Skip to main content
  • Other Publications
    • Philosophical Transactions B
    • Proceedings B
    • Biology Letters
    • Open Biology
    • Philosophical Transactions A
    • Proceedings A
    • Royal Society Open Science
    • Interface
    • Interface Focus
    • Notes and Records
    • Biographical Memoirs

Advanced

  • Home
  • Content
    • Latest issue
    • All content
    • Subject collections
    • Special features
    • Videos
  • Information for
    • Authors
    • Reviewers
    • Readers
    • Institutions
  • About us
    • About the journal
    • Editorial board
    • Author benefits
    • Policies
    • Citation metrics
    • Publication times
    • Open access
  • Sign up
    • Subscribe
    • eTOC alerts
    • Keyword alerts
    • RSS feeds
    • Newsletters
    • Request a free trial
  • Submit
You have accessRestricted access

Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement

George Roff, Tara R. Clark, Claire E. Reymond, Jian-xin Zhao, Yuexing Feng, Laurence J. McCook, Terence J. Done, John M. Pandolfi
Published 7 November 2012.DOI: 10.1098/rspb.2012.2100
George Roff
School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, AustraliaAustralian Research Council Centre of Excellence for Coral Reef Studies, Centre for Marine Science, University of Queensland, St Lucia, Queensland 4072, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tara R. Clark
Radiogenic Isotope Facility, Centre for Microscopy & Microanalysis, University of Queensland, St Lucia, Queensland 4072, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Claire E. Reymond
Leibniz Center for Tropical Marine Ecology (ZMT), Fahrenheitstrasse 6, 28359 Bremen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jian-xin Zhao
Radiogenic Isotope Facility, Centre for Microscopy & Microanalysis, University of Queensland, St Lucia, Queensland 4072, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yuexing Feng
Radiogenic Isotope Facility, Centre for Microscopy & Microanalysis, University of Queensland, St Lucia, Queensland 4072, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Laurence J. McCook
School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, AustraliaGreat Barrier Reef Marine Park Authority, Townsville, Queensland 4810, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Terence J. Done
School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, AustraliaAustralian Institute of Marine Science, PMB#3, Townsville, Queensland 4810, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
John M. Pandolfi
School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, AustraliaAustralian Research Council Centre of Excellence for Coral Reef Studies, Centre for Marine Science, University of Queensland, St Lucia, Queensland 4072, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF
Loading

Abstract

The inshore reefs of the Great Barrier Reef (GBR) have undergone significant declines in water quality following European settlement (approx. 1870 AD). However, direct evidence of impacts on coral assemblages is limited by a lack of historical baselines prior to the onset of modern monitoring programmes in the early 1980s. Through palaeoecological reconstructions, we report a previously undocumented historical collapse of Acropora assemblages at Pelorus Island (central GBR). High-precision U-series dating of dead Acropora fragments indicates that this collapse occurred between 1920 and 1955, with few dates obtained after 1980. Prior to this event, our results indicate remarkable long-term stability in coral community structure over centennial scales. We suggest that chronic increases in sediment flux and nutrient loading following European settlement acted as the ultimate cause for the lack of recovery of Acropora assemblages following a series of acute disturbance events (SST anomalies, cyclones and flood events). Evidence for major degradation in reef condition owing to human impacts prior to modern ecological surveys indicates that current monitoring of inshore reefs on the GBR may be predicated on a significantly shifted baseline.

1. Introduction

Marine ecosystems are showing evidence of global decline, resulting in long-term losses of abundance, diversity and habitat structure [1,2]. Humans are known to alter both the temporal and spatial scales of natural disturbance regimes, impacting upon the potential of marine ecosystems to recover following perturbation [3,4]. Trajectories of decline have been observed in coral reefs throughout the Caribbean and Indo-Pacific, attributable to the synergistic effects of anthropogenic disturbances [5,6]. In the Caribbean region, palaeoecological reconstructions of coral reefs have highlighted the collapse of coral communities at a regional level, which is unprecedented within the Holocene [7,8] and Pleistocene [9,10] records. Despite clear evidence of anthropogenic impacts on Indo-Pacific reefs [5], there is a general lack of historical data or palaeoecological baselines, particularly from the Great Barrier Reef (GBR).

Recently, several authors have highlighted the importance of the ‘shifting baseline syndrome’ [2,11], whereby our current perception of ecosystem health is biased by a lack of long-term baselines prior to anthropogenic impacts. This phenomenon strongly implies that no reef can be considered ‘pristine’ [2]. Using historical evidence, Pandolfi et al. [1] argued that altered anthropogenic disturbance regimes resulted in regional decline of the GBR long before the onset of modern monitoring programmes (approx. 1980), and prior to more recent threats such as ocean acidification and coral bleaching. Such studies provide an invaluable starting point for reversing long-term trajectories of decline by placing marine ecosystems in context of their historical baselines [12].

Following European settlement of the Queensland coastline in the late nineteenth century, extensive catchment clearing for livestock and agriculture (e.g. sugarcane) has resulted in substantial increases in sediment, nutrients and herbicides to the inshore GBR [11,13,14]. Since the onset of monitoring of the inshore GBR in the early 1980s [15], declines in coral cover [11,16–19], local removal of coral species [20] and persistent phase shifts to macroalgal-dominated ecosystems [21,22] have been reported across the inshore reefs. This decline has largely been attributed to altered disturbance regimes associated with coral bleaching events in the last few decades [17,23]. However, few historical baselines of coral assemblages exist prior to the 1980s [11], and the relationship between water quality and decline of the inshore GBR remains a controversy [11,19,24–27].

We present the results of palaeoecological reconstructions of coral assemblages from Pelorus Island, an inshore reef from the Palm Islands region of the central GBR. We surveyed three sites along the leeward side of the island (figure 1). To examine temporal changes in coral assemblages, we compared the community structure of life assemblages (living scleractinian corals) and death assemblages (dead coral fragments directly adjacent to modern corals), an approach commonly used to identify signals of anthropogenic disturbance and shifts in benthic community structure in the absence of historical baselines [28,29]. We obtained high-precision U-series dates [30] from dead coral samples within death assemblages to estimate the timing of mortality and to explore the age structure of the death assemblages. Finally, we extracted core samples from the reef matrix and quantified long-term (centennial to millennial) trajectories in coral community structure to determine historical baselines of coral assemblages. Our results imply a shifting baseline and a previously undetected historical collapse in coral communities coinciding with increased sediment and nutrient loading following European settlement of the Queensland coastline.

