Download Ecology of algae in coral reefs

Ecology of algae in coral reefs
Guillermo Diaz‐Pulido
Centre for Marine Studies &
ARC Centre of Excellence for Coral Reef Studies, The University of Queensland, Australia
[email protected]
&
Universidad del Magdalena, Colombia
All photos by G. Diaz-Pulido,
(unless noted)
1
THE PLAN
1. Overview of benthic algae on coral reefs
2 Ecological roles
2.
3. Spatial & temporal distribution
4. Phase shifts & causes
5 Interactions between corals and algae
5.
6. Climate change impacts on reef algae
2
Taxonomic Groups
• Macroalgae are a polyphyletic group of organisms
are a polyphyletic group of organisms
• Macroalgae include members of 4 different phyla
–
–
–
–
–
•
Rhodophyta ( “Red Algae”)
H t k t h ( “Brown Algae”)
Heterokontophya
( “B
Al ”)
Chlorophyta ( “Green Algae”)
Cyanobacteria (= Cyanophyta, “Blue‐green Algae”)
These phyla have very different evolutionary histories. h
h l h
d ff
l
h
Systematic classification is mostly based on the composition of
pigments
i
t involved
i
l d iin photosynthesis
h t
th i
3
Functional Group Diversity of Macroalgae
• Instead of a taxonomic classification Æ “functional form” groups
• Based on key plant attributes and ecology:
– Form & size; Plant toughness
– Photosynthetic ability and growth
Ph t
th ti bilit
d
th
– Grazing resistance
•
Useful:
– Understand the distribution of algal communities and responses to
environmental factors
– Algae with similar ecological characteristics have similar responses to
environmental factors
– Whereas taxonomically related algae Æ different ecological responses.
– Algae difficult to identify to species level in the field
•
Approach has been widely used in ecological studies on coral reefs
4
Algal categories
Algal turfs
Macroalgae
(upright)
Crustose
calcareous algae
5
Steneck & Dethier, 1994
Functional Group Diversity
Algal turfs
•
Algal turfs
–
–
–
–
–
Assemblages or associations of many species of minute algae
Mainly filamentous
Fast growth and high productivity, and high colonization rates
Ubiquitous; low biomass /m2, but dominate a large area
Turfs persist because constant grazing (prevents their overgrowth by larger, fleshy seaweed
Wurdemannia
6
1 cm
Algal turfs
7
Functional Group Diversity
Algal turfs
•
Algal turfs
–
–
–
–
–
•
Assemblages or associations of many species of minute algae
Mainly filamentous
Fast growth and high productivity, and high colonization rates
Ubiquitous; low biomass /m2, but dominate a large area
Turfs persist because constant grazing (prevents their overgrowth by larger, fleshy seaweed
Fleshy macroalgae or seaweeds
–
–
–
–
Fleshy macroalgae
Large algal forms
More rigid and anatomically more complex than algal turfs
Abundant in zones of low herbivory
herbivory, such as intertidal reef flats
Often produce chemical compounds that deter grazing
8
Upright macroalgae
9
Functional Group Diversity
Algal turfs
•
Algal turfs
–
–
–
–
–
•
Fleshy macroalgae or seaweeds
–
–
–
–
•
Assemblages or associations of many species of minute algae
Mainly filamentous
Fast growth and high productivity, and high colonization rates
Ubiquitous; low biomass /m2, but dominate a large area
Turfs persist because constant grazing (prevents their overgrowth by larger, fleshy seaweed
Fleshy macroalgae
Large algal forms
More rigid and anatomically more complex than algal turfs
Abundant in zones of low herbivory
herbivory, such as intertidal reef flats
Often produce chemical compounds that deter grazing
Crustose algae
–
–
–
Hard plants that gro
grow as cr
crusts,
sts closel
closely adhered to the
substrate
Generally slow growth rates
Most crustose algae produce calcium carbonate and may have
important roles in cementing the reef framework together
Crustose
10
Crustose calcareous algae
11
Photo by L. McCook
Attributes of functional groups
Grazing susceptibility
Foliose
Filamentous Corticated
Leathery
Articulated
calcareous
Crustose
Littl ett all 1983
Littler
12
Littler et al 1983
Grazing susceptibility
Foliose
Filamentous Corticated
Leathery
Articulated
calcareous
Crustose
Variability within FFG:
Due to 2ry metabolites
13
Littler et al 1983
Productivity, palatability, toughness
14
Littler et al 1983
