Feeding Ecology of Four Species of Sea Urchins (Genus <I>Echinometra</I

BULLETIN OF MARINE SCIENCE, 81(1): 85–100, 2007

Feeding Ecology of Four Species of Sea Urchins (Genus Echinometra) in Okinawa

Yuji Hiratsuka and Tsuyoshi Uehara

Abstract We studied the feeding ecology of four Echinometra species at five different sites in Okinawa in terms of distribution, food availability, and gut contents. Echinome- tra sp. A was widely distributed from the lower intertidal to submerged areas, while Echinometra mathaei (Blainville, 1825) was common in the upper subtidal and lower intertidal areas. Echinometra sp. C and Echinometra oblonga (Blainville, 1825) were restricted to the upper intertidal zone. Although the diets of Echinometra spp. showed remarkable differences among sites and between seasons, 39.2%–80.7% of their gut contents usually consisted of plant material. Echinometra sp. A ingested a greater variety of plants than the other three species. The availability of major plants in the field was generally proportional to their abundance in the gut, except when Echinometra relied on imported drift plants or when feeding was restricted because of severe hydrodynamics. Benthic grazing was the primary feeding mode of Echinometra living on rock platforms, while drift feeding was pronounced when macrophytes were abundant in the habitat or surroundings. Our results suggest that despite differences in physical and nutritional environments among their micro- habitats, the four urchin species have essentially similar feeding types, modes, and preferences.

The sea urchinEchinometra mathaei (Blainville, 1825) is reported to be widely distributed throughout the tropical to warm Indo-Pacific regions and shows extensive morphological variation in test shape and spine color (Mortensen, 1943). Tsuchiya and Nishihira (1984, 1985) divided E. mathaei at Okinawa into two types—type A and type B, based on the differences in distribution pattern, habitat, and agonistic behavior. Uehara and Shingaki (1984) demonstrated that these two types would not cross-fertilize and differed in larval morphology and karyotype. Uehara and Shin- gaki (1985) and Uehara et al. (1986, 1990) discovered two additional types—type C and type D—from studies of chromosomes, spicule characteristics, and gamete incompatibility. Biochemical studies of enzyme electrophoresis (Matsuoka and Hat- anaka, 1991), mitochondrial DNA (Palumbi and Metz, 1991), and the binding of gamete recognition proteins (Metz and Palumbi, 1996) suggest that these four types are distinct but very closely related species. Currently, type B is regarded as Echinometra mathaei (Arakaki et al., 1998), while type D is recognized as Echinometra oblonga (Blainville, 1825), which may be a cryptic species composed of at least three species (Arakaki and Uehara, 1999). It is likely that both type A and type C are new species (Arakaki et al., 1998), but because they have not been described and named, types A and C are herein referred as Echinometra sp. A and Echinometra sp. C, respectively. Recent studies of the taxonomy, ecology, and molecular biogeography of sea urchins have referred to the occurrence of these four species of Echinometra from various lo- cations in Indo-West Pacific P( alumbi, 1996; Uehara et al., 1996; Arakaki and Kusen, 2000; Peyrot-Clausade et al., 2000; Paulay, 2003; Appana et al., 2004). Feeding ecology of E. mathaei in various regions of the Indo-West Pacific has been examined through gut content analysis or direct observation (Mortensen, 1943; Khamala, 1971; Herring, 1972; Black et al., 1984; McClanahan, 1988; Coppard and