Figure 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 1.

Map of the Palm Islands region (central Great barrier Reef) and study sites at Pelorus Island (green boundaries indicate land, yellow boundaries indicate reef outlines).

2. Material and methods

Pelorus Island (18°33 S, 146°29 E) is situated in the Palm Islands region, central GBR (figure 1) between the Dry Tropics and Wet Tropics regions, and is surrounded by Holocene fringing reefs. During peak flood years, fine sediment discharge from the Burdekin River (approx. 165 km south of the study site) reaches the fringing reefs of the Palm Islands [13,31], in addition to flood plumes from the Herbert River to the north, and adjacent local rivers [31].

(a) Comparisons of life and death assemblages

We surveyed three leeward reef sites at Pelorus Island (figure 1). At each site, four belt transects (1 m width, 20 m length) were surveyed on SCUBA at 4–6 m depth. Life assemblages were defined as living scleractinian corals, and death assemblages defined as surficial dead corals adjacent to modern life assemblages [28]. Transects were photographed at intervals using a 1 m2 quadrat (n = 20, 20 m2 per transect) and the per cent cover of life and death assemblages determined using Coral Point Count with Excel extensions (CPCe [32]). The taxonomic structure of life and death assemblages was determined at the genus level and compared between assemblages and sites using hierarchical single linkage cluster analysis and a three-factor permutation multivariate analysis of variance (PERMANOVA [33]) repeated measures model based on Bray–Curtis similarities, where assemblage (life and death assemblages as repeated measures) and site were considered fixed factors, and transect as a random factor. Growth forms of Acropora were defined following Wallace [34]. To provide an estimate of morphological differences between living and dead Acropora, 10 live colonies and 10 dead fragments of Acropora were selected at random from each 20 m transect, and the primary growth form and branch thickness (measured by the broadest diameter of the branch) was determined (total n = 40 per site).

(b) Age structure of death assemblages

Surficial death assemblages were collected by hand on SCUBA at eight points (n = ∼40 fragments per point) at random across a single 20 m transect at each site. From these collections, fragments of the dominant genus/growth form present in death assemblages were identified, and samples were selected for U-series dating haphazardly (i.e. with no bias for taphonomic state of fragments). Sample fragments were sectioned laterally, and a sub-sample (2–3 g) of skeleton was taken from the cleanest section (i.e. unaffected by internal bioerosion) in closest proximity to the growth margin. Approximately 1 g of carefully cleaned material from each sub-sample was used for thermal ionization mass spectrometry (TIMS) and multi-collector inductively coupled plasma mass spectrometer (MC-ICPMS) U-series dating (see the electronic supplementary information for detailed methodology). Ages are reported with 2σ error bars, which represent two standard deviations from the mean true age. Averages (Tukey's biweighted means [35]) and relative probability distributions of U-series ages were determined using Isoplot v. 3.0 [36].

(c) Long-term trajectories in coral community structure

Four cores were extracted from the reef matrix at random along a single 20 m transect at each site (5 m water depth, total n = 12) using a standard percussion coring method (10 cm wide aluminium pipe, 2 m length). Cores were sectioned lengthways using a circular saw and imaged using a multi-slice computed axial tomography (CAT) scanning instrument (Lightspeed VCT, General Electric Healthcare, Milwaukee, WI, USA, 625 μm slice thickness at 400 mA and 120 kV). Longitudinal sections of CAT scans were imported into Adobe Illustrator CS3 (Adobe systems, San Jose, CA, USA), and the outlines of each coral genus were traced to form taxonomic core logs.

(d) Palaeoenvironmental baselines

To understand historical environmental baselines, we combined available continuous palaeoenvironmental records from a range of published and sclerochronological databases within the Palm Islands region, including cyclone tracks (1906–present [37]), HADISST 1.1 sea surface temperature (1870–present [38]), observed coral bleaching events (approx. 1980–present [17,23]), Pacific Decadal Oscillation records (PDO, 1900–2000 [39]), Burdekin River discharge (1921–1999 [13]) and Ba/Ca proxies of sediment flux from the Burdekin River derived from coral cores (1758–1998 [13]). No historical baselines exist for other biotic disturbance events such as disease or crown-of-thorns starfish outbreaks within the Palm Islands region prior to the onset of monitoring programmes in 1987.

3. Results

(a) Comparisons of life and death assemblages

Life assemblages at sites A and C were composed of isolated colonies of massive Porites, and individual Montipora and Acropora colonies (figure 2a). Both sites were characterized by low coral cover (4.4±1%, and 3.5±1%, respectively, see the electronic supplementary material, table S1) compared with the GBR average (21.7% [19]) and other inshore reefs within the region (26.9% [21]). In contrast to sites A and C, life assemblages at site B were dominated by Pavona, Millepora and Echinopora (figure 2a), characteristic of modern inshore reefs in the region [15], and coral cover was considerably higher than the average of the inshore GBR (36.3±8%) and 8–10 times higher than sites A and C.

Figure 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 2.

Life and death assemblages at Pelorus Island, Great Barrier Reef. (a) Relative abundance of the six most common coral genera at each site (±s.e.), (b) relative abundance of Acropora growth forms (pooled between sites), (c) branch thickness of Acropora corals (±s.e.).

The community composition of death assemblages at all sites was dominated by a framework of Acropora (53–97% composition, figure 2a). Low densities of Acropora were present in life assemblages across all sites, yet were fundamentally different in growth form (χ2 = 278.7, p < 0.01, figure 2b) and branch thickness (ANOVA, F249, p < 0.01, figure 2c) to those found in death assemblages. Living Acropora assemblages were composed of thinly branched determinate growth forms of Acropora (corymbose and caespitose morphologies, figure 2b), while death assemblages were formed by expanses of thick arborescent Acropora spp. (see the electronic supplementary material, figure S1), which were largely absent from life assemblages (figure 2b).

