Efectos de la fragmentación del encinar en las interacciones planta‐suelo‐microorganismos Effects of forest fragmentation on the plant‐soil‐microbial interactions TESIS DOCTORAL DULCE YAAHID FLORES RENTERÍA MADRID,JUNIO DE 2015 Memoria presentada para optar al título de Doctor en Ecología por la Universidad Autónoma de Madrid a través del programa de Doctorado en Ecología. Directores: Fernando Valladares Ros Jorge Curiel Yuste Dpto. de Biogeografía y Cambio Global Museo Nacional de Ciencias Naturales (MNCN‐CSIC) Ana Rincón Herranz Dpto. de Protección Vegetal Instituto de Ciencias Agrarias (ICA‐CSIC)
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Habitat Fragmentation can Modulate Drought Effects on the Plant‐soil‐microbial System in Mediterranean Holm Oak (Quercus ilex) Forests. Microbial Ecology 69(4): 798-812 (2015). doi: 10.1007/s00248‐015‐0584‐9. http://hdl.handle.net/10261/128289
Estetrabajohasidorealizadograciasalafinanciación proporcionada por losproyectosVULGLO (CGL201022180C0303),MyFUNCO(CGL2011‐29585‐C02‐02)y VERONICA (CGL2013‐42271‐P) delMinisterio de Economía ycompetitividad; REMEDINAL 3‐CM (ref.S2013/MAE‐2719) de la Comunidad deMadrid. Así como al Programa debecarios en el extranjero del ConsejoMexicano de Ciencia y Tecnología(CONACyT)delgobiernodeMéxico.
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El capítulo IV de la tesis doctoral: FLORES-RENTERÍA, Dulce. Efectos de la fragmentación del encinar en las interacciones planta‐suelo‐microorganismos = Effects of forest fragmentation on the plant‐soil‐microbial interactions (2016, está publicado en: Flores‐Rentería, D., J. Curiel Yuste, A. Rincón, F. Brearley, J. García‐Gil and F. Valladares (2015). Habitat Fragmentation can Modulate Drought Effects on the Plant‐soil‐microbial System in Mediterranean Holm Oak (Quercus ilex) Forests. Microbial Ecology 69(4): 798-812 (2015). doi: 10.1007/s00248‐015‐0584‐9. http://hdl.handle.net/10261/128289
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The chapter IV of the thesis: FLORES-RENTERÍA, Dulce. Effects of forest fragmentation on the plant‐soil‐microbial interactions = Efectos de la fragmentación del encinar en las interacciones planta‐suelo‐microorganismos (2016), is published in: Flores‐Rentería, D., J. Curiel Yuste, A. Rincón, F. Brearley, J. García‐Gil and F. Valladares (2015). Habitat Fragmentation can Modulate Drought Effects on the Plant‐soil‐microbial System in Mediterranean Holm Oak (Quercus ilex) Forests. Microbial Ecology 69(4): 798-812 (2015). doi: 10.1007/s00248‐015‐0584‐9. http://hdl.handle.net/10261/128289
Published in: Flores‐Rentería, D., J. Curiel Yuste, A. Rincón, F. Brearley, J.García‐Gil and F. Valladares (2015). Habitat Fragmentation canModulateDroughtEffectsonthePlant‐soil‐microbialSysteminMediterraneanHolmOak(Quercus ilex)Forests.MicrobialEcology:1‐15.doi:10.1007/s00248‐015‐0584‐9
Table4.1.Physicochemicalcharacteristicsofsoilsfromtwoclimaticallydifferentregions and two fragment sizes of holm oak forest in Spain. Data = mean (SE)(n=12). The effect of factors is summarized on the left of the table. SOM = soilorganic matter; CEC=cation exchange capacity. Significant differences (P<0.05)betweenmaineffectsareindicatedwithcapital letters(amongregion)andlowercaseletters(amongfragmentsize).
Similarly,significant interactionsbetweencondition, regionand fragment
size were observed for bacterial richness and between condition and
region forbacterialdiversity (Table S4.3).Both interactions showedvery
similarpatterns: a significantdecreaseofbacterial richnessanddiversity
during drought, and a partial recovery after rewetting (Fig. 4.1d and e),
beenmoreevidentinsoilsfromthenorthernregion.
