The Environment InstituteWhere ideas grow

Assoc. Prof. Bronwyn Gillanders

Giant Australian cuttlefish: a globally unique species under threat?

Bronwyn Gillanders

Population structure Melita de Vries

Steve Donnellan

Mike Gardner

PhD/Hons students Jackie Dupavillon

Nick Payne

Leanne Trott

Giant Australian cuttlefish & the issues

Population structure

Potential impacts of desalination brine

Photo: Kaufmann Productions

Weighs up to 13 kgGrows up to 1 mLives 1-2 years

Ningaloo ReefMoreton Bay

Adelaide

8 km of coastlineWinter – May to August

8 km of coastlineWinter – May to August

Habitat map: SA DEH

Rocky reef

Males larger than females

High male:female sex ratio

Males ‘battle’ for females

Females may or may not mate with a male

Small males have other strategies (e.g. sneakers)

Shear numbers impressive

Photos: Fred Bavendam

Skewed towards males (4:1) based on counts of each sex

Assumes individuals on breeding aggregation similar amounts of time

Population sex ratio may be 1:1 with sexes spending different amounts of time on the breeding aggregation

Predict males spend more time than females

Males n = 13Females n = 6

Payne, PhD project

Male:Female = 3.7 : 1

Residence time

Male:Female = 4.6 : 1

Residence period

0

10

20

30

40

50

60

Males FemalesM

ean

Res

iden

ce P

erio

d (

da

ys ±SE

)

*

0

5

10

15

20

25

30

35

Males Females

Mea

n R

esid

ence

Tim

e (d

ay

s ±

SE

)

*

Payne, PhD project

Population composed of equal numbers of males & females

0

30

60

90

120

150

180

210

240

270

300Ca

tch (to

nnes

)

1984

1985

1986

1987

1988

1993

1989

1990

1991

1992

1994

1995

1999

1998

1997

1996

2000

2001

2002

2003

2004

2005

2006

2007

Renewable moratorium on fishing introduced in 1998

Now permanently closed to taking of cuttlefish

Need to establish long-term scientific based management plan

From: SARDI Catch Data

BHP Olympic Dam expansion Preferred option: coastal desalination plant in USG

Point Lowly preferred location (18 ha site)

Bulk commodities export facility Feasibility study by Spencer Gulf Port Link Consortium

(SGPLC), led by Flinders Ports

7-13 million tonnes of ore could be exported through new facility

Need to understand population structure for appropriate spatial management

Demographic processes & population dynamics may vary

From: Keough & Swearer (2007)

Strongest inferences use a suite of techniques

Genetic & phenotypic approaches

Might not necessarily expect concordance among approaches

Evolutionary history vs. environmental variation

Spatial resolution varies by technique

Genetic approaches may be more conservative

Marine populations

Genetic homogeneity over large distances

High dispersal life history characteristics

Squid

High levels of gene flow among populations

Cuttlefish

Sepia officinalis – extensive population structuring

Determine population structure of giant Australian cuttlefish using a multidisciplinary approach Molecular (microsatellite DNA markers)

Morphometrics

Statolith chemistry

Investigate spatial & temporal variation in population structure

Microsatellite genotyping

12 microsatellite loci screened per individual Kassahn et al. (2006) Marine Biology

Wheaton et al. (2007) Molecular Ecology Notes

Temporal variation South Australia

Five yrs between 1998 & 2006

Spatial variation 18 sites across Australia

18

WA

SA

QLD

NSW

VIC23

4 56

Whyalla

13 14

151617

Breeding aggregation

Spencer

GulfGSV

Ningaloo

Bass Strait

Moreton

Bay

Wallaroo

Glenelg

Aldinga

Cape

Jervis

Edithburg

19982000200420052006

20042005

19982005

20052006

1998

2005

1

Bayesian clustering approach

Triplicate runs for 1 (panmixia) to 6 populations

Used admixture model

Assumed correlated alleles across populations

Examined each of K populations further to detect sub-population structure

STRUCTURE

1 2 3 4 5 6K, number of populations

-24500

-23500

-22500

-21500

-20500

Ln P

r(X |

K)

Shows overall population structure & individual assignmentLength of each line proportional to estimated membership in each group

1.00

0.80

0.60

0.40

0.20

0.00

Why

alla

199

8

Why

alla

200

0

Why

alla

200

4

Why

alla

200

5

Why

alla

200

6

Wal

laro

o 19

98

Wal

laro

o 20

05

Edith

burg

200

5

Cap

e Je

rvis

200

5

Cap

e Je

rvis

200

6

Ald

inga

/Myp

onga

19

98

Ald

inga

/Myp

onga

20

05

Gle

nelg

199

8

wes

tern

AU

S 19

98-2

006

VIC

200

2

NSW

20

02/2

003

Q

Breeding aggregationWhyalla

NSWWallarooSpencer Gulf

Gulf St Vincent WA

Vic

Est

imat

ed m

emb

ersh

ip c

oef

fici

ents

1.00

0.80

0.60

0.40

0.20

0.00

Q

Wol

long

ong

Jerv

is B

ay

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Cof

fs H

arbo

ur

Jerv

is B

ay

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

Wol

long

ong

New

cast

le

New

cast

le

New

cast

le

New

cast

le

JervisBay

Wollongong Newcastle Coffs Harbour

Northern NSWCentral & Southern NSW

Est

imat

ed m

emb

ersh

ip c

oef

fici

ents

Spatial information – sampling location 1 to 10 populations (n=5 replicate runs)

