironmental factors ofsuccesstages trend overwhelming ascribedtothe strong can be dominanceof detritivore Article carnivores, which showedaclear Significant correlations(H’). werefound fewOverall, trophicgroupspatterns showedstrong forPielou’sevenness and Shannondiversity succession, suddenwith a increa of mostly consisting species richness, which offleveled towards late ( succession along richness the latertowards successional stages. richnessgeneral, species groups ofbrown trophic exhibitedalinear web richness Species
diversity marked and showedevenness adecreasetowardslatesuccession. This Fig. ast successionalast stage(Fig. was sion.
4 of G start absent. succession
trophic groups trophic groups in brown the web showedastrikingly different p ) but we found a much lower value fortheearliest stage ofsuccessionwhere ) butwemuchlowervalue founda ed
predatory mites ed
off towards the older stagesoff older towards the id
below 1cmbelow in Soils were Soils
not show a leveling off aleveling not show gradient se after 45y optimum succession ( atintermediate Especially microbivores ,
oxic inearlyoxic s over successionover also showed increasealso asteady richness in species along
( Fig.
the first the stageofsuccession and 4
only depth of the C ).
3
ea E). Also Vegetation biomassVegetation exhibit
for rs rs ( Shannon Fig. (Fig 4
uccession (Fig 4
in the amount o
sediment oversuccession( layer macro 3 G). E
D), litterwhereas
- showed in astrong increase species F).
diversity ofdiversity plants andbelow
Fig. -
detritivore (Fig Soil moistureSoil decrease
Orchestia gammarellus Orchestia 3 F). Below 4 H) f baresoil(Fig.
and Fig s showedanincrease in , continuous increases upto26cmincreases ed s
became more anoxic layer depth and a clear increasea clear over
3 ground predators, ground predators, D & 3 attern. attern. G).
increase d 4
A). Fig. over over Macro
in
ground In
later 4 B). - This article isThis article by protected copyright. All rightsreserved. Acceptedanalysis b valuesAlso stress for stages amount in ofvariation onNMDS based Pielou’s analyses analysis species richness aggregate detritivore andrichness species richnessaggregate herbivore of consumers algal accumulation = (r Article with soil redox = potential (r with was trophic groupsaggregate clearly differences inthe The NMDSanalysis Relationship betweenfood and webcomposition environmental factors but depthas the of layer increased clay
soils negatively soil moisturesoil (r (Fig (0.133) indicated areliable outcome became ased onShannon
s species richness,microbivore speciesand richness aboveand below
5
B
correlated percentagewith the ofbaresoil(r =
& 5 rapidly subsequent - 0.54, andp<0.001) aggregated with aggregated with the stageof earliest succession,
C = based on these alessreliableoutcome, analysesindicated ) in food web
0.77; and
ox d - ic
diversity and correlations with the stages later ofsuccession P
- stages of succession
in stages later the 0.79,
species richness <
d 0.001)
with diffe
. T evenness andexplainedShannon diversity amuchsmaller compositional differences thedifferentcompositional between P
he < thickness thickness of .
0.001)
with NMDS 2was axis
45 species - rent stages ofsuccessio stages rent y
the the ea ( Oksanen
and per . r
environmental factorswere alsomuch weaker. successional stage successional evenness d , as centroids for the species, ascentroidsrichness forthe ofthe
trophic although significantalthough the the with intermediate stages. succession
clay layer clay et al.et
, respectively group strongly and
2011
- (Fi 0.85; p<0.001) and
resulted inclear resulted (r = g ;
n
R Core Team, 201 5 was most anoxic whereas A) ( - Fig
0.47, 0.215 0.215
, less strongly , lessstrongly with . . Thestress negatively
.
5 A).
P plant species and <
ground predator NMDS axis NMDS axis
0.001).
0.200 diversity -
positively correlated valu successional ( 4 Fig ) for the e forthis . R Macro
ichness ichness 4 litter H 1 ) , -
This article isThis article by protected copyright. All rightsreserved. whichelevation, isoften case in the chronosequences this ( differentshowing that the ages indeed reflectdifferent stages temporal the locations conditions A dead organic mat to related changes in diversitytheir patterns Our NMDSanalysis indicated thatthis green discrepancy in webrichnessand brown species species therefore support the hypothesis that brown web brown web inspecies towards stages decrease richness later trophicgroupsof the whereas in succession, green groups the Trophic in webshow for patterns investigated Along the DISCUSSION Olff
Accepted potential Article chronosequence onSchiermonnikoog beentestedextensively has salt marsh prevents in variation
et al. et richness along chronosequence the is likelycaused bydifferent
( Pickett 1989
at successional early stages 1997 problem with studies on problemcommunity withstudies assembly current chronosequences is that along continued to in increase changes in changes . While.