Penetration Resistances of Penetration Resistances of Macroalgae
Macroalgae
Foliose
Filamentous Corticated
Leathery
Articulated
calcareous
Crustose
15
Littler et al 1983
Ecological Roles
16
The “good guys”
• Crustose calcareous algae
‐Key roles in calcification
‐Key roles in calcification
‐Coral recruitment
17
The “bad guys”
Chonospora Community, GBR
18
The “bad guys”
19
Keppel Is, GBR
Lobophora variegata
Primary
Primary Production (PP)
Production (PP)
• Contribute significantly to PP (algal turfs )
• Planktonic microalgae and algal symbionts of corals also contribute to reef PP
– but to a lesser degree but to a lesser degree
• Most organic matter enters the reef food chain by several paths
several paths
– Herbivores (fishes, crabs, sea urchins and zooplankton)
– Algae also “leak” organic carbon into the water
• It is consumed by bacteria, in turn consumed by filter feeders. • Significant amounts of organic matter are exported to adjacent ecosystems, such as seagrass meadows, mangroves or the sea floor
20
Primary Production
Larkum et al 2003
• GBR algal communities are highly productive
21
Primary Production
From Diaz-Pulido et al 2007
22
Algal Turfs
High light, high rates of O2 evolution
For comparison in g C m-2 d-1:
Algal Turfs
Corals
M
Macro
algae
l
Benthic Microalgae
Tree Leaves
Maize
Larkum et al. 2003
0.9 -15
0.8-2.8
2 – 40
0.5
5
15
23
Productivity of crustose corallines
Algal
g Turfs
Corals
Macroalgae
Benthic Microalgae
Crustose corallines
Tree Leaves
Maize
Chisholm 1998
0.9 -15
0.8-2.8
2 – 40
0.5
09-5
0.9
5
15
24
Convoluted surfaces means more
than 1m2 area in 1 m2 projection
Variability in PP on the GBR
25
Variability in PP on the GBR
Macroalgal production
•Varies across the continental shelf: Higher offshore
Inshore: Low
Offshore: High
150 g C /m2 /yr
500 g C /m2 /yr
Klumpp & McKinnon, 1989
•Varies with season (being highest in summer and lowest in winter)
•No clear latitudinal gradient has been observed (few data)
26
Variation of PP with depth
•Higher in shallow reefs
•Lower in deep zones
•Higher in the reef crest
•Lower in the slope
Oxigen
n productio
on
Algal
turfs
Algal
turfs
438 /y
183 /y
73 /y
Russ, 1993
27
Depth
Kulmpp & McKinnon, 1989
Diurnal variation in PP
Diurnal variation in PP
-Photosynthate accumulation
-Rapid
p build up
p of p
photosynthetic
y
C through
g the day
y
-Peaking in the afternoon
-At nigh: no photosynthesis, remaining C is utilised in
respiration
Algal
turfs
28
Polunnin & Klumpp , 1989
Grazing and Production are correlated
• Grazing follows production
Grazing R
G
Rates
• production & grazing: + correlated
Grazing Rates+ correlation
Cause or consequence?
• Higher PP due to higher grazing
– by reducing self shading effects on
photosynthesis
– Grazing stimulates PP through release of
nutrients (e.g. waste products)
•
•
29
Nutrient fixation in enhanced by grazing
Grazers are attracted to areas of greatest
PP (food availability) on coral reefs ??
Nitrogen fixation in coral reefs: Nitrogen fixation in coral reefs: Roles of algae
Roles of algae
Cyanobacteria: Calothrix
• Inorganic nitrogen (N2) is the most common element in the air, but organic
nitrogen is a limiting nutrient in reefs. • Nitrogen Fixation:
Heterocysts (fix N2)
– Inorganic N2 ‐Æ organically available N
•
N2 is fixed by blue-green algae
((cyanobacteria;
y
; common in algal
g turfs))
•
Blue-green algae have rapid growth rates,
but are intensely grazed
– Fixed nitrogen is distributed throughout the
reef ecosystem
•
Rates of N2 fixation on the GBR are high,
particularly
p
y on substrates exposed
p
to fish
grazing
30
0.1 mm
Sediment consolidation:
Macroalgae
Macroalgae contributed to sediment stabilisation
contributed to sediment stabilisation
Succession in a
Seagrass Community
31
Sediment consolidation
Traps and binds sediments among its rhizoids and branches
32
Gelidiella sp.
Reef Construction
Reef Crest, Heron Is
• Macroalgae contribute to reef construction (building and cementing) by depositing calcium carbonate in algal tissues
l i
b
t i l l ti
– Aragonite: Halimeda: Form bioherms
– Hi‐Mg Calcite: Crustose coralline algae: form algal ridges; – Defensive adaptation to inhibit grazing, resist wave shock, and provide mechanical support, magnify light fields.
