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Cyclone and bioturbation effects on sediments from coral reef lagoons
Estuarine, Coastal and Shelf Science
(1988)
27,687-695
Cyclone and Bioturbation Effects on Sediments from Coral Reef Lagoons
Martin
J. Riddle
Australian Australia
Institute of Marine
Science, PMB No 3, Townsville MC, QLD 4810,
Received 2 February 1988 and in revised form
Keywords: cyclones; Barrier Reef
16 June 1988
coral reefs; sediments;
bioturbation;
infauna;
Great
Despite the severity of tropical cyclone ‘ Winifred ‘, which crossed the Great Barrier Reef on 1 February 1986, there were little long-term effects on lagoon surface sediments from reefs in its path. Short-term effects were apparent only at one particularly exposed area. These were: an increase in proportion of the coarse fraction, the establishment of sand ripples, arid the destruction of the mounds produced by callianassid shrimps (normally the dominant topographic feature). Within six weeks this area was indistinguishable from a typical reef lagoon. This is probably the result of sediment reworking by callianassid shrimp, involving selective burial of the coarse fragments and transport to the surface of finer particles. Sediment turnover rates by callianassids are commensurate with change to the sediment within the relatively short period observed. The sediment fauna responded quickly to the changes in sediment type. Immediately after the cyclone the disturbed area supported a fauna typical of the coarse sediments on the shallow reef flat, as the sediment reverted to a more normal type so the fauna changed back to that typical of a reef lagoon.
Introduction The waves generated by tropical cyclones are the most extreme hydrodynamic forces exerted on coral reefs. They may be expected to have a significant and lasting influence on many aspects of the coral reef system, with the unconsolidated sediments of the reef lagoon being particularly vulnerable. The distribution of grain size in sediments is partially determined by the hydrodynamics of overlying water masses. Abnormally energetic conditions will resuspend particles that are usually saltation load and move by saltation those that are normally traction load deposits. The net effect is the redistribution of normally stable sediments (Flood & Jell, 1977; Davies & Hughes, 1983; Frith, 1983). Tropical cyclone ‘Winifred ’ crossed the Great Barrier Reef north of Townsville between 19.00 and 22.00 h on 1 February 1986 at low tide. ‘ Winifred ’ was classed as a severe cyclone at intensity 3 on the 5-point Safiir-Simpson scale, with a central pressure of 957 mb and maximum wind gusts estimated at 198 km h-’ (Walker & Reardon, 1986). Records over the past 120 years suggest that an average of about two intensity 3 cyclones Contribution 0272-77
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+ 09
$03.00/O
No. 441 from the Australian
Institute
of Marine
Science.
@ 1988 Academic
Press Limited
688
M. J. Riddle
crossthe Great Barrier Reef each decade (Walker & Reardon, 1986). The coincidence of severecyclonic winds with the low tide resulted in hydrodynamic forces, predicted to be the most extreme exerted on the reefsin the region for several decades,possibly for this century. This study seeksto answer the question: do cyclones influence the sediments and sediment animals of coral reef lagoonsand are the effects lasting? Evidence on the nature, extent and duration of change was obtained by sampling lagoon sediments and fauna before and on two occasions after cyclone ‘ Winifred ‘. The effects of the cyclone are discussedin terms of their significance in relation to bioturbation by callianassidshrimps. Materials
and methods
The cyclone occurred in the middle of astudy of the spatial and temporal variability of coral reef sediment communities (Riddle, in press), data from which are usedhere to indicate the range of communities expected under normal conditions. One reef in the cyclone track (Potter Reef) and one near the edge of the area of disturbance (Rib Reef) were surveyed before the cyclone (Figure 1). Three reefs in the path of the cyclone (Gilbey, Feather and Potter Reefs) were surveyed within six days of the cyclone, and Rib Reef was surveyed for the secondtime a week later. Six weeksafter the cyclone, repeat observations were made at Potter and Rib Reefs and Otter and Noggin Reefs were visited for the first time. Reef lagoonsin this region are protected from the prevailing south-east trade winds by the reef front and are usually open to the north-west. Under normal conditions the shallowest part of the reef flat is submerged by at least 0.5 m at low tide. Observations on topography, sediment type and surficial detritus of lagoon sediments from each reef were made at 15-s intervals from a manta board towed at 2 knots. Sites representative of each lagoon at about 10m depth were sampled with a diver operated corer of 55 cm internal diameter; 20 cores to 20 cm depth were collected for fauna1 analysis. These cores were in four groups of five: each group was taken from an area of about 1 m*; the groups were about 4 m apart. The five cores from eachgroup were bulked to form the basic sampleunit (119 cm’). In addition three surface scrapingswere collected from each reef lagoon for analysis of sediment characteristics. Fauna1 samples were washed on a 0.5-mm square-meshed sieve, fixed with lo”,, formalin solution in seawaterand stained with Rose Bengal to aid sorting. Identification wasrestricted to family level or above. Samples for sediment analyses were stored at - 18°C. Total organic carbon was determined by the method of Sandstrom et al. (1986) using a Beckman Tocamaster Total Carbon Analyser. Total carbon and organic nitrogen were measured on a Leco Model 600 CHN analyser. Calcium carbonate was estimated as (Total C-Organic C) x 8.33. Analysis of the sediment grain size followed the methods of Folk (1974). Data analysis The relationships between sites with fauna1abundance asattributes was examined using an agglomerative hierarchical classification on the PATN package (Belbin, 1987). Counts were transformed by log,&+ 1). The Bray-Curtis similarity coefficient was used with a ‘ flexible ’ sorting strategy (unweighted pair group average, with the cluster intensity coefficient /I= - 0.25; Clifford & Stephenson, 1975). Site groups were tested for significance using the procedure of Sandland and Young (1979a,b). The pseudo-Cramer value, C, was used to identify those taxa contributing most to the diagnosis of site groups (Abel et al., 1985).