The relative generic abundance of coral assemblages varied significantly among sites (PERMANOVA, F2 = 2.736, p < 0.05). Hierarchical cluster analysis of life and death assemblages indicated that death assemblages across all sites formed a single cluster at the 50 per cent similarity level, while life assemblages formed distinct clusters largely separate from the death assemblages (figure 3). Post hoc pairwise tests revealed significant differences between sites A and B (p < 0.05), and between sites B and C (p < 0.01), yet no significant difference between sites A and C (p > 0.5), consistent with the results from the cluster analysis (figure 3). The discordance between life and death assemblages was significant across all sites (PERMANOVA, F1 = 25.367, p < 0.001), yet no interaction was observed between the site and assemblage, indicating that the difference between life and death assemblages was consistent across all sites (table 1).

View this table:
  • View inline
  • View popup
Table 1.

PERMANOVA results for differences of coral community structure between sites (A,B,C) and assemblages (life and death assemblages). SS = sum of squares, MS = mean square.

Figure 3.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 3.

Single linkage cluster analysis of life and death assemblages at transect level across sites A–C. Nearest neighbour (single linkage) clustering indicates a clear difference between life and death assemblages. Six separate clusters (shaded) are evident at the 50% similarity level, with more than 90% of death assemblages within sites clustering in a single group (open circle, life assemblage; filled circle, death assemblage).

(b) Age structure of death assemblages

A total of 48 high-precision U-series dates were obtained from dead arborescent Acropora branches (sites A, B and C) and a further 15 U-series dates from dead Pavona fragments at site B (figure 4a). U-series calendar ages for all samples ranged between 1778±10 and 2007±1 (table 2), demonstrating the potential for considerable analytical precision obtained by our method of dating young corals (see the electronic supplementary material, table S2). Relative probability distributions of Acropora ages (figure 4b) revealed distinct peaks of mortality in the mid-1940s at site A (1945±6) and late 1930s at site C (1938±4), with a less defined peak of mortality occurring at site B (1917±41). The mortality of Acropora across all sites was largely constrained to a single time period, with 79.1 per cent of U-series ages falling between 1920 and 1955 (figure 4a). Few U-series ages obtained from Acropora assemblages occurred after 1980 (8.3%), while the majority of ages obtained from Pavona assemblages occurred after 1980 (80%), and centred around the late 1990s (average 1998±4).

View this table:
  • View inline
  • View popup
Table 2.

Average ages (AD±2σ errors) for death assemblages and reef matrix cores. Weighted averages calculated from U-series analytical error using Tukey's biweight.

Figure 4.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 4.

U-series ages from death assemblages at Pelorus Island, Great Barrier Reef (a) U-series ages (AD±2σ errors) from arborescent Acropora (n = 48) and Pavona (n = 15) assemblages (ordered from oldest to youngest age), (b) relative probability curves (Gaussian fit) derived from U-series ages (AD±2σ errors) from 1900 to 2010 and average ages (AD±2σ errors) as determined by the Tukey's biweight method.

(c) Long-term trajectories in coral community structure

Computed axial tomography (CAT) scans of reef matrix cores revealed an Acropora-dominated framework at sites A and C, interspersed with minor genera (mainly Pocillopora and Montipora, figure 5), similar to the composition of surficial arborescent Acropora death assemblages. U-series ages obtained from the base of each core show evidence of accretion of reef matrix since the early sixteenth century (1513±5) at site A, and mid-ninth century (846±8) at site C. Cores similarly extracted from site B show a comparable pattern of Acropora-dominated matrix since the mid-third century (266±12). An abrupt transition from arborescent Acropora assemblages to Pavona assemblages in the upper layers (0–30 cm) was observed in all four cores at site B (figure 5). The U-series ages obtained from the uppermost Acropora assemblages at the Acropora–Pavona transition in the sediment cores (figure 5) place the timing of the underlying Acropora mortality at site B to between 1928 and 1944.

Figure 5.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 5.

Core logs of fossil coral assemblages at Pelorus Island, Great Barrier Reef. Colours represent individual coral genera within the reef matrix (see the inset key), depth of each core is represented in cm, and U-series ages (AD±2σ errors) from the cores are shown adjacent to where they were taken from each core.

(d) Palaeoenvironmental baselines

Consistent with previous analysis [40], five phases were identified in the PDO record (figure 6): 1905–1915 (cool phase), 1916–1943 (warm phase), 1944–1976 (cool phase), 1977–1998 (warm phase) and 1998–2010 (cool phase). Meteorological records indicate 27 cyclones passed within 100 km of Pelorus Island between 1910 and 2010 (figure 6), including three category 2 (1915, 2000), three category 3 (1940, 1956, 1986) and three category 4 cyclones (1955, 1971, 2006). Annual average SST anomalies (calculated relative to 1900–2010) from HADISST [38] indicate that more than 2.5°C thermal anomalies occurred in 8 out of 110 years (1935, 1962, 1970, 1973, 1977, 1987, 1998 and 2004, figure 6). Hydrographic records from the Burdekin River indicate that outflow varied between approximately 10 × 101 to 27.5 × 107 l per month, with monthly flood peaks exceeding 10 × 107 l per week occurring in 1946, 1950, 1951, 1954, 1955, 1958, 1968, 1974 and 1991 (figure 6). Ba/Ca proxies of sediment flux from the Burdekin River derived from coral cores between 1760 and 1998 have previously identified a significant (5–10-fold) increase in sediment flux following 1870, with large peaks occurring in 1927, 1936, 1968, 1970 and 1988 (figure 6) following periods of drought [13].

Figure 6.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 6.

Relative probability curves from U-series ages (Acropora = red lines, all sites, Pavona = blue lines, site B) and regional palaeoenvironmental records for cyclone activity (T = tropical storm, 1–5 = tropical cyclone intensity scale), SST anomalies, Pacific Decadal Oscillation (PDO) index (LOWESS-smoothing at t = 10 points), sediment flux (Ba/Ca proxy) and Burdekin River discharge between 1900–2010.