Crustose coralline alge
• Heavily calcified algae: Crustose coralline algae ‐CCA
– CCA bind adjacent substrata and provide a calcified tissue barrier against erosion
calcified tissue barrier against erosion
– Calcification important Æ reef crests & algal ridges (Panama, Mexico, Pacific, GBR)
– Calcification rates
• CCA: 1 to 10.3 kg CaCO3 m2 yr1: Lizard Island CCA: 1 to 10 3 kg CaCO3 m2 yr1: Lizard Island
33
• Algal Ridge, Panama.
34
Macintyre et al. 2001.
Green algae
Udotea spp
Red algae
Amphiroa sp
35
Penicillus sp
Galaxaura sp
36
Littler & Littler 1984
Halimeda with intercellular calcification
Heavily calcified zone between cortical siphons
Siphons
37
Verbruggen 2005
Coralline algae with calcification within cell walls
Lithothamnion
38
Adey et al.
Cementing
m
g reefs
f
Chisholm 2000
•Calcification dependent on light and
photosynthesis
Capable of high rates1.5-10
rates1.5 10 kg CaCO3 m-1 y-139
•Capable
•Actual rate is less due to bioerosion
Rhodoliths
Foster 2001
Important in the
Southern GBR
40
Foster 2001
Facilitation of coral settlement
• Crustose coralline algae induce settlement of coral larvae in the GBR •
Harrington et al. 2004
41
Bioerosion
Ostreobium
• Endolithic algae:
– Live within the skeletons of healthy and d d
dead corals and of other calcareous l
d f th
l
substrates
– Contribute to reef erosion & destruction
–
•
algae
Fil
Filamentous,
microscopic
i
i & fform a thin
hi d
dark
k
green band underneath the coral / CCA
Examples of carbonate-boring algae:
–
–
–
–
–
•
1mmEndolithic
Green algae Ostreobium spp
Cyanobacteria Mastigocoleus testarum,
Plectonema terebrans, and Hyella spp.
Red algae
Penetrate & dissolve the CaCo3 ((by
yp
physical
y
and chemical processes), weakening the reef
framework
ÆFacilitates other erosive activities
Rates of bio
bio-erosion
erosion by endolithic algae:
–
20 – 30 g m2 /yr at One Tree Island, GBR
Endolithic
algae
42
Bioerosion
Following coral diseases, the
white bare skeleton changes to
green as a result
lt off endolithic
d lithi
algal blooms.
This occurs as a consequence
q
of
increased light levels.
Endolithic algal bloom may result
in respiration-induced
respiration induced dissolution
of the CaCO3.
Roles in coral bleaching
43
Fine et al 2006
Reef degradation
• Involved in ecological phase shifts
– Reef‐building corals are replaced by fleshy macroalgae
– Example from Jamaica (Hughes 1994): reefs are dominated by algae
• Phase shifts are usually associated to
– R
Reductions in herbivory (overfishing and d ti
i h bi
(
fi hi
d
diseases)
– Eutrophication
– Coral mortality (bleaching, cyclones, diseases)
• Increases in fleshy macroalgal abundance may lead to:
–
–
–
–
–
coral overgrowth
smothering and/or shading of corals
smothering and/or shading of corals
exclusion of coral recruitment
increases in pathogens
Resulting in reef degradation
Diadema
die-off
Hughes 1994
44
Example of phase shift driven by herbivory loss
Reef degradation
45
THE PLAN
1. Overview of benthic algae on coral reefs
2 Ecological roles
2.
3. Spatial & temporal distribution
4. Phase shifts & causes
5 Interactions between corals and algae
5.
46
Spatial Distributions
San Andres
Colombia
Panama
47
Distributions vary with depth
48
Hay, 1981
Macroalgal Assemblages in the Caribbean
Shallow
Deep &
calmed
&
exposed
49
Diaz-Pulido & Diaz, 1997. Proc. 8th Int. Coral Reef Symp. 1: 827-832
Dictyota spp.
L b h
Lobophora
variegata
i
t
Crustose coralline algae: Porolithon
50
Halimeda spp.
Algal distributions: GBR
51
Cross shelf distribution
Inshore reefs
•
Abundant fleshy macroalgae
–
–
•
•
•
Low cover of CCA
Abundance of Sargassum due to low grazing
Abundance of fleshy macroalgae:
–
–
•
Sargassum & other Fucales (3 m tall)
Lobophora, Colpomenia, Chonoospora
Sign of eutrophication and reef degradation?
(sediment and nutrient inputs from the land).
