252 (2000) 1–14
www.elsevier.nl / locate / jembe
Spatial differences and seasonal changes of net carbonate
accumulation on some coral reefs of the Ryukyu Islands,
Japan
* K. Hibino, R. van Woesik
Department of Marine Sciences, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213,
Japan
Received 9 September 1999; received in revised form 6 April 2000; accepted 20 April 2000
Abstract
This study sought to understand short-term spatial changes in accretion and erosion on (experimental) carbonate blocks on three coral reefs of the Ryukyu Islands, Japan. The principal objectives were to differentiate net accretion / erosion according to season, location, depth and substrate-type. At all locations the summer season showed more positive net weight changes and higher coralline algal coverage than the winter season. Windward reefs revealed higher net accretion and higher coralline algal coverage than leeward reefs. Massive (Holocene) Porites blocks showed highest net loss, followed by Pleistocene carbonate and (Holocene) Acropora blocks. High population densities of Echinometra mathaei (de Blainville) were recorded on reefs adjacent to large human populations and overall net carbonate loss significantly correlated to densities of E. mathaei type A. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Coral reefs; Bioaccretion; Bioerosion; Carbonate; Echinometra mathaei; Coralline algae
1. Introduction
Coral reefs are a culmination of contemporary processes that have produced net carbonate accretion on ancient foundations throughout the Holocene (Adey, 1978; Hopley, 1982; Davies, 1983). Net reef growth is a product of accretional, sedi-mentological and erosional processes. Accretion may be biological, through the growth
*Corresponding author. Fax:181-98-895-8552.
E-mail address: [email protected] (R. van Woesik).
of framework building corals and other calcareous organisms, or physical or microbial through mineralisation of existing framework, or geological through sediment accumula-tion and in-filling (Smith and Kinsey, 1976; Glynn, 1997). Reefs may erode because of the activity of urchins (Bak, 1990, 1994; Mokady et al., 1996), herbivorous fishes (Bellwood, 1995), endolithic sponges, bivalve molluscs, and polychaetes (Davies and Hutchings, 1983; Hutchings, 1986; Scoffin, 1992; Glynn, 1997). Erosion of carbonate can also occur through physico-chemical processes, either by physical abrasion by waves or suspended sediment (Ball et al., 1967), or by geochemical shifts, when the addition of carbon dioxide causes an acid shift in the water chemistry, enhancing calcium carbonate dissolution (Gattuso et al., 1998; Kleypas et al., 1999).
Grigg (1982) and Grigg and Epp (1989) reported a threshold for coral reef growth, which they termed ‘the Darwin Point’. At this threshold net reef production is at equilibrium with tectonic subsidence, and production below this threshold invokes ‘reef drowning’, where reef growth is unable to keep pace with apparent sea level. Grigg (1982) suggested that this threshold exists at latitude 298N at the northern end of the Hawaiian Archipelago. Along similar lines, Done et al. (1996) argued that human impacts might reduce net reef production beyond a threshold, where erosion exceeds production. With a caveat that reef growth is dependent on sea surface temperatures, ‘healthy’ reefs may be viewed as those inclined to net accretion, whereas ‘unhealthy’ reefs tend more toward net erosion.
2. Materials and methods
2.1. Study location
The Ryukyu Islands are an island chain that extend from 308N–1308E to 248N–1238E in southern Japan (Fig. 1). The warm Kuroshio Current largely influences sea surface temperatures. The average sea surface temperature in Okinawa (latitude 268N) in summer is 30 and 198C in winter (data from the Tropical Biosphere Research Center, Sesoko Island, University of the Ryukyus), allowing the proliferation of reef corals (Nishihira and Veron, 1995) and coral reefs (Kan et al., 1995). Although reefs in the northern Ryukyu Islands are typical high latitude reefs, with little carbonate develop-ment, reef development in Okinawa is extensive.
