Evidence of very rapid reef growth under high turbidity and terrigenous sedimentation
Chris T. Perry1, Scott G. Smithers2, Pauline Gulliver3 and Nicola K. Browne2,4
1
Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, EX4 4RJ. UK
School of Earth & Environmental Sciences, James Cook University, Townsville, Qld 4811Australia
3
NERC Radiocarbon Laboratory, Scottish Enterprise Technology Park, Rankin Avenue, East
Kilbride, Scotland, G75 0QF, UK
4
DHI Water & Environment (S) Pte Ltd, 200 Pandan Loop, #08-03 Pantech 21, Singapore 128388
2
Email: nkb@dhi.com.sg
ABSTRACT
Global-scale deteriorations in coral reef health are projected to lead to a progressive
decline in reef-building potential and ultimately to states of net reef erosion. The
ecological changes may be driven by a wide range of direct human disturbances and by
climate change, butincreased terrestrial sediment and nutrient yields from
anthropogenically modified coastal catchments are widely recognised as a major threat.
As water quality deteriorates , reduced coral cover and species diversity are commonly
inferred, and lower reef accretion rates and impaired reef development are an assumed
consequence. Here we present a detailed chronostratigraphic growth history,
constrained by 40 AMS radiocarbon dates for Middle Reef, an inshore turbid-zone reef
(ITZR) on Australia’s Great Barrier Reef, which challenges the simplistic assumption
that high terrestrial sediment inputs restrict reef accretion rates and inhibit reef
development . We establish that Middle Reef has vertically accreted very rapidly for
more than 700 years, at an average rate of 8.3 mm yr-1. Accretion rates have varied
across the reef at different times but, significantly, the periods of most rapid vertical
accretion (averaging 13.0 mm yr-1) coincide with phases of reef development dominated
by fine-grained terrigenoclastic sediment accumulation. Both maximum and siteaveraged accretion rates match or exceed those documented for most clear-water, midand outer-shelf reefs in the region at any point over the last ~9,000 years, and those
determined for many reefs throughout the Indo-Pacific over the same time period.
Whilst examples of inshore coral reefs that have been degraded in the short-term by
excessive terrestrial sedimentation clearly exist, others clearly tolerate high
sedimentation and turbidity, and our data confirm that sustained and long-term rapid
vertical reef growth can occur in these environments. Indeed, in contrast to many reefs,
where there is often an order of magnitude difference between coral growth rates and
net long-term reef accretion rates, largely due to biologically-driven post-mortem
breakdown of the coral framework, long-term vertical accretion rates in these turbid
zone environments more closely approximate short-term coral growth rates.Our
findings of such rapid reef growth thus necessitate a re-think over the assumed negative
influence of terrestrial sedimentation on coral reef development.
INTRODUCTION
Regional-scale deteriorations in coral cover and reef architectural complexity, linked to a
suite of environmental and climate-change related disturbances, have been documented
(Bruno and Selig 2007; Gardner et al. 2003; Alvarez-Filip et al. 2009). These changes raise
important questions about reef resilience and often have immediate ecological consequences
for reef-associated species (Graham et al. 2007). A growing debate has thus arisen about the
impact of ecological change on reef growth potential and the maintenance of reefs as threedimensional structures (Hoegh-Gulberg et al. 2008; Pandolfi et al. 2011), underpinned by the
knowledge that in most ‘healthy’ reef ecosystemscorals are the primary reef-builders,
promoting high rates of carbonate production, and rapid vertical reef accretion and structural
development. Conversely, factors that degrade environmental conditions, or a reef’s
ecological condition, are inferred to limit reef accretion potential, either by reducing coral
growth rates and/or by increasing rates of reef erosion (Perry et al. 2008b).
Increased terrestrial sediment and nutrient yields, linked to anthropogenic modification of
coastal catchments, are widely regarded as a major threat to continued coral reef ‘health’ and
development (Kleypas and Eakin 2007). This is because nearshore turbidity and/or
sedimentation rates, as well as nutrient and contaminant concentrations, can be increased to
levels that directly influence reef communities (Fabricius 2005). Resultant impacts may
include lowercoral cover and diversity, reduced coral calcification and linear skeletal
extension, and modified competitive interactions between corals and macroalgae. Because
many inner-shelf and fringing reefs occur close to the point sources of sediment and nutrient
input (rivers), and because tropical coastal land use is changing at an unprecedented rate in
many regions, these water quality issues are increasingly relevant in the context of the ongoing debate about present and future coral reef ‘health’ and reef accretion potential.