Uncertain to what extent current abundances
are natural or result from human activities
(no good historical data)
High nutrients
High sedimentation
Low visibility
Low herbivory
Offshore reefs
Offshore
reefs
• Low abundance of fleshy macroalgae
–
•
•
High cover of CCA: roles in construction
Some green fleshy macroalgae
–
•
Caulerpa, Chlorodesmis, Halimeda, Some Reds:
–
•
•
Large brown algae Sargassum are virtually absent
Laurencia, Spyridia: in low abundance Algal turfs: Æ
Al
l f Æ widespread and abundant
id
d d b d
Their cross‐shelf distribution is influenced by fish grazing and water quality
Low nutrients
Low sedimentation
High visibility
High herbivory
52
Within reef distribution
Within reef distribution‐‐Zonation
53
Within reef distribution
Within reef distribution‐‐Zonation
Offshore reef
•Limited growth
•Sandy bottom
•Diverse
•Low grazing
•Abundant CCA
•Abundant turfs
•Intense grazing
•Abundant Turfs & CCA
•Intense grazing
• Decrease with depth
54
Cribb, 1983
Temporal variability
55
Hay, 1981
Temporal variability
• Highly seasonal: Strong seasonal changes in biomass
• Reproduction is seasonal • More clear in Sargassum
– Most are summer species (dieing in winter)
in winter)
•
Martin-Smith 1993
Lobophora:
– Winter – spring species
Causes:
Lobophora Cover
– Temperature
– Day length
– Variability in grazing
50
45
40
35
% Cover
•
Goold
G
ld Fl
Flat
Goold Slope
30
Palm Flat
Palm Slope
25
20
Rib Flat
Rib Slope
15
56
10
5
0
A
S
O
N
1998
D
J
F
M
A
M
J
J
A
S
O
1999 Date
N
D
J
F
M
A
M
J
J
A
2000
Diaz-Pulido 2009
THE PLAN
1. Overview of benthic algae on coral reefs
2 Ecological roles
2.
3. Spatial & temporal distribution
4. Phase shifts & causes
5 Interactions between corals and algae
5.
6. Climate change impacts on reef algae
57
Roles of algae in coral reefs
Guillermo ia Pulido
Guillermo Diaz‐Pulido
Centre for Marine Studies &
ARC Centre of Excellence for Coral Reef Studies, The University of Queensland, Australia
g diazpulido@uq edu au
[email protected]
58
THE PLAN
1. Overview of benthic algae on coral reefs
2 Ecological roles
2.
3. Spatial & temporal distribution
4. Phase shifts & causes
5 Interactions between corals and algae
5.
59
THE PLAN
1.
2.
3
3.
4.
5.
6.
Phase shifts
Causes
Nutrient limitation (Eutrophication)
Grazing (Overfishing)
Grazing vs. Nutrients
Coral Disturbances
60
Evidence of coral decline
• Worldwide decline in coral reefs
61
Gardner et al. 2003. Science. 301:958-960
Phase Shifts: Caribbean
Corals
Algae
Diadema
die-off
62
H
Huges
1994
Hughes 1994
Lessios 1988
Phase shifts:
Great Barrier Reef
2004
Algae?
Corals
Bleaching
63
64
Photo by GBRMPA
Phase shifts /
State transition
65
Ecological phase shifts
(Alternate stable states)
(Alternate stable states)
•How to reverse the macroalgal
state?
•Need to understand algal ecology
Bellwood et al. 2004
66
Factors regulating algal abundance
•What control the abundance & distribution of
macroalgal populations?
Individual rates:
•Dispersal
•Recruitment
R
it
t
•Mortality
Species Interactions
•Competition
•Predation
P d ti
(Herbivory)
Resource availability: Environmental factors:
•Light
•Temperature
•CO2
•Salinity
67
•Nutrients
•Water movement
•Substratum
•Disturbances
Control of algal abundance on coral reefs
Eutrophication:
Overfishing:
Increased Nutrients
Decreased Herbivory
Coral
Disturbances
Increased algal growth
Increased algal abundance
Competition
Decreased coral abundance
Adapted from McCook, 1999 &
Diaz-Pulido & McCook 2002
68
Sediments
Algal
Density
y
•Sediment addition ↓ density of Sargassum
Umar et al. 1998
69
%Coverr of coralliine crusts
s
Sedimentation affects Coralline algae
R
P
Ph
M
D
JB
Fabricius and De’Ath 1990
Relative distance across the shelf
Abundance
Ab
d
correlated
l t d with
ith reduced
d
d sedimentation
di
t ti and
d
higher visibility
70
Sedimentation effects on reef algae
Hi h (Additi
High
(Addition))
Sediment
treatments
Low ((Removal))
Medium (Ambient)
71
Settlement
treatment
High (Ambient)
(Initial Propagule
Density)
Moderate (Limited)
72
Reduced (Brushed)
Dens
sity (no. th
halli / plate)
Lobophora variegata Density
15
Sediment treatment
Addition (A)
Natural (N)
Removal (R)
Complex interactions:
Effects of sediments depended on
the levels of herbivory:
Addition of sediments reduced
density when herbivores were
absent, BUT
10
5
Additions of sediments p
probably
y
protected the alga from predation.