Cyclone and bioturbation
effects on sediments
689
0 5
147” I Figure 1. Location of reefs and study sites (*) in relation estimated maximum 10 min mean windspeeds (km h-‘) Wind speed estimates from Walker and Reardon (1986).
kilometres
p
I
to the cyclone track and the during cyclone ‘ Winifred ‘.
Results Observations
All but one of the areas visited soon after the cyclone had the appearance of typical undisturbed reef lagoons. The sediments were predominantly medium to fine sand and the major topographic features were large mounds (up to 30 cm high) built by callianassid shrimp frequently covering 100% of the lagoon floor. The exception wasPotter Reef in a
690
M. J. Riddle
SOON
BEFORE CYCLONE
AFTER
6 WEEKS AFTER
LEl 6 days after
Potter
cyclone
Root
Rib Reef
L-A
Gilbey
Reef 20%
7 days after cyclone
10
Feather
Reef 01
-2 >4
-1
0
1
I Lagoon
2
0.25
3
4
$
0.062 mm
sediments
Otter
Noggin
Reel
l-2clL
Reef
LA!5 Figure 2. Particle size distribution of lagoon sediments from reefs in the path of cyclone ‘ Winifred ‘, before and on two occasions after the cyclone (mean + standard error for those from replicated samples).
part of the lagoon behind a large break in the reef front. In this area the surface layer was predominantly coral fragments, (0.5-1.0 cm diameter), lying in ripples about 10 cm high and 50 cm apart. Evidence of callianassidactivity wassparse;their presencewasindicated by small, widely dispersedmounds (up to 5 cm high by 15 cm across)of liner carbonate sand. This samearea when revisited six weeks after the cyclone appeared indistinguishable from a typical lagoon. The sediment wasline and callianassidmounds were abundant and large. Sedimentcharacteristics The grain-size distribution of the sediment from Potter Reef immediately after the cyclone wasvery different from that of other lagoonsand the sameplace before the cyclone (Figure 2). There wasa considerably greater proportion of gravel, a moderate increase in
Cyclone
and bioturbation
effects on sediments
691
1. Levels of organic carbon and nitrogen (mean & 1 SE) in lagoon sediments from reefs in the path of cyclone ‘ Winifred ’ before, several days after and six weeks after the cyclone. Levels are not significantly different (Kruskal-Wallis test, p > 0.05)
TABLE
Organic carbon (“u dry 4
n Before cyclone Rib and Lodestone
Reefs
Soon after cyclone Potter Reef (disturbed sediment) Rib, Gilbey and Feather Reefs (undisturbed sediment) Six weeks after cyclone Potter Reef Rib Reef
3uter
shelf
reefs
Reef
Organic nitrogen Coo dry wt)
5
0.24kO.021
0.07kO.012
3
0.21*
0.003
0.09 * 0.009
5
0.21+
0.007
0~07~0~01
3 3
0.24&O 0.23kO.018
0.07 & 0.003 0.07 * 0.009
fiats
Lagoons Reef
flats
r
6 days
after
before
cyclone
-
‘otter Reef
Rib Reef
Figure 3. Dendrogram representing the relationship between the sediment communities from the disturbed lagoon on Potter Reef six days after the cyclone with those from other reefs of the central Great Barrier Reef.
the coarse sand component and a corresponding decrease in medium to fine sand. The sediment conforms to the Sediment Type I, described by Flood and Orme (1977), and usually found on shallower areas of the reef flat (Riddle, in press). All other particle distributions, including that same area of Potter Reef 6 weeks after the cyclone, conform to Sediment Type III of Flood and Orme (1977). This is the sediment typical of reef lagoons (Riddle, in press). Organic carbon and nitrogen did not vary significantly (Kruskal-Wallis test, p > 0.05) over the period sampled (Table 1). Fauna1 composition Before the cyclone the fauna of Potter Reef lagoon was similar to that of the deeper part of Rib Reef lagoon (Figure 3). Six days after the cyclone it was more like that of a shallow reef
692
M. J. Riddle
2. Density (m ‘) (k 1 SE) of those taxa most significant in distinguishing the immediate post-cyclone samples from Potter Reef from comparable sites on mid-shelf reefs. S, sipunculid; P, polychaetes; C, crustacea.