4. Discussion

In the absence of historical baselines, comparisons of life and death assemblages provide a valuable tool for determining ecological change and signals of anthropogenic disturbance in benthic communities [28,29]. Our analysis of assemblages from leeward reef sites at Pelorus Island indicates a historical shift in community structure from once dominant arborescent Acropora assemblages at all sites, to either novel low coral cover assemblages (sites A and C), or in the case of site B, high live coral cover composed of non-Acropora assemblages characteristic of modern inshore reefs in the region [15]. While Acropora was present in our surveys of modern assemblages at low cover, in contrast to thick arborescent (branching) Acropora dominant in death assemblages, life assemblages were largely composed of small individual colonies of caespitose and corymbose colonies of Acropora, typical of early stage succession following disturbance [41].

High-precision U-series dating of historical Acropora death assemblages revealed that the majority of ages (92.2%, n = 48 samples across all sites) occurred prior to the onset of broad-scale surveys of the GBR in the 1980s [15,23,42]. Despite high cover of arborescent Acropora from windward reef flat and slope environments throughout the Palm Islands region (including Pelorus) prior to the 1998 mass bleaching event [43], only a single Acropora age was obtained after 1990 from Pelorus Island. Indeed, the majority of U-series ages (79.1%) obtained from Acropora death assemblages occurred between 1920 and 1955. Critically, this historical mortality occurred prior to the mass bleaching events of 1998 and 2002 [44,45], and prior to the onset of monitoring of the GBR in the early to mid 1980s. The absence of previously dominant arborescent Acropora growth forms in the living coral assemblages, and the low number of recent Acropora U-series ages (above 1980) indicates a lack of recovery of arborescent Acropora populations at Pelorus Island following mortality in the early to mid-twentieth century.

U-series ages obtained from the Pavona death assemblage at site B provide evidence of more recent mortality, with 80 per cent of U-series dates occurring after 1980. In contrast, and similar to results from sites A and C, 75 per cent of U-series ages obtained from Acropora death assemblages at site B occurred prior to 1980. We interpret the timing of mortality at site B to indicate a transition in recent decades from historically dominant arborescent Acropora to modern Pavona assemblages, consistent with the high cover and abundance of Pavona in the life assemblages at site B. The timing of the Pavona transition detected in reef matrix cores places the timing of the preceding Acropora mortality at site B to between 1928 and 1944, which is strikingly consistent with the U-series ages obtained from the Acropora death assemblages. Several Pavona ages clustered closely around 1998 (1996±8, 1997±7, 1998±3, 1998±5, 1999±8), and probably represent mortality associated with the 1998/1998 mass coral bleaching event, which was particularly severe in the Palm Islands region [44].

Mismatches between living and dead assemblages can be used to detect signs of anthropogenic ecological change [28], but are not without caveats. Despite the clear potential for time averaging (e.g. the mixing of temporally distinct cohorts [8]) and taphonomic bias (e.g. differential preservation among coral growth forms [46]) in palaeoecological analysis of coral death assemblages, the clustering of U-series ages obtained from historical Acropora indicates a narrow constraint in the timing of mortality, and suggests that Acropora death assemblages are largely autochthonous (i.e. relatively unaltered by taphonomic alteration, vertical mixing of surface layers and fragment transportation [28,29,46]), as expected in low-energy leeward reef habitats [47].

In the Caribbean region, widespread losses of Acropora in the early 1980s have been followed by transitions to coral assemblages dominated by Agaricia sp. [48] and Porites sp. [29] that are unprecedented in the Holocene and Pleistocene records [9]. Our core records indicate that persistent Acropora-dominated framework existed across all sites at Pelorus Island throughout the late Holocene. The timing of the transition from historically dominant arborescent Acropora to modern Pavona assemblages at site B in the core records (1935±7, 1941±3, 1936±6, figure 5) with one exception (1624±7) are consistent with ages obtained from arborescent Acropora death assemblages, and further supports the systematic collapse of arborescent Acropora across all sites between 1920 and 1955. Importantly, this transition is without precedence over the past 1700 years of record, despite a high frequency of ‘super-cyclones’ [49] and climatic fluctuations [50] during this period. Such an abrupt transition over relatively recent timescales precludes an explanation of natural trajectories of geomorphic decline [51], and strongly implicates extrinsic (i.e. anthropogenic) forcing in the early–mid-twentieth century.

To explore the timing and potential causes of historical coral mortality, we compiled palaeoenvironmental records from the twentieth century for the Palm Islands region. Visual assessment of these records indicates considerable climatic variability (SST, cyclone activity and river discharge) coinciding with U-series ages obtained from Acropora death assemblages (approx. 1920–1955, figure 6). The two decades prior to the Acropora mortality (1902–1921) were characterized by a continuous period of negative SST anomalies associated with a PDO cool phase [40]. The subsequent change to the warm phase of the PDO resulted in an increase in positive SST anomalies (1922–1948), and a period of extreme drought [40,52], which coincides with the onset of Acropora mortality within death assemblages. A shift towards a PDO cool phase in the late 1940s [40] resulted in an increase in the frequency and intensity of cyclones (notably category 4 and 3 cyclones in 1955 and 1956) and higher frequency of high flow events (more than10 × 106 l per week) from the Burdekin River (1946, 1950, 1951, 1954, 1955), coinciding with the later stages of Acropora mortality. Considering the relatively broad range of U-series ages obtained from Acropora assemblages (1920–1955), we suggest that multiple disturbance events (e.g. a period of extended SST anomalies followed by increased cyclone activity and flooding, figure 6) may be implicated as a proximal cause of mortality, rather than a single disturbance event.

In the absence of underlying chronic stressors, coral reefs are capable of rapid recovery from acute disturbance events within relatively short timescales [53]. In peak flood years, the Burdekin River disperses large amounts of fine sediment (105 to 106 tonnes) in freshwater flood plumes, affecting inshore and mid-shelf reefs throughout the Palm Islands region [13,31]. Following European settlement of the Burdekin region in 1862, widespread catchment clearing and introduction of cattle and sheep in large numbers [52], resulted in a 5–10-fold increase in sediment flux from the Burdekin river during flood events from 1870 onwards [13]. In addition to land clearing activities in the late nineteenth and early twentieth century, historical records indicate that agricultural fertilizer usage became widespread throughout adjacent catchments from approximately 1930 onwards [54]. Modelling estimates suggest that in the catchments directly adjacent to the Palm Islands, exports of total suspended sediments, herbicides and nutrient loads have increased between 2.1- to 19.5-fold since European colonization [14], resulting in a significantly altered disturbance regime. We suggest that the increase in sediment flux and nutrient loading to the region following European settlement in the late nineteenth century may have acted as the ultimate cause for the lack of recovery in historical Acropora assemblages in the early-to-mid-twentieth century, following mortality owing to a series of acute disturbance events (SST anomalies, cyclones and flooding).

