Journal of Oceanography, Vol. 61, pp. 183 to 186, 2005

Short Contribution

Quality of the ovalis on a Thai Intertidal Flat as Food for the

1 2 MASUMI YAMAMURO * and ANONG CHIRAPART

1Geological Survey of Japan, AIST Tsukuba Central 7, 1-1-1 Higashi, Tsukuba 305-8567, Japan 2Department of Fishery Biology, Faculty of Fisheries, Kasetsart University, Chatuchak, Bangkok 10900, Thailand

(Received 26 September 2003; in revised form 28 May 2004; accepted 28 May 2004)

To determine whether along the Thai coast prefer relatively faster-growing Keywords: Halophila ovalis due to its nutritional value, we analyzed the contents of carbon (C), ⋅ Growth rate, nitrogen (N), phosphorus (P), ash, fiber, and lipids in several species of seagrass ⋅ lipid, ⋅ collected near dugong feeding trails. CNP concentrations in the faster-growing H. fiber, ⋅ ovalis were distinctly lower than those in the slower-growing species. Lipid concen- nitrogen, ⋅ phosphorus. trations were comparatively not as low; they were equivalent to the values of the slower-growing Enhalus acoroides in the leaves and to Thalassia hemprichii and Cymodocea rotundata in the rhizomes and roots. The ash content of H. ovalis was the highest of all species in both the above and below ground parts. The reason that dugong feeds exclusively on H. ovalis at this site may be the potentially large supply due to its high growth rate, rather than its nutritive qualities.

1. Introduction carbohydrate content are good descriptors of nutrient The dugong (Dugong dugon) is a seagrass-depend- value. De Iongh et al. (1995) further suggested the possi- ent marine mammal of tropical and subtropical coastal bility that dugongs preferentially graze with waters. It feeds mainly on seagrass species in the genera higher rhizome organic C content. Zostera, Posidonia, Thalassia, Enhalus, Cymodocea, No study has so far compared the nutritional values— Halodule, Syringodium, and Halophila (Heinsohn and CNP, fiber (=partially digestible), and lipid (=easily di- Birch, 1972; Heinsohn et al., 1977; McRoy and gestible) content—of faster- and slower-growing Helfferich, 1980), generally selecting the faster-growing seagrasses in areas where dugongs selectively forage on species Halodule uninervis and Halophila ovalis over the the former. It is therefore not clear whether the animals sympatric, slower-growing Cymodocea rotundata, prefer faster-growing seagrasses due to their nutritional Thalassia hemprichii, and Zostera capricorni (De Iongh quality or their greater availability. et al., 1995; Preen, 1995). Relative leaf growth rates were In 1998, a seagrass bed of approximately 3-ha ex- similar between C. rotundata and T. hemprichii, while tended over the intertidal flat at Khao Bae Na, located in the growth rate of Enhalus acoroides was 20% lower the Haad Chao Mai Marine National Park on the south- (Cebrián et al., 1998). western coast of Thailand (Fig. 1). Mukai et al. (1999) Cebrián and Duarte (1998) hypothesized that herbiv- estimated the total biomass of H. ovalis and C. rotundata ores feed selectively on faster-growing seagrass species in that bed to be 1300 kg and 545 kg dry weight, respec- because of the higher nutritional quality compared with tively. From 11 to 23 March 1998, they also observed the slower-growing species. They suggested that herbivore behavior of a dugong, the seagrass distribution, and the preference for faster growing species is independent of grazing trails left by the dugong in the seagrass bed. At leaf nutrient concentrations (i.e., C:N, C:P), and that a high tide during the daytime, the dugong (probably the low content of indigestible fiber (i.e., lignin) and a high same individual) left 6 to 29 (15 on average) new feeding trails per day in the 1-ha quadrat, mostly feeding in the H. ovalis bed and avoiding the slower-growing C. * Corresponding author. E-mail: [email protected] rotundata and E. acoroides (Mukai et al., 1999). Copyright © The Oceanographic Society of Japan. By the end of October 1998, the bed had become

