Coral growth on three reefs: development of recovery ... - Springer Link

Coral Reefs (2010) 29:815–833 DOI 10.1007/s00338-010-0637-y

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Coral growth on three reefs: development of recovery benchmarks using a space for time approach T. J. Done • L. M. DeVantier • E. Turak • D. A. Fisk • M. Wakeford • R. van Woesik

Received: 16 February 2009 / Accepted: 3 May 2010 / Published online: 26 May 2010  Springer-Verlag 2010

Abstract This 14-year study (1989–2003) develops recovery benchmarks based on a period of very strong coral recovery in Acropora-dominated assemblages on the Great Barrier Reef (GBR) following major setbacks from the predatory sea-star Acanthaster planci in the early 1980s. A space for time approach was used in developing the benchmarks, made possible by the choice of three study reefs (Green Island, Feather Reef and Rib Reef), spread along 3 degrees of latitude (300 km) of the GBR. The sea-star outbreaks progressed north to south, causing death of corals that reached maximum levels in the years 1980 (Green), 1982 Electronic supplementary material The online version of this article (doi:10.1007/s00338-010-0637-y) contains supplementary material, which is available to authorized users. Communicated by Ecology Editor Prof. Peter Mumby T. J. Done (&)  L. M. DeVantier  E. Turak  D. A. Fisk  M. Wakeford Australian Institute of Marine Science, PMB #3, Townsville MC, QLD 4810, Australia e-mail: [email protected] R. van Woesik Department of Marine Biology, James Cook University, Townsville, QLD 4811, Australia L. M. DeVantier 20 Val Cres, Noosaville, QLD 4566, Australia E. Turak 1 rue Francois Villon, 95000 Cergy, France D. A. Fisk P.O. Box 1833, Cairns, QLD 4870, Australia R. van Woesik Florida Institute of Technology, 150 West University Boulevard, Melbourne, FL 32901-6988, USA

(Feather) and 1984 (Rib). The reefs were initially surveyed in 1989, 1990, 1993 and 1994, which represent recovery years 5–14 in the space for time protocol. Benchmark trajectories for coral abundance, colony sizes, coral cover and diversity were plotted against nominal recovery time (years 5–14) and defined as non-linear functions. A single survey of the same three reefs was conducted in 2003, when the reefs were nominally 1, 3 and 5 years into a second recovery period, following further Acanthaster impacts and coincident coral bleaching events around the turn of the century. The 2003 coral cover was marginally above the benchmark trajectory, but colony density (colonies.m-2) was an order of magnitude lower than the benchmark, and size structure was biased toward larger colonies that survived the turn of the century disturbances. The under-representation of small size classes in 2003 suggests that mass recruitment of corals had been suppressed, reflecting low regional coral abundance and depression of coral fecundity by recent bleaching events. The marginally higher cover and large colonies of 2003 were thus indicative of a depleted and aging assemblage not yet rejuvenated by a strong cohort of recruits. Keywords Climate change  Resilience  Benchmarks  Diversity  Acropora  Recovery

Introduction Rate of recovery from disturbance is one benchmark by which to judge ecosystem ‘wellbeing’, with slowing representing the approach of a critical tipping point, toward a less desirable state (van Nes and Scheffer 2007). For coral reefs, recent disturbances include diseases and bleaching from high sea temperatures (Hoegh-Guldberg 1999; Harvell et al. 2002; Hughes et al. 2003), over-fishing (Jackson et al. 2001),

123

816

run-off from rapid land-use change (van Woesik et al. 1999) and sea-star predator outbreaks (Endean and Cameron 1985; Done 1987). Such disturbances have resulted in a steady net decline in cover of living reef-building corals in many regions over the past several decades (Gardner et al. 2003; Bruno and Selig 2007). Yet there are few historical baselines by which to judge recovery (Connell 1997) or improve our understanding of the ecological trajectory of reef ecosystems through time. While the geological record can provide evidence of past events on reefs, taphonomic variability and ‘time-averaging’ often mask ecological change (Aronson 2007). Such change, operating on timescales of years to centuries, is more a reflection of the interplay between onsite ecological processes and exogenous disturbances (Hughes 1989). Understanding the nature of ecological change on timescales shared by individual corals and humans (i.e., years to decades) is particularly important, especially in light of increasing climate-related and local pressures on reefs this century (Done 1999; Hoegh-Guldberg 1999; Bellwood et al. 2004). Comparisons of rates of change with recent historical benchmarks should reveal whether present recovery rates have slowed (van Nes and Scheffer 2007). For example, in recovering coral assemblages, ‘slowing down’ in the rate of increase in the common monitoring parameter ‘percent coral cover’ could be a net outcome of lower rates of coral recruitment, colony growth rates, and/or higher ‘background’ mortality from predators, disease or other factors. Different species have different degrees of reliance on recruitment, versus repair and survival of older individuals, to maintain populations that are subject to disturbance (Linares et al. 2008). However, where coral-reef areas become denuded by catastrophic disturbance, recruitment of new individuals (from larvae or imported fragments— Done et al. 2007) is essential to rebuild coral cover and diversity. In field studies, delay or failure of recruitment may be inferred from absence of smaller size classes from post-disturbance coral size-frequency distributions (Bak and Meesters 1998). Since the 1960s, the principal cause of coral decline on the hundreds of mid-shelf GBR reefs between 15 and 20S has been three outbreaks of predatory sea-stars (Acanthaster planci Linnaeus) (Sweatman 2008). The outbreaks have been occurring at approximately 15-year intervals (Reichelt et al. 1990; Miller 2002). Densities of thousands of A. planci per hectare effectively denuded long sections of reef slopes of their living coral, while producing a prodigious output of planktonic larvae. On each occasion, the epicenter of the sea-star outbreak moved south, propagating at around one degree of latitude (100 km) every 2 years mainly through larval dispersal (Reichelt et al. 1990; Miller 2002). Short periods (weeks to months) of the sea-star’s most recent north–south propagation through the

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study area (Fig. 1b) (Miller 2002; Sweatman 2008) coincided with the 1998 and 2002 heatwaves that caused widespread coral bleaching events (Marshall and Baird 2000; Berkelmans et al. 2004). These disturbances, simultaneous in some places and sequential in others, might be expected to produce more coral mortality and sublethal effects than either disturbance alone. For example, sublethal bleaching is known to reduce the fecundity of affected corals (e.g., Szmant and Gassman 1990; Ward et al. 2000). The combination of regionally suppressed population sizes and reduced fecundity may undermine recovery of hard coral cover and diversity through reduced rates of recruitment of the affected coral species into denuded areas (DeVantier et al. 2006; Thompson and Dolman 2009). The current study investigates these propositions through observations on three reefs following the two most recent A. planci events, the first (early 1980s) without coincident bleaching, the second (turn of the century) with bleaching. The genus Acropora (Cnidaria; Anthozoa; Scleractinia) dominates most undamaged shallow reef slopes across the Indo-Pacific region. These corals are structurally analogous to trees and bushes in providing food and shelter in coralreef scapes. The genus Acropora comprises well over 100 species worldwide (Wallace 1999; Veron 2000). Accordingly, ‘…few aspects of the ecology of coral reefs are independent of the ecology of [Acropora] corals’ (Wallace 1999). Resilience of Acropora-dominated assemblages is therefore important in the long-term sustenance of reefs as structures (Kleypas et al. 2001; Perry et al. 2008) and of their mega-diversity (Patton 1994; Munday 2004; Graham et al. 2006; Carpenter et al. 2008). Acropora resilience is increasingly being put to the test: Acropora is the most favoured prey for A. planci (De’ath and Moran 1998; Pratchett 2007); Acropora is also extremely susceptible to high irradiance and heat stress, causing it to bleach and die over large areas of the GBR (and elsewhere) in 1998 and 2002 (Marshall and Baird 2000; Berkelmans et al. 2004). Among those colonies that recover from bleaching, reproductive output may be absent or greatly reduced in following spawning periods (Ward et al. 2000). In the GBR and Indo-Pacific more generally, rebuilding of local Acropora abundance is highly reliant of settlement of planktonic larvae (Harrison and Wallace 1990). This is unlike the Caribbean, where losses of the only two major reef-building Acropora species, to disease, have been catastrophic (Gardner et al. 2003) and recovery has a high reliance on vegetative reproduction from a steadily declining parent stock (Aronson and Precht 2001). Several meta-analyses (Pandolfi et al. 2003; Bellwood et al. 2004; Bruno and Selig 2007) report substantial declines in Acropora coral cover over large parts of the GBR and elsewhere. But there have also been places and

