Diversity, origin and speciation of
diatoms of Lake Ohrid
Zlatko Levkov
Institute of Biology, Faculty of Natural Sciences,
Ss Cyril and Methodius University, Skopje
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
Molecular analyses Surirelloids
Campylodiscus
Plagiodiscus & Spirodiscus
Helissella & Iconella
Surirella imbuta
La
ke O
hrid
Multiply colonization and speciation Ruck 2010
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
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,
0102030405060708090
100110120130140150160170180190200210220230240250260270280290300310320330340350360370380390400410420430440450460470480
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
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.