; along along the studiedchronosequence ter accumulation ter S chrama, Olff2012 &Berg green web above
; gradi species richnessinthe greenandbrown Mattews 1992
ent in ground predictors ground predictors (
species richness ) were much stronger ) were muchrelated stronger
primary succession, richness richness climatic conditions ed ) may past conditions atolder necessarily reflect not . However, the However, the
an increase fromincrease stagefollowed successional early bya towards the later successional ) . Also, lack the variation topographic on of large vegetati ,
richness belowground predictors belowground predictors ( .
on glaciers andvolcanic substrates
developmen our results showstrikingly different
on diversityandstructure associated
becomes d
to environmental compartment
brown web with t of vegetation patternst ofvegetation along ecoupled from web ecoupled green
in long
in vegetation succession small in differences soil variablessoil and
stages - s
term studies, species species richness
of the food of the factors ) were strongly strongly ) were . Our results . Ourresults driv web. ing .
This article isThis article by protected copyright. All rightsreserved. where wealso We find likely that observedand suggest the chronosequence heightvegetation increase over on chronosequences. measured environmental al. seawater nutrientexternal in systeminput our study substitution. Thisfastsuccession ZemunikLaliberté, 2014 Turner & community assembly were The t designedwere specifically minimize to effects. such below diversity ( Kaufmann2001
Accepted Article 2002 the the chronosequence ime scales relatively short(100 years)
represent ground (soil ground from (soil cores specimens extractedinthe lab) were which
) the highest diversity ofspecies diversity highest inthegreenweb inintermediate the stages successional . Rates of ecological . Ratesofecological maysuccession in mainland higher beeven salt marshes , whereclayaccretionoften Nonetheless, atamuchmany rate. happens faster measurements
found
similar along which studie ) . S pecies
the highest plant highest diversitythe species and For example, ( s Mattews 1992
changes other in primary sequences.succession on (
del Moraldel 1993 variables showvariables similartrends to anddirectional those other in studies whereas whereas d
colonisations areas fromare adjacent often chronosequences along along
food web
changes in , much faster mostthan for studies other on
reflects succession soil organicmatter build
) the amountthe soiland moisturebare soil of c , assumption whichhelps inthe ofspace ; Kaufmann 2001
assembly ; species the the Kaufmann 2001 by . However, . These correspondwith findings ma high rates of high rates
regular flooding withslightlyregular operates alongoperates diversity diversity
; Hodkinson, Coulson & WebbHodkinson, Coulson& 2004 our above
; clay accretion in combination with patterns - WebbHodkinson, Coulson& 2004 up, standing highest our
ground (closed ground (closed traps) along ourchronosequence
vegetation studied a confoundingin factor
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chronosequence chronosequence eutrophicated - successional biomass and for time lear structural ny other ly
decrease ( of the Bakker and
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et et , This article isThis article by protected copyright. All rightsreserved. brownwebcould reactthe much changesinplantdiversity to greenspecies slower than web mechanism brownbetween biomass weband deadplant caused diversity may been by have continuous microbivore studiesnumber ofprevious biomass species richness s Our results expla structural complexity 2012 often showa were mostlycommunities, where doneinnatural structure vegetation andplantspecies richness that astrongstudies report on influence of structure vegetation al. arthropod richness mostInterestingly, that report effect studies a positive ofplant species richness on 1997 richness complexity. uccession,
Accepted Article 1999 ; ; i n van Klink Siemann, Haarstad&Tilman 1999
invertebrate herbivoreinvertebrate species richness
; and ( Siemann, &Haarstad 1999 Tilman Brown & Southwood1983
s. First, First, s. increase in species increase inspecies succession. over richness also without adropwithout andlaterHence, stages. successional thisincrease
Both factorshavebeenshown importantfor tobe explaining richness andrichness belowground predator species richness, wefound a an hump
increase increase in
showed coincides with et al. , were - this pattern could causedthis byatimehave been shaped
(both highestat intermediate pr 2014
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the depththe layer of oxygenated the ) relation ( . Therefore, we Scheu 1996& Schulz brown web a decreaseinplant in diversity,anincrease species ship with ; Brown &Ewel 1987 species richnessspecies ; Hawkins &Porter2003 suggest ; productivity Symstad, Siemann &Haarstad 2000
in webs green ; Carlson
that oductivity and
We both
increases continuously during ( Hawkins Porter 2003 & ;
Steffan et al. et suggest suggest , inagreementwhich is witha
. plant speciesrichness plant
herbivore herbivore -
lag effect, where diversity in where effect, lag 2010 ; - Rickert Dewenter &Tscharntke Dewenter late late that ) . successional age) Especially for Especially the relation the
arthropod arthropod richness herbivor
et in brown web major al.
