EFFECT OF LIGHT REGIME ON THE SEASONAL CYCLE

OF ANTARCTIC KRILL Flavia Höring Mathias Teschke, Fabio Piccolin, Lavinia Suberg, Felix Müller, So Kawaguchi, Bettina Meyer

3rd International Symposium on Krill, St. Andrews, Scotland Ecosystems: why are krill so successful? 14 June 2017

Why are krill so successful?

The Southern Ocean – a strongly seasonal habitat

Sea ice extent Primary production Photoperiod

Meyer 2012 Meyer et al. 2010 NASA Earth Observatory maps by Joshua Stevens, using AMSR2 data supplied by GCOM-W1/JAXA.

Spring Summer Seasonal and interannual variability

Autumn 2004 Autumn 2005 Autumn 2006

2

Seasonal rhythms in E. superba

Lipid dynamics

Maturation cycle

Respiration Meyer 2012

Meyer 2012

Latitudinal differences: Ø  Lower lipid stores and

higher feeding activities observed at lower latitudes in winter

Kawaguchi et al. 2006

How are these rhythms modulated?

3

r

al

n

m

XII

VI

IIIIX

Biological timing in E. superba

What do we know? •  Photoperiod has an impact on: > Maturity

> Body composition > Respiration rate > Gene expression

•  Clock genes and an endogenous timing system in Antarctic krill

INPUT OUTPUT

Light

Food

Rhythms

The concept of biological clocks

Internal Oscillator

Short-term studies only

4

Aim of the study

Research objectives:

Ø Investigation of the effect of different latitudinal light regimes on the phenology of E. superba

1) Growth 2) Maturity 3) Lipid metabolism 4) Gene expression

Ø Long-term lab experiments over 2 years with constant food supply

Hypotheses: I.  Light regime triggers seasonal

rhythms in Antarctic krill.

II.  Seasonal rhythms are maintained by an endogenous timing system.

5

0 2 4 6 8 10 12

05

1015

20

Simulated light regimes

Month

Hou

rs o

f lig

ht

52°S

62°S

66°S

DD

Long-term lab experiments

Light regime 52°S

Light regime 62°S

Light regime 66°S

Constant darkness

(DD)

Australian Antarctic Division, Kingston, Tasmania

Experimental set-up Recorded data

Ø  Carapax length Ø  Gender and sexual maturity

stage

Thorax

Thelycum (female)

Petasma (male)

Photos: Fabio Piccolin

Hypothesis I: Light regime triggers seasonal rhythms in Antarctic krill.

Hypothesis II: Seasonal rhythms are maintained by an endogenous timing system.

6

Growth Generalized additive mixed model (GAMM):

Carapax length ~ General trend + Seasonal trend

General trend

5 10 15 20

−11

3

Treatment 52°S

Experimental duration[months]

5 10 15 20

−11

3

Treatment 62°S

Experimental duration[months]

5 10 15 20−1

13

Treatment 66°S

Experimental duration[months]

5 10 15 20

−11

3

Treatment DD

Experimental duration[months]

Car

apax

leng

th *** p<0.001 *** p<0.001 *** p<0.001 *** p<0.001

Similar trend in all treatments:

Ø  Shrinkage in beginning of experiment – related to experimental conditions

0 2 4 6 8 10 12

05

1015

20

Simulated light regimes

Month

Hou

rs o

f lig

ht

52°S

62°S

66°S

DD

7

Seasonal trend

2 4 6 8 10 12

−11

3

Treatment 52°S

Month

Car

apax

leng

th

2 4 6 8 10 12

−11

3

Treatment 62°S

Month

2 4 6 8 10 12−1

13

Treatment 66°S

Month

2 4 6 8 10 12

−11

3

Treatment DD

Month

0 2 4 6 8 10 12

05

1015

20

Simulated light regimes

Month

Hou

rs o

f lig

ht

52°S

62°S

66°S

DD

Growth

*** p<0.001 *** p<0.001 *** p<0.001 p=0.0533

Generalized additive mixed model (GAMM):

Carapax length ~ General trend + Seasonal trend

Similar trend in all treatments:

Ø  Seasonal trend observed in all treatments – influenced by light regime

Ø  Rhythmic pattern under constant darkness – Indication for an endogenous seasonal timing system

summer autumn winter spring summer autumn winter spring summer autumn winter spring summer autumn winter spring

8

Maturity analysis

5 10 15 20

Males

Hours of light

Mat

urity

sco

re

23

45

5 10 15 20

Females

Hours of light

Mat

urity

sco

re

23

45

9

Relationship between maturity and photoperiod:

Ø  Different pattern in females and males

Ø  Further maturity analysis carried out with females only

Differences between females and males

2 4 6 8 10 12

−0.2

0.0

0.2

Treatment 52°S

Month

Mat

uri

ty s

core

2 4 6 8 10 12

−0.2

0.0

0.2

Treatment 62°S

Month

2 4 6 8 10 12−0

.20.

00.

