Benthic microbes - organisms and ecology newkomp · Benthic microbes – organisms and ecology Helmut Hillebrand Plankton Ecology Group ICBM Lecture aims ... the benthos and their

Benthic microbes – organisms and ecology

Helmut HillebrandPlankton Ecology Group

ICBM

Lecture aims

At the end of this lecture, students are supposed to

Know basic features of benthic microbial organisms and their substrataUnderstand the importance of ecological interactions in benthic microbial communitiesAre acquainted with experimental approaches to microbial ecology

Lecture structure

Introduction to microbial eukaryotes in the benthos and their substratumCompetitionGrazingNutrients and grazingConsumer versus resource control

Benthic eukryotic miroorganisms encompass a majority of phylogenetic groups

Autotrophic eukaryotes

Heterotrophic eukaryotes

Ciliates, flagellates, amoeba

Meiofauna

MeiofaunaRotifersNematodesCopepodsOstracods

Benthos

Sediment Hard substrate

SedimentSediments areinherently instableUnderwood & Paterson 1995: Diatoms enhancesediment stability byEPS production

Correlation betweenChlorophyll and EPS in sedimentsPhotographs: Lowdiatom and high diatom sediment, withEPS coating

Sediment

Kühl & Jörgensen1992: Verticalprofile of light and phtosynthesisin a 3mmsediment core

Sediment

Hüttel et al. 1996: Sediment-Topographyalters fluidand particleintrusioninto thewatercolumn

Sediment

Intertidal marine microalgae migrate to the surface to enhance light useMicrobial mats

Sediment

Bioturbation

Hard substrates

Periphyton

Hard substrates

Benthic boundary layer

Hard substrates

Burkholder et al. 1990: Uptake of P by adnate algae (AD) is only a fraction of loosely attached algae (LA) at control and P-enriched site

periphyton

grazers

phytoplankton

macrophytes

light

physical forcing

nutrients

substratum

competition

internal processes

nutrient regeneration

grazing

Hard substrates

Periphyton composition

Colonization

Biomass and species richness increase asymptotically, dominance increases over time.

Hillebrand & Sommer 1999, Aquat Bot

Colonization

Increasing dominance of erect species

Hillebrand & Sommer 1999, Aquat Bot

Competition on sediments

Competition between cyanobacteria and diatoms on sediments of different grain size and at different temperatures

Watermann et al. 1999 MEPS

Competition on sediments

Watermann et al. 1999 MEPS

Competition between benthic and pelagic microalgae

Resource supply affects both phytoplankton and benthic microalgaeHighest benthoic proportion at low light

Flöder et al. 2006 Aquat Ecol

Competition between benthic and pelagic microalgae

Vadeboncoeur et al. 2006 LO

Fertilization experiments

Series of hard substrate experiments at the Kiel Fjord

Hillebrand & Sommer 1997, MEPS

Fertilization

Hillebrand & Sommer 1997, MEPS

Growth and stoichiometryCN

µ

Hillebrand & Sommer 1999, L & O

NP

µ

N-limited

P-limited

N-limited

17

7

05

101520253035404550

0 20 40 60

N:P

C:N

0

100

200

300

400

500

C:PPlim

Nlim

Growth and stoichiometry

Hillebrand & Sommer 1999, L & O

Grazing

Architecture and biofilms

Exp 1: 3 grazer treatments at low ambient nutrient concentrations (N-limited)

Sampling at day 0, 2, 4, 8, 15, 23

Grazing

control

Theodoxus

Bythinia

Theodoxus

Bythinia

Exp 2: Factorial combination of 3 grazer- and 2 light-manipulations (P-

limited)