TABLE
Pseudo-Cramer Aspidosiphonidae (S) Phascolosomatidae (S) Magelonidae (P) Nereidae (P) Pisionidae (P) Phyllodocidae (P) Amphinomidae (P) Ostracoda (C) Nephtyidae (P) Phoxocephalidae (C)
0.96 0.85 0.87 0.86 0.81 0.69 0.67 0.92 0.72 0.64
Disturbed lagoon (Potter Reef) (n=4) 358k 110 63k21 884+ 121 421f119 379&219 484k 147 126k80 0 42+46 0
Undisturbed Lagoon (n = 24) 0 0 35+18 18kll 0 6Ok29 0 3600+442 319137 887+ 146
flat. Six weeks after the cyclone it had returned to the pre-cyclone condition. The fauna from Rib Reef showed no change following the cyclone. Several taxa were characteristic of the disturbed area on Potter Reef (Table 2). The two sipunculid families, Aspidosiphonidae and Phasiolosomatidae(commonly found in gastropod shellsand coral fragments) were previously absent. Their abundance following the cyclone and the size and appearanceof the animals, suggeststhat they arrived with the fragments and did not settle opportunistically on a newly available microhabitat. The polychaete families Nereidae, Pisionidae, Phyllodocidae and Amphinomidae were all present in the disturbed area in high numbers. These taxa are commonly found in the coarsesedimentsof the reef flat and are usually either in low numbers or are absent in the finer sedimentsof the reef lagoon. The sedentary polychaetes, particularly those living in tubes, were expected to be most vulnerable to disturbance of this type. This did not appear to be the case, sedentary polychaetes contributed 299, of the total fauna immediately after the cyclone (Figure 4) representing nine families, including the three tube-dwelling families Maldanidae, Oweniidae and Terebellidae. Crustacea were very poorly represented at the disturbed site, contributing only 3% of the total. In contrast they were a significant component of the fauna from the areabefore the cyclone (75::,), six weeksafterwards (41%) and from other middle-shelf reef lagoons (50?,,). Discussion
Cyclones can change the sedimentsand sediment fauna of coral reef lagoons.However, the study showsthat the reef front affords the lagoon considerable protection. Only in an area behind a break in the front of a reef in the zone of most intense winds were signs of disturbance apparent. No effect was seenon a nearby reef subject to similar wave intensity but with an unbroken windward face. The low tide coincident with the crossing of the Great Barrier Reef by the cyclone may have reduced the effect to the lagoon; with little water lying over the reef front it would form an effective barrier dissipating most of the wave energy. The limited effect on reef lagoon sediments contrasts markedly with the effects on sediments from between reefs where pronounced sand waves were seen to a
Cyclone
and bioturbation
effects on sediments
693
80 -
60-
40 -
20 -
n” before cyclone
-Potter
6 days after
6 weeks after
Reef -
other* reefs
Figure 4. Composition ((I,,) of Potter Reef lagoon sediment fauna before, immediately after and six weeks after cyclone ‘ Winifred ’ compared with the lagoon fauna from other middle shelf reefs on the central Great Barrier Reef. *From Riddle (in press).
depth of 33 m (Birtles, 1986). However, thesefindings are similar to those of Kirby-Smith and Ustach (1986) who concluded that mid-continental shelf live-bottom communities are not significantly damaged by hurricanes and that temporary disturbance of sediment doesnot have a lasting impact. Where disturbance was apparent, the most obvious effect wasan increasein proportion of coarser sediments.This may be due to the removal of fine particles, to the deposition of coarsefragments or to a combination of both mechanisms.Deposition as a contributory factor is supported by the presenceafter the cyclone of large numbers of boring sipunculids not previously recorded in the area. The size and appearanceof theseanimals suggests that they have been associatedwith these coral fragments for sometime previously, this would not have been possible had the fragments been brought to the surface from deeper, anoxic sediments. The most likely explanation is that they were carried from elsewhere with the coral debris. A source for this coarsematerial was suggestedby the observation of a white band of reef matrix at the base of the gutters which run perpendicular to the seawardside of the reef front. This 0.5-l m high band contrasted markedly with the algal encrusted sections higher up and was interpreted as uncolonised reef matrix recently exposed by the removal of gutter sediment. The cyclone-induced changesin sediment type were not lasting. Within six weeks the disturbed area was indistinguishable in terms of topography and grain size from undisturbed reef lagoons. Rates of sediment accumulation on coral reefs (0.5-25 mm y-l; Tudhope, 1983) cannot account for such a rapid recovery, it is probably the result of sediment reworking by callianassid shrimps. These shrimps are ubiquitous in lagoon sedimentson the Great Barrier Reef. They are at their most densewithin the depth range 8-18 m, covering the lagoon floor with a contiguous series of mounds up to 30 cm in height. Sediment turnover by Callianassa spp. (up to 2500cm3 m-* day-‘; Tudhope, 1983; Riddle, 1987) from comparable areas on the Great Barrier Reef equates to the
694
M.
3.
Riddle
return of a layer 25 mm thick to the sediment surface every day. At this rate, six weeks after the cyclone, the layer of reworked sediment at the surface would be IO.5 cm deep. Elsewhere estimates of turnover are up to four times this rate (Aller & Dodge, 1974). The deposit-feeding callianassids found in coral reef sediments are selective in their processing of the sediment (Suchanek, 1985). They preferentially return finer grains to the surface and store larger grains, coral fragments and shell debris in sub-surface galleries (Suchanek, 1983), as a result they destroy any primary sedimentary layering (Tudhope & Scoffm, 1984). Callianassid activity therefore provides a mechanism for major changes to the sediment structure at a rate commensurate with that observed. The fauna of the disturbed sediment was very different from that of an undisturbed reef lagoon. Notable was the absence of crustaceans after the cyclone. This also was a transient change, as within six weeks the fauna had reverted to its pre-cyclone condition with the crustacea once again abundant. Many benthic crustaceans swim nocturnally (Kaartvedt, 1986), enabling rapid recolonization by adults (Santos & Simon, 1980) when favourable conditions return. Representatives of two sipunculid families were only found in the disturbed area immediately after the cyclone, both live in large calcareous fragments. This debris was quickly moved to a deeper layer in the sediment by the activity of callianassids and the sipunculids would inevitably be moved as well. Their survival at these depths is doubtful. The four polychaete families with numbers enhanced immediately after the cyclone were all mobile with the ability to take advantage of a newly available habitat. They are normally found in the coarse material of the reef flat and were quick to colonize the coarse sediment deposited in the reef lagoon by the cyclone. However, as this was reworked by callianassids and returned to its former condition they were also quick to respond, either by leaving or dying. In conclusion, cyclone ‘ Winifred ’ had little long-term effect on the surface sediments and sediment communities of reef lagoons in its path. This was due to the sheltering effect of the reef front largely preventing major sediment disturbance and to the sediment reworking activity of callianassid shrimp which quickly returned disturbed sediments to their pre-cyclone condition. The effect of cyclones on the deeper sediment record will depend on their frequency, the amount of material removed, the rate of sedimentation and the depth to which callianassids rework sediment.
