Proceedingsof the FourthInternational Symposium, Manila, 1981, Voh 2

BROWSING BY HERBIVOROUS REEF- ON THE AGAROPHYTEGRACILARIA EDULIS RHODOPHYTA! AT GUAM, MARIANA ISLANDS

StephenG. Nelsonand Roy N. Tsutsui Marine Laboratory, University of Guam

ABSTRACT Pairedsets of cagedand exposed Gracilaria edulis thalli wereplaced at varioussites within a coral-reef habitatin orderto determine the amount of browsingby herbivorousreef fishes. Both growth rates of thethalli andthe amount of browsingwere dependent upon depth and location within the reef habitat. Growth rates of in- tactthalli were highest in shallowareas and herbivore browsing was greatest in themiddle depths of the reef slope.Surveys ofthe herbivorous reeffishes indicated that the acanthurid lituratus was probably responsi- ble for most of the browsing on Gracilaria in this area.

INTRODUCTION The thalli were removed from the field after periods of 1 to 2 weeks. They were then returned to Severalstudies have demonstratedthat browsing the lab, examined for evidence of breakage and by herbivoreshas a major impact on the production weighed. The apical portions of intact thalli are and distribution of fleshy macroalgae in coral-reef tapered, whereas damaged or browsed thalli have ecosystems Bakus 1967, Ogden 1976, Wanders truncated apical tips. Specific growth rates were 1977, van den Hock et al. 1975 and 1978, Robertson calculated for intact thalli as follows: et al. 1979!. We were especially interested in the ef- fects of reef herbivores on the benthic macrophyte s = 100 [9 n Ne No >!]t > Gracilaria edulis Silva! since this alga is economically valuable on Guam and of this where p = specific growth rate as percent in- genus have been suggested for mariculture in crease in wet weight per day Micronesia Doty 1980, Nelson et al. 1980!. The objectives of this study were to quantify the N = initial wet weight g! effects of browsing by herbivorous reef fishes at Ne = final wet weight g! on day t. various locations within a natural bed of G. edulis on Guam and to determinewhich speciesmight be The mean specific growth rate of the intact thalli responsible for the heaviest browsing. at each site was used to calculate the expected weights of the damaged or lost thalli. The difference between the observed and expected biomass of each MATERIALS AND METHODS set of exposed and caged thalli was used to calculate the biomasslost as a resultof browsing and/orwave Thalli for the study were collected from the study damage. The biomass loss in each caged set was site at Sella Bay, Guam and returned to the Univesi- subtracted from the biomass lost in the correspon- ty of Guam Marine Laboratory. The thalli were ding exposed set to determine the biomass lost as a weighed individually and a mylar identification tag result of browsing. These losses were calculated as was attached to each with nylon monofilament. percentages of the expected biomass. Each thallus was packagedin a plastic bag filled Counts of herbivorous reef-fishes were made five with seawater for transport back to the field site. times during the study. The counts were made at There the thalli were attached to nylon monofi- depths of 0-2 m, 2-4 m, 4-6 m, and below 6 m. Counts lament lines. These lines were anchored at various were conducted at the inner bay, near the river locations in paired sets which were either caged or mouth; the middle bay, 100 m from the river mouth exposed to herbivores. The cages consisted of 2.5 cm along the reef slope; and in the outer bay, 200 m wire mesh tied to 1.5 m X 1.5 m X 0.5 m iron rebar from the river mouth along the reef slope.Fifteen frames which were anchored to the substrate with minute counts were made by scuba divers at each rebar stakes. Exposed lines were attached to rebar location and depth. passing within a 9 X 9 m stakes driven into the substrate. area in front of the diver were included in the 504 NELSON AND TSUTSUI counts. All of the fish surveys were conducted du- ranged from 10 to 85% for the caged sets and from 0 ring the daytime between 1100 and 1300 hours. to 73% for the exposed sets. In all