Diversity, origin and speciation of

diatoms of Lake Ohrid

Zlatko Levkov

Institute of Biology, Faculty of Natural Sciences,

Ss Cyril and Methodius University, Skopje

Lake Ohrid: the oldest lake in Europe

Uppermost Meotian-Pontian ca. 10 Ma

The ancient “sister” lake system: Ohrid and Prespa

(Dumurdzanov et al. 2004) : Digital Map and Chart Series 1: 1-20

Lake Ohrid

• 30 km long, 15 km wide, with area of 358 km2, located at an altitude of 693 m asl

• Age 2-10 My ?

• Known biodiversity hotspot

• High index of endemic

diversity

Albrecht & Wilke 2008

Biological

characteristics

•High diversity

•High level of endemism

•The presence of relict species

•The presence of a high diversity of species in genera primarily considered as marine

Levkov & Williams 2012: Phytotaxa 45: 1–76

Diatoms in ancient lakes Number of Taxa Number of

Endemic Taxa % endemism

Lake Ohrid 789 132 16.7 Lake Baikal 450 148 32.9 Lake Tanganyika 474 30 6.3 Lake Hövsgöl 373 1 0.3 Great Laurentian Lakes 1488 0 0

Biological questions

• What is the origin of the species? ▫ Colonization(s) or intralacustrine

speciation

• What is the age of the species and when they evolve/appear?

• What is the evolution pattern? • Differences in evolution patterns

between benthic and planktonic species?

• How and why they survived in Lake Ohrid?

1. Morphological and biostratigraphic analyses

Jurilj (1948): Prirodoslovna istraživanja 24: 171-260

Three type of analyses:

Main hypothesis and proofs • Surirella and Campylodiscus are

terminal members of the phylogenetic line

• Torsion of the valve (Helissella & Iconella)

• Crossing of the frustule (Plagiodiscus, Klinodiscuss and Campylodiscus)

Time frame Phylogenetic lines Lake Ohrid

23.0-5.3 Ma

5.3 -2.59 Ma

2.59-0.01 Ma

Albrecht & Wilke 2008: Hydrobiologia 615: 103–140 Jurilj 1948: Prirodoslovna istraživanja 24: 171-260.

‘‘Tethys’’ derivate Hypothesis (6.1-5.7 Ma)

Lake Pannon derivate hypothesis (3.4-1.8 Ma)

Mesohellenic Trough derivate (12-11 Ma)

39.0-23.0Ma

Ruck et al. unpublished data

2. Molecular analyses

Jovanovska et al. unpublished data

Molecular analyses Surirelloids

Campylodiscus

Plagiodiscus & Spirodiscus

Helissella & Iconella

Surirella imbuta

La

ke O

hrid

Multiply colonization and speciation Ruck 2010

Surirella sensu lato from Ohrid

Aneumastus

Wagner et al. 2014: Scientific Drilling, 17, 19–29,

3. Biogeochemical analyses

0102030405060708090

100110120130140150160170180190200210220230240250260270280290300310320330340350360370380390400410420430440450460470480

De

pth

(m

)

20 40 60 80 100%

Cyclotella

cf. c

omta

20 40

Cyclotella

cf. c

omta (s

mall)

20 40 60 80 100

Cyclotella

cf. s

tilor

um (large

)

20 40 60 80

Cyclotella

oce

llata

20

Cyclotella

minus

cula

20 40 60 80 100

Cyclotella

cyclop

uncta

20 40 60

Cyclotella

iris (m

edium, e

lliptic

)

20 40 60

Cyclotella

iris (s

mall, e

lliptic)

20 40

Cyclotella

iris (large

, ellip

tic)

Cyclotella

cf. p

resp

anen

sis

20 40 60 80

Cyclotella

cyclop

uncta s

mall >

5 µm

20 40

Cyclotella

cf. s

tilor

um (s

mall)

20

Cyclotella

aff. co

stei

20 40

Cyclotella

cf. p

resp

anen

sis (lar

ge)

