BULLETIN OF MARINE SCIENCE. 41(2): 561-575.1987

RECRUITMENT, ECOLOGY, GROWTH AND HEHA VIOR OF JUVENILE ACANTHASTER PLANCI (L.) (ECHINODERMATA: ASTEROIDEA)

Leon Zann, Jon Brodie, Christine Berryman and Milika Naqasima

ABSTRACT On Suva Reef in the Fiji Islands the refuge substratum of early juvenile A. planet «20 mm) was found to be subtidal coralline algae (Porolithon onkodes) on the windward reef front. Highly cryptic juveniles (10-30 mm maximum diameter) were found under coral blocks and rubble in the boulder zone of exposed reef fronts, on the dead bases of Acropora spp. in more sheltered areas, and in interstices on the reef crest and on the fore reef slope to depths of8 m. Recruitment, monitored over 9 years, was very low in most years (in 1985 the density of8-month-oldjuveniles was 0.004 m-2 in the boulder zone). A massive recruitment occurred in 1984 (density of 7-month-old juveniles was 8.3 m-2 in the boulder zone). Monitoring of this cohort over 2 years indicated that growth was sigmoidal. The maximum diameter in- creased by 2.6, 16.7 and 5.3 mm/month in the algal-feeding, early coral-feeding and adult phases, respectively. An epidemic caused a high mortality between 10-16 months. The diet switched from coralline algae to scleractinian corals at age 13-15 months but behavior remained cryptic. At about 20 months feeding switched from night to day and aggregative behavior began. The onset of sexual maturity commenced at 23 months. Between 26 and 28 months the population migrated into the deeper waters of the reefslope. Mortality between ages 8 and 23 months was very high (ca. 99%) and is attributed to disease, and possibly the effects of rough seas and predation. These findings indicate that recruitment is erratic and that an infestation arises from a single massive settlement.

Large feeding aggregations of the coral-eating asteroid Acanthaster planci have caused widespread damage to Pacific coral reefs during the past 25 years (Endean and Stablum, 1973; Birkeland, 1982; Moran, 1986). Infestations of adult starfish characteristically appear suddenly on a coral reef, consume much of the living coral, and then depart. Where the starfish come from has never been established. The paucity of information on the early life history is perhaps the main reason why the Acanthaster phenomenon is so poorly understood (Moran, 1986). Although A. planci has been raised in the laboratory and the larval stages and juvenile growth and behavior in captivity are well known (Henderson and Lucas, 1971; Yamaguchi, 1973; 1974; Lucas, 1982; 1984) there have been very few reports of early juveniles (< 20-mm diameter) in nature. The young of many coral reef echinoderms are rarely seen (Yamaguchi, 1973) and those of A. planci have remained elusive despite the concerted efforts of researchers. Early juveniles have been reported by Pearson and Endean (1969) in the basal branches of Acropora spp. in shallow water on the reef edge of Green Island and nearby Fitzroy Island on the Great Barrier Reef. Juveniles of 50-100 mm have occasionally been located in similar habitats (Endean and Stablum, 1973; Laxton, 1974; Moran et al., 1985). In this study we describe in detail the habitat of the juveniles and monitor recruitment over a period of 9 years. The growth, behavior and general ecology of a single cohort is traced over almost 2 years.

METHODS

Preliminary surveys of Suva Barrier Reef off Viti Levu Island in the Fiji Group in 1979 identified an isolated population of adult A. planci at the eastern end of the reef. A fixed cross-reef line transect

561 562 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

Reef Crest-exposed at low water Moated Reef Flats Port 9 I I Semi-Moated Pools SUVA ,I HARBOUR ,, Boulder Zone I Acrol2ora Rubble I I I Rubble Bank I I I I Acrol2ora dominated community I I Porites dominated I I, Coral Sand .....•.•.••.. Sea Grass

LAUCALA BAY

N1 I

1000 m

Figure 1. Suva Barrier Reef, Viti Levu Island (18"S 178°E), showing reef zonation, positions of cross- reef transects (a-g), and the major study areas (B and E). was established through the center of the aggregation in June 1979 (Fig. I, transect b). During extreme spring low tides, which enabled walking on most of the reef top, all of the conspicuous adult starfish within 0.5 m of the transect line were measured. The maximum diameter, the distance between optic cushions on opposite arm tips, was measured to the nearest centimeter. The substratum was carefully searched for cryptic individuals. Corals and other attached substrata were examined in situ while all movable boulders and rubble were removed and individually examined. Several juveniles were found under coral blocks in the boulder zone in a 35 x 50-m area about 50-m from the windward reef edge (site B, Fig. I). This site was similarly searched each year from 1980-1984 during the mid-year extreme spring tides and at monthly intervals from July 1984 to December 1986. Few juveniles were located until July 1984 when very large numbers of small juveniles 10-32 mm were found. The densities and distributions of juveniles were then ascertained by searching all substrata in 10 random l_m2 quadrats in the boulder zone at B. Searches were conducted during spring low tides where possible; during neap tides a face mask was used while sampling underwater. To determine the general distribution on the reef, seven cross-reef transects were examined. Between 1 and 4 m2 of substratum were carefully searched for the juveniles at each 15-m interval along these transects. However in habitats where there were no suitable substrata for juveniles (sand flats, seagrass beds) the intervals were extended to 30 or 50 m. A second detailed study site was established in a 50 x 100-m area of high coral cover where there was an aggregation of adult A. planci (site E, Fig. 1). Spot searches were also conducted on adjacent Joskie's, Rat-tail and Makaluva Reefs to determine the wider distribution of the juveniles. The growth of the 1984 cohort at site B was determined by measuring about 100 individuals each month between August 1984 and March 1986. Initially juveniles <40 mm were collected and measured using calipers to the nearest millimeter but as they grew larger they were measured in situ with a ruler and placed into 5-mm size classes for size frequency distributions. As previous work has indicated that the starfish could not be easily tagged (Moran, 1986), the general distribution of the population was delineated each month. Injuries, feeding activity and general behavior were also noted. Lesions on the aboral discs were found between October 1984 and April 1985; affected specimens were placed ZANN ET AL.: JUVENILE ACANTHASTER PLANCI 563