0
Competition may be important:
herbivores removed other fleshy
algae.
Diaz-Pulido et al In prep.
AN R
AN R
AN R
Full
Partial
Open
Cage Treatment
73
Full cage
Open Plot
3 cm
74
10 cm
Nutrients
Increased nutrient
uptake with
increased N
concentrations
Schaffelke & Klumpp 1998
75
Nutrients
Sargassum, GBR
• Some macroalgae are nutrient (N, P) limited
• Increased
I
d nutrients
t i t nott
always enhance algal growth
– May lead to growth inhibition
– Inhibition of reproduction
(receptacles)
Sargassum, GBR
76
Control Medium High
Nutrients
Diaz-Pulido & McCook, 2004. JEMBE
Control Medium High
Nutrients
Schaffelke & Klumpp, 1998
Herbivory
• Grazing
Grazing by herbivores (e.g. Fishes, urchins), by herbivores (e g Fishes urchins)
is one of the most important ecological processes affecting reef macroalgae:
processes affecting reef macroalgae:
–
–
–
–
Productivity : grazing enhances PP
P
d i i
i
h
PP
Distribution: cross shelf & within reefs Abundance of adults & algal recruits
Algal species composition 77
Grazing: Effects on Biomass
McCook 1996
- Grazing
g reduces algal
g biomass midshelf & offshore
- No effects onshore: fish are less important there
78
Grazing: Effects on % Cover
79
Hughes et al 2007
Grazing: Effects on Morphology
80
Grazing: Effects on Morphology
7 days
14 days
30 days
21 days
81
1 mm
Diaz-Pulido et al 2007 Phycologia
Grazing: effects on productivity
No
Grazing
Ambient
• Reduction of grazing: – Increased
Increased algal biomass over 15 algal biomass over 15
months
– R
Reduction
d ti off productivity
d ti it with
ith
reduced grazing.
Ambient
No
Grazing
• Caged regions with higher
bi
biomass
h
have significantly
i ifi
l
lower rates of productivity
(N.B. log scale)
– More
M
shading
h di iin d
denser stands
t d
– No nutrient release by grazers
82
Grazing & algal communities
Grazing alters the algal community type
High
•
Low
Distturbance
Calcareous
algae
Effects of grazing on algae depend
on the functional group
– Fleshy macroalgae are more
susceptible than CCA
– Many fleshy macroalgae have
chemical
h i l compounds
d
Algal turf
• deter feeding by fishes
– Algal turfs are intensively
grazed
Fleshy
Fl
h
Macroalgae
High
Low
Grazing
• but compensate by increasing
growth rates
83
Control of algal abundance on coral reefs
Eutrophication:
Overfishing:
Increased Nutrients
Decreased Herbivory
Coral
Disturbances
Increased algal growth
Increased algal abundance
Competition
Decreased coral abundance
Adapted from McCook, 1999 &
Diaz & McCook 2002
84
Is the high abundance of algae in the inshore reefs a
consequence of human impacts? Is this natural?
Inshore reefs:
-Offshore reefs
‐Dominated by fleshy algae
‐Apparently overgrowing corals
‐High nutrient and sediment inputs
‐Low densities of herbivorous fish
L d ii
f h bi
fi h
- Lower algal biomass
- Lower inputs of N, P & sediments
- Higher density of herbivorous fishes
•Difficult to answer because lack of historical data
•Investigate causes of algal abundance:
•Contribution of herbivory & nutrients
85
Photos by L. McCook
Herbivory vs. Nutrients
• Runoff of nutrients Æ
– Increases
Increases in biomass and in biomass and
shifts in spp composition
– Phase shifts from corals to algae • ENCORE:
(Enrichment of Coral Reefs)
– Used micro atoll reefs
• Laboratory studies – Increased N&P enhanced growth of coral reef algae
• Field experiments:
Fi ld
i
t
– Increased growth may not result in increased biomass in
result in increased biomass in the field One Tree island
– Telemetrically
y controlled
dispensing units (robots):
additions of : N, P, NP
– No effects of Ç N&P on biomass of
86
algal
l l tturfs
f
ENCORE: No effects of nutrient enrichment on algae
Why?
Herbivores might have consumed
algal growth!?