several several
2012
) e ;
above , dead
Rickert species and and whereas ship ( Knops ) .
plant
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et al.et
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This article isThis article by protected copyright. All rightsreserved. Accepted withline otherstudies that find that vertical stratification of isastrong soils of predictor opportunitiescreating formore toco species vertical stratification of factors soil 2015) has abundances species itshighest inlate successional variation may inanincrease niche in space. result 2012 inanincreaseresult inthe amountniches of may a cause with alongstrongly succession (Schrama al et production. Article C:N corresponding inlitter increase dominant webless may green succession inlate to lead and detritivores atherica Walder coinciding decreaseof (vertebrate) herbivory stages later of succession latestthe stage. successional Second, likely aswevery notobservethe did decrease slightest evenin brownrichness species towards While mechanismdiversity. theoretically this may explain the observed effects
) a high a high C:N . Wethat suggest . Inaddition to the development ofathick belowlitter layer,
, which et al. et could related be toactivity of burrowing the amphipod
Indeed, biomassIndeed, hasbeenpreviously greenwebtrophicgroups to shown of decrease further buildfurther
2000 - ( is ratio Hemminga &Buth1991 of l ) . Late
ow quality and this . This -
r up of alitterlayer.The in increase a low degradation a low rate
stages of burrowing behaviour mayburrowing behaviour awell to lead
may be the to
( - both Moore & Francis 1985 & Moore ratio, ratio, marshsalt we observed
. In our studysystem, vertebrate
) 2012). followed by an increase followed byanincrease matterin dead organic . Ifthishypothesis iscorrect, we wouldpredict that a result invegetationof adecrease qualityanda
- ( occur Berg &Bengtsson 2007 ( Van deKoppel succession succession are
In addition, In addition, ( Berg & StaafBerg & 1980 the developmentthe ofa herbivores ( Berg 2012 mat lower
- ; forming grasses Schrama accumulation of depth
an increase an increase in below leaf and consumption a et al. et often dominated ( , Raynaud Kuijper, NijhoffKuijper, 2004 &Bakker Orchestia gammarellus
ground bioturbation
of the layerlitter - 1996 aerated soil withaerated soil a deeper ;
; et al. et McClaugherty Krab thick ; et al. et Olff
2013
(Schrama al et et al. et
low qu litter layer
, 2013
, wedeem not it et al. et by )
, hence
2010
couch ground niche
1997 may turn in ality ality litter ) et al. et
. in Thisis
; activity activity . This Berg towards towards grass grass ;
. 1985 Van
, E.
) )
, This article isThis article by protected copyright. All rightsreserved. microbialthe community composition. experiments, onfunctional studies genes and/or causalitythe oftheselinksbetween anddiversity function web green mayfunctionally linked be green in the web herbivores recyclingnutrient areassociated with late decomposerbetween diversity andrate ofnutrient (Loreau cycling Wijnen(Van brownin the webtow in areseveral There oversuccession.diversity provideoxygenated soil interpretation. mechanisms stages, successional may diversity whytheoverall web organisms ofbrown explain increases generalist ( important for generalist Yanoviak of community structure soil
Acceptedecosystem Forexample, functioning. Article 2009
Krab, (Kuijper
underlying & Bakker Hence, t ) .
towards latersuccessional stages, sugge et al et O indications that ur results , Nijhoff
despite decreasing species plant diversity. However ards later successional later ards stages coincides increase nutrientwith an in cycling . , he
, 1999) 2013)
detritivores. studiesdetritivores. Other found many have that are detritivores indeed these patterns is needed these patternsneeded is to conclusive yield e explanation simultaneous resultofthe increase in ofthe depth litter layer and the
-
dwelling invertebrates & Bakker 200 & Bakker thus , inthe ,
much
the suggest that a maylarger supply resource beespecially s
sense thatnotsense theyare toasingle related plantThis species.