2.2. Experimental design
Three locations on four islands were examined for differences in net carbonate change: (1) Ikei and Miyagi Islands, located on Okinawa’s east coast; (2) Sesoko Island, on Okinawa’s west coast; and (3) Aka Island, 35 km off Okinawa’s south-west coast. There were two study sites at each location, one windward and the other leeward (Fig. 1). At each site two stations were selected approximately 20–30 m apart. Each station included two depths (1 and 5 m below low water datum).
2.3. Laboratory and field techniques
Carbonate tiles were cut from recently dead massive Porites spp. colonies collected from the east coast of Ikei and Miyagi Islands. Samples were cut into hexahedral cubes, 4–6 cm wide and 1 cm thick, using a diamond cutter. Each corner on the upper surface of each tile was filed to 458, taking 3 mm off all sides, in order to avoid any unnaturally acute angles. Any prepared tiles with signs of bore holes or cracks were discarded. The direction of the coral polyps in the skeleton was arbitrary. After cutting the tiles, sequential numbers were scribed into their bases with an electric drill. Tiles were soaked in distilled water and cleaned with an ultrasonic cleaner for 30 min. Tiles were then dried for 24 h at 508C in an oven and subsequently weighed to the nearest milligram. The exposed surface area (excluding the base) was measured on each tile to the nearest millimeter. To prevent bioerosion from underneath, the base of each tile was covered with silicon before field placement.
At each depth, 10 carbonate tiles were attached to the reef substrate using under water cement (brand name Ronji-patte). Field attachment involved: (1) selecting a flat exposed carbonate substrate, away from Stegastes spp. (damselfish) territories, at a gradient of less than 308to the horizontal; (2) cleaning the substrate with a wire brush to remove sediment and algae; (3) applying under water cement to the tile base; and (4) pressing the base firmly against the cleaned substrate. This process was repeated for each tile. Tiles were set at ,1 m apart.
cement and silicon, tiles were bleached with household bleach, and remnant algal filaments were removed with a soft nylon brush (to prevent the dislodgment of encrusting organisms). The tiles were then soaked, dried and weighed as above. Weight change was standardised and presented as milligrams per square centimeter of original
22
surface area, per 3 months of exposure (mg cm 3 months) (note, we extrapolated and pooled the data over the seasons only when we compared our data with the published
22 21
literature, expressed as kg m year in Table 3). This process was undertaken once in summer 1996 (July–October) and once in winter 1996 / 97 (October–January). In total 480 Porites tiles were placed in the field, of which 64% were recovered. Losses were mostly due to a typhoon overpass in summer.
To assess the effect of substrate type, recently dead Acropora hyacinthus plates were collected from approximately a 1-m depth along the west coast of Okinawa. Tiles were cut from the center of the plate where branch density was highest. In addition, Pleistocene tiles were prepared from a cutting taken from a quarry at Minatogama, Gushikami village, Okinawa. X-ray diffraction tests of the tiles from the quarry showed high calcite and almost no sign of aragonite, whereas, as expected, the recently dead corals were all aragonite. Prepared tiles were placed in the lee of Ikei Island over the 1996 / 97-winter season, following the protocol above.
The mean density of each tile-type was determined by cutting off a cube of
3
approximately 1 cm from each tile. Ten cubes were randomly selected from each tile type. All sides were measured to the nearest 0.1 mm, and their dry weight measured as above. Density was calculated using the formulae D5M /V, where D is the density, M is the mass (or dry weight) and V is the volume. The density of massive Porites spp. was
23 23
1.3560.03 g cm , A. hyacinthus 1.9760.04 g cm and Pleistocene substrate
23
2.4260.11 g cm .
The percentage cover of encrusting calcareous organisms was measured on each tile
2
using the point intercept method. A transparent plastic sheet, etched with 5-mm grids, was placed over the top and sides of each tile. Each organism was categorized as either coralline algae or ‘others’; the latter included mainly bryozoans and serpulid poly-chaetes.