The inner-shelf of Australia’s Great Barrier Reef (GBR) provides a particularly useful case
study in this respect. The inner-shelf seafloor is dominated by terrigenous sediment, with
wave-driven sediment resuspension causing conditions of high turbidity and high terrigenous
sediment flux. In addition, many coastal catchments along the Queensland coast were cleared
for pastoral and agricultural purposes following European settlement (from ~1850 AD)
(Lewis et al. 2007). Catchment sediment yields have reportedly increased markedly since
(Neil et al. 2002), possibly increasing five-tenfold (McCulloch et al. 2003). Recent modelling
also suggests that total nitrogen discharge has increased by a factor of four, and nitrate and
total phosphorus by a factor of ten (Devlin and Brodie 2005). These increases have been
argued to negatively impact reef condition, but critical questions are yet to be answered
regarding reef growth and development in these environments. Specifically, what are the
implications of long-term high turbidity and terrigenous sediment flux regimes for reef
accretion, and how do rates of reef accretion differ from those documented in clear water
settings?
FIELD SETTING AND METHODS
To address these questions we examined the accretionary history of Middle Reef, an ITZR
located in Cleveland Bay ~ 4 km offshore from Townsville in the central GBR (Fig. 1A).
Muddy sands dominate the surrounding seafloor (Carter et al. 1993), and the reef is regularly
exposed to high turbidity levels (up to 50 mg l-1) generated by wave-driven sediment
resuspension or by episodic flood plumes (Larcombe et al. 1995). Middle Reef has a complex
morphology but is characterised by relatively high live coral cover and coral species diversity
(Browne et al. 2010). We collected eight cores from three cross-reef transects, located to
ensure a spatially representative record of reef growth (Fig. 1B). Cores were recovered using
percussion techniques (using aluminium core piping with an internal diameter of 9.5 cm) and
had 100 % recovery. Rates and depths of core penetration were recorded throughout to ensure
a reliable depth chronology and to constrain for sediment compaction (typically ~15-20%,
and which, based on core penetration rates, was uniform down-core). All cores penetrated the
entire Holocene reef to terminate in Pleistocene clays. Immediately after collection cores
were split in half using a circular saw and digital photo composites of each prepared. Cores
were logged to record basic biosedimentary facies information. Data collected included; the
ratio of coral clasts to matrix, description of framework fabrics, preliminary coral species
identification, sediment textural characteristics using the Udden-Wentworth nomenclature, as
well as a visual assessment of sediment composition. These criteria were used to delineate
basic facies units within the cores. Facies analysis and the recovery of in-situ coral samples
for AMS Radiocarbon dating (Table S1) allowed the. In-situ coral samples were selected for
AMS radiocarbon dating to allow us to establish a detailed chronostratigraphic record of reef
accretion. Samples were prepared for dating by sectioning and microsampling to remove
surficial calcareous encrustation, washed in distilled water, subjected to ultrasonic agitation
in distilled water to remove detrital particles, oven dried (40oC) and then sealed in plastic
bags. Dates were calibrated using Calib 6.0 and calibration curve Marine04
(http://calib.qub.ac.uk/marine). The conventionally employed Marine Reservoir Correction in
Australian waters is 450 ± 35 years (Gillespie, 1977). However, various studies have
indicated significant deviations in regional marine reservoir signatures. The geographically
closest sites to Middle Reef are from Port Curtis and Gladstone where marine reservoir ages
ranging from 240 ± 61 to 419 ± 61 14C y BP are reported (Ulm, 2002). These combined give
a weighted mean ΔR value of +10 ± 7, currently the best estimate of variance in the local
open water marine reservoir effect for the central Queensland coast (Ulm, 2002). Resultant
calibrated AMS radiocarbon dates were used to determine average rates of accretion, as based
on interpretations of the depth-age relationship of the basal reefal facies compared to the reeftop age in each core, and accretion rates for each facies type based on interpreted depth-age
relationships for the top and bottom of each facies boundary in core.