Coral Reefs (2010) 29:815–833

817

Green Island

Cairns

17°S

Feather Reef

(c) 50 40

0.5 0.4

Green

30

0.3

20

0.2

10

0.1 0

0

18°S Rib Reef

Townsville

Australia 0

2000

2010

40

10 8

Feather

30

6

20

4

10

2

0

20°S

100 km

1990

50

Cover (%)

19°S

1980

0 1980

1990

2000

2010 10

50

Cover (%)

(b) o Latitude ( S)

12 14 16

40

8

Rib

30

6

20

4

10

2

0

0 1980

18

1990 Hard coral

20

COTS per tow

148°E

Decade long reconstructions of recovery trajectories were inferred from short time series (1989–1994) of changes in coral assemblages at three reefs. We adopted a ‘space for time’ approach (Pickett 1989), which requires that the damaged reef areas be of sufficiently similar composition and are following the same recovery trajectory. However, by virtue of their location-specific disturbance histories, the reefs are deemed to be at different stages along that trajectory. Three GBR study reefs that met these criteria were selected at intervals of approximately 1 of latitude (*90– 120 km) apart within the dense tract of mid-continental shelf reefs (Fig. 1a): Green Island (16450 S), Feather Reef

COTS per tow

146°E

Study reefs, disturbances and the space for time approach

COTS per tow

(a)

1–3 m; *15% at 6 m). This study provides a test for that prediction. Here, we develop a comprehensive set of recovery benchmarks, focusing on the Acropora-dominated mid-shelf reefs of the central GBR (Done 1982). Instead of a direct estimate of ‘coral cover’, the raw data comprised identities, densities and sizes of coral colonies per unit area to allow investigation of underlying demographic rates, processes and the resultant ecological trajectories.

Cover (%)

periods of very strong Acropora recovery in the GBR (Ninio and Meekan 2002; Done et al. 2007; Sweatman et al. 2008; Wakeford et al. 2008) and elsewhere (Adjeroud et al. 2009). One such period—the 1980–1990s in the central GBR—is the focus of this report. When large devastated areas in the GBR are re-occupied by corals, the new coral cover initially increases slowly (when the corals are small and sparse) and then more rapidly (Halford et al. 2004; Sweatman et al. 2008), as coral abundances and individual colony sizes and extension rates increase to a maximum rate (Done et al. 1989). Species diversity has a propensity to initially rise rapidly (as new species arrive) and then to plateau (no new species arrive), and then possibly fall (as some inferior competitors for space are lost as the area becomes crowded—Connell 1978; c.f. Tomascik et al. 1996). Awareness of the potential for such non-linearities needs to be taken into account in the development and use of benchmarks. Using coral colony size and abundance data to model coral recovery on an Acanthaster-damaged reef of the central GBR, it was estimated (Done et al. 1989) that it should take 10–15 years (i.e., approaching the turn of the century) for heavily denuded shallow slopes to regain typical pre-disturbance levels of coral cover (*40% at

2000

2010

Year

Crown-of-thorns starfish (COTS)

1992

1996

2000

2004

Coral bleaching years 1998 and 2002 Sampling years (this study)

Fig. 1 Study reefs, disturbances and sampling details. a Location of reefs and study areas (black bars). Scale bar in each reef represents 1 km. b North–south progression of the most recent Acanthaster planci outbreak. Black dots indicate presence of outbreak densities.

Source Sweatman 2008. c Estimates of coral cover and A. planci abundance using 2-min manta-board tows around entire perimeters of the study reefs. Source Sweatman et al. 2008. Years of outbreaks, coral bleaching and sampling are also indicated

123

818

(17320 S) and Rib Reef (18290 S). The reefs lie far enough apart along the recurrent southward propagation path of the Acanthaster planci outbreak (Fig. 1b) that there are approximately 2-year lags between successive study reefs in both the mass arrival of A. planci larvae at the reefs, their growth to dense populations of feeding adults, their decimation of the corals and their disappearance. With outbreak populations in the 1980s typically in residence for 2–3 years (Reichelt et al. 1990), the calendar years of maximum cumulative coral loss and putative commencement of recovery (Fig. 1c) were 1980 at the northernmost reef (Green), 1982 at the reef 90 km to its south (Feather) and 1984 at the southernmost reef (Rib—a further 120 km south). In 1989, therefore, the reefs were 9, 7 and 5 years into a ‘post-Acanthaster’ period. All the reefs had relatively low cover in 1989 (5–10% in perimeter-wide mantatow surveys; Fig. 1c), but personal observations (TD) of the sizes of recruiting corals present in 1989 (largest at Green Island; smallest at Rib) were suggestive that Green Island was the most advanced in recovery and Rib the least advanced. These qualitative observations provided the impetus for the quantitative study reported here. The advent of a further A. planci outbreak that affected the study reefs around the end of the twentieth century provided an opportunity to compare the reefs’ more recent recovery performance against the benchmark trajectory derived from the 1989–1994 data. For the turn of the century disturbances, the calendar years of maximum cumulative coral loss to A. planci predation were 1998 (Green), 2001 (Feather) and 2002 (Rib) (Fig. 1c). The 1998 bleaching event was coincident with a relatively small seastar population at Green Island, and the February 2002 bleaching event was coincident with large outbreaks at Feather and Rib reefs (Fig. 1c; Berkelmans et al. 2004). At each reef, the combination of the 1998 bleaching with A. planci predation reduced live-coral cover to perimeterwide averages of 5% (Fig. 1c; Sweatman et al. 2008): from 10% at Green Island; from 30% at Feather Reef; from *40% at Rib Reef (Fig. 1c). The 2002 bleaching, by contrast, was mostly sublethal, with coral cover averaged around the entire perimeters of the study reefs remaining at the same low levels they had already fallen to after the 1998 bleaching and turn of the century A. planci disturbances, approximately 1, 3 and 5 years previously (Rib, Feather and Green, respectively—Fig. 1c).

