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Centre for Environmental Sustainability (CEnS), School of the Environment, University of Technology, Sydney, New South Wales 2007, Australia
Plant Functional Biology and Climate Change Cluster (C3), School of the Environment, University of Technology, Sydney, New South Wales
2007, Australia
3
School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Victoria 3216, Australia
2
Keywords
Disturbance, genotypic diversity, recovery,
resilience, seagrass, Zostera.
Correspondence
Peter I. Macreadie, Plant Functional Biology
and Climate Change Cluster (C3), School of
the Environment, University of Technology,
Sydney, New South Wales 2007, Australia.
Tel: 61-2-9514 4038; Fax: 61-2-9514 4079;
E-mail: petermacreadie@gmail.com
Funding Information
Financial support for this work was received
from a UTS Early Career Researcher Grant (to
PIM), a Paddy Pallin Science Grant (to PIM),
an ARC DECRA Fellowship (DE130101084, to
PIM), and a UTS Partnership Grant (to PIM),
involving the Office of Environment and
Heritage, New South Wales Department of
Industry and Investment, Gosford City
Council, and Hornsby Shire Council.
Received: 30 July 2013; Revised: 14
November 2013; Accepted: 29 November
2013
Ecology and Evolution 2014; 4(4): 450
461
doi: 10.1002/ece3.933
Abstract
Resilience is the ability of an ecosystem to recover from disturbance without
loss of essential function. Seagrass ecosystems are key marine and estuarine
habitats that are under threat from a variety of natural and anthropogenic
disturbances. The ability of these ecosystems to recovery from disturbance will
to a large extent depend on the internsity and scale of the disturbance, and the
relative importance of sexual versus asexual reproduction within populations.
Here, we investigated the resilience of Zostera muelleri seagrass (Syn. Zostera
capricorni) to small-scale disturbances at four locations in Lake Macquarie
Australias largest coastal lake and monitored recovery over a 65-week period.
Resilience of Z. muelleri varied significantly with disturbance intensity; Z. muelleri recovered rapidly (within 2 weeks) from low-intensity disturbance (shoot
loss), and rates of recovery appeared related to initial shoot length. Recovery
via rhizome encroachment (asexual regeneration) from high-intensity disturbance (loss of entire plant) varied among locations, ranging from 18-35 weeks,
whereas the ability to recover was apparently lost (at least within the time
frame of this study) when recovery depended on sexual regeneration, suggesting
that seeds do not provide a mechanism of recovery against intense small-scale
disturbances. The lack of sexual recruits into disturbed sites is surprising as our
initial surveys of genotypic diversity (using nine polymorphic microsatellite
loci) at these location indicate that populations are maintained by a mix of sexual and asexual reproduction (genotypic diversity [R] varied from 0.24 to 0.44),
and populations consisted of a mosaic of genotypes with on average 3.6 unique
multilocus genotypes per 300 mm diameter plot. We therefore conclude that Z.
muelleri populations within Lake Macquarie rely on clonal growth to recover
from small-scale disturbances and that ongoing sexual recruitment by seeds into
established seagrass beds (as opposed to bare areas arising from disturbance)
must be the mechanism responsible for maintaining the observed mixed genetic
composition of Z. muelleri seagrass meadows.
Background
There is still major uncertainty about how climate change
will affect marine ecosystems, largely because of a lack of
understanding of the processes that provide insurance
against environmental change, that is ecosystem resilience.
In a broad sense, resilience refers to the capacity of ecosystems to cope with disturbance, without switching to an
450
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.
P. I. Macreadie et al.
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
451
P. I. Macreadie et al.
Disturbance/recovery experiments were adapted to measure resilience. Disturbance in seagrass ecosystems typically manifests in the form of habitat loss; thus,
experimental removal of habitat was used to represent
disturbance. Resilience (which includes the ability of a
system to recovery rapidly from loss of structure or function) was measured by the rate of seagrass recovery (i.e.,
time taken for % cover to return to background levels)
452
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Methods
Study location
This study was conducted in Lake Macquarie; Australias
largest coastal saltwater lake. The Lake covers an area of
110 km2 and is situated 130 km north of the city of
Sydney, on the east coast of Australia. The Lake has an
irregular shoreline with many bays and promontories
along its 170 km perimeter. It has an average water depth
of ~8 m and is connected to the ocean via a constricted
entrance that limits tidal variation. Seagrass is abundant
in the Lake, although restoration efforts and dedicated
management efforts have been necessary for reverting
declines in seagrass cover due to urbanization around the
Lake over the past few decades. The Lake now contains
one of the largest seagrass populations on the New South
Wales coast, representing 10% of the total seagrass area
in NSW.
The main species of seagrass in Lake Macquarie are
Zostera muelleri, Posidonia australis, Heterozostera nigricaulis, Halophila ovalis and Halophila decipiens. This study
focused on Z. muelleri; the most abundant species within
the Lake. We selected four study locations within the
Lake: Sunshine (330629.82S, 1513352.31E), Valentine
(325946.04S, 1513756.08E), Wangi (330351.54S,
1513459.70E), and Point Wolstoncroft (330707.61S,
1513520.95E). Each location contained relatively continuous meadows of subtidal (~0.21.5 m below mean
low water spring; MLWS) seagrass running parallel to the
shore.