2.4. Urchin densities
The density of echinoids was determined at each site during the 1996 summer season. The abundance of E. mathaei (de Blainville) type A was distinguished from E. mathaei types B, C and D (Uehara and Shingaki, 1985; Arakaki et al., 1998) because the former was most likely to graze on the tiles since they are most mobile, and E. mathaei types B, C and D are quite sedentary (Nishihira et al., 1991). Echinoid density was estimated
2
using 10 randomly placed 1-m quadrats at each depth; observations were conducted during daylight hours.
2.5. Data analysis
test, respectively. These tests were undertaken on four primary variables: (1) net weight change of carbonate tiles; (2) E. mathaei densities; (3) calcareous encrustation cover; and (4) substrate type. With the exception of net weight change, the results of the a priori tests revealed that transformations were necessary. A one-way analysis of variance (ANOVA) was undertaken on net weight change first testing for significant seasonal differences (note that a four-way ANOVA was not possible, testing season, location, windward / leeward and depth, because the summer typhoon dislodged numerous tiles). There was a significant seasonal difference. Therefore, to avoid inappropriate pooling each successive factor was analysed for each season separately and each variable required a Ln transformation. Both E. mathaei densities and substrate types failed a priori tests and subsequent transformation attempts, therefore the non-parametric Kruskal–Wallis one-way ANOVA was used to test the hypotheses that there were no significant differences in (1) E. mathaei densities among locations, between windward and leeward reefs and between depths, and (2) percentage net weight change according to substrate type. Least-squares regression analyses were undertaken to examine whether there was a functional relationship between net weight carbonate change (in the summer season) and the density of E. mathaei type A. An arcsin(sqrt(x)) transformation was applied to the percentage cover of calcareous organisms on the tiles and each factor was subsequently tested via one-way ANOVA separately and pooled only when significant differences were not apparent.
3. Results
3.1. Net weight carbonate changes
A total of 45% of the tiles remained attached in summer, and 83% in winter. Among the 307 tiles collected, only two tiles were found to have extensive boreholes. The weight of Porites carbonate tiles increased at all sites except at Location 1 (1 m). Net weight carbonate change was significantly different between seasons (P,0.001) (Table 1). Significant differences were also apparent between locations in both seasons (P50.005, P,0.001 for summer and winter, respectively) (Fig. 2a) and windward and leeward sites in the winter season (P50.012) (Fig. 2b), but not between windward and leeward sites in summer (P50.522) and between depths (P50.071, P50.074 for summer and winter, respectively). More positive net weight changes were found in the summer season than in the winter season for all locations, for windward and leeward reefs at both depths. Location 1 showed generally lower net increases than other localities, and Location 2 showed higher net increases than other localities.
Table 1
One-way analysis of variance (ANOVA) for net weight carbonate change according to season
Effect df MS F P
Season 1 916.3 13.0 ,0.001
Fig. 2. Mean net weight change of experimental massive Porites spp. tiles (a) between different seasons and locations and (b) between different seasons and windward and leeward reefs. Data are mean6S.E. Treatment results with the same letter above the error bar are not significantly different (a 50.05) based on one-way
ANOVA tests.
3.2. Echinometra mathaei densities
The number of E. mathaei type A exceeded the combined number of types B, C, and D at all localities except at 1 m on the windward side of Location 2 (Table 2). The density of E. mathaei type A was significantly different between locations (H 587.1,
2,240 P,0.001), windward and leeward reefs (H 54.8, P50.028) and depths (H 5
1,240 1,240
19.3, P,0.001). Location 3 had significantly less E. mathaei type A than other locations. Leeward reefs on average supported a higher density of E. mathaei type A than windward reefs, and the 1-m habitat supported significantly more E. mathaei type A than the 5-m habitat. There was a significant negative relationship between the density of E. mathaei type A and net weight carbonate change of the tiles in the summer season
2
Table 2
Mean Echinometra mathaei densities and percentage hard coral cover in replicate quadrats (n520) 2
Echinometra mathaei density (m ) Hard coral cover (%) Type A Other types
mean (6S.E.)
mean (6S.E.) mean (6S.E.)