Methods Field work Green, Feather and Rib reefs were surveyed in 1989, 1990, 1992 and 1994, which spanned years 5–14 of the recovery

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period, allowing for the lags caused by the *50 km year-1 southward progression of outbreaks discussed earlier (Table 1). The same reefs were re-surveyed opportunistically in mid-2003, about 1.5 year after a January–February 2002 period of thermal stress that caused the sub-lethal coral bleaching. The objectives of the field work were, first, to establish whether the coral assemblages were sufficiently similar to warrant a space for time approach and, second, to characterize and merge their recovery trajectories to obtain a generalized picture of recovery. The latter was done using large samples of the abundance, identity and sizes of corals at each reef through time. Two comparable sites, comprising a near-horizontal reef shoulder and adjacent shallow reef slope, were chosen on each reef, one in the north to north-east and the other in the south-west sector (Fig. 1a). Within the selected areas, sampling was haphazard. Three belt transects (usually 32 9 0.6 m—see Table 1) were placed (separated by *10–15 m) along three depth contours approximately 1, 3 and 6 m below the reef flat. The reefs were sampled to follow the trajectory of their coral assemblages through time. The identity and maximum lateral dimension of each hard coral colony C2 cm included in, or intercepted by, the belt transect was recorded to at least genus level (See Appendix 1 in Electronic Supplementary Material; ESM). The number of colonies sampled thus ranged from 1832 to 8679 per year (Table 1). The narrow belt transects used here provide an assessment of the Acropora-dominated coral understory, not the massive ancient colonies that emerge in places, and for which much larger sampling units are appropriate (Done 1987, 1988). The present analysis is confined to ‘hard’ corals: Anthozoan ‘hard’ corals, orders Scleractinia ([99% of colonies) and Helioporacea (\1%) and also Milleporina (class Hydrozoa; \1%); soft corals were abundant in patches, but they were not consistently identifiable or measurable by all team members. Whereas most hard coral observations were reported to species level in the field, in much of the present analysis they are grouped to the level of genus, or genus plus growth form (Appendix 1 in ESM), at which levels all the authors are equally competent. This grouping circumvented a potential source of amongobserver bias. The one exception was the important genus Acropora, for which all observers could recognize species, therefore allowing an analysis of changes of richness and composition within this genus. Because of time and logistic constraints, some transects were missed. Nevertheless, good samples were obtained at all reefs and all depths in all years, except Green Island at 6 m in 1993. In 2003, these same constraints meant transect length had to be reduced to 16 m (Table 1). The 2003 sample was obtained in the same general areas and depths,

Coral Reefs (2010) 29:815–833

819

Table 1 Study reefs showing years at the end of major Acanthaster planci (L.) predation event, time of census and putative time between end of predation event and census Reef

Green

End of predation

Year of census

1980

1989

9

2 (3)

18

6,217

1990

10

2 (3)

18

4,506

1993 1994

13 14

2 (2) 2 (3)

12a 18

4,743 7,018

2 (3)

18*

1,832 3,146

1998 Feather

Rib

1982

Time since end of first predation (years)

Time since end of second predation (years)

2003

5

Sample Sites (depths)

Transects

Colonies

1989

7

2 (3)

18

1990

8

2 (3)

18

2,630

1993

9

2 (3)

15b

1,857

1994

12

2 (3)

15c

2,281

2 (3)

18*

3,854

2000

2003

1984

1989

5

2 (3)

18

5,423

1990

6

2 (3)

18

4,388

1993

9

2 (3)

18

8,597

1994

10

2 (3)

18

6,181

2 (3)

18*

2,144

2002

3

2003

1

Outbreak populations of adult A. planci tended to take about 2 years to consume most reef slope corals on these reefs. Standard transect length was 32 m a

There were no 6-m transects at Green in 1993

b

There were no 6-m transects at Feather south site in 1993

c

There were no 6-m transects at Feather north site in 1994

* Non-standard transect length was 16 m in 2003 due to constraints of time and logistics

but with only half the linear and areal coverage. The efficacy of the transects in sampling generic richness was checked by plotting cumulative genus count versus cumulative colony count for each reef and year. Coral community parameters The Shannon–Weiner Diversity index H0 (genera) was calculated as: X H0 ¼  pi ðlog2 pi Þ; ð1Þ where pi is the proportion of colonies in genus ‘i’ and Evenness E (genera) as: E ¼ H0= log2 G;

ð2Þ

where G is the number of genera. The belt transect technique, as used in the present study, does not produce a standard estimate of percentage coral cover, so the following index was developed (based on Marsh et al. 1984): C ¼ 100  ðN  pD2 =4Þ= ðW þ DÞ  L;

ð3Þ

where C is the percentage cover, N is the number of colonies, D is the mean dimension of the N colonies, W is the width of the belt transect in centimeters (in this case

60 cm) and L is the length of the belt transect in centimeters (usually 3,200 cm). This equation assumes that all colonies are circles in a plane with a diameter equal to the mean lateral dimension recorded and that the width of the belt is the nominal width (60 cm), plus the mean diameter of all colonies to account for colonies extending beyond the 60 cm belt width. This index over-estimates true coral cover compared with the line intercept and point-sampling techniques when a large number of large corals extend beyond the belt (see also Zvuloni et al. 2008). However, there was no comparative bias in the present study because the same technique was used for all estimates. Descriptive and statistical analyses Microsoft Excel was used to store the data and generate descriptive statistics and graphs. Generic richness was plotted against number of colonies recorded on each sampling occasion as a check for the adequacy of sampling effort. The Statistix package was used to undertake twoway ANOVAs to investigate the general null hypothesis that there were no differences in coral cover and mean colony diameter among: (1) reefs and calendar years; (2) reefs and elapsed years; (3) depth and calendar years; (4) depth and elapsed years. Sampling units used included

123

820

both individual belt transects and sets of belt transects (see ‘‘Results’’).

Coral Reefs (2010) 29:815–833

Results Coral composition

Space as a proxy for time To develop performance benchmarks, data were ordered against time since A. planci disturbance (viz. years 5–14, Table 1). This is referred to as ‘years since disturbance’, ‘elapsed time’ or ‘putative recovery time’. This approach represents the use of space as a proxy for time and makes the simplifying assumption that the coral assemblage on each reef was indeed the same, differing only by its stage of recovery (i.e., time since disturbance). Pie diagrams of the generic composition of hard corals at each reef (sum of all diameters pooled across all depths and years for each reef and genus) were produced in Excel to illustrate the validity of this assumption. Sum of diameters for the dominant genera were then plotted as a stacked histogram versus ‘t’ (year since disturbance). For years 9 and 10 (for which there were 3 and 2 sets of observations, respectively—see Table 1), averages were used in the plot. Noise in the time-series plot was smoothed using a 3-point running mean across years. For each year of elapsed time for which there were data, size-frequency distributions were plotted for selected abundant corals. Coral size data were first grouped into 3-cm bins (up to 99 cm), plus single bins for 99–150 cm and 151–200 cm and [200 cm. These plots included the percentage of colonies and the percentage of area covered, smoothed across bins using two-point running means. The curve-fitting toolbox of Matlab 6.5 was used to produce plots and derive functions for rates of change in first, second and third quartile diameters of selected corals (‘all corals’ and two dominant Acropora growth forms) against years since disturbance ‘t’. Excel was used to fit trend lines for cover, H0 and E. Functions presented are those whose correlation coefficient R2 value best explained the variance in the data. The degree of congruence between ‘expected’ and ‘observed’ coral sizes in 2003 was examined to see where the 2003 reefs were in comparison with the benchmark trajectory derived from 1989 to 1994 data. The ‘years since disturbance’ functions for Acropora tables—the most visually prominent coral in recovery assemblages—were used to predict the ‘expected’ first, second (median) and third quartile diameters of these corals at years 1, 3, 5, 10 and 15. These quartiles were then compared graphically with the ‘observed’ first, second and third quartiles diameters recorded for Acropora tables in 2003 (nominally 1, 3 and 5 years into recovery). The degree to which the two plots did or did not match was a test of the veracity of the assumption that the 2003 reefs were indeed 1, 3 and 5 years along a trajectory, from a comparable starting condition.