in aquaria for observations, specimens were preserved for histological examination in Bouin's fluid and formalin, and sterile samples were taken for bacterial culture. The reef-wide distribution of the 1984 cohort was again ascertained in December 1985. As they were then very conspicuous and confined to the reef crest zone the total number in a 35 x 50-m area adjoining site B was determined. A continuous 5-m-wide transect along the entire reef crest (ca. 7,500 m in length and average of 30 m in width) was conducted between 5 and 15 m from the reef edge. The population size was estimated by extrapolation to the total area of reef crest, as determined from ground studies and aerial photographs. The dispersal of the starfish in aggregations was described from photographs taken at site E at low water. In estimating the age of each cohort, it was assumed that spawning occurs in early January of each year as suggested by reports of synchronous spawning between December and February on similar latitudes on the Great Barrier Reef (Pearson and Endean, 1969) and in Fiji (Owens, 1972). As the cohort began to approach sexual maturity between July 1985 and February 1986, a sample of 10-12 starfish was dissected each month to determine the development of the caeca and gonads. These organs were weighed and indices were calculated (wt. organ/total wt. of specimen x 100). Juveniles were held in closed system aquaria between August and November 1984 for feeding and growth experiments. Two to four specimens of 13-22 mm were placed in each 100 liter aquarium. Rocks encrusted by coralline algae and a selection of corals were replaced at about weekly intervals and small dead shrimps were added several times each week as an alternative food. Diameters were measured monthly.

RESULTS General Ecology of Suva Reef -Suva Reef is a barrier reef lying between 1 and 5 km off the south west coast of Viti Levu Island. It is separated by a narrow lagoon about 10m deep from the city of Suva (population 120,000). The eastern reef has a strong estuarine influence from the Rewa River while the west is more oceanic. The sea surface temperature range is about 23-28°C while the normal salinity is 350/00, dropping after heavy rain to 10-150/00. The oceanography of the area is described by Penn, 1983. The reef is heavily gleaned and fished at a commercial and subsistence level (Zann, unpubl. data). Details of the reef zonation vary according to the degree of wave exposure at each site. Most of the reef has a high wave energy reef front because of prevailing south east trade winds but the western reef edge is more sheltered. With the exception of the uplifted western end, most of the reef flat is moated at low water. The reef zonation and dominant sessile space-holding organisms along the seven transects are given in Figure I and Table 1. The dominant groups along transect b are described in detail here. The back reef on transect b has a wide sandy lagoonal flat (250-m wide) dom- inated by species of seagrass (Syringodium sp.) and algae (Padina sp.) with a low cover of scleractinian corals (total cover ca. 5% Acropora spp., Porites spp., Po- cillopora spp.). A ridge of coral rock, dominated by soft corals (Sarcophyton sp., Nephthya sp.), separates this zone from the reef flat. Much of the reef flat (300-m wide) is moated at low water enabling a moderate development of corals (cover ca. 5- I0% Porites lobata microatolls, P. andrewsi. Acropora spp. and others). An infestation of A. planci between 1978-1982 caused a pronounced decline in the coral cover in this area. The flat is dominated by echinoderms (Echinometra mathaei. Diadema setosum, Tripneustes gratilla. Linckia laevigata, Holothuria atra, Stichopus chloronotus). The reef front (100-m wide) comprises a zone of coral rubble behind a belt of coral boulders and blocks resulting from cyclone and tsunami damage. Part of the boulder zone is moated; the upper and some of the lower surfaces of the coral blocks are encrusted by coralline algae. Sciaphilic communities dominated by encrusting bryozoans, sponges and ascidians are well developed beneath many of the blocks. Coral coverage is very low «0. 1%). The reef edge (35-m wide) is largely a coralline pavement, dominated by zoan- 564 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

Table I. Distribution and abundance (no. m-') of juvenile A. planci in cross-reef transects in Aug! Sept 1984, related to reef zone (refer to number legend). High wave energy aspects (transects a~): (I) reef front and crest, spurs and grooves, coralline algae, few corals; (2) boulder zone, exposed at low tides; (3) boulder zone, moated at low tide; (4) Acropora rubble, exposed at low tide; (5) reef flat, moated pools, sand and living corals (Acropora and Porites); (6) a1cyonarian zone; and (7) lagoon flats, sand and seagrass. Low wave energy aspects (transects f and g): (8) coral rock platform, exposed at low water; (9) eroded platform; and (-) lagoon. Note: (*) most stations where juveniles were not found are deleted for brevity