Acknowledgements This study was undertaken during a Post Doctoral Research Fellowship at the Australian Institute of Marine Science. Advice from T. Done was invaluable and readily forthcoming throughout. I thank T. Done, C. Wilkinson and A. Dartnall for reading and criticising the manuscript. References Abel, D. J., Williams, W. T. &Williams, D. M. 1985 A fast classificatory algorithm for large problems under the Bray-Curtis measure. Journal of Experimental Marine Biology and Ecology 89,237245. Aller, R. C. & Dodge, R. E. 1974 Animal-sediment relations in a tropical lagoon Discovery Bay, Jamaica. Journal of Marine Research 32,209-232. Belbin, L. 1987 PA TN Pattern Analysis Package Reference Manual. Canberra: CSIRO Division of Wildlife and Rangelands Research. Birtles, A. 1986 Some preliminary observations from a survey of the soft sediment biota of the inner and middle shelf of the Great Barrier Reef following cyclone Winifred. In The Ofshore Effects of Cyclone
Cyclone
and bioturbation
effects on sediments
695
Winifred (Dutton, I. M., ed.). Workshop series No. 7. Townsville: Great Barrier Reef Marine Park Authority, pp. 47-49. Clifford, H. T. & Stephenson, W. 1975 An Introduction to Numerical Classification. New York: Academic Press. Davies, P. J. & Hughes, H. 1983 High-energy reef and terrigenous sedimentation, Boulder Reef, Great Barrier Reef. Bureau of Mineral ResourcesJournal of Australian Geology and Geophysics 8,201-209. Flood, P. G. & Jel, J. S. 1977 The effect of cyclone ‘David ’ (January 1976) on the sediment distribution patterns on Heron Reef, Great Barrier Reef, Australia. Proceedings of third International Coral Reef Symposium 2,120-125. Flood, P. G. & Orme, G. R. 1977 A sedimentation model for platform reefs of the Great Barrier Reef, Australia. Proceedings of third International Coral Reef Symposium 2,11 l-l 16. Folk, R. L. 1974 Petrology of Sedimentary Rocks. Austin, Texas: Hemphills. Frith, C. A. 1983 Some aspects of lagoon sedimentation and circulation at a One Tree Reef, Southern Great Barrier Reef. Bureau of Mineral ResourcesJournal of Australian Geology and Geophysics 8,2 11-221. Kaartvedt, S. 1986 Die1 activity patterns in deep-living cumaceans and amphipods. Marine Ecology Progress Series 30,243-249. Kirby-Smith, W. W. & Ustach, J. 1986 Resistance to hurricane disturbance of an epifaunal community on the continental shelf off North Carolina. Estuarine, Coastal and Shelf Science 23,433-442. Riddle, M. J. 1987 Bioturbation by callianassid shrimp as a determinant of the infauna of coral reef lagoon sediments. In Australian Marine Sciences Association and Australian Physical Oceanography Joint Conference (Marsh, H., Heron, M. L., eds). 1,53. Riddle, M. J. (in press) Patterns in the distribution of sediment communities from coral reefs across the central Great Barrier Reef. Marine Ecology Progress Series. Sandland, R. L. & Young, P. C. 1979a Probablistic tests and stopping rules associated with hierarchical classification techniques. AustralianJournal of Ecology 4,399-406. Sandland, R. L. &Young, P. C. 19793 Tables of Probabilities associated with the fission of replicate samples in classification. CSIRO Australian Division of Fisheries and Oceanography Report, 108. Sandstrom, M. W., Tirendi, F. & Nott, A. 1986 Direct determination of organic carbon in modern reef sediments and calcareous organisms after dissolution of carbonate. Marine Geology 70,321-329. Santos, S. L. & Simon, J. L. 1980 Marine soft-bottom community establishment following annual defaunation: Larval or adult recruitment. Marine Ecology Progress Series 2, 235-241. Suchanek, T. H. 1983 Control of seagrass communities and sediment distribution by Callianassa (Crustacea; Thalassinidea) bioturbationJourna1 of Marine Research 41,281-298. Suchanek, T. H. 1985 Thalassinid shrimp burrows: ecological significance of species-specific architecture. Proceedings of the Fifth International Coral Reef Congress $205-210. T&hope, A. W. 1983 Processes of lagoonal sedimentation and patch reef development, Davies Reef, Great Barrier Reef of Australia. Ph.D. Thesis, University of Edinburgh. T&hope, A. W. & Scoffin, T. P. 1984 The effects of Callianassa bioturbation on the preservation of carbonate grains in Davies Reef lagoon, Great Barrier Reef, Australia. Journal of Sedimentary Petrology 54, 1091-1096. Walker, G. R. & Reardon, R. F. 1986 Wind speeds in the Great Barrier Reef region from cyclone Winifred and their effect on buildings. In The Offshore Effects of Cyclone Winifred (Dutton, I. M., ed.). Workshop Series No. 7, Townsville: Great Barrier Reef Marine Park Authority, pp. 28-40.