123

The composition of the major coral genera and their bathymetric distribution on the reefs was sufficiently uniform to encourage a space for time exploration of the data set. The genera Acropora, Porites, Pocillopora, Montipora and Stylophora accounted for 75–80% of the total hard coral cover (Fig. 2a). Acropora was the dominant genus, both in terms of its cover, numbers of colonies (see below) and species diversity (50–52 species). Forty-eight other hard coral genera (114–121 species) accounted for the other 20–25% of hard coral cover. Acropora was the dominant genus in all 1- and 3-m transects and in most of the 6-m transects (Fig. 2b). The percentage cover of Acropora increased dramatically during 1989–1994 (Fig. 2c): 10–40% at 1 m; 5–25% at 3 m; 2–20% at 6 m. By year six of elapsed time (Fig. 2c), Acropora species accounted for one to two-thirds of the still relatively low cover (and also half the number of colonies—see below). By year 13, it had increased its relative contribution to total hard coral cover to almost 80%. By contrast, other genera increased only fractionally if at all above their 1989 starting values. In the 2003 samples, Acropora had declined markedly at all reefs in both absolute cover (Fig. 2c) and relative cover (except for 1 m at Rib Reef—Fig. 2b). Diversity Plots of cumulative genera versus cumulative colonies are presented in Fig. 3. Most of the curves in Fig. 3 reach a plateau (see exceptions below), which indicates that the differences in total numbers of genera per reef (G) reported below are probably real and not an artifact of the variability in total transect lengths sampled. In the 1989–1994 series, G ranged from 45 to 54 (Fig. 4a). In 2003, there were substantially fewer genera at Rib (39) and Feather Reefs (41). Reference to Fig. 3 shows the G curves for Feather and Rib were converging at asymptotes not much above the reported counts and well below the counts of these reefs in 1989–1994. At Green Island, by contrast, the curve was indistinguishable from the earlier series. It appears that in no case would use of full length transects in 2003 have increased G by more than 1 or 2 genera. The Shannon–Weiner diversity index H0 fell in 1990– 1993 because of a decline in E (evenness) (see Fig. 4c). These decreases corresponded to the rapid increase in Acropora cover (Fig. 2c). By contrast, in 2003, H0 and E were at or near their highest values (Fig. 4c), despite the low G and because of the levelling effect of the catastrophic loss of Acropora (Fig. 2—all reefs; all depths).

Coral Reefs (2010) 29:815–833

Rib

(a)

Feather

114 17

(b)

1.0

Green

114

121

52

50 19

8

Relative abundance (by % cover)

Fig. 2 Generic composition of hard corals at the study reefs. a Relative contribution to percentage cover (all years pooled). Numbers indicate numbers of species recorded in the most speciose genera. b Relative abundance of genera by percentage cover. c Comparison of 2003 estimates of coral composition and abundance at Rib Reef, Feather Reef and Green Island reef (left to right as stacked histograms) with 1989–1994 data that has been smoothed using a 3-point running mean (stacked area graphs). The x axis represents elapsed time (=years since disturbance), irrespective of reef

821

52 20

8

6

Depth 1 m

0.5 0.0

1.0

Depth 3 m

0.5 0.0

Depth 6 m 1.0 0.5 0.0

1989 1993 1990 1994

(c)

60

Cover (%)

40

20

2003

Depth 1 m

1989 1993 1990 1994

2003

1989 1993 1990 1994

2003

1989 - 1994 series

2003 series R G F

0

Cover (%)

40

20

0 40

Cover (%)

Depth 3 m

Depth 6 m

20

0 2

4

6

8

10

12

Year

While there was a low number of genera (G) at Rib and Feather Reefs in 2003 (nominally years 1 and 3 in Fig. 4d), there was a relatively high G at Green Island, despite it having the lowest of all colony densities. The latter may reflect Green Island’s accumulation of genera through a longer elapsed time (5 years) since the turn of the century disturbances or the apparently relatively small

impact of the disturbances at Green Island (Fig. 1c) or both. Both H0 and E at Feather Reef (year 3, Fig. 4d) were higher than in any following year. The single high scores for H0 and E in year 3 may be spurious, as may be their apparent declines from years 5 to 14 (suggested by R2 for plotted trend lines of only 0.29 and 0.39 for H0 and E, respectively).

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Coral Reefs (2010) 29:815–833

‘03

50

Hard coral cover and colony size

‘94 ‘93

‘89

The proposition that the north–south series of three reefs represented progressive stages in a coral recovery trajectory was supported by the 1989 data: highest hard coral cover (Fig. 5a) and largest coral colonies (Fig. 5b) were found at Green Island, lowest cover and smallest colonies at Rib Reef and intermediate cover and colony sizes were recorded at Feather Reef. In 1989–1994, average coral cover and colony sizes at all reefs increased from their 1989 base levels, especially at 1 and 3 m depth. The only exceptions were Green Island in 1989–1990 (where neither cover nor colony size increased at any depth) and Feather Reef, where there was no increase in mean cover at 6 m at any time (Fig. 5a), even though the corals at this depth did get larger (Fig. 5b). The two-way ANOVAs (Tables 2, 3, 4, 5) confirmed very strong effects of reef, calendar year, elapsed year and depth on coral cover and colony sizes. Merging the reefs in space for time series, covering recovery years 5–14 (Fig. 5c, d), mean hard coral cover rose rapidly from *5 to 55% (Fig. 5c) and mean coral diameter from *7 to 25 cm (Fig. 5d). Variability (reflected in the error bars) also increased dramatically over that time period, reflecting the broadening size-frequency

‘90

40 30 20

Feather

60

‘94 ‘90

‘89

50

‘03

40

‘93

30 20

Rib

60

‘90

50 40

‘89

‘03

‘93

‘94

30 20 0

5000

10000

No.of colonies Fig. 3 Generic richness. Genera were added in order of increasing abundance of colonies in the sample (which means that the last genus added on every curve was Acropora). Closed symbols represent 1989– 1994 series; open symbols represent 2003 series

No. of genera (G)

(a) 60

50

Green ‘03 Feather ‘03

40

Rib ‘03

60

G

50

4.0

40

H’

3.0

30

2

4

6

8

20

0.8

10

0.6

E

R

2003 F G

1990

1993

1989 - 1994 series

(d) R

1.0 0.1 0.01 All corals Acropora ‘tables’ Acropora ‘corymbose’

6

8

Year

10

12

2003

2003 1989 - 1994 series F G

60

4

1994

Survey year

10.0

2

E

0.4 1989

10

Sample size (# colonies x 10 3)

(b)

H’

2.0

0 0

0

123

(c)

2003 series 1989 - 1994 series

30

No. of colonies x 103

Fig. 4 Sample sizes, richness and diversity. a Number of genera, highlighting small sample size in 2003 due to use of 16-m transects instead of 32-m transects. b No. of colonies in samples in 2003 at Rib (R), Feather (F) and Green (G), and ordered against elapsed time. c Counts of genera (G) and estimates of Shannon diversity H0 and evenness E against year of survey. Mean and standard deviation. N = 3 reefs. d Same as (c), ordered against elapsed time, and for Rib (R), Feather (F) and Green (G) in 2003

No. of genera (G)

Green

60

14

No. of genera (G)

No. of genera

No. of genera

No. of genera

822

G

50 40 4.0

30

H’

3.0

20

H’