Transect

Distance (m) b d e g 0 0 (1) 0 (I) 0 (I) 0 (I) 0(1) 0(1) 0(1) 15 0 (1) 0 (1) 0 (1) 0 (I) 0(8) 0(7) 0(8) 30 0 (I) 0 (2) 0 (1) 0 (1) 0(8) 0(7) 0(7) 45 0 (2) 5.3 (2/3) 2.0 (3) 0 (1) 0(8) 0(7) 0(7) 60 0 (2) 22.8 (2/3) 4.0 (3/4) 0 (1/4) 0(9) 0(7) 0(7) 75 0 (2) 14.6 (2/3) 0 (4) 0 (5) 0(9) 0(7) 0(7) 90 0 (2) 5.5 (3) 0 (4) 1.0 (5) 16 (5) 0(7) 0(7) 105 0 (2) 1.0 (3) 0 (4) 0 (4) 0(5) 0(7) 0(7) 120 0 (2) 0.5 (4) 0 (4) 0 (4) 0(9) 0(7) 0(7) 135 4 (3) 0 (4) 0 (4) 0 (4) 0(9) 0(7) 0(7) 150* 1.2 (3) 0 (4) 0 (4) 0 (4) 0(9) 0(7) 0(7) 180* 0 (4) 0 (4) 0 (5) 1.6 (4) 0(4) 0(7) 0(8) 240* 1.2 (2/4) 0 (4) 0 (5) 0 (3) 0(4) 0(4) 0(8) 255 2 (3/4) 0 (4) 0 (5) 0 (5) 0(5) 0(4) 0(8) 345* 1 (2/4) 0 (5) 0 (5) 0 (5) 0(5) 0(4) 0(8) 360 4 (2/4) 0 (5) 0 (5) 0 (5) 0(5) 0(4) 0(8) 450* 0 (4) 0 (6) 0 (5) 0 (5) 0(5) 0(9) 0(4) 600* 0 (4) 0 (6) 0 (6) 0 (6) 0(7) 0(9) 0(4) 800* 0 (4) 0 (7) 0 (6) (-) 0(7) 0(9) (-) 900 0 (7) (-) 0 (7) (-) (-) (-) Reef width (m) 975 825 1,020 570 800 810 615 x No. juveniles (1m') 0.206 0.904 0.088 0.068 0.226 0 0 thid sheets (Palythoa spp., Zoanthus spp.), coralline algae, and corals (ca. 5-10% Montipora spp., faviids, Acropora spp.) with well developed spurs and grooves. Subtidally, there is a narrow terrace (20 m wide) dissected by surge channels. The reef slope then drops rapidly into very deep water. The reef was infested by A. planci in 1963-1967 (L. Marsh, pers. comm.) and 1968-1970 (Owens, 1972) after which the infestations apparently declined. New aggregations of A. planci were recorded by the senior author in 1979. These comprised mainly of adult starfish (x diameter = 260 mm; SD = 52; r = 140- 380; N = 159) but several juveniles were located (see below). Recruitment. - In 1979 four juveniles 60-80 mm in size were found in the boulder zone at site B in a density of about 0.02 m-2• Isolated juveniles of similar size were also located in this area in very low densities (<<0.02 m-2) between 1980- 1983. More extensive searching at monthly intervals in 1984 revealed 15juveniles 60-100 mm in size and several thousand much smaller juveniles, the average size of which was 19.9 mm in July 1984. It was assumed that the larger juveniles were the previous year's recruits (1 + yr) while the smaller ones were that year's recruits (0+ yr). The density ofthe 1+-year juveniles was 0.07 m-2 while that of the 0+- year juveniles was 20.6 m-2 in the area of greatest abundance (see Distribution and Abundances). The population dynamics of the 1984 cohort are described in this paper. In 1985 only three early juveniles (size 22-40 mm) were seen in about 700 m2 ZANN ET AL.: JUVENILE ACANTHASTER PLANCl 565

of boulder zone (i.e., a density of 0.0043 m2). No 1986 recruits were detected at site B although one small specimen (20-mm diameter) was seen on adjacent Joskie's Reef. No 1987 recruits were seen in March and April 1987. Habitat of Early Juveniles. - Most juveniles < 20 mm were found attached to the undersides of coral blocks and rubble of the boulder zone; they were most abundant in the lower recesses beneath several layers of blocks. In all cases their substrata were encrusted by coralline algae, mainly Porolithon onkodes (Heydrich) Foslie, 1909. Coralline algae was the food of early juveniles (< 10mm) raised in laboratory studies (Yamaguchi, 1973; Lucas, 1984). Some juveniles in transect a were also found beneath Acropora rubble encrusted by coralline algae; in transect e some were also found on the dead bases of living Acropora and on Acropora which had previously been preyed upon by adult starfish. Although the fissures and cracks which honeycomb the reef crest could not be excavated, larger juveniles were later located in this habitat. The subtidal reef front off the transects could not be regularly sampled because of strong wave action but several juveniles were seen off transect fin 6-8 m of water (D. Ellis, pers. comm.) indicating that their distribution extended subtidally, at least in this area. In all habitats juveniles <20 mm were confined to areas which remained permanently submerged at low tide. During these searches juveniles of other echinoderms were also discovered under coral blocks and rubble in the boulder zone. These included the echinoids Diadema sp. (3-5-mm test diameter), Echinothrix calamaris (5 mm), Echinometra mathaei (5-7 mm), and Phyllacanthus imperialis (5-10 mm); the asteroid Linckia multifora (10-15-mm diameter); and at least three Holothuria spp. (5-15-mm length), one of which was present in very high densities (up to 50 m-2). As the adult spicules had not formed, further identification of the holothurians was not possible (R. A. Birtles, pers. comm.). Juveniles of the gastropod Trochus niloticus (3-10 mm diameter) were also found in this area. Adults of the gastropod Astralium calcar shared the habitat of early juvenile A. planci. Description of Juveniles. - Only the smallest juveniles (10-13 mm) were still add- ing arms in July 1984. The mean number of arms of individuals of 10-20 mm was 14.33 (SO = 1.05; r = 11-16; N = 82), not significantly different from the mean of 14.58 arms (SO = 0.96; r = 12-17; N = 82) of this cohort at maturity in December 1985. Specimens < 15 mm were generally uniformly pink in color while those > 15 mm had a bull's-eye pattern of four alternating light and dark bands, described by Yamaguchi (1974) as the "juvenile ring." The juvenile color gradually darkened as they approached maturity and commonly became a drab olive in the adult but the juvenile ring was frequently retained. About 60% ofa sub-sample (N = 98) of 15-35-mmjuveniles were darkly shaded on the aboral disc and 40% were light. Their oral discs were either pink (66%) or white (34%); the pink shading was due to red spines surrounding the mouth and ambulacral grooves. The aboral spines were small and their points were dull; they probably afford little protection as juveniles <50 mm could be handled without InJury. Distribution and Abundances. - The density of early juveniles at the center of the moated boulder zone at site B in August 1984 was estimated to be 20.6 m-2 (SD = 6.2; r = 0-28; N = 10). In September 1984 the O+-year recruits were found on five of the seven cross-reef transects (Table 1). They were most abundant in the 566 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