Experimental design
P. I. Macreadie et al.
LOCATION
Pt. Wolstoncroft
SITE
PLOT
(Treatment)
Sunshine
Valentine
Wangi
1 2 3 4 5
Control (C)
Sampling
Experimental treatments were sampled 0, 2, 6, 12, 18, 36,
and 65 weeks after their establishment (October 20,
2010). Sampling involved visually estimating each replicate for % cover [using Seagrass Watch standard protocols, which involved two observers and use of a % cover
photograph standard; McKenzie et al. 2003], the presence
of flora or fauna, seagrass canopy height (6 haphazard
measurements per replicate), the approximate amount of
epiphyte cover on seagrass blades (low, medium, or high),
and density of shoots (controls only). Photographs of
each replicate were taken for reference purposes. Plastic
star pickets were used to mark each plot. To characterize
locations, we measured wet bulk density, and organic
matter, and mean shoot length at the start of the experiment.
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Procedural
control (P)
Shoot
regrowth (R)
Asexual
regeneration (A)
Sexual
regeneration (S)
Statistical analyses
Data were analyzed using univariate (SPSS) statistical
techniques. The main response variable of interest was
the percent cover of seagrass. Percent cover was analyzed
using a repeated measures ANOVA, with location and
treatment as between subject factors, and time since disturbance as the within subjects factor. The degrees of
453
454
0.001
0.001
<0.001
<0.001
0.001
0.001
<0.001
<0.001
0.001
0.001
<0.001
<0.001
0.009
0.017
<0.001
<0.001
120
119
120
118
Point Wolstoncroft
Sunshine
Valentine
Wangi
Calculated for the seagrass Zostera muelleri from four locations in NSW, Australia.
0.047
0.068
0.001
0.001
0.047
0.068
0.002
0.003
+ZosNSW29
+ZosNSW19
ZosNSW25
N
Population
+ZosNSW02
Genotypic diversity
0.127
0.182
0.008
0.010
+ZosNSW38
Results
1.000
1.000
0.154
0.150
+ZosNSW46
+ZosNSW18
+ZosNSW23
+ZosNSW15
<0.001
<0.001
<0.001
<0.001
P. I. Macreadie et al.
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Resilience experiments
We detected significant differences in percentage seagrass
cover for all the main effects and interactions, with the
exception of disturbance treatment 9 location, which was
marginally non-significant (Table 3). Post hoc tests
showed that each disturbance treatment differed from one
another in their percentage seagrass cover (Fig. 3A): controls had the highest seagrass cover (37%), followed by
the procedural control (30%), regrowth (21%), asexual
regeneration (14%), and sexual regeneration (1%). The
1% recovery in sexual regeneration may actually be the
result of rhizomes jumping over borders; indeed, we did
observe rhizomes jumping borders throughout the experiment, but the reduced frequency of sampling toward the
end of the experiment made it difficult to trace the
rhizomes of plants that had established within plots to
the surrounding meadow. Sunshine, Valentine, and Wangi locations had similar percentage seagrass cover (21%,
24%, and 21%, respectively; Fig. 3B), whereas the percent
seagrass cover at Point Wolstoncroft was significantly
lower (16%; Fig. 3B). Point Wolstoncroft had the shortest
shoot length (Fig. 4A), highest wet bulk density (Fig. 4B),
and lowest sediment organic matter content (Fig. 4C).
Trends through time in percentage seagrass cover for
each location and treatment are shown in Figure 5. The
disturbance treatments all exhibited a similar pattern at
6.0
Calculated as respective probability from Table 1 x population size) for increasing locus combinations for the seagrass Zostera muelleri from four locations in NSW, Australia.
0.04
0.03
<0.01
<0.01
0.07
0.07
<0.01
<0.01
5.68
8.12
0.08
0.13
Point Wolstoncroft
Sunshine
Valentine
Wangi
120
119
120
118
120.00
119.00
18.53
17.72
15.24
21.62
0.98
1.24
5.68
8.12
0.18
0.33
1.05
2.06
0.02
0.03
0.07
0.07
<0.01
<0.01
0.07
0.07
<0.01
<0.01
+ZosNSW15
+ZosNSW02
+ZosNSW29
+ZosNSW19
ZosNSW25
N
Population
Table 2. Expected number of individuals with the same seagrass multilocus genotype.
+ZosNSW38
+ZosNSW46
+ZosNSW18
+ZosNSW23
P. I. Macreadie et al.
5.0
4.0
3.0
2.0
1.0
0.0
Wangi
Sunshine
Valentine
Pt. Wolstoncroft
455
P. I. Macreadie et al.
df
Mean Square
P-value
2.86
11.44
8.58
34.31
217.27
12776.5
1752.1
777.7
403.3
256.8
49.76
6.82
3.03
1.57
<0.001
<0.001
0.002
0.029
25865.4
1708.5
677.5
400.6
64.57
4.27
1.69
<0.001
0.008
0.085
4
3
12
76
(A)
(B)
Repeated measures ANOVA results. D and L were the between subject factors, and T was the within subject factor. The degrees of freedom for the within subject factors were adjusted using the
Greenhouse-Geisser correction to meet assumptions of sphericity.
Bold value represents P < 0.05.
(A)
(C)
(B)
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2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
P. I. Macreadie et al.
(A)
(B)
(C)
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Discussion
We found that Z. muelleri is resilient to both low- and
high-intensity disturbances when asexual regeneration is
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2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
P. I. Macreadie et al.
2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
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Conclusions
Overall, this study suggests that Zostera muelleri in Lake
Macquarie uses clonal growth as a means of rapidly
recovering from small-scale disturbances, and that sexual
recovery from seeds play little to no part in recovery at
small spatial scales.
Acknowledgments
We thank R. Gruber, B. McCarthy, and D. Poulos for
their assistance with data collection, Anna Stanley for
helping to process genetic samples, and Dr Adrian Jones
for assistance with preparing Figure 1.
Conflict of Interest
None declared.
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