Campbell, 2005). These studies have concluded that E. mathaei is a generalist her- bivore, utilizing a variety of vegetal diets by grazing on the substrate or by captur- ing drift materials. However, it should be recognized that some of these studies of E. mathaei may include Echinometra sp. A and/or Echinometra sp. C. Hawaiian E. mathaei and E. oblonga, probably a different species from theE. oblonga of Okinawa (Arakaki and Uehara, 1999), have been the subject of numerous ecological studies that have suggested that Hawaiian populations of the two species mainly subsist on drift materials washed into their burrows (Kelso, 1970; Russo, 1977; Ogden et al., 1989; Hart and Chia, 1990). Unfortunately, very few studies have documented the feeding habits of Echinometra sp. A and sp. C. Much more is known about the feeding strategy of Echinometra lucunter (Linnaeus, 1758), a congeneric species distributed from Florida and Bermuda through the Caribbean and the Gulf of Mexico to Dester- ro, Brazil (Mortensen, 1943; Stevenson and Ufret, 1966; McLean, 1967; McPherson, 1969; Abbott et al., 1974). For example, Abbott et al. (1974) thoroughly documented its feeding behavior, and provided evidence that both drift plants and attached algae were its major foods. Elsewhere, brief reference has been made to the diets of Echi- nometra vanbrunti A. Agassiz, 1863, occurring mainly from central California to Zorritos on the coast of Peru (Mortensen, 1943), and Echinometra viridis A. Agassiz, 1863 confined to south Florida and the West Indies (Mortensen, 1943; McPherson, 1969; McClanahan, 1999). To understand the feeding ecology of the species of Echinometra in Indo-Pacific region, our study focused on the distribution, food availability, and gut contents of the four species at five different sites on Okinawan coral reefs.

Materials and Methods

Study Sites.Field studies were conducted from August 2003 to March 2004 at five different sites (Usahama, Bise, Onna, Yonashiro, and Ikei) located on the coral reefs at Okinawa Island (Fig. 1): Usahama is located at the northernmost part of Okinawa Island, and consists of a narrow fringing reef approximately 1 km long and 150–200 m wide. The moat is a submerged habitat 0.3–1.5 m in depth. The reef margin is affected by both strong wave action at high tide and exposure at low tide. Two study areas were established (1) in the moat to study Echinometra sp. A and E. mathaei, and (2) at the reef margin to study the other two species (Fig. 2A). Bise is on the northwest coast of the Motobu Peninsula in the northern part of Okinawa Island and consists of a well-developed fringing reef. A seagrass bed of about 1 km long and 100–200 m wide occurs on the landward side of the reef flat. The study area lies at the northern part of the seagrass bed, where the depth ranges from 0.5 m at low tide to 2 m at high tide. The bottom of the study area is composed primarily of coral rubble, which is covered by dense stands of seagrass, Thalassia hemprichii(Ehrenberg, 1832), branching corals, and a variety of macroalgae throughout the year (Fig. 2B). Onna is situated on a narrow fringing reef, 1 km in length and 100–300 m in width, on the west coast of the central part of Okinawa Island. A study area was established on the intertidal wave-cut platform near the overhanging cliff (Fig. 2C). The platform, having an area of approximately 250 m2, is subjected to complete exposure during spring tides and intense wave action during high tides. Yonashiro, on the northwest coast of the Katsuren Peninsula of Okinawa Island, has a shallow reef slope extending for several kilometers. The shallow reef bottom consists of a complex of seagrasses and macroalgae interspersed with small round sandy flats (10–20 m in diameter) HIRATSUKA AND UEHARA: FEEDING ECOLOGY OF ECHINOMETRA IN OKINAWA 87

Figure 1. Location of the five study sites at Okinawa Island. lacking vegetation (Fig. 2D). A study area was established within one of the sandy flats (about 300 m2 in area). Ikei, one of the neighboring islands located off the east coast of the Katsuren Peninsula, is surrounded by a 400–600 m wide fringing reef. A study area was set up in the subtidal region near the shore on the south coast of Ikei (Fig. 2E). Distribution of Sea Urchins.The distribution of Echinometra spp. was investigated by measuring the density of sea urchins at each site (except Ikei) during August and Septem- ber 2003. At Ikei, measurements were made in February 2004 because of difficulty in finding urchins in summer 2003 when the bottom was almost entirely covered by dense Sargassum spp. The density of urchins was measured at each site by counting all specimens > 1 cm in test diameter that occurred along ten 10 × 1 m belt transects laid parallel to the shore at intervals of 1.0–1.5 m. Food Availability.Food availability (benthic cover) for Echinometra spp. in the field was investigated at each site in August and September 2003 (summer) and in February and March 2004 (winter). The percent cover of various components was visually estimated from 50 × 50 cm quadrats placed at four evenly spaced points along each of ten 10 × 1 m belt transects deployed for the measurement of urchin density (i.e., 40 quadrats per site). The points where the quadrats were laid in the summer investigation were permanently marked with nails driven into the bedrock, and were surveyed again in the winter. Benthic composition was categorized into the following groups: seagrasses, macroalgae (> 2 cm in height), turf algae (< 2 cm in height; the algal community covering hard substrates, comprising various species of blue-green algae and microscopic algae such as Cladophora, Ec- tocarpus, Sphacelaria, Ceramium, Centroceras, Taenioma, Herposiphonia, and Polysiphonia), encrusting coralline algae, live coral, dead bleached coral, Porifera, Foraminifera, Ascidia, 88 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 1, 2007