Northern region Southern region
Large
fragment
Small
fragment
Large
fragment
Small
fragment
Fragment
effect
Water holding capacity (%) 40.1A,b
(2.4)
49.8A,a
(2.2)
38.9A,b
(0.9)
45.2A,a
(1.6)
CEC (cmolcKg-1) 26.5A,b
(4.3)
39.5A,a
(3.2)
27.6A,b
(1.5)
35.7A,a
(2.3)
Mg2+ (cmolcKg-1) 1.4A,b
(0.1)
2.5A,a
(0.2)
1.6A,b
(0.1)
3.1A,a
(0.5)
Ca2+ (cmolcKg-1) 24.2A,b
(4.1)
35.6A,a
(2.9)
24.5A,b
(1.4)
30.5A,a
(1.8)
Na+ (cmolcKg-1) 0.04A,b
(0.004)
0.07A,a
(0.01)
0.05A,b
(0.003)
0.07A,a
(0.01)
SOM (%) 12.1A,b
(1.9)
19.8A,a
(2.4)
10.3B,b
(0.7)
14.1B,a
(1.8)
N organic (%) 0.4A,b
(0.1)
0.8A,a
(0.1)
0.3B,b
(0.02)
0.5B,a
(0.1)
Region
effect
P2O5 (mg Kg-1) 13.8A,b
(1.0)
34.4A,a
(4.2)
2.5B,b
(0.4)
16.5B,a
(1.7)
K+ (cmolcKg-1) 0.9B,b
(0.14)
1.7B,a
(0.1)
1.5A,b
(0.1)
2.0A,a
(0.1)
pH 7.1B,a
(0.3)
7.3B,a
(0.1)
7.9A,a
(0.04)
7.9A,a
(0.03)
Aggregate stability (%) 56.9A,a
(3.1)
57.1A,a
(4.0)
47.8B,a
(3.7)
49.1B,a
(2.9)
Microbial biomass
(mg C kg -1)
1013.4a
(6 6.9)
625.1b
(96.7)
621.6b
(29.6)
725.4ab
(41.3)
HABITAT FRAGMENTATION CAN MODULATE DROUGHT EFFECTS
140
Fungal evenness increased significantly with drought (Fig. 4.1c), while
Figure4.1Responseofrichness,Shannondiversityandevennessoffungal(a,b,c)andbacterial(d,e, f)communitiesofsoils fromtwoclimaticallydifferentregionsandtwofragmentsizesofHolmoakforestsinSpain,toexperimentalsimulationofdrought and rewetting. Grey/white bars represent large/small fragments,respectively. Open/filled bars represent the northern or the southern regionrespectively.Data=mean±SE.Significantdifferencesgivenbypost‐hocmultiplecomparisonsbyTukey’stest(P<0.05)ofthethree‐wayANOVAareindicated:maineffects by capital letters (among condition) and significant interaction betweenfactorsbylowercaseletters(tripleinthecaseofa,bandd;conditionxregioninthecaseofeandf;seeTableS4.3).
in soils from small fragments (Table S4.3). Additionally, a significant
interactionbetweenconditionandregionwasobserved,whereactivity in
soils from the northern region decreased significantlywith drought (Fig.
4.3b); whereas activity in soils from the southern region remained very
similarduringtheexperiment.
HABITAT FRAGMENTATION CAN MODULATE DROUGHT EFFECTS
142
Figure4.2Principalcomponentanalyses(PCA)forsoilfungal(a)andbacterial(b)communities of soils from two climatically different regions and two fragmentsizes of holm oak forests in Spain, and exposed to experimental drought andrewetting simulations. Soil treatments are represented by different symbols:circles = large fragments from the northern region; inverted triangles = smallfragmentsfromthenorthernregion;squares=largefragmentsfromthesouthernregion; diamonds = small fragments from the southern region. Simulatedexperimentalconditionsarerepresentedbydifferentcolours:white=pre‐drought(Pre‐Dro);grey=drought(Dro);black=rewetting(Rew).Errorbars=SE.
PC 1 (17.4%)
-8 -6 -4 -2 0 2 4 6
PC
2 (
15.8
%)
-8
-6
-4
-2
0
2
4
6
8PC 1 (11.4%)
-10 -8 -6 -4 -2 0 2 4 6
PC
2 (
9.2
%)
-8
-6
-4
-2
0
2
4a)
b)
N Large-DroN Small-DroS Large-DroS Small-Dro
N Large-RewN Small-RewS Large-RewS Small-Rew
N Large-Pre-DroN Small-Pre-DroS Large-Pre-DroS Small-Pre-Dro
HABITAT FRAGMENTATION CAN MODULATE DROUGHT EFFECTS
144
Figure4.3Enzymaticactivities:urease(a)andphosphatase(b)ofsoilsfromtwoclimaticallydifferentregionsandtwofragmentsizesofholmoakforestsinSpain,andexposedtoexperimentaldroughtandrewettingsimulations.Grey/whitebarsrepresent large/small fragments respectively. Open/filled bars represent thenorthern or the southern region, respectively. Data = means ± SE. Significantdifferencesgivenbypost‐hocmultiplecomparisonsbyTukey’stest(P<0.05)ofthethree‐way ANOVA are indicated: main effect of fragment size in phosphataseactivity (not represented), and significant interaction between factors by lowercase letters (triple in the case of urease; condition x region in the case ofphosphatase;seeTableS4.3).