87
Koop, et al, 2001
Experimental Design: herbivory vs nutrients
Nutrients
High
Herbivory
Replicates
p
(Cages=Plates)
Medium
Caged
Open
Partial
1 2 3 4 5 6 7
Pl t
Plants
Response Variables
Ambient
1 2 3 4 5 ….… 25
• Density
• Length • Height
• # branches
88
Full cages
•Herbivore exclusions
Open plots
Partial cages
89
90
Simultaneous manipulation of nutrients and herbivory
Sargassum fissifolium Density
Den
nsity (no.//plate)
2000
1000
Nutrients
Ambient
Medium
High
0
Effects of herbivores >
effects of nutrients:
Grazers consume
the excess of algal
production
Caged
Open
Partial
Herbivory Treatments
Diaz-Pulido & McCook, 2003. Ecology
91
Proportion of Injured Sargassum
Nutrients
Ambient
Medium
High
Proportion of the
total n
no. of rec
cruits
0.4
0.3
0.2
N x H: better food quality for
herbivores after N & P
enrichments
0.1
0
Caged
Open
92
Herbivory treatments
Diaz-Pulido & McCook, 2003. Ecology
Conclusion
• Nutrients have the potential of increase algal p
g
growth but there is little biomass accumulation
• Why?
Why? herbivores consume excess algal herbivores consume excess algal
production (except when herbivores scarce)
• Effects of Herbivores >>> nutrients
• C
Critical role of herbivores in preventing algal iti l l f h bi
i
ti
l l
blooms
Video of Herbivorous fish grazing Surgeon fish
Caribbean P7190030.MOV
93
Roles of coral disturbances
(e.g. bleaching)
on algal dynamics
94
Control of algal abundance on coral reefs
Eutrophication:
Overfishing:
Increased Nutrients
Decreased Herbivory
Coral
Disturbances
Increased algal growth
Increased algal abundance
Competition
Decreased coral abundance
Adapted from McCook, 1999 &
Diaz & McCook 2002
95
GBRMPA
96
Belkelmans & Oliver 1999
1998 Coral Bleaching Event
-How important are coral disturbances to shifts from
corals to algae
97
Orpheus Is., GBR
Conclusions
Healthy Porites
100
Coral
Cove
er (%)
80
60
40
Algal turfs
20
• Coral disturbances are
fundamental to coral - algal
dynamics and algal
recruitment
0
AM J J A S O N D J F M AM J J A S O N D J F M A M J J A
1998
1999
2000
• Coral mortality was
universally followed by algal
recruitment
Bleached Porites
100
Cover (%)
C
80
60
Algal turfs
40
•Healthy
Healthy corals inhibited the
recruitment of algal
propagules
C
Coral
l
20
0
AM J J A S ON D J F MAM J J A S O N D J F MAM J J A
1998
Diaz-Pulido & McCook, 2002. MEPS
1999
2000
98
Apr 1998
Apr.1998
99
5 cm
1 month
10
0
5 months
10
1
-Algae won and corals lost
-Shift from corals to algae
15 months
10
2
Asparagopsis taxiformis
10
3
Nov. 1998, Pandora Reef
10
4
8 months
10
5
16 months
10
6
-Algal colonisation &
Coral recovery are variable
21 months
August 2000,
Pandora Reef
10
7
Coral bleaching and algal increase
Coral bleaching
Coral mortality
Algal colonisation
Diaz-Pulido & McCook, 2002
Hoegh-Guldberg, 1999
Future
F
t
reefs
f
dominated by algae
10
8
Cyclone tracks
Cyclones cause coral mortality and may
enhance algal colonisation, contributing to
reef decline
10
9
THE PLAN
1. Overview of benthic algae on coral reefs
2 Ecological roles
2.
3. Spatial & temporal distribution
4. Phase shifts & causes
5 Interactions between corals and algae
5.
11
0
THE PLAN
• Mechanisms
• Competitive interactions between algae & corals
Effects on coral larvae
Effects on coral recruits
Effects on adult corals
• Coral Recovery: roles of algae
11
1
Importance of coral –
Importance of coral – algal competition
p
in reversal of phase shifts
Coral – Algal
interactions
Bellwood et al 2004
11
2
Why Coral –– Algal Competition is Important?