20 40 60

Cyclotella

hus

tedt

ii (re

ctan

gular +

ellip

tic)

20 40

Cyclotella

fottii (sm

all c

entra

l area)

20

Cyclotella

hus

tedt

ii (sm

all e

lliptic

cen

tral a

rea)

20 40 60

Cyclotella

hus

teditii (s

mall

)

20 40 60 80

Cyclotella

hus

tedt

ii (larg

e)

Asterione

lla fo

rmos

a

20

Step

hano

disc

us cf

. med

ius

20

Step

hano

disc

us tr

ansilva

nicu

s

20 40 60

Step

hano

disc

us cf

.rotula

20 40

Step

hano

disc

us cf

. ves

tibulis/tr

ipor

us

20

Aulac

oseira ambigu

a

20 40 60 80

Aulac

oseira gra

nulat

a

20 40 60

Terti

arius sp

. (sm

all)

20 40 60

Stau

rosir

ella p

inna

ta

Pseu

dostau

rosira bre

vistri

ata

20

Stau

rosir

a sp.

20 40

Plac

oneis

neo

exigua

20 40

Gomph

onem

a exilis

simum

50 100 150

Plan

kton

ic

Fac.

plan

kton

ic

Benth

ic

Diatom zones

DSC 1

DSC 2a

DSC 2b

DSC 2c

DSC 2d

DSC 3a

DSC 3b

DSC 3c

DSC 4a

DSC 4b

DSC 4c

DSC 5a

DSC 5b

DSC 5c

DSC 6a

DSC 6b

DSC 6c

DSC 6d

DSC 6e

BenthicFac. planktonicPlanktonic

20 40 60 80 100 120 140

Total sum of squares

CONISS

The ICDP deep drilling campaign 2013

Scientific Collaboration On Past Speciation

Conditions in Ohrid (SCOPSCO)

Core recovery and lithology from DEEP site

1150-1000 ka

Francke et al. 2016: Biogeosciences, 13, 1179–1196

Major environmental changes but no evidence for salinization events

Largely undisturbed sediments: probably no desiccation events

0102030405060708090

100110120130140150160170180190200210220230240250260270280290300310320330340350360370380390400410420430440450460470480

De

pth

(m

)

20 40 60 80 100%

Cyclotella

cf. c

omta

20 40

Cyclotella

cf. c

omta (s

mall)

20 40 60 80 100

Cyclotella

cf. s

tilor

um (large

)

20 40 60 80

Cyclotella

oce

llata

20

Cyclotella

minus

cula

20 40 60 80 100

Cyclotella

cyclop

uncta

20 40 60

Cyclotella

iris (m

edium, e

lliptic

)

20 40 60

Cyclotella

iris (s

mall, e

lliptic)

20 40

Cyclotella

iris (large

, ellip

tic)

Cyclotella

cf. p

resp

anen

sis

20 40 60 80

Cyclotella

cyclop

uncta s

mall >

5 µm

20 40

Cyclotella

cf. s

tilor

um (s

mall)

20

Cyclotella

aff. co

stei

20 40

Cyclotella

cf. p

resp

anen

sis (lar

ge)

20 40 60

Cyclotella

hus

tedt

ii (re

ctan

gular +

ellip

tic)

20 40

Cyclotella

fottii (sm

all c

entra

l area)

20

Cyclotella

hus

tedt

ii (sm

all e

lliptic

cen

tral a

rea)

20 40 60

Cyclotella

hus

teditii (s

mall

)

20 40 60 80

Cyclotella

hus

tedt

ii (larg

e)

Asterione

lla fo

rmos

a

20

Step

hano

disc

us cf

. med

ius

20

Step

hano

disc

us tr

ansilva

nicu

s

20 40 60

Step

hano

disc

us cf

.rotula

20 40

Step

hano

disc

us cf

. ves

tibulis/tr

ipor

us

20

Aulac

oseira ambigu

a

20 40 60 80

Aulac

oseira gra

nulat

a

20 40 60

Terti

arius sp

. (sm

all)

20 40 60

Stau

rosir

ella p

inna

ta

Pseu

dostau

rosira bre

vistri

ata

20

Stau

rosir

a sp.