RESULTS
Our data show that Middle Reef initiated above a thin transgressive lithic sand and graveldominated unit in water depths of 4-5 m below present Lowest Astronomical Tide (LAT)
level. Abraded coral clasts in this pre-reefal unit return ages of 1,293 and 1,495 cal yBP (Fig.
1C). Dates from corals interpreted as in-situ on taphonomic and orientation criteria collected
from the overlying reefal facies indicate, however, that the main phase of reef development
started in the period ~600-700 cal yBP, initially along the SW flank and towards the SE end
of the reef complex (Fig. 1C), with younger start up dates occurring towards the NW end of
the reef. Vertical accretion has occurred throughout this period, but different areas of the reef
have attained present sea level at different times: those areas with established reef flats
mostly reached sea level in the last < 100 years, whilst vertical accretion continues within
sub-tidal areas. Mud-rich (>50 weight % fines) reefal facies occur in all of the cores
recovered: this distinctive reef growth unit is a volumetrically dominant component of the
reef’s interior structure, and indicates significant net mud deposition within the coral
constructed fabric of the reef. Corals (especially platy forms of Turbinaria sp. and Montipora
sp.) are abundant and exceptionally well-preserved throughout, implying rapid post-mortem
burial occurs. Most importantly, it should be noted that this rapid burial has occurred
throughout reef accretion (i.e., over the last ~700 year period) and has significantly pre-dated
European settlement in the region.
DISCUSSION
Chronostratigraphic reconstructions indicate that Middle Reef has vertically accretedvery
rapidly throughout its history(average across all cores 8.3 mm yr-1: range 4 to 13 mm yr-1)
including over the past 100-200 years. Furthermore, the most rapid vertical accretion rates
(averaging 13.0 mm yr-1) coincide with the parts of the reef dominated by the most mud-rich
facies (Fig. 2). Thus, rather than being inhibitory to reef development and accretion, the
deposition and retention of terrigenous sediment has actually been contiguous with the
periods of most rapid vertical accretion. Clearly it is inappropriate to attribute the rapid
accretion rates to the high terrigenous sedimentation and turbidity, however it must be noted
that the widely inferred inhibitory impacts of this sedimentary regime are also not supported
by our detailed dataset. A scenario of corals growing rapidly upwards above an accumulating
muddy substrate can be envisaged, analogous to the concepts of superstratal growth as
invoked for mud-rich reefal environments in the Jurassic (Insalaco 2008). The presence of an
open Turbinaria and Montipora dominated framework on the contemporary reef surface,
with a muddy sediment infill at the base of that open framework, provides supporting
evidence that this process is on-going.
AMS radiocarbon dating indicates that deposition of this mud-dominated facies has occurred
in a time-independent way, with the timing of its accumulation varying with location on the
reef (Figs. 1C; 2): starting ~600 cal yBP in the SE areas of the reef, but only in the last ~ 100
years along the NE flank. There is thus no indication of an influence of regional European
landuse change and changed sediment yields (since circa 1850 AD) either on styles of reef
fabric development or on rates of vertical accretion. Core records from some areas of the reef
indicate that mud-rich sequences accumulated entirely or largely in the period post-1850, but
in other areas these accumulated entirely before this period. Thus the initial accumulation of
this mud-rich reef framework significantly predates recent landuse changes (and any increase
in sediment flux) and has not resulted in lowreef accretion rates. Rather it has been a natural
and enduring features ofthe reef’s growth history in this inner-shelf setting. The accumulation
of mud is, however, constrained vertically in most parts of the reef, with much lower mud
content in the cores at depths shallower than ~1 m below present LAT level. This most likely
reflects a transition, as respective areas of the reef shallowed (at different times), to water
depths at which rates of sediment re-suspension are much higher, thus slowing net rates of
sediment accumulation (see also Wolanski et al. 2005). Overall rates of reef accretion also
slow in the upper ~1 m of each core, presumably due to increased sediment resuspension and
export, but still remain high and average ~10 mm yr-1.
Rates of reef accretion at Middle Reef are particularly impressive when compared to those
from other reef localities in the region. Both maximum and site-averaged accretion rates
exceed those documented not only for other turbid-zone (inner-shelf) reefs on the GBR (Fig.
