Sea Urchin and Fish Bioerosion on La RÃ©Union and Moorea Reefs

BULLETIN OF MARINE SCIENCE, 66(2): 477–485, 2000 CORAL REEF PAPER

SEA URCHIN AND FISH BIOEROSION ON LA RÉUNION AND MOOREA REEFS

M. Peyrot-Clausade, P. Chabanet, C. Conand, M. F. Fontaine, Y. Letourneur and M. Harmelin-Vivien

ABSTRACT Sea urchins and scarid fishes were the most important grazers on the two reefs of La Saline on La Réunion Island (Indian Ocean) and of Tiahura on Moorea Island (French Polynesia). The total erosive activity of grazers reached a similar maximum value of 8 kg −2 −1 CaCO3 m yr on these two high island reefs. The rates of bioerosion by grazers varied considerably among reef habitats and were linked to the main species of bioeroders. The urchin Echinometra mathaei was the only important grazer on La Réunion reef flats, when on Moorea Diadema savignyi and Echinothrix spp. played an important role on bioerosion on the barrier reef flat, and Chlorurus sordidus (scarid fish) and Echinometra mathaei were very active on the fringing reef.

Reef morphology is a function of the balance between active growth of corals and algae and simultaneous erosion of the substrate (Scoffin et al., 1980; Hutchings, 1986). Ero- sional processes principally involve the mechanical action of waves, and bioerosion which is the destruction of substrate by biological agents (Bromley, 1978; Risk and MacGeachy, 1978; Hutchings, 1986). Among the bioeroders, grazers contribute significantly to the production of carbonate sediments (Ogden, 1977). They scrape away the substrate and may expose burrows which may make the substrate more prone to additional boring and physical erosion. Experimental studies have demonstrated that external bioerosion by grazers is higher than internal bioerosion by macroborers, especially during the first year of immersion of test blocks (Kiene and Hutchings, 1994; Peyrot-Clausade et al., 1995). Fish and echinoids constitute the two major groups of grazers in tropical marine environ- ments (Bak, 1994). In some places, like the Great Barrier Reef, fishes from the family Scaridae are the dominant agents of external erosion (Bellwood and Choat, 1990), whereas the intense bioerosion observed in Galapagos Islands and La Réunion is mainly due to sea urchins (Reaka-Kudla et al.,1996; Conand et al., 1998). The present study has been undertaken, as part of a multidisciplinary study, to compare the role of sea urchins and scarid fishes in the particulate carbonate production on two Indo-Pacific high island reefs.

MATERIALS AND METHODS

SITES AND DATA COLLECTION.—Data were collected in October 1994 on La Saline (Trou d’Eau station) fringing reef at La Réunion (Indian Ocean), and on the same date on Tiahura fringing and barrier reefs at Moorea, French Polynesia (Pacific Ocean). La Réunion Island (21°S, 55°E), located 800 km east of Madagascar in the West Indian Ocean, has only fringing reefs, all located on the west coast of the island (Fig. 1). The Trou d’Eau site presents three different geomorphological zones from the open ocean to the coast (Montaggioni and Faure, 1980): (1) the outer reef flat or compact reef flat (site TR1, 100 m from the reef front) is made up of numerous coral colonies and encrusting algae, (2) the inner reef flat (site TR2, 200 m from the reef front) displays wide strips of branched coral colonies alternating with narrow detrital channels perpendicular to the reef front,

