Seaweed meadows in the light of global climate change

Introduction Distributional changes Acclimation Adaptation Overall conclusions

Seaweed in the light of global climate change

Alexander [email protected]

Marine Ecology Research GroupFaculty of Biosciences and Aquaculture

University of NordlandNorway

53rd NEAS SymposiumAlgae as Model Systems

27.04.2014

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Contributors

Galice Hoarau

Irina Smolina

Jorge Fernandes

James A. Coyer

Spyros Kollias

Jeanine L. Olsen

Heroen Verbruggen Lennert TybergheinHavkyst projects: 196505, 203839, 216484

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CO2 increase since the industrial revolution

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Recent land and ocean warming

Christiansen, J.; Scientific American (2013)

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Climate change responses

..

Temperaturerise

.

Heat waves

.

Seasonalityshi

.

Oceanacidifica on

.

Migra on

.

Acclima on

.

Adapta on

.Species

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High sensitivity of intertidal species

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Seaweeds as model systemsto investigate climate change

Seaweeds provide an excellent system to investigate climate changeimpact

Intertidal key species

Distribution directly limited by temperature tolerance

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Seaweeds are key species in temperateNorth Atlantic regions

© Hoarau, G., 20108 / 60


Seaweeds are key species in temperateNorth Atlantic regions

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Temperate seaweed distribution limited by the10℃ summer and the 20℃ winter isotherm

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Range shifts of seaweeds in response to SST-shifts cantrigger major ecological changes

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Recent warming in the North Atlantic

Shift of the 15°C isotherm330 km north

1985 2000

[McMahon & Hays, 2006; Global Change Biol.]

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Predicted northward shift of SST isotherms

Poleward migration of SST isotherms underIPCC scenario A2 until 2100:

30-90 km/decade along North Atlantic shores

[Hansen et al., 2006; PNAS]

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Predicting seaweed range shifts under climate change

..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed

Predominant seaweeds in the North-Atlantic

Fucus serratus Fucusvesiculosus

Ascophyllumnodosum

Shores with biggest ecological change?

Assemblage shift?

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Ecological Niche ModelingPresent-day conditions

Bio-ORACLE database[Tyberghein et al., 2011; Global Ecol. Biogeogr.].

Georeferenced Occurrences

DA (m−1)SST (℃)

SAT (℃)

Ecological Niche Model (Maxent [Phillips et al., 2006; Ecol. Model.])

2000 2100 ? 2200 ?15 / 60


Ecological Niche ModelingPresent-day conditions

Bio-ORACLE database[Tyberghein et al., 2011; Global Ecol. Biogeogr.].

Georeferenced Occurrences

DA (m−1)SST (℃)

SAT (℃)

Ecological Niche Model (Maxent [Phillips et al., 2006; Ecol. Model.])

2000 2100 ? 2200 ?CO2 emission scenario changes

SST (℃)SAT (℃)

SST (℃)SAT (℃)

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Predicted Niche ShiftsBased on the intermediate IPCC scenario A1B

[Jueterbock et al., 2013; Ecol. Evol.]

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Habitat gain in the Arctic


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Habitat loss in warm temperate areas


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Predominant seaweeds shift northward as anassemblage

West-Atlantic East-Atlantic

F. serratus F. vesiculosus A. nodosum[Jueterbock et al., 2013; Ecol. Evol.]

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Conclusions from prediced niche shifts

..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed

Biggest ecological change inwarm temperate and Arctic areas

Assemblage shift

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..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed


Assemblage shift

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Colonization of Arctic shores

The poleward shift of temperate intertidal seaweeds depends onthree key factors

Dispersal and invasive potentialDark periodCompetitive interactions

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Dispersal and invasive potentialLow dispersal of juvenile stages in fucoid algae

[Braune, 2008; Meeresalgen]

♂ ♀ dioecious

zygote dispersal: <10m

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Dispersal and invasive potential

Flotation vesiclesFucus vesiculosus

Ascophyllum nodosumlow invasive potential

Shipping transport

Fucus serratus

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Dispersal and invasive potentialShipping transport introduced F. serratus to Canada

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Dark period

Poleward shift of Laminaria hyperborea in progress

[Müller et al., 2009; Bot. Mar.]

Recent records

Hiscock, K.

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Competitive interactions

Fucus distichus predominates the Arctic intertidal

Habitat suitability ofF. distichus

based on ENM [Smolina, I., 2012]

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Competitive interactions

[Smolina, I., 2012]

Increase of sympatryzones/hybridization

Competition

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..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed


Assemblage shift

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Climate change impact also on subtidal kelp

[Raybaud et al., 2013; PLOS ONE]

Percentage of models forecasting adisappearance of Laminaria digitata

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Ecological Niche Models neglect biotic interactions

Ecological Niche Models do not takebiotic interactions into account

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Biotic interactionsIncreasing mussel recruitment due to rising sea temperatures

replaces rockweed (A. nodosum) beds in Canada

[Ugarte, 2009; J. Appl. Phycol.]

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Biotic interactionsGrazing pressure

[Harley et al., 2012; J. Phycol]31 / 60


Biotic interactionsGrazing pressure

[Harley et al., 2012; J. Phycol]31 / 60


Ecological Niche Models neglect species responses

Ecological Niche Models do not takethe plastic or adaptive potential

of species into account

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Adapta on

.Inter dalseaweed

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Acclimation potential of Fucus serratus

..

Migra on

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Acclima on

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Adapta on

.Fucusserratus

Local thermal adaptation?

Areas under highest extinction risk?