Location 1 Windward 1 m 29.0 (62.5) 0.1 (60.1) 4.1 (61.6)
(Site 1) 5 m 2.5 (60.5) 0.9 (60.4) 8.8 (61.8)
Leeward 1 m 22.3 (62.8) 0.6 (60.2) 1.3 (60.7)
(Site 2) 5 m 12.3 (62.1) 0.0 1.3 (60.6)
Location 2 Windward 1 m 4.2 (61.2) 9.4 (61.4) 22.8 (62.4) (Site 1) 5 m 8.3 (60.9) 0.0 28.1 (63.4) Leeward 1 m 15.4 (62.0) 0.1 (60.1) 19.1 (62.9) (Site 2) 5 m 5.3 (60.9) 0.0 26.9 (63.7) Location 3 Windward 1 m 4.8 (62.1) 0.4 (60.2) 31.9 (66.7)
(Site 1) 5 m 0.1 (60.1) 0.0 71.9 (64.4)
Leeward 1 m 1.8 (60.4) 0.7 (60.2) 47.8 (65.2)
(Site 2) 5 m 0.9 (60.2) 0.0 22.5 (63.3)
(representing station 2 of the 1-m habitat, leeward, Location 2; marked with an arrow in
2
Fig. 3) was removed (R 50.39, P50.003, n520).
3.3. Accretion
Coralline algal cover on massive Porites spp. tiles exceeded other calcareous
Fig. 3. Simple linear regression of Echinometra mathaei type A density and net weight change on experimental massive Porites spp. tiles during the 1996 summer season. One circle represents 10 replicate quadrat samples of E. mathaei and replicate tiles at each depth per station (n521). The dashed lines show the 95% confidence limits for the regression line; the arrow points to an outlier, which when removed changed the
2 2 2
encrusters in percentage space occupation (mean values; 13.7 and 0.8% for coralline algae and other encrusters, respectively). Coralline algal cover also varied significantly between seasons (P50.013), among locations (P50.032 and P,0.001 for summer and winter, respectively) (Fig. 4a), and between windward and leeward reefs (P50.001 and
P,0.001 for summer and winter, respectively) (Fig. 4b), but did not significantly differ between depths (P50.141 and P5137 for summer and winter, respectively). The summer months had higher coralline algal cover (15.7%) than winter months (12.6%). Highest coralline algal cover occurred at Location 3 (Fig. 4a). Windward reefs, on average, revealed a higher coverage than leeward reefs (Fig. 4b). Coralline algal cover
2
was not significantly correlated with net weight carbonate change (R 50.09, P50.155,
n524).
3.4. Substrate type
Experiments undertaken in the lee of Location 1 showed that all three substrates, Holocene Porites, Holocene A. hyacinthus, and Pleistocene, decreased in weight except for Porites tiles at 5 m. The percentage of net weight change varied significantly among substrate types (H 510.0, P50.007). A. hyacinthus was more resistant to net weight
2, 93
loss than either massive Porites or Pleistocene carbonate (Fig. 5a). The amount of coralline algae encrusting the different substrates also differed significantly (H 5
2, 93
13.2, P50.001). Porites tiles showed generally lower coralline algal accumulation than
Acropora and Pleistocene tiles, especially at 1 m (Fig. 5b), which was coincident with
high net weight loss (Fig. 5a,b).
4. Discussion
We rejected our hypotheses that there were no significant spatial differences and seasonal changes to pre-weighed carbonate tiles when placed on reefs at various localities. Changes were mostly due to accretion by calcareous encrusters or erosion by external grazers in the 3 months of exposure. Bioerosion estimates would undoubtedly increase over time (Hutchings, 1986; Kiene and Hutchings, 1994), however, distinct bore holes were only found in two tiles, suggesting that erosion estimates in this study were almost exclusively external.