477 478 BULLETIN OF MARINE SCIENCE, VOL. 66, NO. 2, 2000

Figure 1. Location of sites and (3) the back reef zone that is mainly biodetrital (site TR3, 450 m from the reef front) and is the deepest part of the reef flat. Moorea island (17°S, 149°W) is a high island in French Polynesia, central Pacific Ocean, that is surrounded by both fringing and barrier reefs (Galzin and Pointier, 1985). Four sites were selected on Tiahura reef from open ocean to the shore. Three sites were located on the barrier reef: one on the compact reef 100 m from the barrier reef front (site B1), one on the reef flat with transverse strips of coral construction 250 m from the reef front (site B2), and one on the reef flat with scattered coral growth (site B3) 450 m from the barrier reef front. On the PEYROT-CLAUSADE ET AL.: SEA URCHIN AND FISH BIOEROSION 479 fringing reef, one site (site F) was located 50 m from the fringing reef front. The numerous studies previously carried out on morphology and community structure on La Réunion (Faure, 1982; Cuet et al., 1988; Letourneur and Chabanet, 1994; Chazottes, 1996) and Moorea (Galzin and Pointier, 1985; Adjeroud, 1997) coral reefs, allowed us to select sites. QUANTIFICATION OF EXTERNAL BIOEROSION.—Sea urchins.—At La Réunion, only Echinometra spp. have been taken into account as the other echinoids involved in bioerosion (Diadema, Stomopneustes, Echinothrix and Echinostrephus) were rare on these reefs. Echinometra spp. is a complex of closely related species, presently described as types A, B, C, D (Nishihira et al., 1991; Palumbi and Metz, 1991). Types B and C were abundant and generally co-occurred on La Réunion reefs, whereas type A only occurred in high energy habitats (Conand et al., 1998) and was not found at the sites studied. Echinometra type D has never been observed on La Réunion reefs. On Tiahura reefs, the sea urchins considered were Echinometra types A and B, Echinothrix diadema and Echinothrix calamaris and Diadema savignyi. Identical methods were used at all sites to evaluate the quantity of calcium carbonate eroded by sea urchins to estimate density and size class distribution of echinoid populations, and quantify the amount of calcium carbonate eroded per day by one individual of each size class. To estimate echinoid population parameters, sea urchin densities and size frequency distribu- tions (test diameter in mm) were determined from counts made during daylight hours in 20 quadrats of 0.25 m−2 at each station. To evaluate the bioeroding activity of Echinometra, 10 individuals per size class were randomly sampled, very early in the morning in order to collect them with filled guts as they feed during the night (Jangoux and Lawrence, 1982; Bak, 1990).The individuals when collected were placed in a plastic bag and then transported to the lab where faeces were collected and added to the gut content. Full gut contents gave an estimation of the minimum calcium carbonate eroded per individual per day, on the assumption that echinoids feed only during the night and their gut are emptied during the day. The test diameter of each individual was measured and after dissection, gut contents were ashed at 450°C for 5 h in a muffle furnace, to remove the organic matter. As the refractory complex organic compounds were not destroyed, CaCO3 was determined by 1N hydrochloric acid digestion of samples, followed by titration of the remaining HCl by so- dium hydroxide. The amount of CaCO3 in the gut content was considered to represent the amount of sustrata removed over 24 h. In the gut content of Echinometra all the CaCO3 ingested came from hard substratum through bioerosion and was not derived from sediment (Bak, 1990). The size frequency distribution and density data were then used to obtain the total echinoid bioerosion, on a daily and yearly basis. Since Conand et al. (1997) indicated no significant difference in rates of daily erosion between the different types of Echinometra, we have pooled the data of the different types for estimating rates of bioerosion for this species. For the E. diadema, E. calamaris and D. savignyi, the mean values given by Bak (1994) were used for each size class. The bioerosion rates of these two species were estimated excluding the CaCO3 belonging to reworked sediments (Bak, 1990). Parrotfishes.—In La Réunion, the density and size frequency distribution of parrotfish populations were determined for each site from four replicates along a permanent 100 m−2 (50 × 2 m) transect parallel to the shoreline. Three size-classes in total length (TL) were previously defined: small (<7 cm TL), medium (7–15 cm TL) and large (>15 cm TL). On Moorea reefs, the density of parrotfishes was estimated on four replicates of 250 m2 (50 × 5 m) transects parallel to the shoreline, at each site and at the same time using the same size-classes. To quantify the bioerosion by scarid fishes, we focused our analyses on the dominant excavating (sensu Bellwood and Choat,1990) species, Chlorurus sordidus. Ten individuals per size class were speared early in the afternoon after feeding and their guts were presumed to be filled, as scarids are typically diurnal feeders, and dissected. To measure the quantity of CaCO3 in the gut contents of parrotfishes, the same procedure used for sea urchins was utilized. As gut turnover was estimated at 10 times per day in the most abundant scarid species, C. sordidus (Polunin et al. 1995), the daily bioerosive activity of an individual of each size class was obtained by multiplying by 10 the quantity of CaCO3 measured in full gut contents. The fact that juvenile scarids ingest a substantial part of reworked sediment (Bellwood, 480 BULLETIN OF MARINE SCIENCE, VOL. 66, NO. 2, 2000