2.0

10

0.8

E

0

0.6 0.4

0

2

4

6

8

Year

10

12 14

E

Coral Reefs (2010) 29:815–833

Rib Reef

(a) Hard coral cover (%)

Fig. 5 Hard coral cover and diameters (mean ± 1 SD) 1989– 1994 and 2003 at Rib (R), Feather (F) and Green (G) reefs and three depths. a Percentage cover as estimated using Eq. 3. b Colony diameter. c Percentage cover versus putative recovery time. d Colony diameter versus putative recovery time

823

Feather Reef

Green Island

80 60 40 20 0

Colony diameter (cm)

(b) 60 40 20 0

1989 1993 1990 1994

2003

1989 1993 2003 1990 1994 1m

(d)

2003 1989 - 1994

60

R

G

40

6m 2003 1989 - 1994

40

R

Diameter (cm)

Cover (%)

(c) 80

3m

F

20 0

1989 1993 2003 1990 1994

G

30 20

F 10 0

0

2

4

6

8

Year

distributions of many dominant corals. In 2003 (when the reefs were nominally at years 1, 3 and 5 in a second recovery period), the mean and variability in coral cover (Fig. 5c) and colony sizes (Fig. 5d) were more like they had been at 7–10 years in the earlier series. Abundance and colony size The contributions of individual taxa to the strong growth of years 5–14 are illustrated in Fig. 6. The size (mean and variability) of several important coral groups tended to increase through some or all of the 5- to 14-year period from very low starting levels: viz., branching Acropora (Fig. 5b), table Acropora (Fig. 6c); massive Faviidae (Fig. 6); massive Porites (Fig. 6g). The abundance of colonies, by contrast, often peaked around year 9 and fell in years 10–14 (as the increasing cover of larger corals overtopped and hid the smaller corals). In 2003, the number of colonies on the reefs was exceptionally low compared with

10

12

14

0

2

4

6

8

10

12

14

Year

peak abundance in the 1989–1994 series (Figs. 4b, 6), even accounting for the shorter transects. This was true for juvenile Acropora (flat 2–4 cm colonies derived from recent larvae settlement, Fig. 6a), Acropora branching forms (Fig. 6b), Acropora tables (Fig. 6c), and for corymbose (compact clumpy) Acropora colonies (Fig. 6d). Foliaceous Montipora were even sparser than they had been previously (Fig. 6e). In 2003, it was only at Feather Reef that densities and sizes of two coral groups matched those of the 1989–1994 series: massive Faviidae (Fig. 6f) and branching Porites (Fig. 6h). The relatively low abundances and large mean size and variability of the majority of coral groups in 2003 (Fig. 6b–i) suggest the specimens sampled were primarily survivors of the end of the century disturbances, not new corals that had recruited 1, 3 or 5 years earlier. In other words, the strong recruitment that characterized the 1989–1994 series was not evident in 2003. The trend of increasing variability in coral sizes in years 5–14 (Figs. 5 and 6) was because of ongoing recruitment of

123

824

Coral Reefs (2010) 29:815–833

Table 2 Hard coral cover Reef (No. of transects)

1989

1990

1993

1994

(a) Hard coral cover [%, (mean, variance)] by reef and calendar year Rib (6)

5 (5)

7 (8)

34 (30)

38 (56)

Feather (6)

15 (58)

21 (131)

41 (80)

48 (103)

Green (6)

20 (75)

17 (41)

31 (266)

34 (445)

Total (18)

13 (80)

15 (90)

35 (130)

40 (212)

Source of variation

SS

df

(b) ANOVA—Hard coral cover (%) by reef and calendar year Reef 1209.062 2 Calendar year Interaction Within Total

10262.350

MS

P-value

F crit

604.5312

5.5787

0.0060

3.1504

3

3420.7847

31.5672

2E-12

2.7581

1.5233

0.1861

2.2541

990.454

6

165.0756

6501.903

60

108.3650

18963.770

71

Year interval (No. of transects)

F

Average

Variance

(c) Hard coral cover (%) by elapsed years of recovery Years 5–7 (18) Years 8–9 (18)

9 25

39 115

Year 10 (18)

32

174

Years 12–14 (18)

38

295

Source of variation

SS

df

MS

F

P-value

F crit

17.9370

1E-8

2.7395

(d) ANOVA—Hard coral cover (%) by elapsed years of recovery Between groups Within groups Total

8377.388

3

2792.4626

10586.38 18963.770

68 71

155.6821

Data summaries and ANOVA tables for reef, calendar year and elapsed year. Elapsed years combined into four groups to provide balanced design for ANOVA. For the small number of missing data cells (see Table 1), means of closest estimate (date and place) were used

small corals and growth of successive year classes. In year 5, most corals were \20 cm across (Fig. 7): in subsequent years, the size-frequency distributions became broader (to [100 cm), although the populations did retain their smallest size classes (most obvious in the fast growing Acropora tables, Fig. 7a). Although small corals continued to recruit to the visible coral assemblage (see also Fig. 6a), their abundance and contribution to total hard coral cover became proportionally reduced through time and the contribution of larger colonies became proportionally greater (shaded shapes in Fig. 7). A similar progression was observed in foliaceous corals (Fig. 7b) and, less obviously, in corals with slow growth rates (e.g., genera such as Favia, Favites, Cyphastrea, Platygyra and Montastrea— Fig. 7c). The variously multi-modal and skewed natures of the size-frequency distributions are also a reminder of the limitations of means and standard deviation as descriptive statistics for such populations: the estimates of means and

123

variability are inordinately influenced by a small number of very large colonies. Plots of the first, second and third quartile diameters against elapsed time (Fig. 8) highlight the contribution of colony growth to the increase in coral cover and variability from year 5 to 14. For all genera combined (Fig. 8a), first, second and third quartile diameters were all small in year 5: viz. 5, 6 and 9 cm, respectively. By year 14, they had increased to *9, 12 and 28 cm. In two abundant corals— Acropora ‘corymbose’ (Fig. 8b) and Acropora tables (Fig. 8c), third quartile diameters had reached 35 and 75 cm (respectively), by years 12–14. Because these larger corals were still relatively abundant in year 14 (Fig. 6c, d), they were making major contributions to total hard coral cover. These Acropora’s first quartile diameters also increased faster than did those of all corals combined (to around 14 and 30 cm, respectively). This increasing trend is a flow-on effect of the fall in abundance of 2–4 cm

Coral Reefs (2010) 29:815–833

825

Table 3 Hard coral diameters through time (1989–1994) Reef (No. of transects)

1989

1990

1993

1994

(a) Hard coral diameter [cm (mean, variance)] by reef and calendar year Rib (6)

8 (2)

10 (4)

16 (12)

21 (23)

Feather (6)

11 (8)

15 (8)

22 (12)

24 (26)

Green (6)

15 (16)

17 (9)

20 (44)

22 (111)

Total (18)

11 (17)

14 (17)

20 (27)

22 (50)

Source of variation

SS

df

MS

F

(b) ANOVA Hard coral diameter (cm) by reef and calendar year Reef 372.246 2

186.1233

8.1218

Year

465.2905

20.3038

Interaction

1395.872

3

0.0008

3.1504 2.7581

0.9643

0.4571

2.2541

MS

F

P-value

F crit

25.4899

4E-11

2.7395

132.591

6

22.0986

1374.987

60

22.9165

Total

3275.697

71 Average

F crit

3E-9

Within

Year interval (No. of transects)

P-value

Variance

(c) Hard coral diameters (cm) by elapsed years of recovery Years 5–7 (18) Years 8–9 (18)