Among the Holocene carbonate, massive Porites spp. tiles showed a higher per-centage of net weight loss than A. hyacinthus tiles (recalling that the density of massive
23 23
Porites spp. was 1.3560.03 g cm , A. hyacinthus 1.9760.04 g cm and Pleistocene
23
substrate 2.4260.11 g cm ). An unexpected outcome showed Pleistocene carbonate, with the highest mean density, lost more carbonate on average than the Acropora tiles. This may be because Pleistocene carbonate was heavily mineralised, filling the otherwise porous matrix. A lack of porosity may have allowed the Pleistocene carbonate to chip easily upon physical forcing, while the Holocene tiles maintained a more porous and flexible nature. Also, in-filling material may be subjected to greater erosion than coral skeleton. The amount of coralline algae that accumulated on the tiles also varied in accordance with substrate type. A higher percentage of coralline algal cover occurred on the hard Acropora and Pleistocene tiles than on the soft massive Porites tiles, possibly because of more active grazing on the softer Porites. These results indicate that reef erosion rates vary in accordance with not only the community that currently inhabits the reef but also with the age of substrata.
The density of E. mathaei type A was significantly negatively correlated with net weight carbonate gain. On Okinawan reefs, especially around Okinawa Island, E.
mathaei occurs at high densities (Tsuchiya and Nishihira, 1984). Some depths revealed 2
mean E. mathaei density of more than 29 individuals per m (Table 2). This number is even higher than reported elsewhere where E. mathaei was shown to cause major reef erosion, but lower than the high densities reported for other eroding echinoids (Russo, 1980; Bak, 1990; McClanahan and Shafir, 1990; Mokady et al., 1996). Some workers have speculated that high urchin numbers are a consequence of fish removal (McClanahan, 1988; McClanahan and Muthiga, 1989; McClanahan and Shafir, 1990; Hughes, 1994) or because of sudden environmental changes (Eakin, 1992, 1996).
Translating our data to an annual net carbonate change shows that Location 1 was
22 22 21
inclined to net erosion at a rate of23.8310 kg m year , while Locations 2 and 3
21 21 22 21
Table 3
Comparative rates of mean net carbonate change using experimental Porites tiles and urchin densities from a
different reefs
Locality Mean net Average density of Major eroding Exposure References 2
carbonate change urchins per m urchin time 2
(kg CaCO / m / year)3
Okinawa 0.2 (20.7 to 0.7) 10 (0–29) Echinometra mathaei 3 months32 This study
French Polynesia 21.6 (210.5 to 0.5) 5 (0–31) Echinometra mathaei 6 months Peyrot-Clausade et al., 1995 b
Galapagos 24.160.2 32 (13–62) Eucidaris thouarsii 14.8 months Reaka-Kudla et al., 1996 GBR 20.9 (22.0 to20.1) – – 2, 2.5, 5 years Kiene and Hutchings, 1994
b
Panama 214.0 to26.3 Approx. 50 Diadema mexicanum 3 months to 1 year Eakin, 1992
a
Values in parentheses show the range. b
˜ Rates measured after 1982–1983 El Nino event.
carbonate change, we speculate that Location 1 tended to be largely erosional, Location 3 accretional, and Location 2 was at equilibrium. Okinawa and adjacent islands (Locations 1 and 2) support a population of 1.3 million people, whereas Aka Island (Location 3) supports a local human population of about 250; this suggests that human activities may also influence net reef growth in the Ryukyu Islands. [RW]
Acknowledgements
This study was part of a thesis conducted at the Department of Marine Sciences, University of the Ryukyus, Okinawa, Japan. We thank Akajima Marine Science Laboratory (AMSL) and the Tropical Biosphere Research Center (TBRC) for providing study sites and invaluable time and equipment for the study. We also thank Sandra van Woesik for editorial comments.
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