Figure 2. Profiles of the study sites showing substrates, vegetation, and distribution patterns of Echinometra (°: Echinometra sp. A; l: E. mathaei; r: Echinometra sp. C; p: E. oblonga). Rectangles represent the study areas.

Hydrozoa, bedrock (a bare surface, including the eroded wall of Echinometra burrows), boulders (> 250 mm diameter), rubble (1–250 mm), and sand (< 1 mm). Gut Content Analysis.To identify the diets of Echinometra in the field, 10 adults of each species were collected from each site in August and September 2003 (summer) and in February and March 2004 (winter). Echinometra sp. A was collected from the five sites, E. mathaei was sampled at three sites (Usahama, Onna, and Ikei), and Echinometra sp. C and E. oblonga were collected from two sites (Usahama and Onna). Mean (± SD) test lengths were Echinometra sp. A: 4.05 ± 0.87 cm (n = 100), E. mathaei: 4.35 ± 0.55 cm (n = 60), Echinometra sp. C: 3.48 ± 0.39 cm (n = 40), and E. oblonga: 3.24 ± 0.38 cm (n = 40). Collected specimens were transferred to the laboratory within 2 hrs and preserved in 5% formaldehyde solution until dissection. Each specimen was carefully dissected and the entire gut was extracted without causing damage. Subsequently, 0.1 g (wet weight) of gut content in the first festoon HIRATSUKA AND UEHARA: FEEDING ECOLOGY OF ECHINOMETRA IN OKINAWA 89 of the intestine was quantified and placed into a screwcap vial containing 5% formaldehyde solution until analysis. The gut contents were spread to an even thickness on a grid slide (1 × 1 mm square grid; 1000 grids in total) and observed under an optical microscope at 100 × magnification. We analyzed the contents of 40 grids that had been marked with red ink. Contents were categorized into the following: macroalgae (including rhizoids and thalluses), seagrasses (including leaves, stems, roots, and sheaths), turf algae (including blue-green algae), encrusting coralline algae, unidentified algae, land plants, Ascidia, Foraminifera,P orifera, Amphipoda, Hydrozoa,

Gastropoda, unidentified debris, and sediment (fragments of CaCO3, mainly originated from sand, rubble, and bedrock). The percent cover of each food item in the 40 fixed grids was visually estimated under the microscope and averaged. The mean ±( SD) percent cover of each food item in the gut contents of 10 specimens was calculated. Fragments of seagrasses, macroalgae, and turf algae found in the gut contents were identified to the species level when possible. The identification of seagrasses and algae followed Toma (1999) and Yoshida (1998), respectively. To examine the food selectivity of Okinawan Echinometra species, the availability of major plant items (seagrasses, macroalgae, and turf algae) at each site was compared with the abundance of these items in the gut, using Strauss’s Food Selectivity Index (L) (Strauss, 1979) calculated as:

L = ri − pi

where ri is the relative abundance of food item i in the gut and pi is the relative abundance of food item i at the site. Strauss’s index ranges from –1 to +1, positive values indicating preference and negative values indicating avoidance. Values were categorized in the manner described by Cobb and Lawrence (2005):