While palaeoecological reconstructions of near-shore reefal shoals on the central GBR suggests that some coral assemblages may be ‘preadapted’ to high turbidity environments [51], the apparent decline of arborescent Acropora assemblages in the earlier part of the twentieth century at Pelorus Island may suggest a level of sensitivity of sub-tidal inshore fringing reefs of the central GBR to increases in sediment flux and nutrient loading. Arborescent Acropora assemblages were dominant in fore-reef environments throughout the Palm Islands region until the 1998 bleaching event [16,23,43,55], yet by the early 1980s, recruitment rates of Acropora corals on inshore reefs of the Palm Islands were strongly suppressed owing to sub-optimal growth conditions [56], and modern studies on nearby inshore reefs indicate that coral recruitment is reduced under exposure to chronic terrestrial runoff [57]. While many growth forms of Acropora exhibit high rates of recruitment (e.g. caespitose and corymbose), arborescent Acropora exhibit sparse larval recruitment and reproduce predominantly by fragmentation [58], suggesting that they may be particularly susceptible to factors affecting recruitment following disturbance.

Collectively, our results indicate a historical change in coral community structure at Pelorus Reef, and suggest that this shift coincided with European settlement of the Queensland coastline. This implies that current monitoring of the inshore GBR may at some locations be predicated on a substantially shifted baseline [11]. On a global scale, our results are consistent with a recent report from the Caribbean region, where land use changes prior to 1960 were implicated in a significant decline in Acropora corals in near-shore reefs [59]. Yet, in contrast to the region-wide collapse of Acropora in the Caribbean, considering the abundance of Acropora within regions prior to the 1998 bleaching event [23,43], the extent of historical mortality on the inshore GBR is likely to vary on local scales. Finally, our results raise two concerns in the interpretation of modern coral assemblages and baseline assessments of coral cover. Firstly, living coral assemblages at site B had relatively high coral cover compared with the GBR average. Yet, modern surveys of live coral cover would significantly underestimate the previously ‘hidden’ shift in coral community structure at the site, resulting in a shifted baseline. Secondly, considering the disparity among Acropora growth forms between life and death assemblages and the near absence of previously dominant framework building Acropora in the present study, modern surveys should consider the dynamics and recovery of corals within genera [23] in addition to the generic level.

Acknowledgements

We thank Orpheus Island Research Station for their help and support during fieldwork, and S. G. Smithers, C. T. Perry, H. Lescinsky and M. Lybolt for critical discussions. We also thank John Bruno and two anonymous reviewers for greatly improving the quality of the manuscript. This project was partially funded by a Marine and Tropical Science Research Facility (MTSRF) Project 1.1.4 to J.X.Z. T.J.D. and J.M.P., Australian Research Council Centre of Excellence for Coral Reef Studies to J.M.P., Australian Research Council LIEF Project LE0989067 to J.X.Z., J.M.P., Y.F. and others, and the Mia J. Tegner and International Society for Reef Studies awards to G.R.

  • Received September 7, 2012.
  • Accepted October 17, 2012.
  • © 2012 The Author(s) Published by the Royal Society. All rights reserved.