(1988)
27,687-695
Cyclone and Bioturbation Effects on Sediments from Coral Reef Lagoons
Martin
J. Riddle
Australian Australia
Institute of Marine
Science, PMB No 3, Townsville MC, QLD 4810,
Received 2 February 1988 and in revised form
Keywords: cyclones; Barrier Reef
16 June 1988
coral reefs; sediments;
bioturbation;
infauna;
Great
Despite the severity of tropical cyclone ‘ Winifred ‘, which crossed the Great Barrier Reef on 1 February 1986, there were little long-term effects on lagoon surface sediments from reefs in its path. Short-term effects were apparent only at one particularly exposed area. These were: an increase in proportion of the coarse fraction, the establishment of sand ripples, arid the destruction of the mounds produced by callianassid shrimps (normally the dominant topographic feature). Within six weeks this area was indistinguishable from a typical reef lagoon. This is probably the result of sediment reworking by callianassid shrimp, involving selective burial of the coarse fragments and transport to the surface of finer particles. Sediment turnover rates by callianassids are commensurate with change to the sediment within the relatively short period observed. The sediment fauna responded quickly to the changes in sediment type. Immediately after the cyclone the disturbed area supported a fauna typical of the coarse sediments on the shallow reef flat, as the sediment reverted to a more normal type so the fauna changed back to that typical of a reef lagoon.
Introduction The waves generated by tropical cyclones are the most extreme hydrodynamic forces exerted on coral reefs. They may be expected to have a significant and lasting influence on many aspects of the coral reef system, with the unconsolidated sediments of the reef lagoon being particularly vulnerable. The distribution of grain size in sediments is partially determined by the hydrodynamics of overlying water masses. Abnormally energetic conditions will resuspend particles that are usually saltation load and move by saltation those that are normally traction load deposits. The net effect is the redistribution of normally stable sediments (Flood & Jell, 1977; Davies & Hughes, 1983; Frith, 1983). Tropical cyclone ‘Winifred ’ crossed the Great Barrier Reef north of Townsville between 19.00 and 22.00 h on 1 February 1986 at low tide. ‘ Winifred ’ was classed as a severe cyclone at intensity 3 on the 5-point Safiir-Simpson scale, with a central pressure of 957 mb and maximum wind gusts estimated at 198 km h-’ (Walker & Reardon, 1986). Records over the past 120 years suggest that an average of about two intensity 3 cyclones Contribution 0272-77
14/88/060687
+ 09
$03.00/O
No. 441 from the Australian
Institute
of Marine
Science.
@ 1988 Academic
Press Limited
688
M. J. Riddle
crossthe Great Barrier Reef each decade (Walker & Reardon, 1986). The coincidence of severecyclonic winds with the low tide resulted in hydrodynamic forces, predicted to be the most extreme exerted on the reefsin the region for several decades,possibly for this century. This study seeksto answer the question: do cyclones influence the sediments and sediment animals of coral reef lagoonsand are the effects lasting? Evidence on the nature, extent and duration of change was obtained by sampling lagoon sediments and fauna before and on two occasions after cyclone ‘ Winifred ‘. The effects of the cyclone are discussedin terms of their significance in relation to bioturbation by callianassidshrimps. Materials
and methods
The cyclone occurred in the middle of astudy of the spatial and temporal variability of coral reef sediment communities (Riddle, in press), data from which are usedhere to indicate the range of communities expected under normal conditions. One reef in the cyclone track (Potter Reef) and one near the edge of the area of disturbance (Rib Reef) were surveyed before the cyclone (Figure 1). Three reefs in the path of the cyclone (Gilbey, Feather and Potter Reefs) were surveyed within six days of the cyclone, and Rib Reef was surveyed for the secondtime a week later. Six weeksafter the cyclone, repeat observations were made at Potter and Rib Reefs and Otter and Noggin Reefs were visited for the first time. Reef lagoonsin this region are protected from the prevailing south-east trade winds by the reef front and are usually open to the north-west. Under normal conditions the shallowest part of the reef flat is submerged by at least 0.5 m at low tide. Observations on topography, sediment type and surficial detritus of lagoon sediments from each reef were made at 15-s intervals from a manta board towed at 2 knots. Sites representative of each lagoon at about 10m depth were sampled with a diver operated corer of 55 cm internal diameter; 20 cores to 20 cm depth were collected for fauna1 analysis. These cores were in four groups of five: each group was taken from an area of about 1 m*; the groups were about 4 m apart. The five cores from eachgroup were bulked to form the basic sampleunit (119 cm’). In addition three surface scrapingswere collected from each reef lagoon for analysis of sediment characteristics. Fauna1 samples were washed on a 0.5-mm square-meshed sieve, fixed with lo”,, formalin solution in seawaterand stained with Rose Bengal to aid sorting. Identification wasrestricted to family level or above. Samples for sediment analyses were stored at - 18°C. Total organic carbon was determined by the method of Sandstrom et al. (1986) using a Beckman Tocamaster Total Carbon Analyser. Total carbon and organic nitrogen were measured on a Leco Model 600 CHN analyser. Calcium carbonate was estimated as (Total C-Organic C) x 8.33. Analysis of the sediment grain size followed the methods of Folk (1974). Data analysis The relationships between sites with fauna1abundance asattributes was examined using an agglomerative hierarchical classification on the PATN package (Belbin, 1987). Counts were transformed by log,&+ 1). The Bray-Curtis similarity coefficient was used with a ‘ flexible ’ sorting strategy (unweighted pair group average, with the cluster intensity coefficient /I= - 0.25; Clifford & Stephenson, 1975). Site groups were tested for significance using the procedure of Sandland and Young (1979a,b). The pseudo-Cramer value, C, was used to identify those taxa contributing most to the diagnosis of site groups (Abel et al., 1985).