Netecosystemexchangeinplant‐soil‐microbialsystem
In the plant‐soil‐microbial system, themain component of net ecosystem
Figure 4.4 CO2 fluxes of the plant‐soil‐microbial system of soils from twoclimaticallydifferentregionsandtwofragmentsizesofHolmoakforestsinSpain.Ecosystem respiration (a) and Gross primary productivity (b) both in droughtsimulation,andecosystemrespirationinrewettingsimulation(c),where0meansimmediately before rewetting. Grey/white bars represent large/small fragmentsrespectively. Open/filled bars represent the northern or the southern region,respectively.Data=means±SE.Significantdifferencesgivenbypost‐hocmultiplecomparisonsbyTukey’stest(P<0.05)ofthethree‐wayANOVAareindicated:maineffects by capital letters (among condition) and significant triple interactionbetweenfactorsbylowercaseletters(conditionxregionxfragmentsize,seeTableS4.4andS4.5).
Days of droughtPre-drought 18 36 55
mol
CO
2 m
-2 s
ec-1
-4
-3
-2
-1
0Days of drought
Pre-drought 18 36 55
mol
CO
2 m
-2 s
ec-1
0
2
4
6
8
10
12
14
Hours since rewetting0 3 24 48
mol
CO
2 m
-2 s
ec-1
0
2
4
6
8
10
N Large N Small S Large S Small
c)
a)
a a a
bb b
b
b bb
b
ba
bb
b
aa
b)
bbbc bc
bc
cd d dcd
e
ff
f
cd
A
B
AB
C
HABITAT FRAGMENTATION CAN MODULATE DROUGHT EFFECTS
Bacterial community structure (i.e. PC1 of bacterial PCA; Fig. 4.2b) was
positively correlated with Reco and urease activity (Table 4.4). Bacterial
richness and diversity were also correlated with Reco and phosphatase
activity(Table4.4).
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Table4.3.Seedlinggrowthandphysiologyduringdroughtsimulationinsoilsfromtwo climatically different regions and two fragment sizes of holm oak forest inSpain.Data=mean (SE) (n=7 for southern large andnorthern small fragments,andn=8forsouthernsmallandnorthernlargefragments).Significantdifferences(P<0.05)areindicatedwithcapitalletters(amongregionforagivenfragmentsize)andlowercaseletters(amongfragmentsizeforagivenregion).
HABITAT FRAGMENTATION CAN MODULATE DROUGHT EFFECTS
148
Figure 4.5 Relationships between Ecosystem Respiration (a), Gross PrimaryProductivity(b)andsoilmoisturefromtwoclimaticallydifferentregionsandtwofragmentsizesofholmoakforestsinSpainexposedtoexperimentaldroughtandrewettingsimulations.Soiltreatmentsarerepresentedbydifferentsymbols:greycircles = large fragments from the northern region; white inverted triangles =smallfragmentsfromthenorthernregion;greysquares=largefragmentsfromthesouthernregion;whitediamonds=small fragmentsfromthesouthernregion.R2andPvaluesofsimplelinearregressionsarepresented.
Soil moisture (%)
10 20 30 40 50
GP
P (m
ol C
O2
m-2
sec
-1)
-8
-6
-4
-2
0
Rec
o (m
ol C
O2
m-2
sec
-1)
0
2
4
6
8
10
12a)
b)N LargeR2=0.032, p>0.05
N SmallR2=0.022, p>0.05
S LargeR2= 0.011, p>0.05
S SmallR2= 0.105, p>0.05
N LargeR2=0.41, p<0.0001
N SmallR2=0.31, p=0.002
S LargeR2= 0.36, p=0.002
S SmallR2=0.40, p<0.0001
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Table 4.4. Correlations between soil functioning and soil moisture, fungal andbacterial diversity in soils from two climatically different regions and twofragment sizes of holm oak forest in Spain. Data were analysed by Pearson’scorrelation (n=36) and significant effects are noted in bold (*<0.05; **< 0.01;***<0.001).Reco= ecosystem respiration; PC1= first component and PC2= secondcomponentofPrincipalComponentAnalysis(PCA).For the fullcorrelationTableseeTableS4.7.
Table4.5. Relationships between fungal and bacterial community structure andexplanatoryphysicochemicalsoilvariablesinsoilsfromtwoclimaticallydifferentregionsandtwofragmentsizesofholmoakforestinSpain.Datawereanalysedbystepwisemultipleregression(t‐test)andsignificanteffectsusingcorrectedP‐value(sequentialBonferronimethod)arenoted inbold(n=36);n.s.notsignificant.β=standardizedcoefficient.SOM=soilorganicmatter.