References

  1. ↵
    1. Pandolfi JM,
    2. et al.
    2003 Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958. doi:10.1126/science.1085706 (doi:10.1126/science.1085706)
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Jackson JBC,
    2. et al.
    2001 Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–638. doi:10.1126/science.1059199 (doi:10.1126/science.1059199)
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Done TJ
    . 1992 Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247, 121–132. doi:10.1007/BF00008211 (doi:10.1007/BF00008211)
    OpenUrlCrossRefWeb of Science
  4. ↵
    1. Nystrom M,
    2. Folke C,
    3. Moberg F
    . 2000 Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417. doi:10.1016/S0169-5347(00)01948-0 (doi:10.1016/S0169-5347(00)01948-0)
    OpenUrlCrossRefPubMed
  5. ↵
    1. Bruno J,
    2. Selig ER
    . 2007 Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 2, e711. doi:10.1371/journal.pone.0000711 (doi:10.1371/journal.pone.0000711)
    OpenUrlCrossRefPubMed
  6. ↵
    1. Gardner TA,
    2. Cote IM,
    3. Gill JA,
    4. Grant A,
    5. Watkinson AR
    . 2003 Long-term region-wide declines in Caribbean corals. Science 301, 958–960. doi:10.1126/science.1086050 (doi:10.1126/science.1086050)
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. Aronson RB,
    2. Precht WF
    . 1997 Stasis, biological disturbance, and community structure of a Holocene coral reef. Paleobiology 23, 326–346.
    OpenUrlAbstract
  8. ↵
    1. Greenstein BJ,
    2. Pandolfi JM
    . 1997 Preservation of community structure in modern reef coral life and death assemblages of the Florida Keys: implications for the Quaternary fossil record of coral reefs. Bull. Mar. Sci. 61, 431–452.
    OpenUrlWeb of Science
  9. ↵
    1. Pandolfi JM,
    2. Jackson JBC
    . 2006 Ecological persistence interrupted in Caribbean coral reefs. Ecol. Lett. 9, 818–826. doi:10.1111/J.1461-0248.2006.00933.x (doi:10.1111/J.1461-0248.2006.00933.x)
    OpenUrlCrossRefPubMedWeb of Science
  10. ↵
    1. Pandolfi JM,
    2. Jackson JBC
    . 2001 Community structure of Pleistocene coral reefs of Curacao, Netherlands Antilles. Ecol. Monogr. 71, 49–67.
    OpenUrlCrossRefGeoRefWeb of Science
  11. ↵
    1. Hughes TP,
    2. Bellwood DR,
    3. Baird AH,
    4. Brodie J,
    5. Bruno JF,
    6. Pandolfi JM
    . 2011 Shifting base-lines, declining coral cover, and the erosion of reef resilience: comment on Sweatman et al. (2011). Coral Reefs 30, 653–660. doi:10.1007/s00338-011-0787-6 (doi:10.1007/s00338-011-0787-6)
    OpenUrlCrossRefWeb of Science
  12. ↵
    1. Campbell LM,
    2. Gray NJ,
    3. Hazen EL,
    4. Shackeroff JM
    . 2009 Beyond baselines: rethinking priorities for ocean conservation. Ecol. Soc. 14, 14.
    OpenUrl
  13. ↵
    1. McCulloch M,
    2. Fallon S,
    3. Wyndham T,
    4. Hendy E,
    5. Lough J,
    6. Barnes D
    . 2003 Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421, 727–730. doi:10.1038/nature01361 (doi:10.1038/nature01361)
    OpenUrlCrossRefGeoRefPubMed
  14. ↵
    1. Kroon FJ,
    2. Kuhnert PM,
    3. Henderson BL,
    4. Wilkinson SN,
    5. Kinsey-Henderson A,
    6. Abbott B,
    7. Brodie JE,
    8. Turner RDR
    . 2012 River loads of suspended solids, nitrogen, phosphorus and herbicides delivered to the Great Barrier Reef lagoon. Mar. Pollut. Bull. 65, 167–181. doi:10.1016/j.marpolbul.2011.10.018 (doi:10.1016/j.marpolbul.2011.10.018)
    OpenUrlCrossRefPubMedWeb of Science
  15. ↵
    1. Done T
    . 1982 Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1, 95–107. doi:10.1007/BF00301691 (doi:10.1007/BF00301691)
    OpenUrlCrossRef
  16. ↵
    1. Maynard JA,
    2. Anthony KRN,
    3. Marshall PA,
    4. Masiri I
    . 2008 Major bleaching events can lead to increased thermal tolerance in corals. Mar. Biol. 155, 173–182. doi:10.1007/s00227-008-1015-y (doi:10.1007/s00227-008-1015-y)
    OpenUrlCrossRefWeb of Science
  17. ↵
    1. Thompson A,
    2. Dolman AM
    . 2010 Coral bleaching: one disturbance too many for near-shore reefs of the Great Barrier Reef. Coral Reefs 29, 637–648. doi:10.1007/s00338-009-0562-0 (doi:10.1007/s00338-009-0562-0)
    OpenUrlCrossRefWeb of Science
    1. De'ath G,
    2. Fabricius KE,
    3. Sweatman H,
    4. Puotinen ML
    . 2012 The 27-years decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl Acad. Sci. USA 65. doi:10.1073/pnas.1208909109 (doi:10.1073/pnas.1208909109)
    OpenUrlAbstract/FREE Full Text
  18. ↵
    1. Sweatman H,
    2. Delean S,
    3. Syms C
    . 2010 Assessing loss of coral cover on Australia's Great Barrier Reef over two decades, with implications for longer-term trends. Coral Reefs 30, 521–531. doi:10.1007/s00338-010-0715-1 (doi:10.1007/s00338-010-0715-1)
    OpenUrlCrossRefWeb of Science
  19. ↵
    1. DeVantier LM,
    2. De'ath G,
    3. Turak E,
    4. Done TJ,
    5. Fabricius KE
    . 2006 Species richness and community structure of reef-building corals on the nearshore Great Barrier Reef. Coral Reefs 25, 329–340. doi:10.1007/s00338-006-0115-8 (doi:10.1007/s00338-006-0115-8)
    OpenUrlCrossRefWeb of Science
  20. ↵
    1. Wismer S,
    2. Hoey AS,
    3. Bellwood DR
    . 2009 Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar. Ecol. Progr. Ser. 376, 45–54. doi:10.3354/Meps07790 (doi:10.3354/Meps07790)
    OpenUrlCrossRefWeb of Science
  21. ↵
    1. Cheal AJ,
    2. MacNeil MA,
    3. Cripps E,
    4. Emslie MJ,
    5. Jonker M,
    6. Schaffelke B,
    7. Sweatman H
    . 2010 Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29, 1005–1015. doi:10.1007/s00338-010-0661-y (doi:10.1007/s00338-010-0661-y)
    OpenUrlCrossRefWeb of Science
  22. ↵
    1. Done T,
    2. Turak E,
    3. Wakeford M,
    4. DeVantier L,
    5. McDonald A,
    6. Fisk D
    . 2007 Decadal changes in turbid-water coral communities at Pandora Reef: loss of resilience or too soon to tell? Coral Reefs 26, 789–805. doi:10.1007/S00338-007-0265-3 (doi:10.1007/S00338-007-0265-3)
    OpenUrlCrossRefWeb of Science
  23. ↵
    1. Sweatman H,
    2. Syms C
    . 2011 Assessing loss of coral cover on the Great Barrier Reef: a response to Hughes et al. (2011). Coral Reefs 30, 661–664. doi:10.1007/s00338-011-0794-7 (doi:10.1007/s00338-011-0794-7)
    OpenUrlCrossRefWeb of Science
    1. Brodie J,
    2. Waterhouse J
    . 2012 A critical review of environmental management of the ‘not so Great’ Barrier reef. Estuarine Coastal Shelf Sci. (doi:10.1016/j.ecss.2012.03.012)
    1. De'ath G,
    2. Fabricius K
    . 2010 Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol. Appl. 20, 840–850. doi:10.1890/08-2023.1 (doi:10.1890/08-2023.1)
    OpenUrlCrossRefPubMedWeb of Science
  24. ↵
    1. McCook LJ
    . 1999 Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367. doi:10.1007/s003380050213 (doi:10.1007/s003380050213)
    OpenUrlCrossRefWeb of Science
  25. ↵
    1. Kidwell SM
    . 2007 Discordance between living and death assemblages as evidence for anthropogenic ecological change. Proc. Natl Acad. Sci. USA 104, 17 701–17 706. doi:10.1073/pnas.0707194104 (doi:10.1073/pnas.0707194104)
    OpenUrlAbstract/FREE Full Text
  26. ↵
    1. Greenstein BJ,
    2. Curran HA,
    3. Pandolfi JM
    . 1998 Shifting ecological baselines and the demise of Acropora cervicornis in the western North Atlantic and Caribbean Province: a Pleistocene perspective. Coral Reefs 17, 249–261. doi:10.1007/s003380050125 (doi:10.1007/s003380050125)
    OpenUrlCrossRefWeb of Science
  27. ↵
    1. Zhao J-x,
    2. Yu KF,
    3. Feng YX
    . 2009 High-precision 238U–234U–230Th disequilibrium dating of the recent past: a review. Quater. Geochronol. 4, 423–433. doi:10.1016/J.quageo.2009.01.012 (doi:10.1016/J.quageo.2009.01.012)