Cyclone and bioturbation
effects on sediments
689
0 5
147” I Figure 1. Location of reefs and study sites (*) in relation estimated maximum 10 min mean windspeeds (km h-‘) Wind speed estimates from Walker and Reardon (1986).
kilometres
p
I
to the cyclone track and the during cyclone ‘ Winifred ‘.
Results Observations
All but one of the areas visited soon after the cyclone had the appearance of typical undisturbed reef lagoons. The sediments were predominantly medium to fine sand and the major topographic features were large mounds (up to 30 cm high) built by callianassid shrimp frequently covering 100% of the lagoon floor. The exception wasPotter Reef in a
690
M. J. Riddle
SOON
BEFORE CYCLONE
AFTER
6 WEEKS AFTER
LEl 6 days after
Potter
cyclone
Root
Rib Reef
L-A
Gilbey
Reef 20%
7 days after cyclone
10
Feather
Reef 01
-2 >4
-1
0
1
I Lagoon
2
0.25
3
4
$
0.062 mm
sediments
Otter
Noggin
Reel
l-2clL
Reef
LA!5 Figure 2. Particle size distribution of lagoon sediments from reefs in the path of cyclone ‘ Winifred ‘, before and on two occasions after the cyclone (mean + standard error for those from replicated samples).
part of the lagoon behind a large break in the reef front. In this area the surface layer was predominantly coral fragments, (0.5-1.0 cm diameter), lying in ripples about 10 cm high and 50 cm apart. Evidence of callianassidactivity wassparse;their presencewasindicated by small, widely dispersedmounds (up to 5 cm high by 15 cm across)of liner carbonate sand. This samearea when revisited six weeks after the cyclone appeared indistinguishable from a typical lagoon. The sediment wasline and callianassidmounds were abundant and large. Sedimentcharacteristics The grain-size distribution of the sediment from Potter Reef immediately after the cyclone wasvery different from that of other lagoonsand the sameplace before the cyclone (Figure 2). There wasa considerably greater proportion of gravel, a moderate increase in
Cyclone
and bioturbation
effects on sediments
691
1. Levels of organic carbon and nitrogen (mean & 1 SE) in lagoon sediments from reefs in the path of cyclone ‘ Winifred ’ before, several days after and six weeks after the cyclone. Levels are not significantly different (Kruskal-Wallis test, p > 0.05)
TABLE
Organic carbon (“u dry 4
n Before cyclone Rib and Lodestone
Reefs
Soon after cyclone Potter Reef (disturbed sediment) Rib, Gilbey and Feather Reefs (undisturbed sediment) Six weeks after cyclone Potter Reef Rib Reef
3uter
shelf
reefs
Reef
Organic nitrogen Coo dry wt)
5
0.24kO.021
0.07kO.012
3
0.21*
0.003
0.09 * 0.009
5
0.21+
0.007
0~07~0~01
3 3
0.24&O 0.23kO.018
0.07 & 0.003 0.07 * 0.009
fiats
Lagoons Reef
flats
r
6 days
after
before
cyclone
-
‘otter Reef
Rib Reef
Figure 3. Dendrogram representing the relationship between the sediment communities from the disturbed lagoon on Potter Reef six days after the cyclone with those from other reefs of the central Great Barrier Reef.
the coarse sand component and a corresponding decrease in medium to fine sand. The sediment conforms to the Sediment Type I, described by Flood and Orme (1977), and usually found on shallower areas of the reef flat (Riddle, in press). All other particle distributions, including that same area of Potter Reef 6 weeks after the cyclone, conform to Sediment Type III of Flood and Orme (1977). This is the sediment typical of reef lagoons (Riddle, in press). Organic carbon and nitrogen did not vary significantly (Kruskal-Wallis test, p > 0.05) over the period sampled (Table 1). Fauna1 composition Before the cyclone the fauna of Potter Reef lagoon was similar to that of the deeper part of Rib Reef lagoon (Figure 3). Six days after the cyclone it was more like that of a shallow reef
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2. Density (m ‘) (k 1 SE) of those taxa most significant in distinguishing the immediate post-cyclone samples from Potter Reef from comparable sites on mid-shelf reefs. S, sipunculid; P, polychaetes; C, crustacea.