3A), but also the long-term rates calculated for individual clear-water, mid- and outer-shelf
reefs (Fig. 3B). They also far exceed regional average rates of accretion for all reef types on
the GBR over the last ~9,000 years (Fig. 4) and, by some margin, accretion rates measured at
sites over the last 1-2,000 year period. The relatively high rates established in this study are
also significant when compared against many other Indo-Pacific reefs across a range of
settings and depositional environments (Fig. 5). Only a very few of these reefs exhibit
significantly higher maximum accretion rates and only a few have higher average accretion
rates, despite the fact that most are located in ‘more optimal’ marine settings and are mostly
dominated by in-situ carbonate production.
The key questions that arise from these data are why are these rates so high, and what does
this mean in terms of the drivers of reef accretion? The prevailing view of reef development
is that rapid reef accretion occurs as a function of high rate coral growth and the net retention
of largely in-situ produced reefal carbonate (both coral framework and carbonate sediment).
Middle Reef, and other ITZRs, clearly develop under a different set of conditions. In these
environments, a high proportion of the material contributing to the internal structure (and thus
development) of the reefs derives not from within, but from outside the reef, in this case in
the form of fine-grained terrigenous sediments that are resuspended from the surrounding
seafloor or introduced during major flood events. Whilst such inputs are commonlyassumed
to negatively influence both reef communities and reef accretion rates, field evidence argues
strongly against the former (Browne et al. 2010) and ourcore data demonstrates that the latter
view is also incorrect. In these inshore turbid-zone environments a model of reef
development that differs from the traditional ‘clear water’ reef accretion scenario can thus be
envisaged whereby high rates of coral growth, by species adapted to deal with high turbidity
and sedimentation stress, enable rapid vertical reef framework accumulation. Concomitant
high rates of sedimentation rapidly infill the open reef fabric, inhibiting post-depositional
destruction of the coral skeletons, and aiding the preservation of the primary coral framework
structure. Thus in contrast to many reefs, where there is often an order of magnitude
difference between coral growth rates and net long-term reef accretion rates (Dullo 2005),
largely due to biologically-driven post-mortem breakdown of the coral framework, long-term
vertical accretion rates in these turbid zone environments more closely approximate shortterm coral growth rates. Whilst this can probably only occur in locations where the coral
communities are already adapted to deal with high sedimentation regimes and to the
periodically low light conditions associated with fluctuating turbidity, our findings clearly
question the assumption that environments dominated by terrigenous sediments are inherently
detrimental to coral reef development, and necessitate a re-think of prevailing models of reef
growth dynamics.
Methods
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Acknowledgements
We thank The Leverhulme Trust (UK) who funded this research under a Research Fellowship
(RF/4/RFG/2007/0106) to CTP, and the Natural Environment Research Council (UK) for an
AMS Radiocarbon Dating Allocation (1458.0310) to CTP, SGS and PG.
Author contributions
C.T.P. co-conceived and co-designed the study, collected field data, performed data analyses,
and led the writing of the paper. S.G.S. co-conceived and co-designed the study, and
contributed to data collection and writing. P.G. contributed to data analysis, and contributed
to writing. N.K.B. collected field data and contributed to writing.
Additional information
The authors declare no competing financial interests. Supplementary information
accompanies this paper on www.nature.com/naturegeoscience. Reprints and permissions
information is available online at http://npg.nature.com/reprintsandpermissions.
Correspondence and requests for materials should be addressed toC.T.P.
Figure 1. Location map, core sites and core logs from Middle Reef. (A) Location of Middle
Reefs on the inner-shelf of the central Great Barrier Reef; (B) Aerial photograph of Middle
Reef showing the location of core sites; (C) Core logs showing the depositional structure and
age history of Middle Reef relative to Lowest Astronomical Tide (LAT) level. White circles
show the position of radiocarbon dated corals and the age is shown as the median
probability age in calibrated years before present (cal yr BP). Note that samples containing
bomb carbon occur to depths of 70 cm below LAT in some cores and indicate very rapid
rates of vertical accretion in recent years at these localities.