Index range Selectivity –1.00 to –0.75 Strong avoidance –0.74 to –0.25 Moderate avoidance –0.24 to 0.24 Random feeding 0.25 to 0.74 Moderate preference 0.75 to 1.00 Strong preference

Results

Distribution of Sea Urchins.In the moat at Usahama, E. mathaei had the highest density (216.4 ind 10 m–2), followed by Echinometra sp. A (55.5 ind 10 m–2); Echinometra sp. C was scarce, and E. oblonga was absent (Fig. 3A). Urchins in the moat generally inhabited shallow burrows excavated in the bedrock. The only species at the reef margin were Echinometra sp. C and E. oblonga (Fig. 3A′) and these were always found in deep, narrow burrows. In the seagrass bed at Bise, Echinometra sp. A was the dominant species (Fig. 3B), found commonly among the branching corals scattered in the seagrass meadows. Only one individual of E. mathaei was found; the other two species of Echinometra were absent in the belt transects. On the intertidal reef platform at Onna, the four species of Echinometra were found mostly in burrows excavated on the platform. E. oblonga generally occupied the upper intertidal substrate nearest the wave-cut notch. The distributions of the other 90 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 1, 2007

Figure 3. Densities (mean ± SD; n = 10 transects) of sea urchins at each of the five study sites. Ea, Echinometra sp. A; Em, E. mathaei; Ec, Echinometra sp. C; Eo, E. oblonga; Eca, Echinothrix calamaris; Ds, Diadema setosum; Dsa, D. savignyi; Sv, Stomopneustes variolaris; Tg, Tripneus- tes gratilla; Tp, Toxopneustes pileolus.

three species partially overlapped and intermingled on the platform (Fig. 2C). In some cases, the four species occurred in adjacent burrows. The density ofE. mathaei was highest (143.7 ind 10 m–2), while the densities of the other three species ranged between 13.4–29.0 ind 10 m–2 (Fig. 3C). On the small sandy flat at Yonashiro, Echinometra sp. A was found under coral boulders or in crevices of bedrock in a mean density of 24.4 ind 10 m–2 (Fig. 3D). We did not encounter any of the other three species of Echinometra in the belt transects. Large urchins—Diadema setosum (Leske, 1778), Diadema savignyi (Michelin, 1845), and Echinothrix calamaris (Pallas, 1774)—occurred at densities of 28.3 ind 10 m–2, 0.7 ind 10 m–2, and 0.8 ind 10 m–2, respectively. The subtidal region at Ikei was mostly occupied by Echinometra sp. A (13.3 ind 10 m–2) and E. mathaei (183.6 ind 10 m–2), both inhabiting shallow burrows in the bedrock (Fig. 3E). The other two species, Echinometra sp. C and E. oblonga, existed in very low densities (0.4 ind 10 m–2) in the subtidal area, although they were common in the adjoining intertidal area. HIRATSUKA AND UEHARA: FEEDING ECOLOGY OF ECHINOMETRA IN OKINAWA 91

Figure 4. Benthic cover (mean ± SD; n = 40) at each of the five study sites. Food Availability.A benthic cover of turf algae was prominent in the moat at Usahama both in summer 2003 (70.3%) and in winter 2004 (66.8%); macroalgae comprised < 10% cover in both seasons (Fig. 4A). The dominant benthic component on the reef margin also included turf algae, which covered approximately 87% in both seasons. Neither sand nor rubble was recorded at the reef margin, probably due to strong waves and currents. The major benthic components of the seagrass bed at Bise were seagrasses, branching corals, and macroalgae such as Cladophoropsis vaucheriaeformis (Areschoug, 1853), Halimeda simulans Howe, 1907, Lobophora variegata (Lamouroux, 1809), Galaxaura rugosa (Ellis and Solander, 1786), and Ceratodictyon spongiosum Zanar- dini, 1878 in both seasons (Fig. 4B). Large clumps of Hypnea spp. covered the seagrass fronds in winter. This caused a slight increase in benthic cover of macroalgae and a decrease in that of seagrasses. Turf algae dominated the limestone platform at Onna, and covered 67.1% and 69.4% of the bottom in summer and winter, respectively (Fig. 4C). The bare bedrock surface, mainly observed in and around the burrows of Echinometra species, ranked second in the benthic cover: 20.1% in summer and 23.3% in winter. On the sandy flat at Yonashiro, three benthic components (sand, rubble, and bare bedrock) together represented > 80% of the benthic cover in both seasons (Fig. 4D). Consequently, neither seagrasses nor macroalgae accounted for more than 3% of the benthic cover. Some drift plant materials (seagrasses and macroalgae) that probably originated from the surrounding seagrass-macroalgal bed were scattered on the bottom, but benthic cover could not be estimated due to instability. 92 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 1, 2007