TABLE
Pseudo-Cramer Aspidosiphonidae (S) Phascolosomatidae (S) Magelonidae (P) Nereidae (P) Pisionidae (P) Phyllodocidae (P) Amphinomidae (P) Ostracoda (C) Nephtyidae (P) Phoxocephalidae (C)
0.96 0.85 0.87 0.86 0.81 0.69 0.67 0.92 0.72 0.64
Disturbed lagoon (Potter Reef) (n=4) 358k 110 63k21 884+ 121 421f119 379&219 484k 147 126k80 0 42+46 0
Undisturbed Lagoon (n = 24) 0 0 35+18 18kll 0 6Ok29 0 3600+442 319137 887+ 146
flat. Six weeks after the cyclone it had returned to the pre-cyclone condition. The fauna from Rib Reef showed no change following the cyclone. Several taxa were characteristic of the disturbed area on Potter Reef (Table 2). The two sipunculid families, Aspidosiphonidae and Phasiolosomatidae(commonly found in gastropod shellsand coral fragments) were previously absent. Their abundance following the cyclone and the size and appearanceof the animals, suggeststhat they arrived with the fragments and did not settle opportunistically on a newly available microhabitat. The polychaete families Nereidae, Pisionidae, Phyllodocidae and Amphinomidae were all present in the disturbed area in high numbers. These taxa are commonly found in the coarsesedimentsof the reef flat and are usually either in low numbers or are absent in the finer sedimentsof the reef lagoon. The sedentary polychaetes, particularly those living in tubes, were expected to be most vulnerable to disturbance of this type. This did not appear to be the case, sedentary polychaetes contributed 299, of the total fauna immediately after the cyclone (Figure 4) representing nine families, including the three tube-dwelling families Maldanidae, Oweniidae and Terebellidae. Crustacea were very poorly represented at the disturbed site, contributing only 3% of the total. In contrast they were a significant component of the fauna from the areabefore the cyclone (75::,), six weeksafterwards (41%) and from other middle-shelf reef lagoons (50?,,). Discussion
Cyclones can change the sedimentsand sediment fauna of coral reef lagoons.However, the study showsthat the reef front affords the lagoon considerable protection. Only in an area behind a break in the front of a reef in the zone of most intense winds were signs of disturbance apparent. No effect was seenon a nearby reef subject to similar wave intensity but with an unbroken windward face. The low tide coincident with the crossing of the Great Barrier Reef by the cyclone may have reduced the effect to the lagoon; with little water lying over the reef front it would form an effective barrier dissipating most of the wave energy. The limited effect on reef lagoon sediments contrasts markedly with the effects on sediments from between reefs where pronounced sand waves were seen to a
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80 -
60-
40 -
20 -
n” before cyclone
-Potter
6 days after
6 weeks after
Reef -
other* reefs
Figure 4. Composition ((I,,) of Potter Reef lagoon sediment fauna before, immediately after and six weeks after cyclone ‘ Winifred ’ compared with the lagoon fauna from other middle shelf reefs on the central Great Barrier Reef. *From Riddle (in press).
depth of 33 m (Birtles, 1986). However, thesefindings are similar to those of Kirby-Smith and Ustach (1986) who concluded that mid-continental shelf live-bottom communities are not significantly damaged by hurricanes and that temporary disturbance of sediment doesnot have a lasting impact. Where disturbance was apparent, the most obvious effect wasan increasein proportion of coarser sediments.This may be due to the removal of fine particles, to the deposition of coarsefragments or to a combination of both mechanisms.Deposition as a contributory factor is supported by the presenceafter the cyclone of large numbers of boring sipunculids not previously recorded in the area. The size and appearanceof theseanimals suggests that they have been associatedwith these coral fragments for sometime previously, this would not have been possible had the fragments been brought to the surface from deeper, anoxic sediments. The most likely explanation is that they were carried from elsewhere with the coral debris. A source for this coarsematerial was suggestedby the observation of a white band of reef matrix at the base of the gutters which run perpendicular to the seawardside of the reef front. This 0.5-l m high band contrasted markedly with the algal encrusted sections higher up and was interpreted as uncolonised reef matrix recently exposed by the removal of gutter sediment. The cyclone-induced changesin sediment type were not lasting. Within six weeks the disturbed area was indistinguishable in terms of topography and grain size from undisturbed reef lagoons. Rates of sediment accumulation on coral reefs (0.5-25 mm y-l; Tudhope, 1983) cannot account for such a rapid recovery, it is probably the result of sediment reworking by callianassid shrimps. These shrimps are ubiquitous in lagoon sedimentson the Great Barrier Reef. They are at their most densewithin the depth range 8-18 m, covering the lagoon floor with a contiguous series of mounds up to 30 cm in height. Sediment turnover by Callianassa spp. (up to 2500cm3 m-* day-‘; Tudhope, 1983; Riddle, 1987) from comparable areas on the Great Barrier Reef equates to the
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return of a layer 25 mm thick to the sediment surface every day. At this rate, six weeks after the cyclone, the layer of reworked sediment at the surface would be IO.5 cm deep. Elsewhere estimates of turnover are up to four times this rate (Aller & Dodge, 1974). The deposit-feeding callianassids found in coral reef sediments are selective in their processing of the sediment (Suchanek, 1985). They preferentially return finer grains to the surface and store larger grains, coral fragments and shell debris in sub-surface galleries (Suchanek, 1983), as a result they destroy any primary sedimentary layering (Tudhope & Scoffm, 1984). Callianassid activity therefore provides a mechanism for major changes to the sediment structure at a rate commensurate with that observed. The fauna of the disturbed sediment was very different from that of an undisturbed reef lagoon. Notable was the absence of crustaceans after the cyclone. This also was a transient change, as within six weeks the fauna had reverted to its pre-cyclone condition with the crustacea once again abundant. Many benthic crustaceans swim nocturnally (Kaartvedt, 1986), enabling rapid recolonization by adults (Santos & Simon, 1980) when favourable conditions return. Representatives of two sipunculid families were only found in the disturbed area immediately after the cyclone, both live in large calcareous fragments. This debris was quickly moved to a deeper layer in the sediment by the activity of callianassids and the sipunculids would inevitably be moved as well. Their survival at these depths is doubtful. The four polychaete families with numbers enhanced immediately after the cyclone were all mobile with the ability to take advantage of a newly available habitat. They are normally found in the coarse material of the reef flat and were quick to colonize the coarse sediment deposited in the reef lagoon by the cyclone. However, as this was reworked by callianassids and returned to its former condition they were also quick to respond, either by leaving or dying. In conclusion, cyclone ‘ Winifred ’ had little long-term effect on the surface sediments and sediment communities of reef lagoons in its path. This was due to the sheltering effect of the reef front largely preventing major sediment disturbance and to the sediment reworking activity of callianassid shrimp which quickly returned disturbed sediments to their pre-cyclone condition. The effect of cyclones on the deeper sediment record will depend on their frequency, the amount of material removed, the rate of sedimentation and the depth to which callianassids rework sediment.