20 40

Plac

oneis

neo

exigua

20 40

Gomph

onem

a exilis

simum

50 100 150

Plan

kton

ic

Fac.

plan

kton

ic

Benth

ic

Diatom zones

DSC 1

DSC 2a

DSC 2b

DSC 2c

DSC 2d

DSC 3a

DSC 3b

DSC 3c

DSC 4a

DSC 4b

DSC 4c

DSC 5a

DSC 5b

DSC 5c

DSC 6a

DSC 6b

DSC 6c

DSC 6d

DSC 6e

BenthicFac. planktonicPlanktonic

20 40 60 80 100 120 140

Total sum of squares

CONISS

Diatoms from DEEP site on Lake Ohrid

122 taxa > 2 % 75 taxa 23 Cyclotella taxa

Wagner et al. 2014: Scientific Drilling, 17, 19–29,

Diatoms from DEEP site on Lake Ohrid

Cvetkoska & Jovanovska unpbl. data

0102030405060708090

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Dep

th (m

)

20 40 60 80 100%

Cyclotel

la cf.

comta

20 40

Cyclotel

la cf.

comta

(small

)

20 40 60 80 100

Cyclotel

la cf.

stilo

rum (la

rge)

20 40 60 80

Cyclotel

la oce

llata

20

Cyclotel

la minu

scula

20 40 60 80 100

Cyclotel

la cy

clopun

cta

20 40 60

Cyclotel

la iri

s (med

ium, ellip

tic)

20 40 60

Cyclotel

la iri

s (sm

all, e

lliptic

)

20 40

Cyclotel

la iri

s (lar

ge, ell

iptic)

Cyclotel

la cf.

prespan

ensis

20 40 60 80

Cyclotel

la cy

clopun

cta sm

all >

5 µm

20 40

Cyclotel

la cf.

stilo

rum (s

mall)

20

Cyclotel

la aff

. coste

i

20 40

Cyclotel

la cf.

prespan

ensis

(larg

e)

20 40 60

Cyclotel

la hus

tedtii

(recta

ngula

r + el

liptic

)

20 40

Cyclotel

la fo

ttii (s

mall ce

ntral

area)

20

Cyclotel

la hus

tedtii

(small

ellip

tic ce

ntral

area)

20 40 60

Cyclotel

la hus

teditii

(small

)

20 40 60 80

Cyclotel

la hus

tedtii

(larg

e)

Asterio

nella f

ormosa

20

Stepha

nodisc

us cf. m

edius

20

Stepha

nodisc

us tra

nsilv

anicu

s

20 40 60

Stepha

nodisc

us cf.r

otula

20 40

Stepha

nodisc

us cf. v

estib

ulis/tr

iporus

20

Aulaco

seira

ambig

ua

20 40 60 80

Aulaco

seira

gran

ulata

20 40 60

Tertiar

ius sp

. (small

)

20 40 60

Stauro

sirell

a pinna

ta

Pseudo

staur

osira

brev

istria

ta

20

Stauro

sira s

p.

20 40

Placon

eis ne

oexigua

20 40

Gomphon

ema e

xiliss

imum

50 100 150

Plankto

nic

Fac. p

lankto

nic

Benth

ic

Diatom zones

DSC 1

DSC 2a

DSC 2b

DSC 2c

DSC 2d

DSC 3a

DSC 3b

DSC 3c

DSC 4a

DSC 4b

DSC 4c

DSC 5a

DSC 5b

DSC 5c

DSC 6a

DSC 6b

DSC 6c

DSC 6d

DSC 6e

BenthicFac. planktonicPlanktonic

20 40 60 80 100 120 140

Total sum of squares

CONISS

Cyclotella species groups 1.