The benthic environment at the subtidal area in Ikei showed a dramatic change between the two seasons (Fig. 4E). In summer, dense fronds of Sargassum spp. covered the greater part of the substrate. As a result, macroalgae, consisting mainly of Sargassum spp., constituted 72.1% of the benthic cover. By winter, the Sargassum bed had disappeared and the exposed substrate was occupied by turf algae. Consequent- ly, turf algae became the dominant item in winter (40.5% cover). The proportion of macroalgae remained 19.4% in the winter, since new fronds of Sargassum species had begun to grow on the substrate. Gut Content Analysis.In the gut contents of Echinometra sp. A and E. mathaei collected from the moat in Usahama, turf algae was the dominant food item in both seasons, accounting for 47.7%–51.9% of gut contents (Fig. 5A). Sediment (i.e.,

fragments of CaCO3) represented 18.4%–20.6% of the gut contents of these two species. These carbonate fragments probably originated from material associated with turf algae and/or material on the surface of the bedrock in and around burrows, and were ingested together with food during grazing. The gut contents of Echinometra sp. C and E. oblonga collected from the reef margin at Usahama were also dominated by turf algae (36.7%–43.3%) in both seasons. Sediment accounted for 25.6%–27.5% of the gut contents of these two species. Seagrasses were a significant proportion of the gut contents of Echinometra sp. A collected from Bise: 58.5% in summer and 55.7% in winter (Fig. 5B). Macroalgae, mainly consisting of C. spongiosum, C. vaucheriaeformis, G. rugosa, and Hypnea spp., represented 16.8% and 15.1% of the gut contents in summer and in winter, respectively. In contrast, turf algae accounted for < 6% of the gut contents. The proportion of sediment in the gut contents of Echinometra sp. A was low: 9.1% and 12.0% in summer and winter, respectively. The gut contents of all four species ofEchinometra collected from Onna were very similar in their composition (Fig. 5C). Regardless of species and season, the dominant item in the gut content was turf algae (37.5%–44.9%), followed by sediment (28.0%–33.0%). The proportion of macroalgae in the gut contents was < 5%, as macroalgae were rare in the study area (Fig. 4C). Seagrass fragments found in the gut of E. oblonga collected in summer probably derived from drift. The composition of the gut contents of Echinometra sp. A from the sandy flat at Yonashiro was markedly inconsistent with food availability in this area. The bottom of the sandy flat was mostly sand, rubble, and bare bedrock, and the availability of macroalgae and seagrasses was < 3% throughout the year (Fig. 4D). Nevertheless, total macroalgae and seagrasses in the gut contents of Echinometra sp. A reached > 60% in both seasons (Fig. 5D). The fraction of sediment in the gut contents was low: 8.0%–8.9% in both seasons. Urchins collected from the subtidal region at Ikei showed a remarkable seasonal change in the composition of their gut contents. In summer, macroalgae, mostly Sar- gassum spp., constituted 69.3% and 66.5% of the gut contents of Echinometra sp. A and E. mathaei, respectively (Fig. 5E). In winter, when turf algae replaced Sargassum spp. as the major benthic component, the turf algae represented 26.3% and 30.7% of the gut contents of Echinometra sp. A and E. mathaei, respectively. A high proportion of sediment also occurred in the gut contents of the two species: 35.0% and 28.6% in Echinometra sp. A and E. mathaei, respectively. The total number of species of turf algae in the gut contents of each Echinometra species was similar, ranging from 36 to 40 (Table 1). Five species of seagrasses and HIRATSUKA AND UEHARA: FEEDING ECOLOGY OF ECHINOMETRA IN OKINAWA 93

Figure 5. Percentage composition (mean ± SD; n = 10) of the gut contents of Echinometra species collected from each of the five study sites.