    OpenUrlCrossRef
  28. ↵
    1. Bainbridge ZT,
    2. Wolanski E,
    3. Álvarez-Romero JG,
    4. Lewis SE,
    5. Brodie JE
    . 2012 Fine sediment and nutrient dynamics related to particle size and floc formation in a Burdekin River flood plume, Australia. Mar. Pollut. Bull. 65, 236–248. doi:10.1016/j.marpolbul.2012.01.043 (doi:10.1016/j.marpolbul.2012.01.043)
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  29. ↵
    1. Kohler KE,
    2. Gill SM
    . 2006 Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput. Geosci. 32, 1259–1269. doi:10.1016/j.cageo.2005.11.009 (doi:10.1016/j.cageo.2005.11.009)
    OpenUrlCrossRefWeb of Science
  30. ↵
    1. Anderson MJ
    . 2001 A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46.
    OpenUrlCrossRefWeb of Science
  31. ↵
    1. Wallace C
    . 1999 Staghorn corals of the world: a revision of the coral genus Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis on morphology, phylogeny and biogeography, p. 421. Collingwood, Australia: CSIRO Publishing.
  32. ↵
    1. Hoaglin DC,
    2. Mosteller F,
    3. Tukey JW
    . 1983 Understanding robust and exploratory data analysis, p. 447. New York, NY: Wiley-Interscience.
  33. ↵
    1. Ludwig KR
    . 2003 User's manual for Isoplot v. 3.0, A geochronological toolkit for Microsoft Excel. In Berkeley Geochronology Center Special Publication No 4.
  34. ↵
    BOM. 2010 Australian Government Bureau of Meteorology: tropical cyclones since 1906 Australian region (http://www.bom.gov.au/cyclone/history/index.shtml)
  35. ↵
    1. Rayner NA,
    2. Parker DE,
    3. Horton EB,
    4. Folland CK,
    5. Alexander LV,
    6. Rowell DP,
    7. Kent EC,
    8. Kaplan A
    . 2003 Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J. Geophys. Res. 108 (D14), 4407. doi:10.1029/2002JD002670 (doi:10.1029/2002JD002670)
    OpenUrlCrossRef
  36. ↵
    1. Trenberth KE,
    2. Hurrell JW
    . 1994 Decadal atmosphere–ocean variations in the Pacific. Clim. Dynam. 9, 303–319. doi:10.1007/BF00204745 (doi:10.1007/BF00204745)
    OpenUrlCrossRefWeb of Science
  37. ↵
    1. Lough JM
    . 2007 Tropical river flow and rainfall reconstructions from coral luminescence: Great Barrier Reef, Australia. Paleoceanography 22. PA2218 (doi:10.1029/2006PA001377)
  38. ↵
    1. Wakeford M,
    2. Done TJ,
    3. Johnson CR
    . 2008 Decadal trends in a coral community and evidence of changed disturbance regime. Coral Reefs 27, 1–13. doi:10.1007/s00338-007-0284-0 (doi:10.1007/s00338-007-0284-0)
    OpenUrlCrossRefWeb of Science
  39. ↵
    1. Sweatman H,
    2. Thompson A,
    3. Delean S,
    4. Davidson J,
    5. Neale S
    . 2004 Status of near-shore reefs of the Great Barrier Reef. Marine and tropical sciences research facility research report series, p. 169. Cairns, Australia: Reef and Rainforest Research Centre Limited.
  40. ↵
    1. Gralton C
    . 2002 Coral recovery on inshore reefs following the 1998 bleaching event. Townsville, Australia: James Cook University.
  41. ↵
    1. Marshall PA,
    2. Baird AH
    . 2000 Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155–163. doi:10.1007/s003380000086 (doi:10.1007/s003380000086)
    OpenUrlCrossRefWeb of Science
  42. ↵
    1. Berkelmans R,
    2. De'ath G,
    3. Kininmonth S,
    4. Skirving WJ
    . 2004 A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23, 74–83. doi:10.1007/s00338-003-0353-y (doi:10.1007/s00338-003-0353-y)
    OpenUrlCrossRefWeb of Science
  43. ↵
    1. Pandolfi JM,
    2. Greenstein BJ
    . 1997 Taphonomic alteration of reef corals: effects of reef environment and coral growth form. I. The Great Barrier Reef. Palaios 12, 27–42. doi:10.2307/3515292 (doi:10.2307/3515292)
    OpenUrlAbstract/FREE Full Text
  44. ↵
    1. Pandolfi JM,
    2. Minchin PR
    . 1996 A comparison of taxonomic composition and diversity between reef coral life and death assemblages in Madang Lagoon, Papua New Guinea. Palaeogeogr. Palaeoclimatol. Palaeoecol. 119, 321–341. doi:10.1016/0031-0182(95)00016-X (doi:10.1016/0031-0182(95)00016-X)
    OpenUrlCrossRefGeoRef
  45. ↵
    1. Aronson RB,
    2. Precht WF,
    3. Macintyre IG
    . 1998 Extrinsic control of species replacement on a Holocene reef in Belize: the role of coral disease. Coral Reefs 17, 223–230. doi:10.1007/s003380050122 (doi:10.1007/s003380050122)
    OpenUrlCrossRefWeb of Science
  46. ↵
    1. Nott J,
    2. Hayne M
    . 2001 High frequency of 'super-cyclones’ along the Great Barrier Reef over the past 5,000 years. Nature 413, 508–512. doi:10.1038/35097055 (doi:10.1038/35097055)
    OpenUrlCrossRefGeoRef
  47. ↵
    1. Hendy EJ,
    2. Gagan MK,
    3. Alibert CA,
    4. McCulloch MT,
    5. Lough JM,
    6. Isdale PJ
    . 2002 Abrupt decrease in tropical Pacific Sea surface salinity at end of Little Ice Age. Science 295, 1511–1514. doi:10.1126/science.1067693 (doi:10.1126/science.1067693)
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  48. ↵
    1. Perry CT,
    2. Smithers SG,
    3. Palmer SE,
    4. Larcombe P,
    5. Johnson KG
    . 2008 1200 year paleoecological record of coral community development from the terrigenous inner shelf of the Great Barrier Reef. Geology 36, 691–694. doi:10.1130/g24907a.1 (doi:10.1130/g24907a.1)
    OpenUrlAbstract/FREE Full Text
  49. ↵
    1. Lewis SE,
    2. Shields GA,
    3. Kamber BS,
    4. Lough JM
    . 2007 A multi-trace element coral record of land-use changes in the Burdekin River catchment, NE Australia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 246, 471–487. doi:10.1016/j.palaeo.2006.10.021 (doi:10.1016/j.palaeo.2006.10.021)
    OpenUrlCrossRefGeoRefWeb of Science
  50. ↵
    1. Osborne K,
    2. Dolman AM,
    3. Burgess SC,
    4. Johns KA
    . 2011 Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995–2009). PLoS ONE 6, e17516. doi:10.1371/journal.pone.0017516 (doi:10.1371/journal.pone.0017516)
    OpenUrlCrossRefPubMed
  51. ↵
    1. Pulsford JS
    . 1996 Historical nutrient usage in coastal river catchments adjacent to the Great Barrier Reef Marine Park. In Research Publication No 40, p. 30. Townsville, Australia: Great Barrier Reef Marine Park Authority.
  52. ↵
    1. Souter P,
    2. Willis BL,
    3. Bay LK,
    4. Caley MJ,
    5. Muirhead A,
    6. van Oppen MJH
    . 2010 Location and disturbance affect population genetic structure in four coral species of the genus Acropora on the Great Barrier Reef. Mar. Ecol. Progr. Ser. 416, 35–45. doi:10.3354/meps08740 (doi:10.3354/meps08740)
    OpenUrlCrossRefWeb of Science
  53. ↵
    1. Sammarco PW
    . 1991 Geographically specific recruitment and postsettlement mortality as influences on coral communities: the cross-continental shelf transplant experiment. Limnol. Oceanogr. 36, 496–514. doi:10.4319/lo.1991.36.3.0496 (doi:10.4319/lo.1991.36.3.0496)
    OpenUrlCrossRefWeb of Science
  54. ↵
    1. Smith LD,
    2. Devlin M,
    3. Haynes D,
    4. Gilmour JP
    . 2005 A demographic approach to monitoring the health of coral reefs. Mar. Pollut. Bull. 51, 399–407. doi:10.1016/J.Marpolbul.2004.11.021 (doi:10.1016/J.Marpolbul.2004.11.021)
    OpenUrlCrossRefPubMedWeb of Science
  55. ↵
    1. Wallace CC
    . 1985 Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar. Biol. 88, 217–233. doi:10.1007/BF00392585 (doi:10.1007/BF00392585)
    OpenUrlCrossRefWeb of Science
  56. ↵
    1. Cramer KL,
    2. Jackson JBC,
    3. Angioletti CV,
    4. Leonard-Pingel J,
    5. Guilderson T
    . 2012 Anthropogenic mortality on Caribbean coral reefs predates coral disease and bleaching. Ecol. Lett. 15, 561–567. doi:10.1111/j.1461-0248.2012.01768.x (doi:10.1111/j.1461-0248.2012.01768.x)
    OpenUrlCrossRefPubMed
View Abstract
Back to top