cav

itat

a

2. s

olev

ata

3. o

cell

ata

com

ple

x

4.ro

ssii

/ de

lica

tou

la

5. o

hrid

ana

6. a

ff p

resp

anen

sis

7. f

otti

i/ h

ust

edti

i

com

ple

x

0102030405060708090

100110120130140150160170180190200210220230240250260270280290300310320330340350360370380390400410420430440450460470480

Dep

th (m

)

20 40 60

Cyclot

ella h

usted

tii (re

ctang

ular +

ellip

tic)

20 40

Cyclot

ella f

ottii (

small

centra

l are

a)

20

Cyclot

ella h

usted

tii (sm

all el

liptic

centr

al are

a)

20 40 60

Cyclot

ella h

usted

itii (s

mall)

20 40 60 80

Cyclot

ella h

usted

tii (la

rge)

Diatom zones

DSC 1

DSC 2a

DSC 2b

DSC 2c

DSC 2d

DSC 3a

DSC 3b

DSC 3c

DSC 4a

DSC 4b

DSC 4c

DSC 5a

DSC 5b

DSC 5c

DSC 6a

DSC 6b

DSC 6c

DSC 6d

DSC 6e

20 40 60 80 100 120 140

Total sum of squares

CONISS

Cyclotella fottii/hustedtii complex

Cyclotella fottii/hustedtii complex

ca. 620 ka

240 m

Diatom response to “press events”

(MIS13-1: 650 ky to present)

Extinction events or?

Cyclotella cavitata vs Cyclotella fottii

Tofilovska et al. 2016: Fottea, 16(2): 218–233

Cyclotella ohridana prov. nom.

Intermediate forms

Ultrastructural characteristics Cyclotella ohridana Cyclotella fottii

Anagenetic evolution (chronospecies)

Tim

e (~1.1 M

y to

presen

t)

Cribrionella/Cyclotella minuscula Cribrionella ohridana Cyclotella minuscula Cyclotella/Pantocsekiella sp.?

Location of the rimoportula in

Cyclotella and related genera

Nakov et al. 2015: Phytotaxa 217 (3): 249–264

Jovanovska et al. 2016: Biogeosciences, 13, 1149–1161, 2016

Diatom response to “pulse events” –

Y-5 tephra layer

Changes in multidimensional scaling diatom

community compositions

Lake Ohrid Lake Prespa

Jovanovska et al. 2016: Biogeosciences, 13, 1149–1161

Resilience and resistance

• Lake Ohrid WAS resilient/resistant to environmental disturbances

Matzinger et al. 2007

Catastrophic events • Lake Ohrid didn’t experience catastrophic events

in the past (what about present?)

Lake Malawi

Lake Titicaca

Fritz et al. 2012 Cohen et al. 2007

The role of catastrophic events: A

comparison (mollusks)

05

Titicaca

05

Malawi

05

Baikal

05101520

Wilke et al. 2016

Ohrid

Driving forces for biotic evolution

• “Press” (glacials) vs. “pulse” (tephra deposition) events can cause regime shifts

• Each ecosystem has different resilience/resistance strength

• Reservoir function: Evolutionary refugia assuring the survival of outside species

• Relatively stable environments allow accumulation of lineages due to reduced extinction rates (phyletic gradualism)

• Environmental changes may promote rapid ecological speciation

Why Lake Ohrid is a biodiversity hot

spot?

• Lake Ohrid WAS resilient/resistant to environmental disturbances

• Lake Ohrid didn’t experience catastrophic events in the past (what about present?)

• Distinctive reservoir function (presence of Iconella, Helissella, Plagiodiscus and Klinodiscus)

• Present cradle function (Surirella with ~30 species and Campylodiscus with ~ 10 species)

Acknowledgements • Alexander von Humboldt

Foundation • ICDP • SCOPSCO project • Alfred Wegener Institute for Polar

and Marine Research • British Scholarship Trust • Synthesys • International Association for Plant

Taxonomy • Students: S. Tofilovska, D. Mitić-

Kopanja, A. Cvetkoska, E. Jovanovska, A. Pavlov et al.

Thank you for your attention