but one case, the percentage of intact thalli was higher for the caged than for the exposed set. RESULTS AND DISCUSSION The percent of the expected biomass lost to surge and to herbivore browsing is shown for each pair of The mean growth rates of intact thalli ranged thalli sets in Table 1. The percent biomass loss at- from 1 to 8% per day and were strongly influenced tributed to breakage ranged from 4 to 34% while by depth as shown in Fig. 1. The relation between that attributed to herbivore browsing ranged from 0 specific growth rate and depth is curvilinear, similar to 48%. Lowest losses from breakage occurred at a to that of light attenuation in tropical inshore protected, shallow location in the inner bay .4%! marine waters van den Hock et al. 1978!. In culture, and at a location on the sand bottom, away from the the growth rate of G. edulis was also shown to be reef slope, in the middle bay .9%!. Neither the per- related to depth Nelson et al. 1980!. The effect of cent lost to breakage nor that lost as a result of her- depth on specific growth rate at the Sella Bay site bivore grazing were correlated with depths, but was most pronounced at depths less than 5 m. both were influenced by location within the reef habitat. For those locations on the reef-face, losses to 10 browsing were less in the shallowest .0 m! and deepest 5.0 m! areas. Browsing losses were greatest at intermediate depths {4 to 6 m!. In a study of the coral reefs of the NetherlandsAntilles, van den Hock et aL 978! noted that the fleshy algae were prevalent in the shallowestand deepest zones but were scarce in the middle depths. They at- tributed this to the effect of herbivores since fish ll Cl and echinoid herbivory on fleshy algae has been I 2 2 0. reported in that location Wanders 1977!. 2 MIII A summary of the fish counts for specific sites within Sella Bay is presented in Table 2. The most common fish in the area was Ctenochaetus striatus. 0u. I- These were most abundant at depths of 2 to 4 m and 2 III were often observed biting Gracilaria However, it IL was unclear whether they were ingesting bits of the thalli or only ingesting the sedimenttrapped on the surface of the thalli. The latter seems more reason- able since Jones 968! and Robertson et al. 979! reported that Ctenochaetusspecies ingest diatoms, detritus, sand and sediment at Enewetak and Aldabra Atoll respectively. This species was most abundant in the inner bay, where the sedimentation was high. 10 15 Included in the counts with this species were DEPTH M! Ctenochaetus binotatus snd Acanthurus nigrofus- cus since these were difficult to distinguish from C. Figure1. The relation betweenthe specificgrowth rate of intact Gracilaria thalli and depth in Sells Bay, Guam. striatus in the field and were much less common. The clown surgeonAcanthurus lineatus and the Damage and loss of the thalli occurred from surge convict tang A. triostegus were also commonin the in both the caged and exposedsets of thalli. Our shallow zones. Robertson et al. 980! reported that results are for calm periods in Sella Bay. When the diet of these specieson Aldabra Atoll consisted tropical storms passed near Guam, thalli sets and primarily of microalgae. However, A. triostegus has cages were often destroyed by surge and wave ac- been observed to eat the apical tips of Gracilaria tion. During our study approximately two thirds of edulis in tank culture Nelson et al. 1980!. our thalli sets were lost as a result of this problem. At depths of 4 to 6 m the acanthurid, Naso litu- The data presented here therefore represent conser- ratus, and the siganid, Siganus argenteus, were vative estimates of thalli damage and loss to wave abundant. Species of both genera are known to con- action and may overestimate the effect of her- sume Gracaaria Robertson et al. {1979! reported bivores somewhat. The intact thalli at each location that at Aldabra Atoll the diets of N. lituratus and BROWSING BY FISHES ON GRACILARIA EDULIS 505

Table1. Losses inexpected Gracilaria biomass attributed tosurge and to herbivore browsing atsites within SeQa Bay, Guam.

