Stable isotope evidence for mechanisms by which climate-driven variations in phytoplankton growth influence higher trophic levels

Clive N Trueman, Kirsteen M MacKenzie

WESSEX SALMON and RIVERS TRUST

Acknowledgements

Particular thanks to Cathy Cole, Ed Westwood & Mike Bolshaw (UoS), Anton Ibbotson & Bill Beaumont (CEH/GWCT), Andy Moore, Bill Riley & Barry Bendall (Cefas), & Ian Davidson (EA)

Climate effects on high trophic levels

• Physiological mechanisms connecting SST and trophic cascades are less clear

• This hampers prediction of response of plankton and higher trophic levels to future warming (more or less production at higher SST?)

• Here we use high trophic level animals (Atlantic salmon) as natural samplers to probe connections between climate (SST), plankton and higher trophic levels

Stable isotopes in ecology

15N

13C

Primary producer

Primary consumer

Secondary consumer

t-d

Graham et al., 2009

Low growthHigh [CO2]aq

High growthLow [CO2]aq

Laws et al., 1995, Cassar et al., 2005

Atlantic salmon as natural autonomous samplers

• Feed in open ocean and return to natal river

• Occupy waters significantly cooler than growth optimum

• Cultural and economic interest – abundant archives

Apatite

Collagen

Scales as a target for isotope analysis

Hutchinson & Trueman, 2006

© Guy Mawle

W

Last season of marine growth

Fish sample the physiological status of plankton integrated over an 8 month feeding season

N = 235

N = 289

Todd et al 2008

Scales sampled from fish returning to two UK areas…

..sampling marine conditions in feeding grounds

Frome 1SW

Frome MSW

NEC 1SW

NEC MSW

SST

d13C

SSTd13C

Identifying Marine Location

Time TimeTime

d13C

Time

SST

TimeSST

Time

d13C

Unlikely Likely

Results: Feeding areas identified

NECM

NECG

RFG

RFM

• New method to identify location in migratory pelagic fish• Use these results to

investigate SST – plankton relationships in the areas sampled by the salmon

19871988

/[CO2]aq13

C org

-ve

+ve

Low growthHigh [CO2]aq

High growthLow [CO2]aq

All significant relationships between SST and d13C values are negative

As the solubility of [CO2]aq decreases with increasing SST, the negative slope implies either a reduction in mean plankton growth rates, or reduced removal of [CO2]aq with increasing SST

warmer years

colder years

Plankton growth rates and/or production fell with increasing SST in sub arctic N Atlantic

Possibility to predict magnitude of the resposnce of primary production to SST change in a region-specific fashion

Conclusions• Across much of the sub-

arctic NE Atlantic, increases in SST are linked with DECREASES in average phytoplankton growth rate

• Impacts on predictions of fish production in high latitudes under climate warming scenarios

• Fish tissue isotopes may provide an indirect proxy for plankton growth rates

Higher trophic level effects - Temporal (mass standardised) d15N

River Frome: 14 to 15 year cycles Northeast Coast: 7 to 9 year cycles

0 5 10 15

-0.5

0.0

0.5

1.0

Lag

ACF

Series NCMcNTS

0 5 10 15

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

Lag

ACF

Series NCGcNTS

NECG NECM

NECMNECG

Lag (Years) Lag (Years)0 5 10 15

-0.5

0.0

0.5

1.0

Lag

ACF

Series RFMcNTS

0 5 10 15

-0.5

0.0

0.5

1.0

Lag

ACF

Series RFGcNTS

RFG RFM

RFG RFM

Lag (Years) Lag (Years)

Results: Trophic variation and herring

Salmon trophic level (δ15N values) vary with Scottish herring abundance (SSB) for both cohorts of the River Frome population.

ºC dependant

Temporal d13C variation

0 5 10 15

-0.5

0.0

0.5

1.0

Lag

ACF

Series NCGCTS

0 5 10 15

-0.5

0.0

0.5

1.0

Lag

ACF

Series NCMCTS

NECG NECM

NECMNECGNECG

River Frome: 14 to 15 year cycles Northeast Coast: 7 to 9 year cycles

RFMRFG

0 5 10 15

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

Lag

ACF

Series RFMCTS

0 5 10 15

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

Lag

ACF

Series RFGCTS

RFG RFM

Lag (Years) Lag (Years)Lag (Years) Lag (Years)

Salmon - temperature relationship

Complex pattern of positive and negative correlations with SST

Positive Responses Negative Responses

Post smolt growth 1SW growth

Increased size R. Dee returns Decreased size R. Esk

Reduced condition of returns

1SW European returns 2SW Scottish returns

Suggesting differential response to SST in different stocks that likely feed in different regions

Possible direct and indirect effects of changes in SST – indirect effects linked to bottom-up control through SST effects on primary production

(Friedland et al 1993; 1998; 2005; Todd et al., 2008; ICES 2009)

Summary• Spring-summer plankton growth rates appear to fall

with increasing SST in the sub-arctic N Atlantic

• Suggests a mechanism for negative impacts of increased SST on salmon growth via bottom-up control

• Supported by a (weak) relationship between herring SSB and salmon d15N values

• Fish tissues can provide a good record of climate – plankton – ecosystem linkages providing location of feeding is well known