Fixed K at modal value to estimate assignment of individuals to populations (n=10)

Continued hierarchical analyses to detect subpopulation structure

GENELAND

Population 2Population 1 Population 4

Population 3

Population 5

Population 4

Population 5

Contact zone

Breeding aggregation

100 km

South Australia

28 measurements per individual

Removed allometric effects of body size

Sexually dimorphic sexes analysed separately (n= 173 females & 342 males)

No difference in size among years pooled years

-5 -3 -1 1 3 55

3

1

1

3

5 Breeding aggregationGSV & Southern SGWestern SA

Discriminant function 1

Dis

crim

inan

t fu

nct

ion

2

90% correctly classified

3 variables used for classification

3 variables important: cuttlebone width & 2 beak parameters

LRL UHL

-5.0 -2.8 -0.6 1.6 3.8 6.0-5

-1

3

7 Breeding aggregationGSV & Southern SGWestern SA

Discriminant function 1

Dis

crim

inan

t fu

nct

ion

2

90% correctly classified

8 variables used for classification

3 beak parameters contribute to differences

Dissolved traceelements

Uptake bycephalopod

Statolithincorporation

Sr:Ca prehatchling seawater (mmol mol-1

)

0 5 10 15 20 25 30 35

Sr:

Ca

pre

hat

chli

ng s

tato

lith

(m

mol

mol-1

)

0

5

10

15

20

25

30

35

Sr:Ca hatchling seawater (mmol mol-1

)

0 5 10 15 20 25 30 35

Sr:

Ca h

atc

hli

ng

sta

toli

th (

mm

ol

mo

l-1)

0

5

10

15

20

25

30

35

Sr:Ca seawater (mmol mol-1) Sr:Ca seawater (mmol mol-1)

Sr:C

ast

atol

ith(m

mol

mol

-1)

Sr:C

ast

atol

ith(m

mol

mol

-1)Prehatchling Hatchling

Trott, Hons thesis

-7 -3 1 5-5

-3

-1

1

3

5

Discriminant function 1

Dis

crim

inan

t fu

nct

ion

2

Mg:Ca, Sr:Ca & Ba:Ca

Discriminant Function AnalysisAll years – 77% correctly classified2004 – 78% correct2005 – 79% correct2006 – 83% correct

Breeding aggregationGSV & Southern SGWestern SA

Not one panmictic population Evidence for 5 populations across species range Breeding aggregation differs from elsewhere

Evolutionary & ecological implications

Possibly incipient species

Adaptive divergence along an environmental

gradient

Recent & rapid differentiation

Ocean again at ~ 7KYA

From: Andrew Hugall

Mating behaviour differs Physiological tolerance & condition in relation to

temperature & salinity▪ Two populations may be prevented from significant overlap due to

differing tolerances

Are individuals from two populations able to mate, are eggs viable, are offspring fertile▪ Testing degree of reproductive isolation

Determine degree of genetic isolation – genome wide screening

Ecological implications of morphological differences

Breeding area

Intake pipe

Out take pipe320 ML SW/day

from USG;Salinity >40 ppt

200 ML SW/dayreturned in more

concentrated form;Salinity 78 ppt

120 ML FW/day via 320 km pipeline

From: Olympic Dam EIS website

Proposed locations

Discharge of large volumes of highly concentrated brine back to ocean

Elevated salt concentration & contaminants

Elevated temperature & turbidity levels

Decreased oxygen levels

Brine high specific density sinks to bottom

Could impact adult mating behaviours, & benthic life history stages

Salinity effects embryonic development Resources diffuse across membrane Solubility of gases (e.g. O2) decreased in

hyper-saline water Increased salinity causes a diffusion limitation

Control39ppt 40ppt 45ppt 50ppt

Brine55ppt

n =12

Dupavillon, Hons thesis

Treatment

Brine: Increased Sr, Ca, K & Mg

High Mg causes mortality and reduced mobility

High concentrations found in 45, 50 and 55‰.

Mean field concentration

Dupavillon & Gillanders (2009)Treatment - salinity

Increase 1‰ = ~7%

decrease in survival

Total mortality

Treatment - salinity

Dupavillon & Gillanders (2009)

Treatment - salinity

Smaller size at higher salinitySmaller individuals less well developed for feeding & swimming

Dupavillon & Gillanders (2009)

If brine disperses & background salinity levels reached close to discharge outfall May be little impact on eggs

But USG already hypersaline environment

Strong tidal currents, but are USG waters flushed & mixed with ocean waters given bathymetry?

Also, dodge tides

Potential for major impact on GAC

Mating behaviour highly visual Inbound migratory routes of cuttlefish

Will adults move up and over high salinity, benthic plumes?

Will adults migrate around benthic plume to reach breeding sites?

Only known breeding aggregation of cuttlefish in world!

Population at Point Lowly likely a different species

Little if any input from SSG population

Potential for brine to impact early life history stage

Unsure about impacts on adult behaviour & migration

Species can’t move elsewhere to lay eggs

Cephalopods short lived (1-2 years)

No storage effect in population

Need to be more cautious cf. managing finfish

Recent ABC Catalyst story:http://www.abc.net.au/catalyst/stories/2695601.htm

Photos: Fred Bavendam, Sean Connell, Jackie Dupavillon, Kaufman Productions, Nick Payne, Tim Rogers

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Environmentally-sensitive design