observed observed in line with theoretical predictions in linewiththeoretical predictions . for theobservedcontinuing increase in
However, we would like tostressHowever, wewouldlike show that, in order to o ur results ur results indicate richness that increase inspecies the - successional, plant species,whichtaller inturnrepell 4 ). Indeed patterns inspecies richness linkedto are studies that ( Berg & Berg & 2007Bengtsson , we observed astrong , weobserved decrease in richness sting changessting brownthat inthe and
,
it isnecessary out tocarry diversity link
observed inrichness observed changes 2001) vidence for this , more research , the into on the relationshipon the
. even in late even in
These changes ; brown web Kaspari & changes changes in
to This article isThis article by protected copyright. All rightsreserved. AcceptedData Accessibility aNWOthrough PIONIERto grant HO they declare have noconflictofinte analyzed on specimens Vorst,Oscar Ping ofcollection the salt We permission Vereniging Natuurmonumentenforgrantingus thank work field forthe onthe Acknowledgements Article andfunctions services Lefcheck can highly detritus dynamicsthe ofbothabove contrasting responses to envi In summary, the NMDSthe marsh - detritivore
the et et al.
of Schiermonnikoog that belong to belong that web green groups vary in impacttheir onecosystemfunction and processes data data our study .
MS, HO and MPB designed theMS, HOandMPBdesigned 2015 data - together FvdP with Ping Janssenfor Chen andMaurice onthe assistance identification of the -
based richness (brown web)species )
. We grateful are PaulBeuk, to TheodoorHeijerman, BerendAukema, , thus stressing the
that highlights that in diversity different partsofthefoodweb exhibit
human we
ground, plant ronmental gradien . We thank also allcolleagues theand friends who helpedduring rest regarding man this ; MS ll - .
being depends on potential - , FvdP,HO andMPB herbivore . Roel van Klink Roel vanKlink is gratefully acknowledged forhelp
t research; s,emphasizing thus importance of our results importance ofour results - based (green web)andbelowground,
simultaneously .
MS out carried the work field
uscript
wrote wrote . Thiswork was the
( Duffy the the .
need fora D ifferent trophicgroups paper for theecosystem
et al. et . T
2007 funded joined study ofjoined study he authors ; ; MS
This article isThis article by protected copyright. All rightsreserved. Fraser, L.H., Pither, J., Jentsc Elton, C.S.(1958) Edwards, J.S. & Edwards Duffy, J.E.,Cardinale, B.J., France, K.E., McIntyre, P.B., Thébault, E. & Loreau, M. (2007) The functional role of del Moral, R. (1993) Mechanismsprimary of succession on volcanoes: a view from Mount Davy, A.J., Brown, M.J.H., Mossman, H.L. & Grant, A.( Crutsinger, G.M.,Rodriguez Connell, J.H. & Slatyer, R.O. (1977) Mechanismssuccession of in natural communities their and rolein community Clements, F.E. (1916) Plant Succession: An Analysis of the development of Vegetation. Chapin, F.S., Walker, L.R., Fastie, C Carlson, M.L., Flagstad, L.A., Gillet, F.& Caballero, M., Baquero, E., Arino, A.H. &Jordana, R. (2004) Indirect biomass estimations in Collembola. Brown, V.K. & Southwood, T.R.E. (1983) Trophic diversity, breadth niche and generation timesexopterygote of Brown, B.J. & Ewel, J.J. (1987) Herbivory inComplex and Simple Tropical Successional Ecosystems. Berg, M.P.,Stoffer, M. & Van denHeuvel, H.H. (2004) Feeding guilds in Collembola based on digestive enzymes. Berg, M.P. & Bengtsson, J. (2007) Temporal spatial and variability insoil food webstructure. Berg, M.P. (2012) Patterns of biodiversity atfineand smallspatial scales. Berg, B. & Staaf, H. (1980) Decomposition rate andchemical changes ofScots pine nee Bakker, J.P.,Esselink, P., Dijkema, K.S., Van Duin, W.E. & de Jong, D.J. (2002) Restoration of salt marshes in the Ausden, M. (2000) Invertebrates. Allan, E.,Crawley, & J. M. (2011) Contrasting effects of Adler, B.,P. Seabloom, Borer, E. W., E. T., Hillebrand, H., Hautier, Y., Hector, A., ... & Bakker, J. D. (2011)
Accepted Article Data are available - long Productivity is apoorpredictor of plant species richness. Science, plant species richness. Bennett, J.A. & Bittel, A. (2015) Worldwide evidence of a unimodal relationship between productivity and Ecology, of a hypothesis. biodiversity inecosystems: incorporatingtrophic Succession on Land 1350 disentangling independent effects ofelevation and redox potential onhalophytes. community assemblages. Fine, P.V. & Rudgers, J.A. (2014)Genetic variation within a dominant shrubstructures green and brown stability organization. and Washi deglaciationat Glacier Bay, Alaska. abiotic factors? chronosequence:above are Pedobiologia, insectsa in secondary succ 108 Pedobiologia, 1804. 136 chemical composition. Netherlands. Cambridge University Press, Jones, G.&Brown, V.K. (1993) Successional trends in insect herbivore population - - ‐ 116. 152. - term fieldexperiment. Ecology letters,
1357. ngton, Washington
Sugg, P. (1993) Arthropod Fallout as aResource inthe Recolonization ofMount St. Helens.