boulder zone near site B; the mean density in this area was 8.8 m-2 (SO = 9.5; r = 0-30; N = 17). Sixteen months later in December 1985 the density of the 1+-year starfish in the 35 x 50-m area of reef crest adjacent to the boulder zone at site B was 0.06 m-2 (SO = 0.05; r = 0-0.3; N = 455). In September 1984 the O+-year juveniles were initially found in only one station at site E but in December 1985 the 1+-year individuals were most abundant in this area; in areas of aggregations, densities of 3.3 m-2 (SO = 4.5; r = 0-20; N = 45) were recorded. The average density along the windward reefcrest in December 1985 was 0.067 m-2 (from the eastern end of reef to intercept with transect a: 0.08; a to b: 0.08; b to c: 0.04; c to d: 0.004; d to e: 0.04; e to f: 0.17). As the starfish were confined to this zone (area 7,500 x 30 m), the total number of the 1984 cohort remaining on Suva Reef was estimated to be about 15,000. Diet. -In August and September 1984 the O+-year juveniles found along transects a-d were all on encrusting coralline algae, mainly Porolithon onkodes. White feeding scars were evident on the Porolithon; on rubble with high densities of juveniles a high proportion of the algae had been consumed. In transect e which intercepted an area of 100% Acropora, several juveniles of 25-40 mm were on the bases of living corals. Living coral cover was very low in the boulder zone on B; this was a natural characteristic of the zone, but the cover was reduced even further by adult A. planci predation in 1979-1982. When algal-feeding juveniles were offered corals in the aquarium most began feeding immediately; species of Acropora, Pavona, Hydonophora, and Poci!lopora (minus commensals) were eaten. Juveniles in site B did not begin feeding on corals until February 1985 when about 30% of the monthly sample were found on corals. Many of the corals upon which they were feeding had been recently deposited into the boulder zone by tropical cyclone Eric and two successive smaller cyclones in January 1985. Twenty juveniles were found on a single piece of Acropora. In June 1985 virtually all the 1984 cohort were found associated with corals, either hidden near a fresh feeding scar or in the bases of corals. However the starfish remained opportunistic feeders; in December 1985 20% of a sample of sexually mature starfish (N = 25) were found to have their stomachs everted on non-coral substrata. Age and Growth. -Based on the assumption of a January spawning, the age of the O+-year juveniles (x = 19.5 mm) when they were first discovered in July 1984 was assumed to be 7 months. Assuming a linear growth rate, the average growth rate in this period would be 2.8 mm/month. Monthly size-frequency distribution histograms are given in Figure 2. The growth curve was sigmoidal (Fig. 3) with the initial growth rate averaging 2.6 mm/month, approximating that previously estimated for the months prior to discovery. Growth of six juveniles held in aquaria on a diet of algae and shrimps increased from a mean of 19.4 mm to 28.7 mm between ages 7-10 months and averaged 3.6 mm/month (SD = 0.37). Rapid growth averaging 16.7 mm/month occurred during the first 5 months after the switch in diet from algae to corals (February to June 1985). Somejuveniles continued to feed on algae during this period and growth rates varied greatly as illustrated by the wide size ranges and standard deviations in Figure 3. The slow growth of many individuals is attributed to the low coral cover at site B and to a disease which affected the population between October 1984 to April 1985 (see Mortality). Growth rates declined to an average of 5.3 mm/month after August 1985. The growth of A. planci which recruited to site B, an area of low ZANN ET AL.: JUVENILE ACANTHASTER PLANCl 567

10..~ 5 o 15 15

10 21 8 84 N-198 10

__ 1983,.c;.u.t$ o _ " o I5 15

'0 10 5 oUl o 15 15

10 H 10 84 N-161 10

o o 15 15

10 '2- 11 84 N-l01 .0

"'---- ... o o ------r 15 :~LL '0 o 15 15 :HI '2 8S N-88 '0 10 9/12 86 N-149

"" ..•....• ------. , ' 1985-r.Cf~'1I o o i- -' _l,-'/ 1015LJ 2ll 3· 85 '--,--NOon 1015~ 5 : J~.I.j. ~ " ...L 'II.. I ''-'-- -,---.--. o o 20 40 60 80 100 120 '''~140 160_' Hio o 20 40 SIZe Class (diameter nlOlI Figure 2. Size-frequency distributions of the 1984 A. p/anci cohort at site B, Suva Reef. The date and size of each sample is indicated. Note I-mm size classes (dark) and 5-mm classes (shaded) as average size increases. The previous year's recruits (1983) and following year's recruits (1985) are circled. Mean size and confidence levels of these data shown in Figure 3. coral cover «0.1 %), was slower than those at E, an area of high cover (ca. 10- 40%). Table 2 compares growth rates of the 1984 cohort in different areas. A logistic growth equation was fitted to these data following the method de- scribed by Yamaguchi (1975) and used for A. planci by Lucas (1984). A least-square linear regression was calculated (where t is in months):

(Lt+1 - Lt)/Lt+1 = 1 - e-k + Lt(e-k - l)/Loo

= 0.15112 - 0.0007489L1 (correlation coefficient = 0.579) Loo= 202 mm, k=0.164 The fitted logistic growth equation is: Lt = 202(1 + 23.4e-O.164ttl where the value - 23.4 for b was determined by using the middle value of the size/age series, 77.2 mm at 16.3 months age.