183 3. Results and Discussion CNP concentrations (Table 1) were within the ranges reported for tropical seagrasses (Duarte, 1990). Among the analyzed seagrasses, CNP concentrations in leaves and petioles were lower in the faster-growing H. ovalis than in the slower-growing species (Table 1). The ash content of H. ovalis was highest in both the above and below ground parts. Leaf blades and sheaths (leaves and peti- oles for H. ovalis) had higher concentrations of N and P than in rhizomes and roots, both in slower-growing spe- cies (E. acoroides, T. hemprichii, and C. rotundata) and in faster-growing H. ovalis (Table 1). Yamamuro et al. (2001) measured the CNP concen- trations of the leaf and petiole of H. ovalis at Khao Bae Na (Fig. 1) every month from April to October 1998. The Fig. 1. Map showing the study site. concentrations were 10.7Ð17.7% for C, 0.62Ð1.2% for N, and 0.70Ð1.4 mg gÐ1 for P. The CNP concentrations of H. ovalis at St-B were thus not exceptionally low for this coast. Similarly low concentrations (19.5% for C, 0.59% buried in silt, reducing the coverage of H. ovalis to 0Ð for N, and 1.5 mg gÐ1 for P) and high ash content (57Ð 10% of the area (Nakaoka and Supanwanid, 1999). After 60%) were also reported from intertidal H. ovalis in Aus- the siltation at Khao Bae Na, the dugong changed its feed- tralia (Birch, 1975), and Yamamuro et al. (2001) suggested ing site to Laem Yong Lam (Fig. 1). Again, its feeding that emersion during ebb tide caused the low nutrient tracks were observed only in H. ovalis patches (M. concentrations of H. ovalis growing on intertidal flats, Yamamuro, personal observation). presumably due to limited access to water column nutri- For the present study we collected several species of ents. The CNP concentrations of C. rotundata at St-B were seagrass near dugong trails on the tidal flat at Laem Yong no lower than the other species at St-A, which may sug- Lam and analyzed their nutritional values (CNP, ash, fiber, gest that limited access to water column nutrients does lipids) to determine whether the dugongs on the coast of not lower the CNP concentrations of slower-growing spe- Thailand prefer the faster-growing H. ovalis because of cies. its nutritional value. De Iongh et al. (1995) suggested the possibility that dugongs preferentially graze seagrass with higher rhizome 2. Material and Methods organic C concentration. Our analysis of seagrasses from We collected E. acoroides and T. hemprichii from the Thai coast did not support that hypothesis, because C the St-A and H. ovalis and C. rotundata from St-B at Laem concentration of rhizome and root in H. ovalis was less Yong Lam in December 1998 (Fig. 1). At St-A, the mean than other seagrasses (Table 1). water depth relative to the mean sea level was 1.3 m, while Cebrián and Duarte (1998) expected that nutritional St-B emerges completely during ebb tide. At St-A, E. quality would be higher in faster-growing seagrass spe- acoroides and T. hemprichii were the dominant seagrasses cies than in slower-growing species. They suggested that (Koike et al., 1999), while H. ovalis was the most abun- a low content of indigestible fiber (i.e., lignin) and a high dant species at site St-B, with some patches of C. carbohydrate content are good descriptors of nutrient rotundata (M. Yamamuro, personal observation). value. On the Thai coast, the fiber content of H. ovalis The samples were collected randomly. Epiphytic leaf was lower than other species. However, this does not materials were removed and the seagrass samples were imply a higher carbohydrate content because the carbon separated into leaf blades, leaf sheaths, and roots plus content of H. ovalis leaf was lower than other species. rhizomes, except in the case of H. ovalis, which was sepa- The lower fiber content of H. ovalis leaf was presumably rated into leaves plus petioles, and rhizomes plus roots. due to the higher content of ash. Thus, the nutritional C and N content were determined by the combustion quality of faster-growing H. ovalis would not be higher method using an elemental analyzer (EA1108, Fisons In- than other species, as far as fiber and carbohydrates are struments). Concentrations of P were determined concerned. colorimetrically after digestion following the method Lanyon and Marsh (1995) found that the mouth-to- described in Ohtsuki (1982). Each measurement was de- anus retention time (146Ð166 h) of dugongs is the long- termined twice. Ash, fiber, and lipid contents were deter- est among the hindgut fermenters. They further suggested mined once as described by the AOAC (1984). that dugongs may prefer seagrasses with lower fiber con-

184 M. Yamamuro and A. Chirapart Table 1. Nutrient concentrations of seagrasses collected along the coast of Thailand.

Sample Carbon Nitrogen Phosphorus Ash Fiber Lipid (relative growth rate) (%dw) (%dw) (mg g−1) (%dw) (%dw) (%dw) Enhalus acoroides leaf blade 31.4 1.90 2.64 24.6 19.8 0.38 (slowest) leaf sheath 29.6 1.38 2.30 28.9 20.8 0.53 rhizome and root 36.0 0.70 0.97 13.8 16.3 0.17