Figure 2. Accretion rate trendlines derived for individual cores from Middle Reef. White
circles denote the age and depth relative to Lowest Astronomical Tide (LAT) of dated corals
in individual cores. The dashed line sections for Cores PC6 and PC7 indicate the lag that
occurred between the top of the transgressive pre-reefal unit (see Fig 1A) and the initiation
of vertical reef growth. Periods of accretion associated with the accumulation of the
terrigenous mud-dominated sequences are shown overlain with the bold grey lines. Note that
the main phases of mud deposition are coincident with the periods of most rapid vertical reef
accretion (the steepest line sections) and that their accumulation has been time independent
i.e., unrelated to the period of European settlement and landuse change.
Fig. 3. Average accretion rates established for Middle Reef, compared to other inner-,
mid- and outer-shelf reefs on the Great Barrier Reef. (A) Average accretion rate trendlines
for individual reef cores from Middle Reef (top left) compared against available data from
other late Holocene turbid-zone reefs from the central-northern Great Barrier Reef. Data
from: Lugger Shoal (Perry et al. 2009); Paluma Shoals (Palmer et al. 2010); Dunk Island
(Perry & Smithers 2010); Offshore Paluma Shoals (Perry & Smithers, unpublished). (B)
Average accretion rate trendlines for individual cores through Middle Reef (top left of plot)
compared with those derived from the most reliable radiocarbon dated cores from mid- and
outer-shelf reefs on the Great Barrier Reef (From: Hopley et al. 2007).
Figure 4. Accretion rates from Middle Reef compared to temporal records from other reef
sites on the Great Barrier Reef. Average growth rates based on core and radiocarbon data
for the last 9000 years for (A) fringing, (B) outer-shelf, and (C) all reefs for which reef
growth data is available for the Great Barrier Reef Shelf (after: Hopley et al. 2007). Average
and range of growth rate data from Middle Reef is shown for comparison.
Figure 5. Vertical accretion rates determined for Middle Reef compared to other reef environments
across the Indo-Pacific. Published mean, minimum and maximum vertical accretion rates (mm yr-1)
for back reef/lagoon, semi-exposed/sheltered reef margin, and exposed reef margin Pacific sites from
outside of the Great Barrier Reef region (data from Montaggioni 2005) shown against the minimum
and maximum (grey box) and mean (bold line) vertical accretion rates established from Middle Reef.
Where multiple data from the same sites exist, only the highest rates are shown. 1. Kabira, Ryukyus;
2. Lord Howe Island, Tasman Sea; 3. SW New Caledonia; 4. Mouillage, Chesterfield Island; 5. Oahu,
Hawaiian Islands; 6. Pukapuka, Cook Islands; 7. Rakahanga, Cook Islands; 8. Tahiti, Society
Islands; 9. Okierabu-Jima, Ryukyus;10. Tonoshiro, Ryukyus; 11. Kabira, Ryukyus; 12. Minna-Jima,
Ryukyus; 13. Tonaki-Jima, Ryukyus; 14. Kuma-Jima, Ryukyus; 15. Okinawa-Hontou, Ryukyus; 16.
Seksei, Ryukyus; 17. Koror, Palau; 18. Lord Howe Island, Tasman Sea; 19. East coast New
Caledonia; 20. West coast, New Caledonia; 21. Moorea, Society Islands; 22. Punta Island, Costa
Rica; 23. Punta Island, Costa Rica; 24. Uva Island, Panama; 25. Secas, Panama; 26. Saboga Island,
Panama; 27. Kabira, Ryukyus; 28. Yoron-tou, Ryukyus; 29. Kuma-Jima, Ryukyus; 30. Kikai-Jima,
Ryukyus; 31. Yam, Torres Strait; 32. Warraber, Torres Strait; 33. Bellona, Chesterfield Island; 34.
Mamie, New Caledonia; 35. Huon, Papua New Guinea; 36. Espiritu Santo, Vanuatu; 37. Rota,
Mariana Island; 38. Guam, Mariana Island; 39. Enewetak, Marshall Island; 40. Tarawa, Kiribati;
41. Funafuti, Tuvalu; 42. Oahu, Hawaiian Islands; 43. Molokai, Hawaiian Islands; 44. Mangaia,
Cook Islands; 45. Tahiti, Society Islands; 46. Moorea, Society Islands; 47. Mururoa, Tuamotu
Core/sample
code
Table S1
Material
Lab Ref.