b = (Lt - Loo)ekt/Lt b = (77.2 - 202)e-O.164xI6.3/77.2

Table 3 and Figure 3 compare the observed growth curve for the 1984 cohort with those of laboratory raised juveniles (Yamaguchi, 1973; Lucas, 1984), juve- niles found on the Great Barrier Reef by various workers, and a growth curve derived from assumed size/age modes by Kenchington, 1977. 568 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

200 15 156

134 180 107 29 26 117 7' 160 73

140 /

120 " ~ '0 100 E g :: Cii 80

60

40

20 (D).•.. .•..A) 0 0 1 4 6 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Presumed Age {months)

280 260 240 220 Q; 200 a; 180 E •• 160 '0 140

~ 120

Ql 100 ~ 80 60 40 20 o o 2 4 6 8 10 12 14 16 182022 24 2628 o 2 4 6 8 10 12 14 16 18 2022 2426 Presumed Age (months) Presumed Age (monthsl Figure 3. Growth of A. planci cohort, Suva Reef, 1984-1986. Sample size, mean diameter (point), standard deviation, range, growth curve fitted by eye (bold) and plot of growth equation (dashed line) are indicated. Major events include: (A) proposed time of settlement; (B) commencement of rapid growth as diet begins to change from algae to coral (tropical cyclone Eric prevented sampling in January 1985); (C) change from cryptic behavior to daytime feeding; (D) onset of sexual maturity and active migration. Bar illustrates diet (coralline algae, white; coral, black). Below, left. Comparison with growth curves from laboratory and other studies: (I) juveniles raised in the laboratory by Yamaguchi, 1974 (means of 7 individuals); (2) juveniles raised by Lucas, 1984 (means of 2-9 individuals); (3) growth curve proposed by Kenchington, 1977, derived from progression of proposed age/size modes. Suva cohort: (4) plot of growth equation; (5) line of best fit (bold). Right. Sizes of juveniles reported from the Great Barrier Reef (details, Table 3) compared with the Fijian juveniles (means and upper and ZANN ET AL.: JUVENILE ACANTHASTER PLANC/ 569

Table 2. Comparison of mean size of 1984 cohort in different habitats (Dec 1985; est. age 23 months)

Locality Size (mm) Habitat details

Suva Reef site B x = 140 (SO = 17.6; initially boulder zone (very low coral cover, r = 110-183; N = 132) <0.1 %), migrating to reef crest and edge (coral cover 5-10%) Suva Reef site E x = 165 (SO = 20.8; initially bases of live Acropora (coral cover r = 130-200; N = 52) 100%), migrating to reef crest and edge (coral cover 20-30%) Makaluva Reef x = 163 (SO = 22.4; early habitat unknown, recorded from reef r = 130-250; N = 23) edge and flat (coral cover 10-30%)

Onset of Sexual Maturity.-Gonads began to develop in October 1985 (age 21 months) in starfish> 120 mm (Fig. 4). By December 1985 (age 23 months) over 50% of the sample had acquired gonads. The pyloric caeca index was monitored monthly as an indicator of reproductive energy storage but although indices os- cillated between 6.9-9.1 there was no apparent relationship with gonad condition. Mortality. -Mortality between the ages of 8 and 23 months at site B, estimated from the initial average density in the boulder zone (8.8 m2) and the densities 2 of the survivors on the reef crest (0.06 m- ), was 99.3%. An epidemic affected the juveniles between October 1984-April 1985. An av- erage of 10% of the individuals sampled each month had necrotic lesions in the center of their aboral discs; others showed sub-clinical symptoms such as irregular central discs, drooping spines and a translucent body wall when held to a bright light. Individuals affected in the aquarium died within 3-6 days of developing the external symptoms. A number of undescribed bacteria and parasites have been isolated from these specimens (D. Sutton and J. Glazebrook, pers. comm.). Details of the epidemic will be presented in a future publication. No predation was witnessed in the field although 13% of juveniles examined (N = 800) showed some signs of sub-lethal predation (missing arms, damaged oral discs and irregular growth); none had any massive injuries which might result in death. In the aquarium a spiny lobster Panulirus penicillatus regularly consumed 30-40-mm juveniles and although hermit crabs were seen attacking juveniles no mortalities were recorded. As the juvenile refuge substratum was physically dis- turbed by cyclone Eric it is possible that heavy seas also contributed to mortality. Behavior. -Small juveniles were very cryptic. About 0.1% of 7- and 8-month-old juveniles (N = 1,200) and 1.25% of 10-month-oldjuveniles (N = 160) were found in the open away from cover. All others were found under coral blocks and rubble, generally in the lowest recesses which still had a cover of Porolithon. Almost all (142 of a sample of 148) early juveniles were found attached to the undersurfaces of blocks and rubble. They were negatively phototactic in aquaria, preferring

~ lower size ranges plotted). Ages are estimated from an assumed January spawning. Mean diameters and ranges are indicated. (1) Green Island, January and February 1967, and (2) Fitzroy Island, February 1969 (Pearson and Endean, 1969). (3) Pelorus Island, April 1986 (B. Kettle, pers. comm.). (4) Rib Reef, May 1986 (R. Bell, pers. comm.). (5) John Brewer Reef, May 1986 (R. Bell, pers. comm.). (6) Nathan Reef, September 1969 (Laxton, 1974). (7) Slashers No.4, January 1971 (Endean and Stablum, 1973). 570 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

Table 3. Estimated age/size of A. planci juveniles, Great Barrier Reef (from various sources). Age estimates based on growth rates of 1984 cohort, Fiji, and a January spawning (*authors' estimate incorrect)