9 18

7 22

Year 10 (18)

20

18

Years 12–14 (18)

22

37

Source of Variation

SS

df

(d) ANOVA—Hard coral diameters (cm) by elapsed years of recovery Between year intervals

1611.868

3

537.2896

Within groups Total

1433.339 3045.208

68 71

21.0785

Reef by calendar year (a) data summary and (b) ANOVA table. Reef by elapsed year (c) data summary and (d) ANOVA table. Elapsed years combined into four groups to provide balanced design for ANOVA. For the small number of missing data cells (see Table 1), means of closest estimate (date and place) were used

juvenile corals starting around year 9 (Fig. 6a). Had this fall not occurred, more juveniles would have grown to the smallest sizes identifiable to species (usually 4–6 cm), tending to keep the first quartile diameter more constant through time. Benchmark trajectories The functions that describe the year 5–14 trajectories for cover, size and diversity (Table 6) varied in their utility as benchmarks for other samples. The functions with the poorest fit (low R2s) were Shannon Wiener’s H0 (R2 = 0.29) and Evenness E (R2 = 0.39). Coral cover was only moderately well modelled (R2 = 0.56). The functions that accounted best for changes against elapsed time were those for number of genera G (R2 = 0.77) and colony sizes (R2 = 0.62–0.79). Function predictions for all variables for years 1, 5, 10 and 15 in a recovery trajectory from a low

base are provided in Table 6. Comparison with predictions of the 2003 quartile colony diameters of table Acropora are illustrated in Fig. 9. The diameters at all three reefs were much larger than predicted for their putative elapsed years since the turn of century disturbances (viz. 1, 3 and 5 years). Along with the very small colony counts (Fig. 9b; see also Fig. 8), this comparison indicates that a recovery sequence (that would be signified by abundant small corals in years 1–5 in Fig. 9a) was yet to commence. Summary of results Figures 5c, 6, 7, 8 and 9 provide some new insights into the reefs in 2003 that are not evident from conventional representations of percent cover (Fig. 5a) and average colony sizes (Fig. 5b) alone. Coral cover and sizes were larger in 2003 than their predicted values for years 1–5 (Figs. 5c, d, 6, 8 and 9). The abundances and colony sizes did not

123

826

Coral Reefs (2010) 29:815–833

Table 4 Hard coral cover—depth variability through time (1989–1994) Depth (No. of transects)

1989

1990

1993

1994

(a) Hard coral cover [%, (mean, variance)] by depth and calendar year 1 m (6)

19 (143)

19 (192)

44 (156)

48 (331)

3 m (6)

12 (46)

13 (61)

30 (126)

39(146)

9 (13)

12 (14)

32 (30)

32 (87)

13 (80)

15 (90)

35 (130)

40 (212)

6 m (6) Total (18) Source of variation

SS

df

(b) ANOVA of hard coral cover by depth and calendar year Depth 1748.866 2 Calendar year Interaction Within Total

10262.350

3

223.689

6

6728.860

60

18963.770

71

Depth (No. of transects)

Years 5–7

MS

F

P-value

F crit

874.4332

7.7972

0.0010

3.1504

3420.7846

30.5025

4E-12

2.7581

0.3324

0.9172

2.2541

37.28155 112.1476

Years 8–9

Year 10

Years 12–14

(c) Hard coral cover [%, (mean, variance)] by depth and elapsed years of recovery 1 m (6) 3 m (6)

12 (73) 7 (25)

32 (67) 25 (120)

39 (321) 25 (138)

48 (444) 32 (290)

6 m (6)

8 (11)

20 (118)

25 (138)

33 (83)

Total (18)

9 (37)

26 (118)

30 (187)

38 (298)

Source of variation

SS

df

MS

F

P-value

F crit

0.0025

3.1504

(d) ANOVA Hard coral cover by depth and elapsed years of recovery Depth Year Interaction Within Total

1909.777

2

954.8889

7914.111 350.888

3 6

2638.0370 58.4815

8625.064

60

143.7538

18799.778

71

6.6427 18.3516 0.4068

-8

1E 0.8717

2.7581 2.2541

(a) Calendar year data summary and (b) ANOVA. (c) Elapsed year data summary and (d) ANOVA. Elapsed years combined into four groups to provide balanced design for ANOVA. For the small number of missing data cells (see Table 1), means of closest estimate (date and place) were used

represent rapid growth, however, but rather revealed an ageing assemblage. There was almost an order of magnitude decline in abundance of corals on the reefs in 2003 compared with 1989–1994 (Fig. 4b), not just half the density, as it would be if it were solely because of the shorter transects. In brief, the coral cover in 2003 comprised very few colonies (Figs. 4b, 6), but the colonies were larger than would be expected of sites that were only 1, 3 and 5 years into a vigorous recovery from a low base situation (Fig. 9). The meager cohort of Acropora juveniles at two of the three reefs (Feather and Green Reefs— Fig. 6a) suggests that there had been no pulses of larval settlement following the turn of the century disturbances. This is in stark contrast to the strong recruitment pulse detectable through the age structure in the 1989–1994 series (Fig. 7).

123

Discussion The present study reports vigorous upward trends in coral growth on three representative mid-shelf reefs on the GBR at a time (1990s) when meta-analyses of its coral cover suggested most reefs were in the middle of a multi-decadal decline (e.g., Pandolfi et al. 2003; Bellwood et al. 2004; Bruno and Selig 2007). Our study reefs of the 1980–1990s had a strong capacity for hard coral recovery following catastrophic disturbance by the crown-of-thorns starfish Acanthaster planci: a north–south wave of coral recovery followed in the wake of the north–south wave of coral mortality caused by A. planci. Unlike many monitoring studies that are established in high coral areas where the only way to go is down, these areas were initially low in coral cover and their recovery was spectacular.

Coral Reefs (2010) 29:815–833

827

Table 5 Hard coral diameters—depth variability through time Depth (No. of transects)

1989

1990

1993

1994

(a) Hard coral diameters [cm (mean, variance)] with depth and calendar year 1 m (6)

14 (26)

15 (22)

23 (36)

28 (81)

3 m (6)

10 (13)

14 (27)

18 (22)

19 (13)

6 m (6)

10 (6)

13 (7)

18 (16)

19 (11)

Total (18)

11 (17)

14 (17)

20 (27)

22 (50)

Source of variation

SS

df

(b) ANOVA of hard coral diameters with depth and calendar year Depth 355.434 2 Calendar year

MS

F

177.7172

7.6367

1395.872

3

465.2905

19.9940

128.102

6

21.3504

0.9174

Within

1396.289

60

23.2715

Total

3275.697

71

Interaction

Depth (No. of transects)

Years 5–7

Years 8–9

P-value

F crit

0.0011

3.1504

4E-9

2.7581

0.4889

2.2541

Year 10

Years 12–14

(c) Hard coral diameters [cm (mean, variance)] by depth and elapsed years of recovery 1 m (6) 3 m (6)

10 (10) 9 (4)

18 (6) 15 (9)

23 (13) 20 (10)

27 (116) 19 (19)

6 m (6)

9 (6)

13 (1)

17 (14)

20 (5)

Total (18)

9 (6)

15 (10)

20 (16)

22 (56)