Elevation
(m rel to
LAT)
14C
age
(yr BP)
14C
age
error
(yr BP)
Calibrated age
range (1)
Median
probability age
Max
Eastern transect
MR-PC7-20
Acropora
MR-PC7-50
Acropora
MR-PC7-115
Montipora
MR-PC7-150
Goniastrea
MR-PC7-275
Goniastrea
MR-PC6-15
Montipora
MR-PC6-45
Montipora
MR-PC6-75
Montipora
MR-PC6-140
Montipora
MR-PC6-155
Acropora
MR-PC6-370
Montipora
MR-PC6-390
Acropora
MR-PC6-430
Acropora
MR-PC11-15
Goniopora
MR-PC11-100 Turbinaria
MR-PC11-140 Acropora
MR-PC11-175 Favid
Central transect
MR-PC8-18
Acropora
MR-PC8-150
Cyphastrea
MR-PC8-210
Acropora
MR-PC4-25
Montipora
MR-PC4-55
Montipora
MR-PC4-135
Montipora
MR-PC4-200
Montipora
MR-PC4-230
Montipora
MR-PC9-20
Montipora
MR-PC9-45
Montipora
MR-PC9-65
Acropora
MR-PC9-100
Acropora
MR-PC9-120
Acropora
MR-PC9-340
Pachyseris
MR-PC9-360
Favid
MR-PC9-400
Goniopora
Western transect
MR-PC10-15
Montipora
MR-PC10-25
Acropora
MR-PC10-49
Acropora
MR-PC10-152 Acropora
MR-PC10-223 Turbinaria
MR-PC10-305 Goniopora
MR-PC10-440 Goniopora
Wk 27408
Wk 27409
Wk 27410
Wk 27411
Wk 27412
SUERC
31713
SUERC
31714
SUERC
31715
SUERC
31716
SUERC
31717
SUERC
31718
SUERC
31719
SUERC
31722
Wk
27421
Wk 27422
Wk 27423
Wk 27424
-0.9
-1.1
-2.2
-2.9
-4.5
+0.1
-0.2
-0.5
-1.2
-1.3
-3.5
-3.7
-4.1
-0.5
-2.5
-3.1
-3.5
663
642
862
975
1753
Modern
Modern
Modern
536
582
698
702
957
111.4
459
469
591
32
37
37
30
33
n/a
n/a
n/a
44
37
37
37
35
0.4
31
32
35
Wk 27413
Wk 27414
Wk 27415
Wk 26563
Wk 26564
Wk 26565
Wk 26566
Wk 26567
SUERC
31723
SUERC
32446
SUERC
32447
SUERC
32488
SUERC
32451
SUERC
32452
SUERC
32453
SUERC
32454
SUERC
32455
Wk 27416
Wk 27417
Wk 27418
Wk 27419
Wk 27420
SUERC
32456
-0.7
-3.0
-4.0
-0.1
-1.2
-2.3
-2.6
-3.2
-0.2
-0.4
-0.6
-0.9
-1.2
-3.4
-3.6
-4.0
114.5
714
1034
113.17
584
531
621
626
Modern
76
514
445
525
637
1144
1149
0.4
31
32
0.6
35
41
54
30
n/a
37
37
35
35
35
35
37
+0.1
-0.5
-1.0
-1.9
-3.2
-3.9
-4.2
Modern
375
459
655
662
1069
1125
n/a
31
31
32
32
29
35
Min
331
258
321
240
508
454
597
575
1324
1261
Modern
Modern
Modern
244
102
292
88
380
286
383
289
1544
1435
Modern
83
0
94
0
273
188
299
280
481
560
1293
Modern
Modern
Modern
157
204
340
343
1495
Modern
59
68
216
Modern
301
563
Modern
165
146
240
97
305
180
300
238
Modern
149
63
200
160
Invalid
233
92
313
239
713
652
718
654
Modern
352
599
Modern
207
152
251
265
Modern
127
145
Modern
Modern
Modern
Modern
59
291
298
630
671
390
634
83
321
330
993
699
0
254
257
603
640
145
275
685
689