Est. age Locality (date) Mean size (mm) (range-No.) (months) Habitat details (source) Green Is. 34.7 2-3* bases of live coral, mainly Acropora (Jan/Feb 1967) (r = 11-69; N = 46) 13 echinata; 2-6 m of water (Pearson and Endean, 1969) Fitzroy Is. 33.8 2-3* in 500 m2 of reef, mainly in A. echi- (Feb 1969) (r = 15-79; N = 142) 13 nata; 2-3 m of water (Pearson and Endean, 1969) Slashers Rf 109 23 SE reef crest (Endean and Stablum, (Jan 1971) (r = 70-150; N = 102) 1973) Trunk Rf (not given) 23 SW reef crest (Endean and Stablum, (Dec 1969) (r = 80-160; N = 36) 1973) Slashers & ca. 110-120 20 windward edge, shallow water (3 m) Lodestone Rfs (r = 80-160; N = 36) (Laxton, 1974) (July/Aug 1969) Nathan Rf 120 21 exposed coral patches behind main (Sept 1969) (r = 40-160; N = 323) reef (Laxton, 1974) John Brewer Rf ca. 100 21 E reef crest shallow water (Moran et (Sept 1984) (N = ca. 50) al., 1985) Pelorus Is. 77.4 16 bases of live Acropora, reef edge (B. (Apr 1986) (r = 35-152; N = 44) Kettle, pers. comm.) Rib Rf 57 17 under coral rocks and rubble, low liv- (May 1986) (r = 30-80; N = 51) ing coral, reef edge to 10 m (R. Bell, pers. comm.) Grub Rf 140 19 bases of live Acropora. shallow water (July 1986) (r = 90-210; N = 24) (to 5 m), high coral cover, on coral patches behind reef (Zann, unpubl. data)

shaded surfaces. Although no nighttime observations were conducted in the field, spot checks of aquarium held individuals suggested that they were more active at night. Small juveniles were capable of only slow locomotion and showed no escape reaction when their rock substrata were overturned in air. When rocks were overturned in water many rapidly detached; these either fell back into the recesses of the boulders or were carried away by wave surge. Although their distribution in the boulder zone was non-random (i.e., they were distributed under blocks with Porolithon and not on those with encrusting scia- philic bryozoa, sponges, ascidians, etc.) they were not aggregated on their preferred substrata and were seldom in contact with each other. The cryptic behavior continued during the early coral-feeding phase (age 13- 18 months). Although feeding scars were conspicuous the juveniles responsible were always well hidden and it was assumed that feeding occurred mainly at night. A marked change in behavior occurred between 16-19 months when they began to prey openly on coral in the daytime and aggregate into clumps in those areas where they were most abundant. By 23 months about 90% of the sample (N = 134) was located in the open. Where 23-month-old starfish were present in low densities (site B, about 0.06 m2) most were sparsely dispersed on their preferred substrata with several meters ZANN ET AL.: JUVENILE ACANTHASTER PLANCI 571

9 o

o 8 ,., I , I ,

7 I. '. -' '.', / 0' 6 ,/ I • I '. 0 X 16 17 18 19 20 21 22 23 24 25 26 UJ o 5 Age (months) 0 ~ «0 0 Z4 0 • C) 0 • 3 0 0

.0 2 • o • • • 0 ·0 • o • • a 50 100 • 150 200 DIAMETER (mm) Figure 4. Onset of sexual maturity in 1984 cohort. Gonad indices of 10 starfish per month. June to September 1985 (age 17-20 months): no gonads. Open circle: October (21 months). Dark circle: November (22 months). Open square: December (23 months). Dark triangle: January 1986 (24 months). Asterisk: February (25 months). Inset: mean gonad index for each month.

between neighboring starfish. Where they were present in high densities (site E, ca. 1.2 m2) they were markedly aggregated. In ten 15-m2 areas surveyed at site E, 2% of starfish were> 5 m apart; 10% were 1-5 m apart; 24% were 0-1 m apart; 42% were touching armtips; and 22% were clumped in piles (N = 209). Migration. - The center of greatest concentration of the population at site B was noted during each monthly sampling. The population of 6-9-month-old juveniles was static but at 10-11 months there was a marked shift when it moved 5-10 m through the boulder zone towards the windward reef edge. This area of reef crest dried at spring low tides indicating an increasing ability to withstand desiccation. The shift towards the windward reef edge continued; at 19 months most had left the shelter of the boulder zone and were preying on sparse corals (ca. 5% cover) on the reef crest. At this time they had moved only 30-50 m from the area in which they were first located. By 23 months the population was moving relatively rapidly across the reef crest (ca. 3-5 m/month). At site E they were moving, often armtip-to-armtip, in a ragged front several hundred meters in length, leaving a trail of recently dead corals behind. At 24 months there were notably fewer starfish on the reef crest 572 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987 and at 25 months only 15 were located along 800 m of reef crest. At 26 months none could be found on the reef top for growth sampling. During the rapid migration across the reef crest the direction of movement was into the prevailing current.