Percentof Expected Percentof Expected Area Zone Depth m! BiomassLost as a Biomass Lost as a Resultof Surge Resultof HerbivoreBrowsing

Inner Bay Reef Slope 2.0 4.4 17.5 Middle Bay Reef Slope 2.0 33.8 0 Middle Bay Reef Slope 2.0 7.5 24.8 Middle Bay Reef Slope 4.0 20.5 43.4 Middle Bay Sand Terrace 6.0 5.9 0 Base of Outer Bay Reef Slope 6.0 23.3 48.1 Base of Outer Bay Reef Slope 15.0 15.9 17.6

Table2. Mean counts + standarderror! of herbivorousreef fish at differentdepths within the inner, middle, and outer portions of Sells Bay, Guam. InnerBay MiddleBay OuterBay 0-2m 2-4m 0-2m 2-4m 44m 6m 0-2m 2-4m 4-6m 6m

Ctenoehuetus 43.0 28.2 13.2 20.6 7.4 2.6 25.0 11.3 5.5 9.5 spp.++ +11.3! +5.1! + 2.5! +4.4! +2.5! +o.s! +7.8! +1.0! + 2.3! +3.1! Acunthurus 3.6 4.2 36.8 8.8 1.8 0.0 1.6 2.0 0.6 0.0 lineatus + 3.6! + 2.3! + 14.5! +4.7! +I.o! +0.0! +1.3! +2.o! + 0.4! +0.0! Acanthurus 2.0 0.8 3.8 6.4 0.0 0.0 1.0 3.0 0.0 0.0 triostegus + 1.2! +o.s! + 2.9! +6.4! +o.o! +o.o! +1.0! +3.O! + o.o! +0.0! Naso lituratus 0.6 0.8 0.4 0.4 10.2 7.0 2.2 0.4 4.0 5.2 + 0.4! +o.s! + O.2! +0.2! +2.7! +3.5! +1.3! + 0.2! + 3.3! +4.0! Si gun us 0.6 0.6 0.6 0.0 2.8 2.0 0.0 0.0 0.0 0.0 argenteus + o.e! 0.6! + o.e! +o.o! +2.1! +1.3! +o.o! +0.0! + o.o! +o.o! Scarus spp. 3.2 0.4 5.2 2.4 5.0 3.8 5.2 1.4 3.8 5.4 + 2.2! M.4! + 3.8! +1.4! +2.0! +2.0! +3.5! +o.9! + 1.4! +2.4! Kyphosus 0.0 0.0 0.0 0.0 0.2 0.4 0.0 0.0 0.0 1.2 cinentscens + 00! +0.0! + o.o! +o.o! +0.2! +0.4! +o.o! +o.o! +o.oo! +o.4!

+Based on Gve 15-min counts from each area. ++ This groupincluded Ctenoehaetus stn'utus, C. binotatus and Acunthurus ni grofuscus in a ratioof 5:1:1.

N. unicornis consistedof large macroalgae.We have Two other groups of herbivorous fishes were in- observedthat this specieswill readily ingest Groci- cludedin the counts.Small parrotfishes Scarus spp. laria in the laboratory. Lundberg and Lipkin 979! were common in some areas. However, it has been reported that Grocilario spp. were among the reported that their diets consist of benthic filamen- natural foods of siganids in the Red Sea. Bryan tous algae scraped from corals Hobson 1974!. It is 975! reportedthat Gracilaria was amongthe algae therefore unlikely that they were browsing on the readily consumed by S. spinus and S. rostrotus in Gracilaria thalli. On the other hand, the sea chub laboratory studies on Guam. Also von Western- Kyphosus cinerascens may browse Gracilaria since hagen 973a! reported that six species of Gracilaria other kyphosids have been reported to feed on were readily eaten by S. concatenata and that marine macrophytes Randall 1967!. This species, agarophytes, including Gracilaria, were found in the however,occurred only infrequently and probably stomachs of wildwaught S. striolattt and S. oramin was not responsible for a major portion of the in the Philippines von Westernhagen 1973b!. observed browsing losses. 506 NELSON AND TSUTSUI