Keywords

coral
Acropora
palaeoecology
historical mortality
Great Barrier Reef
European settlement
Share
Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement
George Roff, Tara R. Clark, Claire E. Reymond, Jian-xin Zhao, Yuexing Feng, Laurence J. McCook, Terence J. Done, John M. Pandolfi
Proc. R. Soc. B 2012 -; DOI: 10.1098/rspb.2012.2100. Published 7 November 2012
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Connotea logo Facebook logo Google logo Mendeley logo
Email

Thank you for your interest in spreading the word on Proceedings of the Royal Society of London B: Biological Sciences.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement
(Your Name) has sent you a message from Proceedings of the Royal Society of London B: Biological Sciences
(Your Name) thought you would like to see the Proceedings of the Royal Society of London B: Biological Sciences web site.
Print
Manage alerts

Please log in to add an alert for this article.

Sign In to Email Alerts with your Email Address
Citation tools

Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement

George Roff, Tara R. Clark, Claire E. Reymond, Jian-xin Zhao, Yuexing Feng, Laurence J. McCook, Terence J. Done, John M. Pandolfi
Proc. R. Soc. B 2012 -; DOI: 10.1098/rspb.2012.2100. Published 7 November 2012

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Download

Article reuse

  • Article
    • Abstract
    • 1. Introduction
    • 2. Material and methods
    • 3. Results
    • 4. Discussion
    • Acknowledgements
    • References
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF

See related subject areas:

  • palaeontology
  • ecology

Related articles

Cited by

Large datasets are available through Proceedings B's partnership with Dryad

Open biology

  • PROCEEDINGS B
    • About this journal
    • Contact information
    • Purchasing information
    • Submit
    • Author benefits
    • Open access membership
    • Recommend to your library
    • FAQ
    • Help

Royal society publishing

  • ROYAL SOCIETY PUBLISHING
    • Our journals
    • Open access
    • Publishing policies
    • Conferences
    • Podcasts
    • News
    • Blog
    • Manage your account
    • Terms & conditions
    • Cookies

The royal society

  • THE ROYAL SOCIETY
    • About us
    • Contact us
    • Fellows
    • Events
    • Grants, schemes & awards
    • Topics & policy
    • Collections
    • Venue hire

Copyright © 2018 The Royal Society