DISCUSSION These findings indicate that reefs are initially infested by A. planci as a result of larval recruitment rather than migration of adults and that this recruitment is discontinuous in both space and time. The early juvenile stages have been rarely reported because of their very cryptic habitats and coloration, the difficulty in searching high wave energy reef fronts, and because they are very uncommon in most years. A major settlement occurred in only 1 year (1984) of 9 years monitored (1979- 1987). Even after the identification of the juvenile refuge substratum in 1984, and despite intensive monthly searches over the next 2 years, few 1985 recruits and no 1986 recruits were found. The general low recruitment (0.004 m-2 in 1985) is probably the "normal" situation which results in the low densities of adults generally seen on reefs (approximately 6 km-2 of reef: Endean, 1974). The massive recruitment of 1984 (averaging 8.8 m-2 of habitat) was three orders of magnitude greater than in the other years. This cohort grew to maturity in the vicinity of the area where they probably first recruited, and sufficient survived to form one of the well known "outbreaks" which have been reported many times over the past 20 years. As suggested by Kenchington (1977), an initial outbreak therefore consists of a single cohort of starfish although in its later stages it may include subsequent years' recruits (Moran et aI., 1985). Echinoderms may vary greatly in reproductive success, both temporally and spatially (Yamaguchi, 1973; Ebert, 1983). For example, Loosanoff (1964) found that the number of early juvenile Asterias forbesi recruiting each year varied by four orders of magnitude over a 16-year period. The refuge substratum of early A. planci juveniles was subtidal coralline alga Porolithon onkodes on the windward reef edge. Juveniles were found on the un- dersides of coral blocks and rubble in the moated boulder zone, on the bases of living and dead Acropora on the reef edge and in the interstices of the reef crest and front, to depths of at least 8 m. The reef edge habitat suggests that the settling brachiolaria either selectively settle into this area (the first part of the reef they might encounter) or they settle more indiscriminately and there is differential survival in suitable reef-front habitats (Ebert, 1983). The boulder zone was also found to be the refuge substratum of other species of echinoderms (Diadema sp., Echinothrix calamaris, Phyllacanthius imperialis, Linckia multifora, Holothuria spp.). The gastropod Astralium calcar which was common in the areas where early juveniles were located may be an indicator of the potential habitat ofjuvenile A. planci. The major events in the development of the cohort after their discovery at an age of about 7 months included an initial period of slow growth on a diet of coralline algae (age 7-13 months); high mortality due to disease (9-16 months); a series of cyclones which disturbed their habitat and probably caused some mortality (13 months); a switch to a diet of coral (13-16 months) and a period of rapid growth (13-18 months). A major behavioral change occurred when they switched from nocturnal to daytime feeding (20 months), they began to aggregate (23 months), and actively migrate over the reef crest into deep water (25 months). The observed growth of the 1984 cohort was sigmoidal. Growth averaged 2.6 ZANN ET AL.: JUVENILE ACANTHASTER PLANCl 573 mm/month in the algal-feeding phase, 16.7 mm/month in the cryptic coral-feeding phase, and 5.3 mm/month in the adult phase. Growth rates of the early juveniles were intermediate between the rates of the laboratory reared juveniles of Ya- maguchi (1973) and Lucas (1984) (Fig. 3). The different rates reported in the laboratory studies were attributed to differences in temperatures (Lucas, 1984). The switch to coral diet occurred later than in the laboratory raised starfish (13 months, cf. 6 months) but as 8-month-oldjuveniles accepted coral in the aquarium it is likely that the paucity of coral in the boulder zone retarded the shift in diet. Low coral cover also retarded growth in the coral-feeding phase as individuals which recruited to parts ofthe reef with a higher coral cover were larger. Mortality was probably higher in areas of low coral cover. The decline in the growth rate which occurred as the population approached maturity took place at an earlier age and smaller size than that seen in the lab- oratory by Lucas, 1984 (i.e., 18 months, cf. 28 months). Whereas growth in the laboratory was determinate (Lucas, 1984), the steady growth which continued after 20 months would suggest that it is indeterminate in the field, as suggested by Kenchington (1977). It is likely that the conditions in which the laboratory starfish were raised represented an optimal situation (i.e., abundance of food, sheltered waters, no predation) while the expenditure of energy on searching for food, active migration and on reproductive effort may result in a slower growth rate in nature. Assuming an adult growth rate of 4.5 mm/month, the average rate between 18- 26 months, adults measured in another aggregation on Suva Reef (x = 270 mm) are estimated to be about 50 months old and the largest individual (380 mm) would be over 70 months old. Many of the starfish raised by Lucas (1984) died of apparent senility between 60-90 months. From studies of caged and aquarium held individuals, Pearson and Endean (1969) estimated that coral-feeding juveniles grew by 11 mm/month and adults grew by 9-14 mm/month. Early growth was considered to be very rapid as they found 30-mm juveniles only 2 months after the spawning period. However, as suggested by Lucas (1984), these juveniles were certainly in their second year and not in their first. As 15-month-old individuals they closely fit the observed growth curve of the 1984 cohort. The assumed age/size intercepts of other previously reported populations of juveniles and those recently located on the Great Barrier Reef also closely fit the growth curve of the 1984 cohort. The early growth rate estimated from modal information by Kenchington (1977) is far higher than the observed growth rate as it was based on the erroneous estimates of age of Pearson and Endean (1969) and Endean and Stablum (1973). The use of modal progression for growth estimates of A. planci is considered dubious because of the great variation in growth rates seen in this study. The high mortality of the 1984 cohort (ca. 99% between ages 8-23 months) is attributed mainly to disease which affected about 10% of the monthly samples between the ages of 10-16 months. Little is known of the diseases of echinoderms although there have been recent reports of mass mortalities in echinoids in Nova Scotia (Miller and Colodey, 1983) and in the Caribbean (Hunte et aI., 1986). Because of the potential of such a disease to the biological control of A. planci, detailed studies are currently underway on the identity of the pathogens and their effects (J. Glazebrook and D. Sutton, pers. comm.). Although about 13% of the population showed signs of generally minor sub-lethal predation, the lack of major injuries suggests that predation may not be an important source of mortality in the juvenile phase. The very high incidence of early juveniles in 1 year of 9, 1984, implies that an 574 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987 unusually high settlement of larvae took place in that year and that either the annual spawning success of the adults, the survivorship of the planktonic larvae, and/or the settlement success of the larvae is variable. These findings add some support to the "juvenile recruitment" hypothesis advanced by various workers (see Potts, 1981). This proposes that larval survival is enhanced by unusual combinations oflowered salinity and raised temperatures (Lucas, 1973), and/or increased nutrients from terrestrial run-off following un- usually high rainfall (Birkeland, 1982). Our findings disprove the "adult aggre- gation" hypothesis of Dana et al. (1972) which proposes that infestations result from aggregations of adults already present in low densities on a reef. Although disease was found to be a major cause of mortality in the 1984 cohort there was no evidence oflarge scale predation and the assumption of the "predator removal" hypothesis (Endean, 1974) that outbreaks occur as a result of over fishing ofnatural predators of the starfish is neither supported nor disproved by our observations.