Sampling at day

0, 4, 15

+ Light

+++ Light

control

Hillebrand et al. 2004 Oikos

Algae: strong reduction already after 2-4 days; Reduction in CON


Time (d)0 4 8 12 16 20 24

0.0

0.1

0.2

0.3

0.4

Alga

l bio

volu

me

(mm

3 cm

-2) Control

Bithynia Theodoxus

Grazing

N-Limitation indicatedC:N Theodoxus << Bithynia; C:P Theodoxus < Bithynia

Time (d)0 4 8 12 16 20 24

4

6

8

10

12

14

16

18

C:N

mol

ar ra

tio

Control Bithynia Theodoxus

• Grazer presence increased periphyton N

• Significant effects of BIT, not THE, on C:N

• Bithynia also increased DIN

ANOVA: graz + graz X time **

Grazing


P-Limitation indicatedC:N Theodoxus << Bithynia; C:P Theodoxus < Bithynia

start HL4 HL15 LL4 LL15Sampling

200

400

600

800

1000

C:P

mol

ar ra

tio

start con bit the

• Both grazers increase periphyton P significantly

ANOVA: graz *** light ** graz X light ns

Grazing



start HL4 HL15 LL4 LL15Sampling

200

400

600

800

1000

C:P

mol

ar ra

tio

start con bit the


• Low light increases periphyton P (and N) - relative release from nutrient limitation


Grazing



• significant effects of Bithynia, not Theodoxus on C:Nstart HL4 HL15 LL4 LL15

Sampling

200

400

600

800

1000

C:P

mol

ar ra

tio

start con bit the


• Low light increases periphyton P (and N) - relative release from nutrient limitation


Grazing


Grazing in sediments

Esptein et al. 1997, Microbial Ecology. Trophic interactions in sedmient microbial food webs

Seasonal patterns of algae and bacteria as well as consumption on algae and bacteria

Esptein et al. 1997, Microbial Ecology. Trophic interactions in sedmient microbial food webs

Seasonal patterns of algae and bacteria as well as consumption on algae and bacteria

Ciliates

Grazing in sediments

Grazing

Factor p ω2 (%)Grazing (F) 0.003 26.0km (F) 0.046 10.110m (R) 0.117 3.1Grazing X km (F) 0.137 10.5Grazing X 10m (R) 0.016 15.8Error 34.6

Nested ANOVA

Hillebrand & Peters, unpublished

Chl

orop

hyll a

(µg

cm-2

)

a b c

0

5

10

15

20

25

NE

Chl

orop

hyll a

(µg

cm-2

)

0

5

10

15

20

25

NW

Chl

orop

hyll a

(µg

cm-2

)

0

5

10

15

20

25

ex op ex ep ex op

SE

10 m distance

km distance

ABS PRS ABS PRS ABS PRS

Chlo

roph

yll a

µg c

m-2

Grazing

Grazing reduces strongly algal biomass across experiments

Grazing reduces absolute but increases relative heterogeneity in biomass

Hillebrand 2008 Ecology

Nutrients and grazing

closed cages open cages uncaged control plots

4 replicates for each factor combination

NPKnutrient addition in two (ambient, enriched) or four (no, low, mid, high) categories


Hillebrand et al. 2000, MEPS

Positive effects of nutrients, negative effects of grazing

Higher grazing effects with higher nutrient supply

“Trade-off” between algal growth types (nutrient uptake vs. grazing resistance)

0

0.02

0.04

0.06

0.08

0.1

no low med high

nutrient treatment

Alga

l bio

volu

me

(mm

3/cm

2)

High nutrient uptake - high grazing risk

Low grazing risk - low nutrient

availability

ANOVA: Graz***; Nut***; GxN+

Nutrients and Grazing

Hillebrand et al. 2000, MEPS


Hillebrand & Kahlert 2001, L&OANOVA: Seas*; Graz***; Nut**; SxG***;NxG*

ABS PRES ABS PRES ABS PRES

aut 1999 espr 2000 lspr 2000 sum 2000

0.0

0.2

0.40.4

0.6

0.80.8

1.0

alga

l bio

volu

me

(mm

3 cm

-2)

AMBENR

Nutrients and grazingEffect r2 F p Int. Variable B

Nutrients 0.546 5.00 0.037 -2.43 Secchi

DIN

TN

1.22 *

0.88 +

-0.04

Grazer

ambient

0.369 3.92 0.065 -0.29 TP

DIP

-1.90

-4.06

Grazer

enriched

0.450 9.18 0.014 0.31 DIP

DIN

-7.33

-1.18

Hillebrand & Kahlert 2001, L&O


Dnut

Dgr

az

-7

-5

-3

-1

1

3

5

-5 -4 -3 -2 -1 0 1AM B ENR Dnut

Dgr

az

-6

-4

-2

0

2

4

-6 -4 -2 0 2

11 experiments at 3 sites, each experiment represented by one point

C:Nnutrients reduce C:N, i.e. increase N contentgrazer inconsistent effects

C:Pnutrients reduce C:P, i.e. increase P contentgrazer reduce C:P, i.e. Increase P content