Why Coral • Key process structuring marine communities
• Key to the overall status of coral reefs
Key to the overall status of coral reefs
– Æ because the relative amounts of both determine reef condition
– Degradation during “phase shifts” amounts to an g
g p
imbalance in coral‐algal competition • Healthy reefs
– Corals often competitively superior to algae
p
y p
g
•
Stressed or disturbed corals (eg bleaching):
– Algae rapidly overgrow corals: i.e. algae are
released from competitive pressure by corals
and grow freely
•
Reduced grazing (e.g. overfishing):
– Fleshy macroalgae may become competitively
superior to corals
– Macroalgae grow unchecked by herbivores
and can potentially overgrow and kill corals
11
3
11
4
Mechanisms of coral ‐
Mechanisms of coral ‐ algal competition
Overgrowth
11
5
Mechanisms of coral ‐
Mechanisms of coral ‐ algal competition
Shading / overtopping
11
6
Mechanisms of coral ‐
Mechanisms of coral ‐ algal competition
Abrasion
11
7
Mechanisms of coral ‐
Mechanisms of coral ‐ algal competition
Chemical
11
8
Mechanisms of coral ‐
Mechanisms of coral ‐ algal competition
Recruitment
barrier
11
9
Mechanisms of coral ‐
Mechanisms of coral ‐ algal competition
Epithelial sloughing
12
Photo: GDP
0
Photo
Harrington
Photo:byL.L.Harrington
Matrix of probable interactions
among functional forms
SIZE
O = overgrowth 64
S = shading
6
C = chemical 15
A = abrasion
21
P = pre-emption 5
R = recruitment barrier 2
SI = epithelial shedding 1
- = none applicable
1
9 x 8 = 72 cells
McCook et al. 2001
12
1
General features of interactions
• About 90% (64/72) of potential interactions are overgrowth (
(resource domination/limitation)
d i i /li i i )
• Interactions more dependent on algal characteristics than on corals
– Algal turfs have minor effects on corals
– Foliose algae strong effects on corals
– Branching & massive coral: no large differences
B
hi &
i
l
l
diff
• Coral recruits are more vulnerable than adults
• Table ignores interactions with coral larvae
• Examples of
– Coral larvae
– Coral recruits
– Adult Corals
12
2
Interactions Macroalgae & coral larvae
12
3
Facilitation of coral settlement by Crustose calcareous algae
Crustose calcareous algae
Heyward & Negri 1999
•
•
Hydrolithon & Peyssonnelia are
preferred substrates for settlement
(Induce settlement)
No coral metamorphosis in the
absence of the crustose algae
12
4
Facilitation of coral settlement
• The CCA Titanoderma prototypum
:
– The most preferred substrates for coral settlement.
l
l
• Settlement rates on this alga:
– Higher than on other CCA • Significance
Significance of this facilitation at of this facilitation at
the ecosystem level:
– Remains unclear
CCA Titanoderma prototypum with coral
spat (white dots; photos by L. Harrington)
Harrington et al 2004
12
5
Different corals respond differentlyy
CCA Induced Settlement
Coral 1: Goniastrea
Coral 2: Stylaraca
CCA
CCA
Turfs, No CCA
Golbuu & Richmond 2007
Turfs, No CCA
12
6
CCA did not induce Settlement
Platygyra dadelea
50
Coral
larvae
15L
1.5
Inhibition of Coral
Settlement by
Macroalgae
2,3,5 days:
Scored larvae
remaining in
th surface
the
f
Porolithon
P
lith
onkodes
3cm
8 days:
% Settlement
12
7
2 Days old larvae
Larvae on water surface
% Coral Larvae
e on Surface
100
P<0.001
90
n=4
• Macroalgae affected g
behaviour:
80
– Effects varied between taxa (incl. same genus)
(incl same genus)
70
– More larvae actively swimming in Sargassum
swimming in Sargassum
tenerrimum
60
50
40
Algal
turfs
Fleshy
algae
Crustose
Algae
12
8
Diaz-Pulido et al 2009.
8 Days old larvae
Coral settlement
% Cora
al larval Settlem
ment
40
P<0.001
30
• Macroalgae affected % g
settlement:
– Effects varied between taxa
– Higher settlement in CCA & Higher settlement in CCA &
algal turfs
– Low settlement in most treatments with fleshy algae 20
10
– Inhibition of settlement
0
Algal
turfs
Fleshy
algae
Crustose Algae
12
9
Diaz-Pulido et al 2009.
Summary Interactions between coral larvae and algae
g
• Most
Most CCA induced settlement
CCA induced settlement
• Strength of settlement induction varies among CCA taxa
among CCA taxa
• Some coral specificity for some CCA
• Fleshy macroalgae reduce settlement
• Mechanisms:
– Chemical
– Shadingg
13
0
Interactions Macroalgae & Coral Recruits
13
1
Macroalgae reduce the abundance of
coral recruits
Numbers of
Di d
Diadema
are
increasing
Diadema
remove algal
biomass
Increase coral
density
13
2
Effects of macroalgae
Effects of macroalgae on coral juveniles
Diameter C
Change of C
Coral Recruitts (cm)
Number of coral recruits
bitten by fish
Algae reduce growth of
coral recruits, BUT..