1996; Bruggemann et al., 1996) was not taken into account, as small scarids contributed a negligible proportion to the bioerosion budgets of both reefs. STATISTICAL ANALYSIS.—Mean densities of sea urchins and parrotfishes were tested for difference between sites on each island by one-way ANOVA (fixed model). Multiple comparisons of means were performed by the Student-Newman-Keuls (SNK) t-test at 5% level.

RESULTS

DISTRIBUTION OF GRAZERS.—Sea urchins.—On La Réunion reef flat, the density of sea urchins was significantly higher at the external site (TR1) than at the two other sites (P = 0.0001) (Table 1). Echinometra type B had a significantly different abundance at the three sites (P = 0.0001) with 21.6 ± 4.1 ind m−2 at TR1, 8.4 ± 4.0 ind m−2 at TR2 and 2.0 ± 2.9 ind m−2 at TR3. Echinometra type C was significantly more abundant at TR1 (52.0 ± 22.2 ind m−2) than at TR2 (10.2 ± 6.2 ind m−2) and TR3 (1.8 ± 3.0 ind m−2). The difference between the two types was significant only at the external site TR1 (P = 0.0101). High values of standard deviation were because transects included some sand channels where urchins were absent. On the Moorea reef flat, the density of the sea urchin population decreased from the most external site on the barrier reef B1 (10 ind m−2) to the fringing reef site F (7 ind m−2) (Table 1), but the difference was not significant (P = 0.5412). During the day, Diadema and Echinothrix were clustered under or around coral colonies and absent from sandy areas. At the external barrier site (B1) D. savignyi was the dominant species. At site B2 Echinothrix was significantly more abundant than Diadema (P = 0.017), and less abundant than Echinometra. The mean density of Echinothrix was around 3–5 ind m−2, but ranged from 0 to 15 individuals. On the barrier back reef (B3), the abundance of Echinothrix was significantly higher than the density of the two other species (P = 0.0017). At the fringing reef site (F), only one species, Echinometra mathaei, was abundant with 6.7 ± 6.2 ind m−2. Of the three sea urchin species taken into account on the reef flat in Moorea, D. savignyi had a significantly higher density at B1 (6.2 ± 5.2 ind m−2, P = 0.0001), Echinothrix was significantly dominant (P = 0.0001) on the inner barrier reef (5.1 ± 4.2 ind m−2 at B2 and 4.2 ± 3.5 ind m−2 at B3) and Echinometra was significantly more abundant (6.5 ± 6.2 ind m−2, P = 0.0095) on the fringing reef site. There was no significant difference between the density of the two Echinometra subspecies at the external site on the barrier reef (P = 0.0825), whereas Echinometra type A was significantly more abun-

Table 1. Mean density (ind m−2)édof total sea urchin populations on La R union (Trou d'Eau) an Moorea (Tiahura) reef flats (n: number of quadrats at each site; SD: standard deviation; similar letters indicate non significant difference on the SNK t-test).

Reeef Snit M%ean density + S DSNK-test 5 Léa R u1nio n T0R 287c3.60 ± 23.5 T0R2 221b8.60 ± 10.1 T0R3 233a.80 ± 5.9 M1oorea B0271a0.10 ± 6.6 B02 299a.69 ± 6.9 B03 297a.35 ± 5.0 F0247a.12 ± 6.0 PEYROT-CLAUSADE ET AL.: SEA URCHIN AND FISH BIOEROSION 481

Table 2. Number of species and size parameters of scarid fish populations on La Réuunion (Tro d'Eau) and Moorea (Tiahura) coral reef flats.