10 species of macroalgae were found in the gut contents of Echinometra sp. A, while 0–1 and 3–4 species, respectively, were found in the gut contents of the other three species. Consequently, 55 species of plants (seagrasses, macroalgae, and turf algae) were found in the gut contents of Echinometra sp. A, while fewer species were found in the gut contents of E. mathaei, Echinometra sp. C, and E. oblonga (41, 39, and 42 species, respectively). Comparison between the availability of major plant items (i.e., seagrasses, macroalgae, and turf algae) at the sites and the abundance of those items in the guts using Strauss’s Feeding Selectivity Index indicates that the four species of Echinometra did not show either a strong preference for these items (index value 0.75–1.00) or strong 94 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 1, 2007

Table 1. Number of species of seagrasses, macroalgae, and turf algae in the gut contents of Echi- nometra species collected from five study sites on Okinawan coral reefs. Data were obtained by analysis of the gut contents of 20 individuals (10 collected in summer 2003 and 10 in winter 2004) per species per site. Blanks indicate no data due to absence or rareness of the sea urchins.

Number of plant species in the gut contents of Echinometra collected from Sea urchin species Food item Usahama Bise Onna Yonashiro Ikei Total Echinometra sp. A Seagrasses 0 2 0 5 0 5 Macroalgae 4 4 1 4 1 10 Turf algae 29 8 30 18 28 40 Echinometra mathaei Seagrasses 0 0 0 0 Macroalgae 3 1 1 4 Turf algae 29 27 29 37 Echinometra sp. C Seagrasses 0 0 0 Macroalgae 3 1 3 Turf algae 30 26 36 Echinometra oblonga Seagrasses 0 1 1 Macroalgae 3 1 3 Turf algae 31 31 38

avoidance of them (–1.00 to –0.75) (Table 2). Echinometra sp. C and E. oblonga on the reef margin in Usahama had low negative values for turf algae (–0.51 to –0.45), while Echinometra sp. A at the sandy flat in Yonashiro had relatively high positive values for seagrasses (0.31–0.45) and macroalgae (0.23–0.30).