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Common-garden heat stress experiments

Norway

Denmark

BrittanySpain

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Norway

Denmark

BrittanySpain

Bodø

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Norway

Denmark

BrittanySpain

Bodø

Acclimation at 9℃

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Common garden heat stress experiments

Heat stress, > 6 ind./pop

MeasurementsPhotosynthetic performancehsp gene expression (hsp70, hsp90, shsp)

1h Stress 24h Recovery

9℃

20℃24℃28℃32℃36℃

T (°C)

Time

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Photosynthetic performance

0 4 8 12 16 20 24 28 32 36 ℃

NorwayDenmarkBrittanySpain

Thermal range in year 2200

Measured response

1

1. Performancein 2200

2

2. Resilience

[Jueterbock et al., 2014; Mar. Genomics]36 / 60



0 4 8 12 16 20 24 28 32 36 ℃



Measured response

1


2

2. Resilience




0 4 8 12 16 20 24 28 32 36 ℃



Measured response

1


2

2. Resilience




0 4 8 12 16 20 24 28 32 36 ℃



Measured response

1


2

2. Resilience




0 4 8 12 16 20 24 28 32 36 ℃



Measured response

1


2

2. Resilience



Heat shock responseConstitutive shsp gene expression before heat shock

23 weeks acclimation

7 weeks acclimation

Normalize

dexpressio

n

High constitutivestress

Norway

DenmarkBrittanySpain

Heat shock response of shsp gene expression after 24h recovery

Fold

change

Reducedresponsiveness

Norway


[Jueterbock et al., 2014; Mar. Genomics] 37 / 60


Heat shock responseConstitutive shsp gene expression before heat shock

23 weeks acclimation

7 weeks acclimation

Normalize

dexpressio

n

High constitutivestress

Norway


Heat shock response of shsp gene expression after 24h recovery

Fold

change

Reducedresponsiveness

Norway


[Jueterbock et al., 2014; Mar. Genomics] 37 / 60


ConclusionsAcclimation

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Acclima on

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Adapta on

.Fucusserratus

Local thermal adaptation

Areas under highest extinction risk?

Brittany and Spain

Confirms predicted habitat loss


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Ribadeo, Spain © Coyer, J.A., 1999[Jueterbock et al., 2013; Ecol. Evol., Fig. S6]

1999: extensive F. serratus meadows

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Ribadeo, Spain © Jueterbock, A., 2010[Jueterbock et al., 2013; Ecol. Evol., Fig. S6]

90% abundance decline in 11 years

[Viejo et al., 2011; Ecography]

Dwarf forms withreduced reproductivecapacity in Spain

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Threatened refugial populations

Ice cover during the Last Glacial Maximum (18-20 kya)

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Genetically diverse refugia under threatFucus serratus

Glacial refugia identified by mtDNA haplotype diversity[Hoarau et al., 2007; Mol. Ecol.]

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Genetically diverse refugia under threatFucus serratus

[Hoarau et al., 2007; Mol. Ecol.]42 / 60


Genetically diverse refugia under threatChondrus crispus

Based on mitochondrial SNPs

[Provan & Maggs, 2012; Proc. R. Soc. London, Ser. B]

180 km retreat since 1971from a Portuguese refugium

Interglacial distribution

Glacial distribution

Stable refugiumunder threat

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Remaining key question

Can ancient refugial populationsadapt to climate change

orwill temperate seaweeds

lose their centers of genetic diversity?

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Adaptation

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Effective population size Ne? Genetic changes (past 10 yrs)?

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Sampling scheme (50–75 ind./pop)

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes

1 decadeof selection

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Methods and analysis

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes


Genotyping31 microsatellite markers (20 EST-linked)

AnalysisEffective population size (Ne)Allelic richness (α)Temporal outlier loci

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Methods and analysis

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes




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Effective population size NeReflecting adaptive capacity

∼ 2000 ∼ 2010

18

6320723

Norway


32

6121026

Estimates excluding outlier loci

[Jueterbock, 2013; PhD Thesis]

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Methods

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes




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Changes in allelic richness

∼ 2000 ∼ 2010

3.1

4.68.04.0

Norway


3.3

4.87.94.6

Significantdecline


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Methods

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes



AnalysisEffective population size (Ne)Allelic richness (α)Genetic differentiation (Dest)Temporal outlier loci

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Temporal outlier loci indicate selective sweeps

Before Selection After Selection

Selective Sweep

based on [Vitti et al., 2012; Trends in Genetics]

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Outlier loci

Temporal outlier loci

0%

6%23%13%

Norway


Strongest selection pressure in the SouthAdaptive to climate change?


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ConclusionsAdaptation

..

Migra on

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Acclima on

.

Adapta on

.Fucusserratus

Adaptive responsivenesshighest in Brittany

and likely insufficient in Spain

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Fucus in the tree of lifedistantly related to other taxa

The genome of Ectocarpus siliculosus is sequenced but Fucalesand Ectocarpales diverged in the Cretaceous (ca. 125 Ma)

[Cock et al., 2010; Nature]

De novo Fucus vesiculosus genome until 2017, part of IMAGOMarine Genome project (University of Gothenburg, Sweden)

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Summary

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Highest responsivenessin Brittany

Adaptive value re-mains unknown

Seaweed meadows:Loss in warm-

temperate regionsArctic invasion?

Ancient refugiaunder threat:

stress in BrittanyExtinction risk in Spain

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Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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Overall conclusionSeaweeds as model systems to investigate climate change

Seaweeds provide an excellent system to investigate climate changeimpact on North Atlantic rocky shores

Intertidal key speciesDistribution directly limited by temperature toleranceAnnotated genome of Fucus sp. needed (IMAGO)

Remaining key question: Adaptation or extinction in geneticallydiverse ancient glacial refugia?

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