Thalassia hemprichii leaf blade 33.5 2.33 2.41 22.6 17.9 0.29 (slow) leaf sheath 31.3 1.46 2.17 32.0 18.2 0.71 rhizome and root 32.0 0.83 1.80 19.8 15.5 0.34

Cymodocea rotundata leaf blade 38.9 3.02 2.36 13.9 23.6 0.28 (slow) leaf sheath 34.3 1.72 2.23 25.4 26.7 0.70 rhizome and root 34.3 0.86 0.74 16.1 19.1 0.34

Halophila ovalis leaf and petiole 25.1 1.30 1.31 42.9 13.5 0.38 (fast) rhizome and root 17.7 0.41 0.53 29.7 22.9 0.35

centration to almost completely digest the fiber. On the At this study site, dugongs feed more efficiently on Thai coast, fiber concentration is the lowest in H. ovalis the above ground parts of H. ovalis than on the below (13.5%) followed by T. hemprichii (18%) (Table 1). How- ground parts—in their feeding trails they leave only 6.1% ever, total organic carbon is higher in T. hemprichii (31Ð of the initial above ground biomass and 39% of the be- 34%) than H. ovalis (25%). Aketa et al. (2001) reported low ground biomass (Nakaoka and Aioi, 1999). These that captive dugongs fed by Zostera marina showed high values are similar to those of Indonesian dugong feeding apparent digestibility both in terms of energy (82%) and on Halodule uninervis—they leave 7% of the initial above dry weight (85Ð86%). Therefore, in terms of digestibil- ground biomass and 25% of the below ground biomass in ity, H. ovalis with higher ash and lower C concentrations their feeding trails (De Iongh et al., 1995). These ungrazed than T. hemprhichii would be poorer nutrition for dugongs. rhizomes may act as nuclei for regeneration of the seagrass At both Khao Bae Na and Laem Yong Lam, H. ovalis bed, helping to preserve areas of H. ovalis in the face of beds were distributed where the flats emerged completely heavy grazing by dugongs, as observed in Australia during ebb tide, so dugongs could feed only during flood (Preen, 1995). tide. The intertidal environment may also decrease the Preen (1995) suggested that dugongs benefit from nutritional value of H. ovalis. Despite these unfavorable heavy grazing on H. ovalis because the new seagrass con- conditions, the dugongs preferred H. ovalis growing on tains more N and less lignin or ash. At our study site, the the intertidal flat. faster-growing H. ovalis contained less N and more ash At St-A, the estimated above ground productivity of than nearby slower-growing species, probably because of E. acoroides and T. hemprichii was 1.40 and 1.34 g-DW its regular emersion during low tide. mÐ2dÐ1, respectively (Koike et al., 1999). In contrast, the Our data suggest that the food preference of faster- growth rates of the above ground parts of H. ovalis on growing seagrasses by dugong is not necessarily due to the Khao Bae Na intertidal flat were 7.5 g-DW mÐ2dÐ1 the nutritional values such as low content of indigestible along the dugong trails, 9.9 g-DW mÐ2dÐ1 at the edge of fiber, and high carbohydrates and nitrogen contents. The the patch, and 15.6 g-DW mÐ2dÐ1 at the center of the patch mechanisms by which dugongs can detect differences in (Nakaoka and Aioi, 1999). The daily rate of consumption nutritional quality so that they can preferentially of H. ovalis by a single dugong (probably the same indi- feed on more nutritious have not yet proposed. High vidual during the observation) on the Khao Bae Na inter- nutritional values may even decrease the grazing rates, tidal flat was estimated to be ca. 0.06 g-DW mÐ2dÐ1 (Mukai as was reported for sea urchins. Valentine and Heck (2001) et al., 1999). This means that the loss of seagrass by enriched the nitrogen content of seagrass leaves with fer- dugong feeding can be fully compensated by the high tilizer and found that sea urchins compensated for low productivity of H. ovalis. In fact, Nakaoka and Aioi (1999) nitrogen levels by eating more leaves rather than enriched estimated that it took less than 10 days for the biomass to leaves. Consequently, sea urchins ate less nitrogen-en- recover from the devegetated state caused by dugong feed- riched seagrass than unenriched seagrass. This result sug- ing on the Khao Bae Na intertidal flat. gests it is a question of how much herbivores can obtain

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186 M. Yamamuro and A. Chirapart