C:N C:P

Hillebrand & Kahlert 2001, L&O

Material imbalance and trophic interactions

Meta-analysis of grazer-periphyton experiments

C-limited grazer increase grazing ratesC-limited grazer increase algal P-content

-2.5 -1.5 -0.5 0.5 1.5 2.5Mismatch C:P (ln(C:P grazer/C:P algae))

C-limitation <> P-Limitation

-0.0002

0.0002

0.0006

0.0010

0.0014

0.0018

Gra

zing

rate

(pro

p pe

r ind

and

day

)

Hillebrand et al (2008)

-2.5 -1.5 -0.5 0.5 1.5 2.5Mismatch C:P

C-Limitation <> P-Limitation

-1.0

-0.6

-0.2

0.2

0.6

1.0

1.4

Gra

zer e

ffect

on

prey

C:P

Gra

zer i

ncre

ase

Gra

zer r

educ

epr

ey P

con

tent

Material imbalance and trophic interactions

periphyton

grazers

phytoplankton

macrophytes

light

physical forcing

nutrients

substratum

competition

internal processes

nutrient regeneration

grazing

Benthic microbial food webs

Biomass of bacteria, heterotrophic nanoflagellates, ciliates and meiofauna also decreased with grazing, but with differentiated temporal dynamics and effect strength. In the ungrazed control, first heterotrophic protists and later meiofaunal biomass increased.

Grazingon MFW

Burgmer et al. 2010 AME

Nutrients and grazing on MFWWeak direct effects of nutrients on ciliates and bacteriaPositive effects of grazing on meiofauna and ciliates, partly on bacteria

due to increased nutrient availability (= positive effects stronger at AMB)due to smaller algal size spectra

Effects similar between coastal and freshwater site

Hillebrand et al. 2002, Ecology

Benthic microbial food webs

MFWIncreased DOC supply increased total periphyton biomass in almost all experiments, whereas increased P supply incresed total biomass only if algae were present.

MFW

The effects of DOC and P on the ratio of heterotrophic to autotrophic abundance strongly depended on trophic structure, where additional resources enhanced the autotroph component when the basal heterotrophs were limited by low organic C or by strong consumerpressure.

MFW

Purely heterotrophic biofilms had higher C:P ratios than autotrophic assemblages. Increased P-supply decreased periphyton C:P throughout except for the experiment with the highest trophic complexity, as including more elements of the microbial food web led to higher retention of P within the assemblage.

Consumer versus resource control

Algal Biomass

Nutrient content

Light

Consumer

Hillebrand 2002, JNABS, 2005, J. Ecol

Nutrients

Meta-analysis => Quantitative summary of factorial experiment: Hedges’ D as effect size (Mean ± 95% confidence intervals)

JS

X-XD CE•=


All effect sizes significant >0 Light effects = nutrient effectsInteraction: light X grazer >> nutrient x grazer

LIGHT NUTRIENTS

From Hillebrand 2002, JNABSHillebrand 2005, J. Ecol


Impact Grazer Nutrient Inter

Realm * *** -

Productivity - - **

Experiments * ** ***

Nutrient manip. not m. ** ***

Season - - -

Enrichm. factor not m. *** (+) -

Amb. biomass ** (+) ** (-) -

Exp. duration - - -

Hillebrand 2002, JNABS


Factor d L LR L d NProductivity + ns nsType of man. ns ns +Factor of enrichment + + +Algal biomass + + -Grazer presence - - -Exp. units s s s

Hillebrand 2002, JNABS2005, J. Ecol

Effects of resource addition depend on context of the experiment


2.2 2.6 3.0 3.4 3.8 4.2 4.6

Mean grazer biomass (log g m-2)

-4

-2

0

2

4

6

8

10

Effe

ct s

ize

dG dI

*** d G *** d I

2.2 2.6 3.0 3.4 3.8 4.2 4.6Grazer biomass (log g m-2)

-1

0

1

2

3

4

5

6

Effe

ct s

ize

LR G LL LR G HL

ns LR G LL *** LR G HL

d

LR

Grazer effects increase with increasing grazer biomass both in absolute and relative terms.