Reef Nfumber of Msean size o % per size clas sscarid species slcarid fishe smmal meediu larg (cmTL)

La Rénu3nio 131.8 ± 8. 3424. 550. 5. Moorea 72144.8 ± 8. 268. 400. 31.

dant than Echinometra type B at sites B2 and B3 (P = 0.0315 and P = 0.0030, respec- tively). On the fringing reef only Echinometra type A was collected. Scarid fishes.—On La Réunion island only three scarid fish species were counted: C. sordidus, Scarus psittacus and S. scaber. C. sordidus constituted 79% of the total scarid population. Small individuals (<7 cm TL) represented a high proportion of the scarid population, whereas large individuals were rare (Table 2). This resulted in a low mean size of scarids on this reef. The density of parrotfishes was significantly higher on the inner reef flat (TR2) (P = 0.0098) than at the two other sites (Table 3). On the Moorea reef flat, seven scarid species were censused: C. sordidus, Leptoscarus vaigiensis, Scarus frenatus, S. globiceps, S. oviceps, S. psittacus and S. schlegeli (Table 3). C. sordidus represented 59% of the parrotfish population in Moorea. A one-way ANOVA showed a significant difference (P = 0.0008) in scarid density between sites on this reef flat. SNK tests indicated a higher density on the fringing (site F) than on the barrier reef flat (sites B) (Table 3). Four species were abundant and present at all sites: S. globiceps, S. oviceps, S. schlegeli and C. sordidus, this last species presenting a significantly higher density on the fringing reef (P = 0.0027). Large size individuals (>15cm) represented about one third of the scarid population (Table 2). The density of individuals in each size class did not differ significantly on the fringing reef nor at sites B1 and B2 on the barrier reef, whereas medium size fish were significantly more abundant at site B3 (P = 0.0004). BIOEROSION.—Sea urchins.—On the La Réunion reef flat, the total bioeroson by sea urchins on a yearly basis, which was mainly due to E. mathaei, was maximum at the external site TR1 and significantly lower at the two inner sites (P = 0.0011), particularly at the back reef site TR3 (Table 4). At Moorea, the total erosional activity of sea urchins per year was high on the barrier reef flat and not statistically different between the three barrier sites, whereas it was very low on the fringing reef flat (Table 4). The rate of bioerosion by D. savignyi decreased

Table 3. Mean density (fish 100 m−2)éof scarid fishes on La R union and Moorea reef flats .

Mean density + Reeef Snit SlD SNK-test 5% leve Léa R u1nio n T4R 2a.7 ± 2. 2 T4R2 1b1.0 ± 6. 1 T4R3 0a.8 ± 1. 5 M1oorea B41a5.8 ± 4. 3 B472 174. ±a3. B43 1a2.8 ± 6. 8 F44b1.1 ± 6. 3 482 BULLETIN OF MARINE SCIENCE, VOL. 66, NO. 2, 2000

−2 −1 Table 4. Yearly bioerosion (kg CaCO3 m yr )énby sea urchins and scarid fishes on La R unio (Trou d'Eau) and Moorea (Tiahura) coral reef flats.

Reeef Snit Sea urchins bioerosio Scarid fishes bioerosion −2 −1 −2 −1 kg CaCO3 m yr + SD kg CaCO3 m yr + SD Léa R u1nio n T1R 82.3 ± 2. 0.05 ± 0.0 T5R2 25.8 ±1. 0.12 ± 0.0 T6R3 03.4 ± 0. 0.03 ± 0.0 M1oorea B949.9 ± 3. 00. ±00. 3 B52 77.5 ± 5. 00. ±00. 3 B83 67.1 ± 4. 00. ±00. 6 F103.6 ± 1. 30. ±01. 1

−2 −1 from the external barrier site (4.3 ± 3.6 kg CaCO3 m yr ) to the fringing reef (0.02 ± 1.1 −2 −1 kg CaCO3 m yr ). Echinometra mathaei had a higher grazing activity (P = 0.0014) on −2 −1 the fringing (0.5 ± 0.3 kg CaCO3 m yr ) than on the barrier reef flat (0.1 to 0.2 kg −2 −1 CaCO3 m yr ). The highest rate of bioeroding activity among sea urchins in Moorea −2 −1 was due to Echinothrix at sites B2 (6.4 ± 5.2 kg CaCO3 m yr ) and B3 (4.4 ± 2.9 kg −2 −1 CaCO3 m yr ).