74, Oxford University press The ecology invasions of by animals and plants
954 Hydrobiologia,
48, 48, from Repository: DryadDigital the Journal of Ecology, Oikos, - 958.
551 589 - (eds J. Miles &D.H. Walton). h, h, A., Sternberg,M., Zobel, M.,Askarizadeh, D., Bartha, Beierkuhnlein,S., C., Cabal, M.A., Roddy, A.B.,
- -
Science, 557. 601. Ecological Bulletins 66, Ecological census techniques: A handbook. , USA Ecology,
American naturalist ession. - 463
ground and below .L. &Sharman, L.C.(1994) Mechanisms primary of succession following
478, Cambridge -
. 471. 349,
, Mitchell, E.A.D. (2010)Community development along a proglacial 29
Oecologia,
Oxford 95,
(
98, Ecological Monographs, - 302 Schrama 51.
387
1084 , UK -
305. , UK - 398. , References
14 373 - .
- 1095.
56, , groundcommunity structure controlled more by biotic than , 1246 .
111, Peay, Bastow, K.G., J.L., Kidder, A.G., Dawson, T.E.,
et al. 2016). al.2016). et - 2011) Colonization of a newly developing saltmarsh: insect andmolluscan herbivores onplant diversitya in
390.
complexity. 220
Blackwell, London
1119 - -
1253. 225.
. University Chicago of Press -
1144. http://dx.doi.org/
Ecology letters, 64,
Soil Ecology and Ecosystem Services 149 333 (ed. W.J. Sutherland), pp. 139 - , 1750 , UK 175.
.
- 1753.
10,
dle litter.II. Influence of 10.5061/dryad.s636m Carnegie Institute of
Journal Ecology, of 522 St Helens.
- densities Oikos, - , Chicago, USA 538.
116, Primary - Ecology,
A field test
1789 - 176.
99, . , pp. -
68,
This article isThis article by protected copyright. All rightsreserved. AcceptedMiles,&J. Walton, D.W.H. (1993) McClaugherty, C.A., Pastor, J., Aber, J.D. & Melillo, (1985) J.M. Forestlitter decomposition in relation tosoil Mattews, J.A. (1992) Manning, P., Gossner, M.M., Bossdorf, O., Allan, E., Zhang, Y. Londo, G. (1976) DecimalReleves for Scale ofPermanent Quadrats. Loreau, M. (2001). Microbial diversity, producer Lefcheck, J.S., Byrnes, J.E., Isbell, F., Gamfeldt, L., Griffin, J.N., Eisenhauer, N., Hensel, M.J., Hector, A., Langellotto, G. & Lang, A. (2000)The pitfalls of pitfalls: acomparison of pitfall trap catches andabsolute density estimatesof epigeal Laliberté, E., Zemunik, G.& Turner, B.L. (2014)Environmental filteringexplains variation inplant diversity along Kuijper, D.P.J., Nijhoff, D.J. & Bakker, J.P. (2004) Herbivory an Kruess, A.& Tscharntke, T. (2002) Grazing intensity andthe diversity of grasshoppers, butterflies,and trap Krantz, G.W. & Walter, D.E. (2009) Krab, E. J., Berg, M. P., Aerts,R., van Logtestijn, R. Krab, E.J., Oorsprong, H., Berg, M.P. & ArticleKnops, J.M.H., Tilman, D., Haddad, N.M., Naeem,Mitchell, S., C.E., Haarstad, J.,Ritchie, M.E., Howe, K.M., Kaufmann, R. (2001) Invertebrate Succession onan Alpine Glacier Foreland. Kaspari, M. & Yanoviak, S.P. (2009) Biogeochemistry the structure and of tropical brown food webs. Irmler, U. &Heydemann, B.(1986) Die ÖkologischeProblematik Beweidung der von Salzwiesen am Beispiel der Hutchinson, G.E. (1959) Homage toSanta Hooper, D.U., D.E. Bignell, Brown,V.K. L. Brussaard, J.M. Dangerfield, D.H. Wall, D.A. Wardle, Coleman,D.C. Hodkinson, I.D., Coulson, S.J.