Source of variation

SS

df

MS

F

P-value

F crit

0.0006

3.1504

(d) ANOVA of hard coral diameters by depth and elapsed years of recovery Depth

299.350

2

149.6751

Elapsed years Interaction

1795.514 143.603

3 6

598.5048 23.9338

Within

1062.050

60

17.7008

Total

3300.518

71

8.4558 33.8122 1.3521

-13

6E 0.2487

2.7581 2.2541

(a) Calendar year data summary and (b) ANOVA. (c) Elapsed year data summary and (d) ANOVA. Elapsed years combined into four groups to provide balanced design for ANOVA. For the small number of missing data cells (see Table 1), means of closest estimate (date and place) were used

The strong recruitment, growth and survival of a dense and diverse assemblage of hard corals revealed by analysis of the 1989–1994 series is a demonstration of the capacity of a heavily damaged area to recover to a coral-dominated state through larval settlement, recruitment and growth. The recruitment of corals to the coral assemblages in 1989– 1994 means the sites—embedded in a dense archipelago of reefs (Fig. 1a)—were well connected oceanographically to adult source populations for larvae. Moreover, the strong increases in coral cover and colony sizes were evidence of the adequacy of (1) the onsite environmental conditions for coral settlement and growth: (substrate, sediment characteristics, light, water quality, hydrodynamic forces) and (2) on-site ecological conditions (such as sufficient grazing to suppress algal competitors (Bellwood et al. 2004; Mumby et al. 2006) that promoted strong growth and survival

among coral recruits. In short, these are the essential prerequisites for resilience that drove the north–south wave of strong coral recovery that followed in the wake of A. planci. This finding is consistent with the findings of Miller (2002) and Sweatman et al. (2008), who reported generally rising trends in hard coral cover on reefs off Cairns and Townsville through most of the 1990s, contrary to the meta-analyses noted elsewhere. However, it was a different story in 2003, when a one time sampling effort compared unfavorably with the 1989–1994 based benchmark trajectory. By criteria of percentage coral cover and colony size, the 2003 samples (putatively at 1, 3 and 5 years post-disturbance) were ahead of the trajectory (years 7–10 equivalent), but the low coral abundance (numbers of colonies per unit area) suggested otherwise. The comparatively large sizes of the

123

828

Coral Reefs (2010) 29:815–833

Diam. (Cm) No. Colonies

(a)

Acropora juveniles (2 - 4 cm)

1000

0 10

1989-94 2003

5

500

0 100

0 100

50

50

0 0

Diam. (Cm) No. Colonies

(d)

2

4

6

8

10

12

14

0

2

4

8

6

0 10

12

14

(e)

(f)

25

500

0 60

0 100

0 40

30

50

20

4

8

6

10 12 14

0

(h)

500

2

4

6

8

0

10 12 14

(i)

Branching Porites

1000

1000

500

500

0

0

0

50

50

25

25

25

2

4

6

8

10

12

14

14

2

4

6

8

10 12 14

Encrusting Porites

0

0 0

12

Year

50

0

10

Massive Faviidae

Year

Massive Porites

1000

8

6

0

0

Year

(g)

4

1000

500

2

2

Year

Foliaceous Montipora

50

0

0

Year

Corymbose Acropora

1000

0

Acropora tables

1000

250

Year

Diam. (Cm) No. Colonies

(c)

Branching Acropora

1989-94 2003

500

0

(b) 500

0

2

4

Year

6

8

Year

10

12

14

0

2

4

6

8

10

12

14

Year

Fig. 6 Sample size and colony sizes (mean diameter ± 1 SD) plotted against elapsed time. Open symbols indicate 2003 samples in the order (left to right) Rib, Feather and Green. Closed symbols indicate 1989–1994 series. a to f Selected groups as indicated

corals in 2003 indicated they were primarily survivors of the end of the century disturbances, not new corals. The low density of coral colonies in general, and Acropora juveniles in particular, and the reduction in the number of coral genera recorded (on Rib and Feather Reefs) in 2003 suggest the sites in 2003 were yet to have a strong recruitment pulse, which augurs poorly for post-2003 recovery. The poor Acropora juvenile count in 2003 (Fig. 6a) may partly reflect suppression of fecundity caused by sublethal bleaching (Ward et al. 2000) in 2002 (Berkelmans et al. 2004) and partly, the very low regional abundance of these reproductively under-performing Acropora, caused by the 1998 bleaching and A. planci predation (also see DeVantier et al. 2006). Sweatman et al. (2008) reported declines to \10% Acropora cover in all reefs in a large sample of reefs surveyed off both Cairns and Townsville in the first few years of this century, due to the combined effects of bleaching and A. planci

123

predation—‘one disturbance too many’ (Thompson and Dolman 2009). By 2008, a slow increase in cover of Acropora was beginning to appear regionally (Sweatman et al. 2008), but it is too soon to tell whether this will accelerate rapidly, similar to the 1980–1990s trajectory (present study; Halford et al. 2004; Ninio and Meekan 2002). It is not clear whether this study’s findings for the reefs in 2003 do represent ‘critical slowing down’ that forebodes impending collapse (sensu van Nes and Scheffer 2007) or merely delayed start-up of recovery (Done et al. 2007). As long as recruitment continues to fail, the coral assemblages are likely to remain species poor, limited by the longevity of old corals already on the reef. That longevity may not be great for those reefs which apparently entered a chronic disturbance phase around the turn of the century, characterized by residual A. planci populations, low-level bleaching and secondary disease (Wakeford et al. 2008).

Coral Reefs (2010) 29:815–833

(a) Acropora tables

Percentage

Fig. 7 Size frequency distribution of selected groups against elapsed time. a Acropora tables; b foliaceous Montipora; c massive Faviidae. Field records grouped into 3-cm bins, plus bins for 99–150 cm, 151–200 cm and [200 cm. Histograms were smoothed using two-point running mean. Shaded areas indicate relative contribution to that group’s bottom cover (also smoothed using two-point running mean)

829

40

Year 5

40

Year 6

40

Year 7

20

Year 8

20

Year 9

20

Year 10

20

Year 11

20

Year 12

20

Year 14

0

24

48

(b)

72

Diameter (cm)

For demersal fish and invertebrates, the decade long rise in coral cover (Fig. 5c) and generic richness (Fig. 4g) of a strongly recovering coral-dominated reef slope during the 1990s represents an expansion of resources for occupation and exploitation. Greater diversity of corals provides more diverse food and micro-habitats for coral-associated fishes (Jones et al. 2004; Munday 2004; Graham et al. 2006) and invertebrates (Patton 1994). The persistence of minor coral genera, while Acropora proliferates (Fig. 2c), suggests that the feeding opportunities for corallivorous fishes at 10–12 years into recovery should be different from (Berumen and Pratchett 2006) and more diverse and abundant than what was available in the first few years (Halford et al. 2004). In the present study, there are negative implications of the turn of the century coral disturbances for demersal coral associates. Until there is strong coral recruitment, any increase in coral cover will be largely based on increases in the size of the survivors (Wakeford et al. 2008). Some larger individuals may have a low life expectancy, and collectively, these assemblages have low generic diversity and under-representation of Acropora. The demersal species with obligate dependence upon Acropora species are extremely vulnerable. For example, at Moorea, when a major disturbance removed Acropora to be replaced by Pocillopora as a transitional dominant genus (Adjeroud et al. 2009), the species composition of obligate corallivorous chaetodonts followed suit (Berumen and Pratchett 2006). In the absence of equivalent data prior to 1980, it cannot be demonstrated that the 1980–1990s ‘recovery’ as

96

0

(c) Massive Faviidae

Foliaceous Montipora

24

48

72

Diameter (cm)