Scarid fishes.—At La Réunion the mean percentage of CaCO3 measured in C. sordidus gut contents was 53%. The annual bioerosion by scarid fishes on the reef flat was very low and did not differ significantly between sites (P = 0.2425) (Table 4).

At Moorea, C. sordidus gut contents comprised 60% of CaCO3. A one-way ANOVA on

the total amount of CaCO3 eroded yearly per square meter by parrotfishes indicated a significant difference between sites (P = 0.0006). Bioerosion due to fishes was higher on the fringing reef than on the barrier reef, where no difference existed between the three sites (Table 4). At all sites, the main erosion was due to the large size class (P = 0.001). The total bioerosion due to the activity of sea urchins and fishes was maximum at the −2 −1 external site TR1 in La Réunion (8.4 kg CaCO3 m yr ) and lower in the back reef area −2 −1 at site TR3 (0.4 kg CaCO3 m yr ). At Moorea, the total bioerosion due to grazers was −2 −1 higher in the middle of the barrier reef flat at site B2 (8.2 kg CaCO3 m yr ) and lower on −2 −1 the fringing reef (3.9 kg CaCO3 m yr ). COMPARISON BETWEEN REEFS.—The species diversity of grazers, sea urchins and parrotfishes, differed greatly between the two reefs studied. Four species of echinoids and seven scarid species were recorded in Moorea, and only one actively grazing sea urchin species plus three scarid fish species in La Réunion. On each reef, the density of sea urchins varied from site to site, with the highest density recorded at the most external site and the lowest at the innermost site. The maximum density of sea urchins at La Réunion was seven times higher than the maximum density present at Moorea (P = 0.0001). In contrast, the mean density of scarid fishes was higher on Moorea reef flats (21.1 ± 14.4 fish 100 m−2) than on La Réunion reef flat (6.4 ± 4.8 fish 100 m−2). The size structure of the scarid population also differed with a higher percentage of large individuals at Moorea resulting in a larger mean size of fish on this reef (Table 2). Sea urchins were the main agent of grazing at all sites studied on La Réunion reef flat, where they accounted for 93 to 99% of the total external bioerosion, and on the barrier reef flat at Moorea (85 to 91% of grazing). The most active sea urchin species were E. mathaei at La Réunion (8.3 kg −2 −1 CaCO3 m yr ), and D. savignyi and Echinothrix on the barrier reef flat at Moorea (re- −2 −1 −2 −1 spectively 4.3 ± 3.6 kg C CaCO3 m yr at B1 and 6.4 ± 5.2 kg CaCO3 m yr at B2). PEYROT-CLAUSADE ET AL.: SEA URCHIN AND FISH BIOEROSION 483

Parrotfishes played a significant part in grazing only on Moorea fringing reef flat, where they accounted for 85% of the external bioerosion at site F.

DISCUSSION

Grazers like sea urchins and scarid fishes are recognized as keystone species in the functioning of coral reefs in both controlling algal communities and bioeroding dead coral substrata (Done et al., 1996). Nevertheless, the action of grazers in the regulation of the coral reef growth depends on their diversity and abundance. This study has demon-