& Hemminga, M.A. & Buth, G.J.C. (1991) Decomposition in Salt Marsh Ecosystemsthe S.W. of Netherlands Hawkins, B.A. &Porter, E.E. (2003) Does herbivore diversity depend on plant diversity? The case of California Grime, (1977) J.P. Evidence for theexiste Grime, P.(1973) J. Competitive Exclusion in Herbaceous Vegetation. Nature, 242, 344 Greenstone, M.H. (1984) chronosequences inthe high Arctic. effects of Biotic and Abiotic factors. butterfli evolutionary theory. availability. nitrogen dyn and primary succession of multiple plantandanimal taxa. Boerschig, C. (2015) Grassland management intensification weakens theassociations among the diversities model. Proceedings of theRoyal Society of London B: Biological Sciences, levels and habitats. Cardinale, B.J. &Duffy, J.E. (2015) Biodiversity enhances ecosystemmultifunctionality across trophic meta invertebrate predatorsin arable land. resource gradients. alonga productivity gradient. bees and wasps. 63 subarctic peat bogs changes Collembola diets and decomposition patterns. Soil Biology and Biochemistry, Ecology, disentangling microclimate substrate and quality effects on vertical distribution ofCollembola. outbreaks, insect abundances and diversity. Reich, P.B., Siemann, E. & Groth, J. (1999) Effe 3342 Leybuch Naturalist, patterns, mechanisms, and feedbacks. BioScience, Wolters. (2000) Interactions between aboveground and belowground biodiversityterrestrial in ecosystems: K. E. Giller, P. Lavelle, W.H. v.d. Putten, P.C. d.Ruiter, J. Rusek, W.L. Silver, J.M. Tiedje, and V. , 106 - - analytical synthesis. 3351. - es. 115. t.
Denno, R. (2004) Responses ofinvertebrate natural enemiescomplex to 24,
Nieders. Landesverwaltungsamt,Fachbehörde fürNaturschutz, Hannover.
93, American Naturalist,
Oecologia,
amicslitter and quality. The ecology of recently 1362
145
ConservationBiology, Determinants ofwebspiderspecies diversity: Vegetation structural diversity vs.prey - - 1369. Science, Nature communications, 159. American naturalist
. Cambrigde UniversityCambridge. Press,
62,
Webb, N.R. (2004) Invertebrate community assembly along proglacial Oecologia, Primary succession on land
299 A manual of Acarology 345, Oecologia,
- Cornelissen, J.H.C. (2010) Turning northern peatlands upside down: 304.
161, nce ofthree primary strategies in plantsand its relevance toecological and 1602 - Rosalia, orwhy are there somany kinds animals?of Ecology, Journal Animal of Ecology, declaciated terrain: a geoecological approach to glacier forelands
Ecology Vegetatio, Anzeiger Fur Schadlingskunde
40 139, -
1605. 16, – - ,
decomposerinteractions andecosystem processes: at 49.
141, 111,
1
1570 96, Ecology Letters,
- S., & Cornelissen, J. H. (2013) Vascular plant litter input in
6 , 10.
,
66,
452
1169
1 1492 92,
- - cts of plant species richnessinvasion on dynamics,disease 1580.
7 266 - . 5
459. . Texas Tech Univers 73 0 - - 1194. 1501. ,1049 - - 275. . Blackwell Scientific Publications.
83. -
Y., Pr d competitiond slow downinvasion of atall grass
-
1061 .
Vegetatio, 2, ati, D., Blüthgen, N., Boch, S., Böhm, & S.
286
73,
-
293. - 556 Journal of Pest Science, Ecology,
33, -
ity Press,Lubbock. 568.
61 268
-
– 82, 64. 7. , 303
-
2261 structured habitats: a
- 309. - American 2278.
Ecology,
73, heoretical Functional
99 ‐ - nesting - the 106.