The production of Gracilaria edulis at specific Jones, R.S. 1968. Ecological relationships in Hawaiian sites within Sella Bay is a function of standing crop, and Johnston Island Surgeonfishes!. thallus growth rate and lossbs which result from Micronesica 4: 309-362. surge and herbivore browsing. Both growth rate Lundberg, B. and Y. Lipkin. 1979. Natural food of the her- and losses to herbivores are dependent on depth. bivorous rabbitfish /Si ganus spp.! in Northern Red Sea. Bot. Mar. 22: 173-181. Browsing pressure is greatest at the middle depths Nelson, S.G., R.N. Tsutsui and B.R. Best. 1980. of the reef slope, the area frequented by Naso Preliminary evaluation of the mariculture potential lituratus and Siganus argenteus. Since N. lituratus of Gracilaria Rhodophyta! in Micronesia: growth is the most abundant fish in this area it is likely that and ammonium uptake. In I.A. Abbott, M.S. it is the species which is responsible for the majority Foster, and L.F. Eklund. Pacific Seaweed Aqua- of browsing on Gracilana in Sella Bay. culture. La Jolla, California: California Sea Grant College Program, University of California. Ogden,J.C. 1976.Some aspects of herbivore plant rela- tionships on Caribbean reefs and sea grass beds. ACKNOWLEDGEMENT S Aquat. Bot. 2: 103-116. Randall, J.E. 1967. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanog. 5: 665-847. Marine Laboratory Contribution No. 155. Robertson, D.R., N.V.C. Polunin and K. Leighton. 1979. This study was supported by a grant from the National The behavioral ecology of three Indian Ocean sur- Oceanicand Atmospheric Administration Office of Sea geonfishes Acanthurus lineatus, A. leucosternon Grant UG/R-l!. We would like to thank Mr. V. Tyndzik, and Zebrasoma scopas!: their feeding strategies Mr. G. Davis, Mr. V. Kamiaz and Dr. D. Matlock for and social mating systems. Env. BioL Fish. 4: assistance in the field, Dr. S. Amesbury aided us in identi- 125-170. fication of the fish species. van den Hock C., A.M. Cortel-Braeman and J.B.W. Wanders 1975. Algal zonation in the fringing coral reef of Curacao, Netherlands Antilles, in relation to zonation of corals and gorgonians. Aquat. Bot. 1: REFERENCES 269-308. van den Hock, C., A.M. Breeman, R.P.M. Bak and C. van Bakus, G.J. 1967. The feeding habits of fishes and Buurt. 1978. The distribution of algae, corals and primary production at Eniwetok, Marshall Islands. gorgoniansin relation to depth, light attenuation, Micronesica 3: 135-150. water movement and grazing pressure in the fring- Bryan, P.G. 1975. Food habits, functional digestive mor- ing coral reef of Curacao, Netherlands Antilles, phology, and assimilation efficiency of the rabbit- Aquat. Bot. 5: 146. 6sh Siganus spinus Pisces, Siganidae! on Guam. von Westernhagen,H. 1973a.A preliminary study on the Pac. Sci. 29: 269-277. food preferencesof Siganus concatenata Cuvier Doty, M.S. 1980. Outplanting Eucheurna species and and Valenciennes!. The Philippine Scientist 10: Gracilaria species in the tropics. In I.A. Abbott, 61-73. M.S. Foster and L.E. Eklund eds.!. Pacific Seaweed . 1973b. The natural food of the rabbitfish Aquaculture. California Sea Grant College Pro- Siganus orarnin and S. strio/ata. Mar. Biol. 22: gram, Univ. Cal. La Jolla, California. 367-370. Hobson, E.S. 1974. Feeding relationships of teleostean Wanders, J.B.W. 1977. The role of benthic algae in the fishes on coral reefs in Kona, Hawaii. Fish. Bull. 72: shallow reef of Curacao Netherlands, Antilles!. III. 915-1031. The significanceof grazing. Aquat. Bot. 3: 357-390.