Protected coral recruits
from parrotfish predation
13
3
D.Venera-Ponton 2009
Interactions
Macroalgae & Adults Corals
13
4
Effects of herbivory on competition
Jompa and McCook 2002
13
5
Effects of herbivory on competition
X
• More coral tissue mortality with algae
• Algae suppressed coral growth
• Caging increased algal d l l
growth
• Algae grew more with coral Algae grew more with coral
damaged
Jompa and McCook 2002
13
6
Coral overgrowth by algae
Lobophora variegata
13
7
Coral overgrowth by algae
13
8
Algae may kill corals by chemical
interactions
+ Corallophila
+ other turfs
Jompa & McCook 2003
13
9
Mechanism:
Chemical ?
Microbial ?
Microbial ? Red alga Corallophila
14
0
Macroalgae may harbour
pathogens that kill corals
+
=
N=40;
50% died
algae
+No
(Control) =
Nugues et al 2004
N=40;
0 % died
14
1
Macroalgae may kill corals by
Algae
Coral
leakage of DOC
• Algae
g leak dissolve organic
g
carbon DOC
• Æ Ç bacterial growth on corals
0.02 um filter
– Corals become stressed as a
result of hypoxia
– Cause coral mortality
– Contribute to reef degradation
• Positive feedback loops
might
g be created during
g
phase shifts:
• Increase algal abundance
Æ higher levels of DOC
Coral mortality
100% dead
50-99% dead
< 50%dead
Death next to algae
Discoloration
No change
14
2
Smith et al 2006
Not every story do with algae on
reefs is negative
Sargassum cover reduced
g
bleaching
McCook, Jompa & Diaz-Pulido. 2001
14
3
Coral
Coral Recovery Following Bleaching
Recovery Following Bleaching
14
4
Ecological phase shifts
Disturbance
Bellwood et al. 2004. Nature
14
5
Coral bleaching in the
Southern Great Barrier Reef, 2006
200 Km
14
6
Feb 2006
%C
Cover
GBRMPA
Feb 2006
Lobophora
Diaz-Pulido et al 2009. PLoS One
Aug 2006
14
7
Feb 2008
Aug 2006
14
8
Diaz-Pulido et al 2009. PLoS One
Feb 2008
Roles of algae in reef resilience
• Mechanisms of Resilience
1) Seasonal dieback in macroalgae
Winter
Summer
14
9
Diaz-Pulido et al 2009. PLoS One
Roles of algae in reef resilience
• Mechanisms of Resilience 1) Seasonal dieback in macroalgae
2) Rapid coral regrowth (No coral settlement)
15
0
Algal overgrowth by Coral
E
Engulfed algae
Old skeleton
1mm
Engulfed layer of algae
Regenerating skeleton
15
1
Diaz-Pulido et al 2009. PLoS One
Roles of algae in reef resilience
• Mechanisms of Resilience 1) Seasonal dieback in macroalgae
2) Rapid coral regrowth (No coral settlement)
15
2
Diaz-Pulido et al 2009. PLoS One
Roles of algae in reef resilience
• Mechanisms of Resilience 1) Seasonal dieback in macroalgae
2) Rapid coral regrowth (No coral settlement)
3) High competitive ability
15
3
Diaz-Pulido et al 2009. PLoS One
Conclusions
• Corals
Corals can be amazingly resilient under particular can be amazingly resilient under particular
circumstances
• Algae can be out competed by fast growing Algae can be out competed by fast growing
corals
• In this example, reef resilience is driven by I hi
l
f ili
i di
b
biological properties of corals & algae, not ecological processes l i l
– e.g. grazing
15
4
Summary
• Cora‐algal competition is an active process
• Outcomes are highly variable
– Algal species / groups
– Coral species
– Life history stages of corals
• Herbivory is important to removing algal biomass, but nutrients also can have an effect on algal growth
• Range of mechanism of competition (algae, corals)
R
f
h i
f
titi ( l
l)
• Climate change may enhance macroalgal dominance, 15
• BUT Æ
Æ large variability in coral reef resilience
5
Questions?
15
6
Field trip
p
• Examine coral algal interactions
– Common interactions in reefs at Bocas del Toro?
Common interactions in reefs at Bocas del Toro?
– Common algae interacting with the corals?
– Impacts of algae on coral tissue?
• Methods
h d
– Examine individual coral colonies along a transect
– Register the type of interaction and the alga interacting with each coral g
yp
g
g
colony
– Determine type of algae/taxa/species that is interacting with the coral
– Examine the damage to the coral colony : bleaching, paling, etc
Examine the damage to the coral colony : bleaching, paling, etc
15
7