90,
This article isThis article by protected copyright. All rightsreserved. Van de Koppel, Huisman, J., van Bochove, E.,Beauchemin, S. & Theriault, G. (2002) Continuous multiplemeasurement of soil redox potential Tilman, D. (1982)Resource competition and community structure. Symstad, A.J., Siemann, E. & Haarstad, J. (2000) An experimentalthe test of effect of plant functional group Steffan Srivastava, Cardinale,D.S., B.J., Downing, A.L., Duffy, J.E.,Jouseau, C., San Siemann, E., Tilman, & D. Haarstad, J.(1999) Abundance, diversity size: body and patterns from agrassland Siemann, E., Haarstad, J.&Tilman, D. (1999) Dynamics plantand of arthropod diversity during old field Schrama, M.J.J., Schrama, Olff, M.J.J., Schrama,Heijning, M., P., Bakker, J.P., van Wijnen, H.J., Berg, M.P. & Olff, H. (2013) Herbivore trampling as an Scheu, S. &Schulz, E. (1996) Secondary succession, soil formation and developmenta of diversecommunity of Rosenzweig, M.L. (1995) Rickert, C., Fichtner, A., Van Klink, R.Bakker, & J.P. (2012) Alpha andBeta diversity in moth communitiessalt in Remmert, (1983) H. The Wrack R Raynaud, X., Jones,C. G., & Barot, S. (2013)Ecosystem eng Pickett, S.T.A. (1989) Space Olsen, Y.S., Dausse, A., Garbutt, A., Ford, H.,Thomas, D.N. & Jones, D.L. (2011) Cattle grazing drives nitrogen Olff, H. & Ritchie, M.E. (1998) Effects of herbivores on grassla Olff, H., de Leeuw, J.,Bakker, J.P., Platerink, R.J., Van Wijnen, H.J. & Oksanen, J.,Blanchet, F.G., Kindt, R.,Legendre, P., O'Hara, R.B., Simpson, G.L., Solymos, P., M.H.H., S.& Mulder, C., Ahrestani, F.S., Lewis, O.T.,Mancinelli, G., Naeem, Penuelas, S., J., Poorter, H., Reich, P.B.,Rossi, L. Moore, P. &Francis, C.H. (1985) Onthe water relations and osmoregulation oftheBeach Mittelbach, G.G., Steiner, C.F., Scheiner, S.M., Gross, K.L.,Reynolds, H.L., Waide, R.B., Willig, M.R., Dodson
Accepted Core Article - T Dewenter,I. &Tscharntke, T. (1997) Early succession of butterfly and plant communitiesset on project.org/package=vegan W. (2011) Vegan: Community Ecology Package. R package version 1.17 of above & Rusch, G.M. (2013) Connecting the green and brown w 131 gammarellus Ecology, S.I. & Gough, L. (2001) What is the observed relationship betweenspecies richness and productivity? gradient: An empiricaltheoretical and investigation. using platinum microelectrodes. diversity arthropod on diversity. fields. Diversity stronger has top arthropodcommunity. succession. http://dx.doi.org/10.5061/dryad.s636m and brown webs during primary succession ina salt marsh duringsalt marsh succession. 172, alternative pathway for explaining differences in nitrogen mineralization in moist grasslands. oribatids and saprophagous soil macro marshes is driven bygrazing management. The (eds C.J. Smit,DenJ. Hollander, W.K.R.E. van Wingerden & W.J. Wolff), pp.70 Statistical Computing, Vienna, Austria. states oflandscapes. Oikos, Ecology, Approaches andAlternatives and carbon cycling in atemperate salt marsh. 13, elevational gradient. succession and herbivory ina marsh:salt changes induced by sealevelrise andsilt deposition along an eam
261 -
Netherlands 150. 231 (201 Oecologia -
van derPlas, F., 265. - -
82, and below 243. 4 ) R:language A and environment statistical for computing. Ecography,
2381 (Pallas) H. H. & Berg, M.P. (2012) Ecosystem assembly rules:theinterplay of greenand brownwebs
. , Species diversityspac in
- 109, 2396. - - for J., Vander Wal, R.& Olff, H. (1996) Patterns of herbivory along a productivity ground networks Journal of Ecology, Cru
Journal of Animal Ecology, - - 294
beds and theirFauna. 22, Time Substitution as anAlternative toLong
Berg, M.P. stacea: amphipoda. - down than bottom . -
4 302. 122 06 Ecology - , 591
414. Soil Science Society America of Journal, Oikos,
&
- . 600. , -
Advances inEcological Research, (ed. G.E. Likens). Olff, H. invertebrates.
93,
89, http://www.R
85, e and time
2353 Biological Conservation, 243
- 799 Journal of Experimental MarineBiology and Ecology, up effects onup decomposition. Soil Biology & Biochemistry, Terrestrial and freshwater fauna of theWadden Sea, Part 10
- (2016)Data from: - 253. - 2364. 814.
68, . Cambridge University Press ineering, environmental decayenvironmental and
Ecology, Biodiversity Conservation, and -
project.org/. 824 nd plant diversity.
Springer, New York.
orlds. allometric andstoichiometric predictability . Princeton - 835. Dryad Digital Repostitory
77,
De Munck, W. (1997) Vegetation
736 Decoupled diversity dynamicsgreen in
-
University Press, Princeton. Term Studies. 146, karan, M. & Wright,J.P. (2009) -
R Core Team, RFoundation for 745.
-
49 TrendsEcology in & Evolution, 66, 6. 6. 24
Ecology, 43, , http://CRAN.R -
69 31 1813
531 - .