96

0

24

48

72

96

Diameter (cm)

characterized here represents normality. Earlier anecdotal observations do suggest that these shallow fore-reef habitats have hosted similar assemblages, at least during the period of human observation. In other habitats, however, Acropora abundance may have been anomalously high, at least in some situations, such as when recently dead massive corals are colonized by the much more ephemeral Acropora (Done and DeVantier 1990). This is potentially a fundamental change in terms of reef building and habitat structure (Endean and Cameron 1985), a matter of concern (biodiversity implications) or mere interest (mode of reef building). With these caveats, however, this study does provide a record of a coral community trajectory that was ‘doing well’ in the 1980 and 1990s by a number of criteria, following catastrophic levels of coral mortality: these criteria are coral cover, colony size and coral composition. The 1980–1990s rates and levels collectively represent useful benchmark trajectories against which other point samples or trajectories can be compared, without implying it is a uniquely appropriate standard trajectory, or that some places cannot do better. Given the GBR’s present state and projected climatechange impacts (Hoegh-Guldberg 1999; Hoegh-Guldberg et al. 2007; Veron 2008), the system’s future resilience appears precarious (Pandolfi et al. 2005). Over the coming decades, climate change is predicted to intensify the disturbance regime to include more severe cyclones and heatwave-driven mass bleaching events and decreasing alkalinity (Hoegh-Guldberg 1999; Webster et al. 2005;

123

830

Coral Reefs (2010) 29:815–833

Fig. 8 Quartile diameters plotted against elapsed time. a All hard corals; b Corymbose Acropora; c Acropora tables. Open symbols indicate 2003 samples in the order (left to right) Rib, Feather and Green. Closed symbols indicate 1989– 1994 series. Lines of best fit and 95% confidence limits derived using Power functions in Matlab 6.5. Functions and R2 are reported in Table 6

(a) Diameter (cm)

1st quartile 30

20

20

10

0

2

++ +

++ + +++ ++ +

6

8 10 12 14

4

80

+++ + + + + +

10

40

++ + +

0 0

2

4

6

8 10 12 14

30

60

20

20

40

10

10

20

0

0

40

4

6

0

8 10 12 14

40

3rd quartile

2

4

6

0

30

60

20

20

40

10

10

20

0 0

2

4

6

8 10 12 14

2

6

8 10 12 14

4 6

8 10 12 14

4

Median

80

30

0

0

0

8 10 12 14

3rd quartile

+ + + +

+ + ++

80

Median

30

2

++ ++

20

0

Median

0

Acropora tables 1st quartile

60

40

40

Diameter (cm)

(c)

Acropora ‘corymbose’

1st quartile

30

0

Diameter (cm)

(b)

All corals 40

40

2

3rd quartile

0

0

2

4

6

Year

8 10 12 14

0

2

4

6

Year

8 10 12 14

Year

Table 6 Model benchmark trajectories describing the 1989–1994 series, and indicative projections for shallow reef slope hard corals in elapsed years (t) = 1, 5 10 and 15 year Hard coral attribute

Mean cover index (%)*

R2

Model

C = 3.9t–10.5 0.1221

Projected Y1

Y5

Y10

Y15

0.56

0

9

29

48

0.77

38

47

51

53

Richness (genera)

G = 38.4t

Diversity (genera)

H0 = -0.0039t2 - 0.002t ? 3.375

0.29

3.36

3.26

2.97

2.47

Evenness (genera)

E = -0.0014t2 - 0.0487t ? 1.2314

0.39

1.18

0.95

0.61

0.19

Mean diameter (cm)

D = 1.7t ? 0.36 cm

0.79

5

12

21

29

0.64

2

4

7

9

0.72

1

6

12

17

0.70

2

9

20

31

0.65

0

6

18

34

0.79

1

9

28

55

0.76

1

13

43

87

Quartile diameters D = a*tb coefficients (and 95% confidence intervals) All corals diameters (cm) First quartile

a = 1.542 (-0.6065, 3.691) b = 0.6487 (0.04994, 1.247)

Second quartile (median)

a = 1.311 (-0.6096, 3.231) b = 0.9434 (0.3233, 1.563)

Third quartile

a = 1.55 (-0.6182, 3.719) b = 1.108 (0.5208, 1.696)48

Table Acropora diameters (cm) First quartile

a = 0.4153 (-0.6023, 1.433) b = 1.63 (0.6215, 2.638)

Second quartile (median)

a = 0.6279 (-0.7305, 1.986) b = 1.654 (0.7645, 2.544)

Third quartile

a = 0.8192 (-0.7085, 2.347) b = 1.722 (0.9572, 2.487)

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Coral Reefs (2010) 29:815–833

831

Table 6 continued Hard coral attribute

R2

Model

Projected Y1

Y5

Y10

Y15

0.62

1

5

11

17

0.65

1

7

16

25

0.64

2

11

22

35

Corymbose Acropora diameters (cm) First quartile

a = 1.035 (-0.5194, 2.59) b = 1.032 (0.3993, 1.665)

Second quartile (median)

a = 1.186 (-0.6944, 3.066) b = 1.128 (0.4626, 1.793)

Third quartile

a = 1.829 (-1.033, 4.69) b = 1.087 (0.4291, 1.745)

* Cover index applies to estimates from belt transect data using Eq. 3

Diameter (cm)

(a) 100

Modelled (1989-94)

80 60 40 20 0 1

Diameter (cm)

(b)100

3

5

10

Observed (2003)

80

1st quartile Median 3rd quartile

60 40 20

15

Rib (39)

Feather

Green (32)

(70)

0 1

3

5

10

fishes on the GBR are only incidental catch, not targeted by fishers. However, there is empirical evidence that suggests the reefs managed as NTAs may be less prone to mass predation by A. planci (Sweatman 2008). The NTA network therefore does maximize the likelihood that there will be numerous coral refugia well connected to other reefs (Almany et al. 2009) in which species abundance and biodiversity are not diminished by direct or cascading effects of fishing (Mumby et al. 2006) and from which these restorative coral cohorts will be released. But even strong resilience has its limits: local and national management initiatives for all living systems must be part of a global strategy that slows warming and ocean acidification by stabilizing atmospheric CO2 at or below 450 ppm CO2 (Hoegh-Guldberg et al. 2007) and which fosters a rapid return to levels \350 ppm (Veron et al. 2009).

15

Year Fig. 9 Acropora tables. First, second and third quartile diameters. a As modelled from the 1989–1994 data series using the functions in Table 6. b As observed in 2003

Hoegh-Guldberg et al. 2007; Veron 2008). For corals, this future represents an increasingly pronounced shift in ambient environmental conditions, compounded by reduced inter-disturbance intervals available for recovery, and with reduced size and number of refuge habitats that escape a particular disturbance. There may be fewer larval cohorts to be dispersed by the GBR’s complex currents, the future potential for coral acclimation and adaptation notwithstanding. The recent creation of a vast network of large no-take areas (NTAs) in the GBR (Fernandes et al. 2005) is a significant initiative, but it offers no direct protection from climate-related impacts (Hughes et al. 2003). Moreover, NTA benefits for the key functional process of grazing (Bellwood et al. 2004) are not definite, since herbivorous

Acknowledgments This work was funded by the Australian Institute of Marine Science with support of Australia’s Cooperative Research Centre (CRC) Program through the CRC Reef Research Centre. We gratefully acknowledge the support of the masters and crews of AIMS ships R. V. Lady Basten, R. V. Harry Messel and R. V Cape Ferguson. We greatly appreciate the thorough and thoughtful reviews of two anonymous reviewers.

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