ACKNOWLEDGMENTS

We are grateful to all who assisted in the sampling, especially F. Manueli, R. Thaggard, H. Haq, S. Maluafenua, and G. Brodie. The field work was partially funded by the Great Barrier Reef Marine Park Authority and the University of the South Pacific made available facilities. Professor D. Ellis, B. Kettle and R. Bell made available unpublished data. R. Birtles identified the juvenile echinoderms and J. Chisolm identified the Porolithon. Dr. W. Craik, E. Eager and 1. Dartnall proof-read the manuscript. We are especially grateful to Dr. J. S. Lucas for his inspiration, enthusiasm and assistance at all stages of the program, and for analyzing the growth data.

LITERATURE CITED

Birkeland, C. 1982. Terrestrial run off as a cause of outbreaks of Acanthaster planci (Echinodermata; Asteroidea). Mar. BioI. 69: 78-185. Dana, T. F., W. A. Newman and E. W. Fager. 1972. Acanthasteraggregations: interpreted as primarily responses to natural phenomena. Pacif. Sci. 26: 355-372. Ebert, T. A. 1983. Recruitment in echinoderms. Pages 169-203 in M. Jangoux and J. M. Lawrence, eds. Echinoderm studies, Vol. I. Balkema, Rotterdam. Endean, R. 1974. Acanthaster planci on the Great Barrier Reef. Proc. 2nd Int. Coral ReefSymp. I: 563-576. -- and W. Stablum. 1973. A study of some aspects of the crown-of-thorns starfish (Acanthaster planci) infestations of reefs of Australia's Great Barrier Reef. Atoll Res. Bull. 167: 1-62. Henderson, J. A. and J. S. Lucas. 1971. Larval development and metamorphosis of Acanthaster planci (Asteroidea). Nature 232: 655-657. Hunte, W., I. Cote and T. Tomascik. 1986. On the dynamics of the mass mortality of Diadema antillarum in Barbados. Coral Reefs 4: 135-139. Kenchington, R. A. 1977. Growth and recruitment of Acanthaster planci (L) on the Great Barrier Reef. BioI. Conserv. 11: 103-118. Laxton, 1. H. 1974. Aspects of the ecology of the coral-eating starfish Acanthaster planci. BioI. J. Linn. Soc. 6: 19-45. Loosanoff, V. L. 1964. Variation in time and intensity of settling of the starfish, Asterias forbesi, in Long Island Sound during a twenty-five year period. BioI. Bull. 126: 423-439. Lucas, J. S. 1973. Reproductive and larval biology of Acanthaster planci (L.) in Great Barrier Reef waters. Micronesica 9: 197-203. --. 1982. Quantitative studies of feeding and nutrition during larval development of the coral reef asteroid Acanthaster planci (L.). J. Exp. Mar. BioI. Ecol. 65: 173-194. --. 1984. Growth, maturation and effects of diet in Acanthaster planci (L.) (Asteroidea) and hybrids reared in the laboratory. J. Exp. Mar. BioI. Ecol. 19: 129-148. Miller, R. J. and A. G. Colodey. 1983. Wide-spread mass mortalities of the green sea urchin in Nova Scotia, Canada. Mar. BioI. 78: 153-164. Moran, P. J. 1986. The Acanthaster phenomenon. Oceanogr. Mar. BioI. Ann. Rev. 24: 379-480. --, R. H. Bradbury and R. E. Reichelt. 1985. Mesoscale studies of the crown-of-thorns/coral interaction: a case history from the Great Barrier Reef. Proc. 5th Inter. Coral Reef Congress Tahiti 5: 321-326. ZANNETAL.:JUVENILEACANTHASTER PLANCI 575

Owens, D. 1972. Acanthaster pland starfish in Fiji. Survey of incidence and biological study. Fiji Agric. J. 33: 15-23. Pearson, R. G. and R. Endean. 1969. A preliminary study of the coral predator Acanthaster planci (L) (Asteroidea) on the Great Barrier Reef. Qld. Dept. Harbours Marine, Fish Notes 3(1): 27-55. Penn, N. 1983. The environmental consequences and management of coral sand dredging in the Suva region, Fiji. Ph.D. Thesis, University of Wales, Wales. 252 pp. Potts, D. C. 1981. Crown of thorns starfish-man-induced pest or natural phenomenon? Pages 55- 83 in R. L. Kitching and R. E. Jones, eds. The ecology of pests. CSIRO, Melbourne. Yamaguchi, M. 1973. Early life histories of coral-reef asteroids with special reference to Acanthaster planci (L). Pages 369-387 in O. A. Jones and R. Endean, eds. Biology and geology of coral reefs, 2, Vol. II. Academic Press, New York. ---. 1974. Effect of elevated temperature on the metabolic activity of the coral reef asteroid Acanthaster pland (L). Pacif. Sci. 28: 139-146. ---. 1975. Estimating growth parameters from growth rate data. Oecologia 20: 321-332.

DATEACCEPTED: January 9, 1987.

ADDRESSES:(L.2., J.B., C.B., M.N.) University of the South Pacific, Box 1168, Suva, Fiji; PRESENT ADDRESS:(L.2.) Great Barrier Reef Marine Park A uthority, Box 1379, Townsville, Qld. 4810, Australia.