175. - , UK H - - 73. - 1820. Long opper
541.
90, . 5,
. Balkema, Rotterdam
235
1073
-
Term Studies in Orchestia - - 250. - Oecologia, 1083. - aside
94,
H.,
,
, This article isThis article by protected copyright. All rightsreserved. of graphs. the using calculated all modelafter Only selection. fits those that orinclude alinear q (H’)(D C), Shannondiversity composition, respectively gradient. From panels give right,the the leftto total 2. Figure Olffsee years,from 200 last whichwasderived topographic maps thisused in study.Greyshadingsindicatethegradual increaseof island east the tothe over animpressionof Samplegive of thevegetationstructure. site andbrowngreen we study. stageofin this measurements Atevery succession, doneonspeciesdiversity were of The Netherlands. 1.100Figure captionsFigure Van Wijnen, H.J. & Bakker, J.P. (1999) Nitrogenand phosphorus limitation i Van Straalen, N.M. & V Van der Wal, R.,Van Lieshout, S.,Bos, D. & Drent,R.H. (2000) Are spring staging brent geese evic
Accepted Articlean Klink, R., van der Plas, F., van Noordwijk, C., WallisDeVries, M.F. &Olff, H. (2014)Effects of large implications for vegetationsuccession. Journal of Ecology, Seasonal herbivores on grassland arthropod diversity. vegetationsuccession? et al et
Changes in overall diversityChanges in species richness, andevenness alongsuccessio the ., 1997). -
year year saltchronosequence atthemarsh ofthe -
Changes in Age Structure of Soil ArthropodPopulations.
Black dots indicate sampling
Rijninks, P.C. (1982) The Efficiency ofTullgren Apparatus with Respect to Interpreting five b
trophic trophic
sampling perlocation, points withR . From top to bottom, the panels show patterns show richness. Fromto bottom, panels patterns forspecies the (A top Ecography, groups groups aboveand environmental Thepictures variables. t - F) and Pielou’s evenness (E) G
23,
60 - 69. Biological Reviews
locations at every stage at locations ofvegetationsuccession food web, 87
and aerial pic and aerial barrier , 265 . 2
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- - 366 value at the bottomvalue atthe of each were based on AICvalues tures (for furthertures (for details,
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- This article isThis article by protected copyright. All rightsreserved. Acceptedof differents the ofE) ineach trophic indexAge the and groups, ontheShannondiversity (H’). C)NMDSbased richness ineachon species groups, onspecies ofthetrophic evenness B)NMDSbased (Pielou’s 5. Figure perlocation, with points R quadraticthat or include terma linear areshown.Fits in Schrama al. et ofsuccession and stages the late towards succession. redoxH) Soil at2cm potential decrease depth ofpercentage SE)firstshow soilvolume(± succession. livebiomassF) Standing increase increase Vegetation height B) Sediment layer Article standardrepresent ofbare errors. A)Thepercentage SE) soil(± decrease 4. Figure bottom the at of graphs. ofthe each shown. are Fits onAICbased after values model Onlythosefits selection. that includeaquadratic termlinear or trophic groups SE);closed (± brown symbolsindicate SE). groups (± webtrophic (A Each row sho panels 3.DiversityFigure for trop all d , but lev NMDS of plots group trophic diver environmentalChanges in and parameters abiotic over the chronosequence. Bars w for patterns species richness, Shannon evenness (H’)andPielou’s diversity (E). - G) gives forG) gives differentresults a trophicgroup.Open symbolsgreenweb indicate were calculated usingall uccession stages is shown polygonand ingiven each isindicated with a ( els off late towards succession.
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- ease strongly towardssuccession late value atthe bottom eachofthegraphs. of
increase d
again. Panelsagain. A,B, CandG published werepreviously five ed d sity the along gradient.succession A)NMDS based
d sampling pointslocation, per withR with
a strongincrease andagradual decreasingtrend
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E) Litter layerE) Litter increase succession 16cm toabout thick were calculated usingwere calculated all after model Onlythose selection. fits
rds late.G)Soilmoisture as a gradient. From right,the leftto .
D) Standing live biomass d d
d strongly in strongly in the firs
linearly linearly late towards
with succession
five 2 F .
and its its sampling C) were P - value value al age.al t
This article isThis article by protected copyright. All rightsreserved. Accepted Article 1. Figure ground pred: Above ofthein each Closedgreycircles depict graphs. forcentroids ofthe each trophic different color
. Vectors . Vectors indicate different environmental are and proportionally variables scaled
ground predators.
groups: above
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