Figure4.6Schematicoverviewofsimultaneousvariationsinfungalandbacterialrichness, soil moisture, ecosystem functioning and their modulation thoughfragmentsize,assuggestedbytheresultsofthepresentstudy.
Bacterial richness
Fungal richness
Large fragmentSouthern region
Small fragmentSouthern region
Large fragmentNorthern region
Small fragmentNorthern region
Soil moisture HighLow
Ecosystem function HighLow
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Our results, therefore, suggest that the drier conditions expected in the
future for the already water limited Mediterranean basin will favour
HABITAT FRAGMENTATION CAN MODULATE DROUGHT EFFECTS
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FigureS4.1Schemaof the chamberused formeasuringCO2 fluxesof theplant‐soil‐systeminMediterraneanholmoakforestsfragments,showingtheconnectionswiththeEGM‐4ofPP‐systems®.Theframeofthebottomandtopofthechamberweremade of acrylic, and connectedwith aluminium rods.Walls weremade of“NRS90 clear” polyester film of 75 μm thickness (Llumar®, Martinsville, USA).Arrowsindicatetheairflowinsidethechamber.
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Figure S4.2 Water content in the plant‐soil‐system during the experimentaldroughtfromtwoclimaticallydifferentregionsandtwofragmentsizesofholmoakforestinSpain.Differentsymbolsrepresentdistinctsoiltreatment:circles=largefragments from northern region; inverted triangle = small fragments fromnorthern region; squares = large fragments from southern region; diamonds =smallfragmentsfromsouthernregion.Errorbars=SE(n=7forsouthernlargeandnorthernsmallfragments,and8forsouthernsmallandnorthernlargefragments).
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TableS4.2Soilmoistureandseedlingresponseduringdroughtsimulationtothefactorsregionandfragmentsizeinsoilsfromtwoclimaticallydifferentregionsandtwo fragment sizesof holmoak forest in Spain.Datawere analysedby repeatedmeasures analysis of variance (n= 7 for southern large and northern smallfragments, and n= 8 for southern small and northern large fragments) andsignificanteffectsarenotedinbold(*<0.05;**<0.01;***<0.001).
Region(R) Fragment
size (F)
R x S Drought (D) D x R D x F DxRxF
Soil moisture F 24.21 45.71 3.7 291.95 8.11 3.73 0.94
P <0.001*** <0.001*** 0.065 <0.001*** <0.001*** <0.001*** 0.49
Fv/Fm predawn F 0.553 0.556 1.586 12.880 0.394 0.581 1.663
P 0.464 0.463 0.219 <0.001*** 0.758 0.629 0.182
Fv/Fm midday F 0.794 0.366 1.737 23.342 0.386 1.825 1.877
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Reco rewetting
Time (T) P <0.001***
F 200.55
Region (R)
P <0.001***
F 104.82
Fragment size (F)
P <0.001*** F 25.43
T x R
P <0.001*** F 8.45
T x F
P 0.258F 1.37
R x F
P 0.821 F 0.05
T x R x F
P 0.038* F 2.39
Reco GPP
Drought time (Dt) P <0.001*** <0.001***
F 48.86 14.19
Region (R) P <0.001*** 0.76 F 62.12 0.09
Fragment size (F) P <0.001*** 0.739 F 71.88 0.11
Dt x R
P 0.505 0.172F 0.79 1.69
Dt x F
P 0.537 0.319 F 0.73 1.18
R x F
P <0.001*** 0.287 F 25.43 1.15
Dt x R x F
P 0.609 0.399 F 0.611 0.99
Table S4.4 Ecosystem respiration and Gross Primary productivity responses tocondition(C=drought simulationandrewetting), region (northernandsouthern)andfragmentsize(largeandsmall),insoilsfromtwoclimaticallydifferentregionsandtwofragmentsizesofholmoakforestinSpain.Significanteffectsofthethree‐way ANOVA (n=120) are noted in bold (*<0.05; **< 0.01; ***<0.001). Reco=ecosystemrespiration;GPP=GrossPrimaryProductivity.
Table S4.5 Ecosystem respiration responses to time (T=3, 24 and 48 hrs afterrewetting),region(northernandsouthern)andfragmentsize(largeandsmall),insoils from two climaticallydifferent regionsand two fragment sizesof holmoakforestinSpain.Significanteffectsofthethree‐wayANOVA(n=90)arenotedinbold(*<0.05;**<0.01;***<0.001).Reco=ecosystemrespiration.