Discussion

Analysis of the gut contents of the four species of Echinometra collected from the five sites showed a high proportion of vegetal food items: 39.2%–79.6%, 43.7%–80.7%, 45.2%–49.7%, and 45.5%–48.7% in Echinometra sp. A, E. mathaei, Echinometra sp. C, and E. oblonga, respectively. This result indicates that the four species of Oki- nawan Echinometra are herbivorous in the field, consistent with many other studies that have noted the occurrence of various vegetal diets, such as turf algae, seagrasses, macroalgae, and coralline algae in the gut contents of Echinometra (Herring, 1972; Abbott et al., 1974; Ogden et al., 1989). Herbivory of Echinometra was also documented by McClanahan (1988), who showed that 54% (by volume) of the gut contents of Kenyan E. mathaei consisted of vegetal food items (i.e., seagrasses and algae). Animal tissues, which originated mainly from ascidians, foraminiferans, porifer- ans, amphipods, hydrozoans, and gastropods, were also recorded in the gut contents of the Okinawan Echinometra species. However, the proportion of these animals in the gut content was low, ranging between 0.2%–3.3%, 0.1%–5.0%, 0.7%–4.8%, and 1.3%–2.9% in Echinometra sp. A, E mathaei, Echinometra sp. C, and E. oblonga, respectively. The animals found in the gut presumably derived from the epifauna on seagrasses, macroalgae, and turf algae, and were likely ingested incidentally while feeding on these plants and algae. Thus these animals are a secondary food for the four species of Okinawan Echinometra, at least in habitats where plant material is abundant. Most studies on the feeding habits of echinoids, including the present study, have found echinoids to be herbivores. However, urchins do feed on animals if given a choice. For instance, food preference experiments on the Caribbean E. lu- HIRATSUKA AND UEHARA: FEEDING ECOLOGY OF ECHINOMETRA IN OKINAWA 95 − − –0.08 –0.10 −0.10 −0.14 Winter Ikei − − 0.01 –0.06 −0.03 −0.05 Summer 0.31 0.30 0.15 Winter Yonashiro 0.45 0.23 0.07 Summer − − − − 0.03 0.02 0.04 0.04 −0.27 −0.31 −0.32 −0.32 Winter Onna − − − 0.00 0.00 0.02 0.04 0.00 −0.25 −0.22 −0.25 −0.25 Summer 0.21 0.03 −0.02 Winter Selectivity indices for food items at the study sites Bise 0.15 0.04 0.05 Summer at the study sites on Okinawan coral reefs. The selectivity index was calculated from the abundances the from calculated was index selectivity The reefs. coral Okinawan on sites study the at − − − − 0.01 0.06 0.03 Winter −0.19 −0.02 −0.18 −0.51 −0.51 Echinometra Usahama − − − − 0.03 0.04 −0.04 −0.19 −0.01 −0.18 −0.45 −0.48 Summer Seagrasses Seagrasses Macroalgae algae Turf Seagrasses Macroalgae Turf algae Turf Macroalgae Turf algae Turf Seagrasses Macroalgae Food item Turf algae Turf sp. C sp. A sp. Echinometra mathaei Echinometra Echinometra Echinometra oblonga Sea urchin species of each food item at the site and in the gut of each species. range Values from –1.00 Dashes indicate that the food item was not present in gut or environment. Blanks no data due to absence rareness of sea urchins. (avoidance) to +1.00 (preference) with 0.00 indicating random feeding. Table 2. Food selectivity of the four species of species four the of selectivity Food 2. Table 96 BULLETIN OF MARINE SCIENCE, VOL. 81, NO. 1, 2007 cunter revealed that its feeding response was equally strong for an animal diet as for a plant diet (McClintock et al., 1982). While Okinawan Echinometra may also be at- tracted to or prefer animal foods under some specific conditions, this was not found in our field study. The diet of echinoids typically depends on food availability (Lawrence, 1975), and in this regard, Okinawan Echinometra species are no exception. The present study shows that turf algae constituted the major food item in the gut contents of the four species of Echinometra living in the burrows excavated on the limestone platforms at Usahama and Onna. On the other hand, seagrasses and macroalgae were the most important diets for Echinometra sp. A inhabiting the seagrass bed at Bise. The popu- lation of Ecinometra sp. A living on the sandy flat in Yonashiro subsisted almost entirely on drift plants. Furthermore, in the subtidal area at Ikei, Echinometra sp. A and E. mathaei changed their principal diets according to the seasonal change in benthic flora composition. These results clearly show that the diets of the four species, especially Echinometra sp. A, vary markedly among sites and occasionally between seasons. They suggest that the four species of Okinawan Echinometra are opportunistic herbivores. While the comparison between food availability and gut composition revealed a general correlation between the availability of major plant items and their abundance in the gut contents of Echinometra, there were two exceptions. Echinometra sp. A on the sandy flat inY onashiro showed relatively high selectivity indices (moderate preference) for seagrasses and macroalgae. However, this result is mainly due to lack of data on the availability of drift plant material in this study area. Including such data would likely have reduced the inconsistency and, consequently, the selectivity indices. Another exception was Echinometra sp. C and E. oblonga on the reef margin at Usahama, both of which showed very low selectivity indices (moderate avoidance) for turf algae. However, gut contents analysis demonstrated that turf algae was the principal food for both species at this site. Instead, the likely interpretation is that severe hydrodynamic conditions on the reef margin greatly restrict the grazing activities of these species and consequently increase the difference between the proportions of turf algae in the field and in the gut. In general, while other urchins have been shown to exhibit feeding preferences for and/or avoidance of certain plant species due to factors such as food availability, the nutritional values of food, and the presence of chemical substances in foods that act as attractants, repellents, stimulants, or deter- rents (Vadas, 1977; Vadas et al., 1982; Lison de Loma et al., 2002; Vaïtilingon et al., 2003; Cobb and Lawrence, 2005), Okinawan Echinometra typically feed randomly on abundant vegetal food (including drift plants) available in a particular habitat during a particular season. The feeding behavior of Echinometra can be roughly divided into two modes: (1) ingestion of drift plants washed or falling into the shelter, such as burrows and crevices; and (2) grazing on benthic algae in and around the shelter (Kelso, 1970; Russo, 1977; Lawrence, 1987; Hart and Chia, 1990; McClanahan and Muthiga, 2001). We commonly observed high proportions of turf algae and sediments in the gut contents of urchins collected from the reef platforms at Usahama and Onna. Since a large amount of sediment in the gut of Echinometra is circumstantial evidence of benthic grazing, most turf algae in the guts of the four species collected from these sites (Usahama and Onna) was likely obtained by grazing on the substrate in and around their burrows. Indeed, Echinometra sp. C and E. oblonga living on the reef margin HIRATSUKA AND UEHARA: FEEDING ECOLOGY OF ECHINOMETRA IN OKINAWA 97