strated that the total erosive activity of grazers is similar on both islands at 8 kg CaCO3 m−2 yr−1 maximum. The rates of bioerosion by grazers varied considerably among reef habitats, with higher erosion on the outer reef flat at La Réunion and on the barrier reef flat with transverse stripes at Moorea. Grazing was due to different species when consid- ering both islands and sites. E. mathaei was the only important grazer on La Réunion reef flats. At Moorea, the main grazers were the sea urchins D. savignyi and Echinothrix spp. on the barrier reef flat, and the parrotfish C. sordidus on the fringing reef. On both reefs, the most active parrotfish involved in bioerosion is the excavating species C. sordidus. The other scarid species recorded on these reef flats belonged to the scrappers which had a lower importance in bioerosion (Bellwood and Choat 1990, Bellwood 1996, Bruggemann et al. 1996). The impact of scarids as bioeroders is mainly related to the individual size of fishes within and between species. The negligible role of parrotfishes in carbonate budget on La Réunion reef flats was related to the low density and small size of fishes. Bellwood (1995) related the higher annual erosion rate of C. gibbus at Lizard Island compared to C. sordidus, to its much larger size. Thus, fishes are important bioeroding agents only on reefs where fishing remains low or is prohibited. Peyrot-Clausade et al. (1995) and Pari et al. (1998 ) indicated a high rate of bioerosion −2 −1 by E. mathaei (6.9 ± 2.2 kg CaCO3 m yr ) in French Polynesia at Faaa (Tahiti), a very degraded reef where no scarids were observed. In the lagoon of Tikehau atoll (Pari, 1998) where scarid fishes were abundant and sea urchins absent from pinnacles, the external −2 −1 erosion due entirely to fish grazing reaches 9.1 ± 6.6 kg CaCO3 m yr . In Lizard Island, Great Barrier Reef, where the density of bioeroding echinoids was very low (Sammarco, 1985) and scarid fishes abundant (Kiene and Hutchings, 1994), the external erosion re- −2 −1 sulting of grazer activity reached 2 kg CaCO3 m yr . Thus, it appears that on highly degraded reefs like Faaa reef in Tahiti, or overfished like La Saline reef in La Réunion and Diani reef in Kenya (McClanahan and Muthiga, 1988), E. mathaei is the most active bioeroder. On reefs with low fishing pressure, like Tiahura in Moorea, various echinoids and fish grazer species are active bioeroders. On reefs where fishing is very low or forbidden as at Lizard island (Kiene and Hutchings, 1994) and Bonaire, in the Caribbean (Bruggemann, 1994) scarids are the most active eroders. If sea urchins and scarid fishes may be broadly viewed as redondant species in bioerosion, their respective roles are not totally equivalent. −2 −1 Rates of bioerosion by parrotfishes stay at a medium level (2 to 7 kg CaCO3 m yr , −2 −1 Bruggemann, 1994, 2 to 9kg CaCO3 m yr , Pari, 1998), even on reefs where their density and size are high, whereas on degraded reefs rates of bioerosion by echinoids can −2 −1 exceed 22 kg CaCO3 m yr (Glynn, 1988; Reaka-Kudla et al., 1996), producing a seri- ous decline in carbonate budget on these reefs. 484 BULLETIN OF MARINE SCIENCE, VOL. 66, NO. 2, 2000

ACKNOWLEDGMENTS

This work was funded by the French National Programme on Coral Reef (PNRCO-INSU). The experiments comply with the current laws of the country in which the experiments were performed.

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DATE SUBMITTED: September 28, 1999. DATE ACCEPTED: December 2, 1999.

ADDRESSES: (M.P.-C.) Université de la Méditerranée, Centre d’ Océanologie de Marseille, CNRS UMR 6540, Station Marine d’ Endoume, 13007 Marseille, France, and Centre de Recherches Insulaires et Observatoire de l’Environnement, B.P. 1013 Moorea, French Polynesia. (P.C.) Université de La Réunion, Laboratoire d’ Ecologie marine, 15 Avenue René Cassin, 97715 Saint-Denis Cedex 9, La Réunion. (C.C.) Université de La Réunion, Laboratoire d’ Ecologie marine, 15 Avenue René Cassin, 97715 Saint-Denis Cedex 9, La Réunion. (M.F.F.). Université de la Méditerranée, Centre d’ Océanologie de Marseille, CNRS UMR 6540, Station Marine d’ Endoume, 13007 Marseille, France. (Y.L.) Université de la Méditerranée, Centre d’ Océanologie de Marseille, CNRS UMR 6540, Station Marine d’ Endoume, 13007 Marseille, France, and Université de La Réunion, Laboratoire d’ Ecologie marine, 15 Avenue René Cassin, 97715 Saint-Denis Cedex 9, La Réunion. (M.H.-V.) Université de la Méditerranée, Centre d’ Océanologie de Marseille, CNRS UMR 6540, Station Marine d’ Endoume, 13007 Marseille, France, and Centre de Recherches Insulaires et Observatoire de l’Environnement, B.P. 1013 Moorea, French Polynesia.