2

Treatment 66°S

Month

2 4 6 8 10 12

−0.2

0.0

0.2

Treatment DD

Month

Generalized additive model (GAM):

Maturity score ~ Seasonal trend

Maturity analysis

** p<0.01 *** p<0.001 ns p=0.085 ns

10

Seasonal trend 0 2 4 6 8 10 12

05

1015

20

Simulated light regimes

Month

Hou

rs o

f lig

ht

52°S

62°S

66°S

DD

summer autumn winter spring summer autumn winter spring summer autumn winter spring summer autumn winter spring

Ø  Seasonal pattern observed under light regimes 52°S, 62°S and 66°S

Ø  No seasonality under constant darkness

Maturity analysis

Maturity under constant darkness

11

Ø  Sexual regression in beginning of experiment

Ø  Indication for an endogenous timing system

5 10 15 20

3.0

3.5

4.0

4.5

5.0

Treatment DDM

atur

ity s

core

Experimental duration [months]

*

0 2 4 6 8 10 12

05

1015

20

Simulated light regimes

Month

Hou

rs o

f lig

ht

52°S

62°S

66°S

Maturity analysis

12

Binomial model:

Probability of maturity score 5 ~ Hours of light

Probability to be sexually mature

Data

Maturity score 5?

yes

no

0 5 10 15 20

0.0

0.2

0.4

0.6

0.8

1.0

Binomial model

Hours of light

Prob

abilit

y of

mat

urity

sco

re 5

52°S62°S66°S

Ø  Probability of sexual

maturity higher with

longer photoperiod

Are the critical photoperiods different between treatments?

Critical photoperiod (CPP):

= Photoperiod for 50% sexual maturity

Maturity analysis

13

0 5 10 15 20

0.0

0.2

0.4

0.6

0.8

1.0

Binomial model

Hours of light

Prob

abilit

y of

mat

urity

sco

re 5

52°S66°S

Ø  Critical photoperiods (CPPs) are different

between treatment 52°S and 66°S

Ø  CPP is longer in higher latitude light regime

CPP 52°S: 12.56±0.68 CPP 66°S: 14.80±1.48

Analysis of critical photoperiods

Binomial model:

Probability of maturity score 5 ~ Hours of light

0 2 4 6 8 10 12

05

1015

20

Simulated light regimes

MonthH

ours

of l

ight

52°S

62°S

66°S

CPP 52°S CPP 66°S

What is the advantage of different critical photoperiods?

Ø  Longer CPPs − an adaptation to the light

regime at higher latitudes

Ø  Krill is able to start sexual regression and

maturation at the right time

Conclusions 1)  Growth

•  Seasonal growth patterns are influenced by light regime •  Growth patterns are modulated by an endogenous timing system

2)  Maturity

•  The maturity cycle is light-dependent •  The observation of sexual regression under constant darkness

suggests an endogenous timing system in krill •  Krill under the high latitude light regime have a longer critical

photoperiod (an adaptation to more extreme light conditions)

Take-home message

Seasonal cycles of growth and maturity in E. superba are triggered by different latitudinal light regimes and governed by an

endogenous timing system.

INPUT OUTPUT

Rhythms Internal Oscillator

Growth & Maturity E. superba Light regime

Acknowledgments

Literature •  Brown, M., Kawaguchi, S., King, R., Virtue, P., Nicol, S. (2011). Flexible adaptation of the seasonal krill

maturity cycle in the laboratory. J. Plankton Res. 33, 821–826. •  Brown, M., Kawaguchi, S., Candy, S., Yoshida, T., Virtue, P., and Nicol, S. (2013). Long-Term Effect of

Photoperiod, Temperature and Feeding Regimes on the Respiration Rates of Antarctic Krill (Euphausia superba). Open J. Mar. Sci. 03, 40–51.

•  Mazzotta, G.M., De Pittà, C., Benna, C., Tosatto, S.C.E., Lanfranchi, G., Bertolucci, C., and Costa, R. (2010). A cry from the krill. Chronobiol. Int. 27, 425–445.

•  Kawaguchi, S., Yoshida, T., Finley, L., Cramp, P., and Nicol,S. (2006). The krill maturity cycle: a conceptural model of the seasonal cycle in Antarctic krill. Polar Biol. 30, 689-698.

•  Meyer, B. (2012). The overwintering of Antarctic krill, Euphausia superba, from an ecophysiological perspective. Polar Biol. 35, 15–37.

•  Meyer, B., Auerswald, L., Siegel, V., Spahić, S., Pape, C., Fach, B.A., Teschke, M., Lopata, A., and Fuentes, V. (2010). Seasonal variation in body composition, metabolic activity, feeding, and growth of adult krill Euphausia superba in the Lazarev Sea. Mar. Ecol. Prog. Ser. 398, 1–18.

•  Schmidt, K., Atkinson, A., Pond, D.W., and Ireland, L.C. (2014). Feeding and overwintering of Antarctic krill across its major habitats: The role of sea ice cover, water depth, and phytoplankton abundance. Limnol. Oceanogr. 59, 17–36.

•  Seear, P., Tarling, G.A., Teschke, M., Meyer, B., Thorne, M.A., Clark, M.S., Gaten, E., and Rosato, E. (2009). Effects of simulated light regimes on gene expression in Antarctic krill (< i> Euphausia superba</i> Dana). J. Exp. Mar. Biol. Ecol. 381, 57–64.

•  Teschke, M., Kawaguchi, S., and Meyer, B. (2007). Simulated light regimes affect feeding and metabolism of Antarctic krill, Euphausia superba. Limnol. Oceanogr. 52, 1046–1054.

•  Teschke, M., Kawaguchi, S., and Meyer, B. (2008). Effects of simulated light regimes on maturity and body composition of Antarctic krill, Euphausia superba. Mar. Biol. 154, 315–324.

•  Teschke, M., Wendt, S., Kawaguchi, S., Kramer, A., and Meyer, B. (2011). A Circadian Clock in Antarctic Krill: An Endogenous Timing System Governs Metabolic Output Rhythms in the Euphausid Species Euphausia superba. PLoS ONE 6, e26090–e26090.