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What is limiting marine heterotrophic microorganisms ?
Johnny Berglund
Marine ecology
Department of Ecology and Environmental Science
Umeå University
Aquatic food web
by Kristina Wiklund, UMF
Some marine protists...
Rhynchomonas nasuta
Parvicorbicula sp.Plagioselmis prolonga
Bodo saliens
Copyright ©, Mats Kuylenstierna & Bengt Karlson
Mesodinium rubrum5m
5m
Heterotrophic nanoflagellates (HNF)
Ciliates
18E 20E 22E 24E 26E
U m eå
Lu leå
Turku
Vaasa
N orrbyn
Sweden
F in land
A5
A1 3
B3B7
C 1C 3
C 1 4
60N
62N
64N
66N
18E 20E 22E 24E 26E
60N
62N
64N
66N
Study area:Gulf of Bothnia
Gulf of Bothnia• Low salinity from 3 psu to 7 psu• Mean depth of 40 m in B.Bay and 66 m in B.Sea• Strong seasonality, ice-cover of 120 and 60 days• High river runoff
Annual average, Kuparinen et al. 1996
0
1
2
3
4
5
Bacterial biomass Phytoplankton biomass Zooplankton biomass
mm
ol
C m
-3
Bothnian Bay
Bothnian Sea
Seasonal pattern in bacterial and HNF abundance
HNF <5 ym
0
500
1000
1500
2000
2500
3000
3500
0 10 20 30 40 50
N m
l-1
Bothnian Bay
Bothnian Sea
Bacteria
0.0E+00
1.0E+06
2.0E+06
3.0E+06
4.0E+06
5.0E+06
0 10 20 30 40 50
N m
l-1Bothnian Bay
Bothnian Sea
week
week
Question:
What is limiting growth of heterotrophic nanoflagellates (HNF)?- especially small flagellates <5m
Why?Because small flagellates (1-3 m) are most important predators on heterotrophic bacteria (Wikner & Hagström 1988 and others)
Hence, small flagellates are an important link to higher trophical levels
Definition (Osenberg & Mittelbach 1995):
Limitation is the extent to which a population’s, or trophic level’s, per capita growth
rate is depressed by the action of a particular factor, for example resource availability or predator risk.
Bothnian Sea
0
500
1000
1500
2000
2500
3000
3500
4000
0 10 20 30 40 50
Week
N m
l-1
0.00E+00
5.00E+05
1.00E+06
1.50E+06
2.00E+06
2.50E+06
3.00E+06
3.50E+06
4.00E+06
Bac
t. m
l-1
Bothnian Bay
0
500
1000
1500
2000
2500
3000
3500
4000
0 10 20 30 40 50
N m
l-1
0.00E+00
5.00E+05
1.00E+06
1.50E+06
2.00E+06
2.50E+06
3.00E+06
3.50E+06
4.00E+06
Bac
t. m
l-1
HNF < 5 Bact.
Factor 1:
~1.5*106 ml-1
~2.5*106 ml-1
Natural threshold for HNF growth
Bacteria as resource
f.w. <90 <10 <5 <0.80.00
0.02
0.04
0.06
0.08
0.00
0.02
0.04
0.06
0.08
Bio
volu
me
(mm
3 l -1)
0.00
0.02
0.04
0.06
0.08
Treatment
f.w. <90 <10 <5 <0.80.0
0.2
0.4
0.6
0.8
0.0
0.2
0.4
0.6
0.8
0.00
0.02
0.04
0.06
0.08
Gro
wth
ra
te (
d-1)
0.0
0.2
0.4
0.6
0.8
0.0
0.2
0.4
0.6
0.8
0.0
0.2
0.4
0.6
0.8
1.0
A. Heterotrophic bacteria
0.0
0.2
0.4
0.6
0.8
1.0
Initial growth rate Maximal biovolume
B. Small flagellates
C. Medium flagellates
D. Large flagellates
E. ChoanoflagellatesSamuelsson, K. & Andersson, A. 2002Predation limitation in the pelagic microbial food web,AME in press
• 0.8 – 5 m flagellates most important predator on bacteriaHeterotrophic
bacteria
HNF
PROBLEM...to distinguish effect of predation and effect of reduced competition for bacteria (resource)
Medium HNF
f.w
.
<90
<10
<5
<0.
8
f.w
.
<90
<10
<5
<0.
8
Factor 2:
• thightly size structured food-chain
Predation by large flagellates and ciliates
Hence, there are two factors limiting the
heterotrophic nanoflagellates
1. resource
2. predation
Lets setup an experiment to evaluatethe importance of the factors
•Limitation can be measured by quantifying the increase in a population’s per capita growth rate following the removal of a particular form of limitation, for example after the addition of a surplus resource or removal of predators.
(Osenberg & Mittelbach 1995)
2 after removal of limitation
1 in natural conditions
Timet1t0
lnN2
lnN1
LnN
0
1 = (lnN1 –lnN0) / (t1-t0)
Limitation L = 2 -1
+ bacteria
no addition
< 90 m < 10 m < 5 m
Experimental setup to determine limiting factors for HNF
Treatment Resource limitation Predator 5-10 m limitation
Predator 10-90 m limitation
< 90 m + + + < 90 m + bakt. - + + < 10 m + + - < 10 m + bakt. - + - < 5 m + - - < 5 m + bakt. - - -
Dialysis bags incubated in situ at 4 m
depth
Duration: 4 days with sampling every day
Performed in June 2001
Results
0.000
0.005
0.010
0.015
0.020
0.025
0.030
0.035
0.040
+ pred.90 -bakt.
+ pred.90 +bakt.
+ pred.10 -bakt.
+ pred.10+bakt.
- pred.-bakt.
- pred.+bakt.
HN
F g
row
th r
ate
h-1
Highly significant (p<0.001) effect of adding bacteria (resource)
Weak effect of predation (p<0.05) by large protozoans (10-90m)
(No effect of predation by large flagellates (5-10 m))
Results...
Relativ importance (change in pop. Growth)
resource 62 % and predation 38 %
Ls (h-1) Lp (h
-1)
B2 - B1 0.0092
B4 - B3 0.0110 B5 - B1 0.0062
B6 - B5 0.0084
B6 - B2 0.0054 Mean 0.0095 Mean 0.0058 Stdev. 0.0013 Stdev. 0.0006
To evaluate possible seasonal variations a second experiment was performed in September 2001
-same experimental setup
Experiment 2
Results...
0
0.005
0.01
0.015
0.02
+ pred.90 -bakt.
+ pred.90 +bakt.
- pred.- bakt. - pred. +bakt.
HN
F gr
owth
rat
e
Again significant (p<0.005) effect of adding bacteria
Relativ importance of resource 81 % and predation 19 %,
though effect of predation not significant
Conclusions
• HNF growth mostly resource limited
microbial food web bottom-up regulated
Modelling still to come....
Thank you for your attention!
Acknoledgements:
Agneta Andersson
Kristina Samuelsson
Thomas Kull
Umeå Marine Science Center