Hillebrand 2005, J. Ecol

Meta-analysis of herbivore and fertilization effects on producer diversity shows strong system-overarching response patterns for richness and evenness.

Does this hold for higher trophic levels?

Hillebrand et al. (2007) PNAS

Algal diversity nutrients herbivores

Regulation of biodiversity

Growth versus disturbance

In-situ data show diversity patterns corroborating the DEM

85 streams in NE USAProductivity = algal growth rate on tilesDisturbance = # of large floods yr-1Richness = microscopical assessment of algae

Cardinale, Charles, Hillebrand (2006)

Chesapeake Bay

100 km

Chesapeake Bay

100 km

bi P

Int. 2.31 0.00

P 0.42 0.00

D 2.96 0.11

P2 -0.02 0.00

D2 -4.59 0.08

P*D 0.60 0.00

-10.0 -0.6 8.8 18.2 27.6 37.0Productivity

-0.55

-0.14

0.27

0.68

1.09

1.50

Dis

turb

ance

freq

uenc

y

-11-6-14914

S_RESID

Kondoh 2001

Growth versus disturbance

Evenness peaks at mid disturbance x mid productivityDominance high at all 4 extremes

Species traits of dominant species corresponds to predictions from DEM

-10.0 -0.6 8.8 18.2 27.6 37.0Productivity

-0.55

-0.14

0.27

0.68

1.09

1.50

Dis

turb

ance

freq

uenc

y

0.00.20.40.60.81.0

E_BIOM

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

10

20

30

40

1

2

Rel

ativ

e bi

omas

s

Produ

ctivit

y

Disturbance

Sp188

Speciesevenness

0.0

0.1

0.2

0.3

0.4

0.5

0.6

10

20

30

40

1

2

Rel

ativ

e bi

omas

s

Prod

uctiv

ity

Disturbance

sp 68Melosiralineata (D)

Stigeocloniumsp. (CH)

0.05

0.10

0.15

0.20

0.25

0.30

0.35

10

20

30

40

1

2

Rel

ativ

e bi

omas

s

Produ

ctivit

y

Disturbance

sp60Gomphonema parvulum (D)

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

1020

3040

1

2

Rel

ativ

e bi

omas

s

Productivity

Disturbance

Sp16Cocconeis placentula (D)

Cardinale, Charles, Hillebrand (2006)

Mixotrophy

Mixotroph abundance in sediments of Kiel Bight

- increases in the dark- only <5% of total abundance

September Octoberab

unda

nces

/ cm

³ sed

imen

t darklight

0

1x105

2x105

Station 3

sediment depth (mm)

0-3 3-6 6-9

% to

tal n

anof

lage

llate

s

0

20

40

60

80

100

Moorthi, PhD thesis

Mixotrophy

Proportion of mixotrophs increase with salinity

0 10 20 30 40 50

salinity (psu)

0 10 20 30 40 50

% to

tal n

anof

lage

llate

s(m

ean

+ SE

)

12345678

0 10 20 30 40 50

% to

tal n

anof

lage

llate

s(m

ean

+ S

E)

0

2

4

6

8

10

12

September, GemanyMarch, CaliforniaJuly, Greenland Sea

sediment (+brine) light sediment, dark

salinity (psu)

0 10 20 30 40 50

plankton, light plankton, dark

r=0.70, p<0.01, N=48 r=0.70, p<0.01, N=48

r=0.68, p<0.01, N=30 r=0.64, p<0.01, N=30

Moorthi, PhD thesis

Summary

Benthic eukryotic miroorganisms interact by important direct (feeding, competition) and indirect (nutrient regeneration) interactions.

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Benthic microbes - organisms and ecology newkomp · Benthic microbes – organisms and ecology Helmut Hillebrand Plankton Ecology Group ICBM Lecture aims ... the benthos and their