Acknowledgements This study was undertaken during a Post Doctoral Research Fellowship at the Australian Institute of Marine Science. Advice from T. Done was invaluable and readily forthcoming throughout. I thank T. Done, C. Wilkinson and A. Dartnall for reading and criticising the manuscript. References Abel, D. J., Williams, W. T. &Williams, D. M. 1985 A fast classificatory algorithm for large problems under the Bray-Curtis measure. Journal of Experimental Marine Biology and Ecology 89,237245. Aller, R. C. & Dodge, R. E. 1974 Animal-sediment relations in a tropical lagoon Discovery Bay, Jamaica. Journal of Marine Research 32,209-232. Belbin, L. 1987 PA TN Pattern Analysis Package Reference Manual. Canberra: CSIRO Division of Wildlife and Rangelands Research. Birtles, A. 1986 Some preliminary observations from a survey of the soft sediment biota of the inner and middle shelf of the Great Barrier Reef following cyclone Winifred. In The Ofshore Effects of Cyclone
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Winifred (Dutton, I. M., ed.). Workshop series No. 7. Townsville: Great Barrier Reef Marine Park Authority, pp. 47-49. Clifford, H. T. & Stephenson, W. 1975 An Introduction to Numerical Classification. New York: Academic Press. Davies, P. J. & Hughes, H. 1983 High-energy reef and terrigenous sedimentation, Boulder Reef, Great Barrier Reef. Bureau of Mineral ResourcesJournal of Australian Geology and Geophysics 8,201-209. Flood, P. G. & Jel, J. S. 1977 The effect of cyclone ‘David ’ (January 1976) on the sediment distribution patterns on Heron Reef, Great Barrier Reef, Australia. Proceedings of third International Coral Reef Symposium 2,120-125. Flood, P. G. & Orme, G. R. 1977 A sedimentation model for platform reefs of the Great Barrier Reef, Australia. Proceedings of third International Coral Reef Symposium 2,11 l-l 16. Folk, R. L. 1974 Petrology of Sedimentary Rocks. Austin, Texas: Hemphills. Frith, C. A. 1983 Some aspects of lagoon sedimentation and circulation at a One Tree Reef, Southern Great Barrier Reef. Bureau of Mineral ResourcesJournal of Australian Geology and Geophysics 8,2 11-221. Kaartvedt, S. 1986 Die1 activity patterns in deep-living cumaceans and amphipods. Marine Ecology Progress Series 30,243-249. Kirby-Smith, W. W. & Ustach, J. 1986 Resistance to hurricane disturbance of an epifaunal community on the continental shelf off North Carolina. Estuarine, Coastal and Shelf Science 23,433-442. Riddle, M. J. 1987 Bioturbation by callianassid shrimp as a determinant of the infauna of coral reef lagoon sediments. In Australian Marine Sciences Association and Australian Physical Oceanography Joint Conference (Marsh, H., Heron, M. L., eds). 1,53. Riddle, M. J. (in press) Patterns in the distribution of sediment communities from coral reefs across the central Great Barrier Reef. Marine Ecology Progress Series. Sandland, R. L. & Young, P. C. 1979a Probablistic tests and stopping rules associated with hierarchical classification techniques. AustralianJournal of Ecology 4,399-406. Sandland, R. L. &Young, P. C. 19793 Tables of Probabilities associated with the fission of replicate samples in classification. CSIRO Australian Division of Fisheries and Oceanography Report, 108. Sandstrom, M. W., Tirendi, F. & Nott, A. 1986 Direct determination of organic carbon in modern reef sediments and calcareous organisms after dissolution of carbonate. Marine Geology 70,321-329. Santos, S. L. & Simon, J. L. 1980 Marine soft-bottom community establishment following annual defaunation: Larval or adult recruitment. Marine Ecology Progress Series 2, 235-241. Suchanek, T. H. 1983 Control of seagrass communities and sediment distribution by Callianassa (Crustacea; Thalassinidea) bioturbationJourna1 of Marine Research 41,281-298. Suchanek, T. H. 1985 Thalassinid shrimp burrows: ecological significance of species-specific architecture. Proceedings of the Fifth International Coral Reef Congress $205-210. T&hope, A. W. 1983 Processes of lagoonal sedimentation and patch reef development, Davies Reef, Great Barrier Reef of Australia. Ph.D. Thesis, University of Edinburgh. T&hope, A. W. & Scoffin, T. P. 1984 The effects of Callianassa bioturbation on the preservation of carbonate grains in Davies Reef lagoon, Great Barrier Reef, Australia. Journal of Sedimentary Petrology 54, 1091-1096. Walker, G. R. & Reardon, R. F. 1986 Wind speeds in the Great Barrier Reef region from cyclone Winifred and their effect on buildings. In The Offshore Effects of Cyclone Winifred (Dutton, I. M., ed.). Workshop Series No. 7, Townsville: Great Barrier Reef Marine Park Authority, pp. 28-40.