or the upper intertidal platform near shore graze on turf algae immediately adjacent to the burrow entrance during the late ebb tide and the early flood tide, when their habitats are splashed (Y. Hiratsuka, unpubl. data). Similar grazing behavior can be observed in E. mathaei, which generally lives in calmer environments, and grazing by the comparatively mobile species Echinometra sp. A can occur dozens of centime- ters away from its shelter (Y. Hiratsuka, unpubl. data). In contrast, the individuals of Echinometra sp. A inhabiting the sandy flat at Yo- nashiro provide a typical example of subsistence on drift plants. There is almost no vegetation inside the sandy flat because of high grazing pressure from large urchins (e.g., D. setosum and D. savignyi). However, a steady supply of drift plants such as seagrasses and macroalgae enables Echinometra sp. A to obtain sufficient food without migrating into the surrounding seagrass–macroalgal bed. Likewise, Echinometra spp. in the seagrass bed at Bise and in the Sargassum bed at Ikei are presumably drift plants feeders, obtaining macrophytes that fall into their shelters. The low proportions of turf algae and sediment found in the gut content of the urchins collected from Yonashiro, Bise, and Ikei provide strong evidence that these urchins gave prior- ity to feeding on drift material rather than grazing on the substrate. It is likely that Echinometra spp. employ a sedentary mode of feeding when there is a constant supply of drift food, and benthic grazing when drift food is insufficient or unavailable. Echinometra sp. A ingested a greater variety of food than the other three species. This is obviously related to habitat differences among the Okinawan Echinometra (Nishihira et al., 1991; Aslan, 2000; Suzuki and Kan, 2004). Echinometra sp. A is the most widely distributed, occurring in tide pools, lower intertidal zone, moats, and occasionally on the reef slopes, while E. mathaei occurs mainly from the upper subtidal to the lower intertidal region. The other two species,Echinometra sp. C and E. oblonga, primarily inhabit the upper intertidal areas near shore or reef margins. Thus, it is not surprising that Echinometra sp. A, the most widespread species, con- sumes a greater variety of food than the other more restricted species. Our results reveal that despite habitat segregation, the four urchin species have essentially similar feeding types (herbivorous), modes (benthic and drift feeding), and preferences (random feeding).

Acknowledgments

We are grateful to J. Lawrence, University of South Florida, for discussions and critical comments on this manuscript. We also thank two anonymous reviewers for their valuable suggestions. This study was partially supported by the 21st Century COE program of the University of the Ryukyus.

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Date Submitted: 11 July, 2006. Date Accepted: 18 April, 2007.

Addreses: (Y. H., T. U.) Graduate School of Engineering and Science, University of the Ryuky- us, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan. Corresponding Author: (Y.H.) E- mail: .