Coral Reefs (2004) 23: 493504 DOI 10.

1007/s00338-004-0427-5

R EP O RT

James P. Gilmour

Size-structures of populations of the mushroom coral Fungia fungites : the role of disturbance

Received: 9 May 2003 / Accepted: 11 April 2004 / Published online: 9 September 2004 Springer-Verlag 2004

Abstract Changes in the size-structure of populations of the mushroom coral Fungia fungites were quantied at two reefs during four annual surveys. Exposure to disturbance was predicted to aect the size and frequency of life history stages of polyps at each reef and their variability through time. The Mainland reef experienced frequent and intense disturbances, primarily as exposure to cyclones and substantial sedimentation, which were comparatively absent from the East Lewis reef. Disturbance to the Mainland reef was evident in the smaller size of polyps, and the many parent polyps, asexual buds, and polyp skeletons, which were all absent from the East Lewis reef. Over three years, the number and area cover of polyps at the Mainland reef decreased to 9% and 3% of their initial values respectively, compared with 73% and 36% at East Lewis. The size-structure of polyps at East Lewis remained comparatively stable; whereas, the abundance of all life history stages at the Mainland reef had high but variable rates of decline each year. Changes in the size-structure of polyps at the Mainland reef indicated it was exposed to levels of disturbance that it had not experienced, and would not recover from, for many years. Keywords Coral Cyclone Sedimentation Size-frequency distributions Fungiid Dampier Archipelago

Introduction
Coral reefs and disturbance Coral reefs are exposed to periods of environmental stability and disturbance (Connell 1997; Jackson et al. 2001; Perry 2001). Disturbances vary in space, time, and intensity, and because there is often a complex interplay between disturbances that act at both an individual and population level, it can be dicult to isolate the eects of a single event (Karlson and Hurd 1993; Connell et al. 1997; Hughes and Connell 1999; Nystrom et al. 2000). However, it is possible to identify populations that are exposed to comparatively high levels of disturbance, often because they are aected by multiple stresses (e.g., Loya 1976; Dayton et al.1992; Hughes 1994; Meesters et al. 2001). The levels of disturbance to which corals are exposed inuence their life history traits, such as their rates of recruitment and survival, and this is evident in their size-frequency distributions (Fadlallah 1983; Sebens 1983; Ebert et al. 1993; Bak and Meesters 1998). Size-structure analysis of coral populations Size-frequency distributions provide insights into the eects of disturbance on the population dynamics of corals because their life history traits are strongly inuenced by size (Hughes and Jackson 1980; Babcock 1991; Bak and Meesters 1998). Size-frequency distributions vary according to the species of coral and the type, severity, and frequency of disturbances to which they have been exposed. For example, storms and cyclones generally reduce the proportion of large branching corals via fragmentation, but can have less eect on massive and encrusting corals (e.g. Woodley et al. 1981; Hughes 1989; Van Woesik et al. 1995). Conversely, predation by crown of thorns starsh reduced the proportion of large massive corals, but had little eect on the size-structure of branching and soft

Communicated by: Ecological Editor P.F. Sale J. P. Gilmour Department of Zoology, University of Western Australia, 35 Stirling Hwy., 6009 Crawley, Australia E-mail: jgilmour@aims.gov.au Tel.: +61-8-94334440 Fax: +61-8-94334443 Present address: The Australian Institute of Marine Science, Po Box 83, 6959 Fremantle, Western Australia, Australia

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corals (Fabricius 1997; Fong and Glynn 1998). In these examples, disturbance reduced the proportion of individuals in large size classes; whereas, in coral communities exposed to anthropogenic disturbances there was a species-specic reduction in the proportion of individuals in small size classes, due to their higher mortalities and reduced sexual recruitment (Bak and Meesters 1998; Meesters et al. 2001). Dierent disturbances will have a variable eect on the size-structure of dierent species of corals, which will also be confounded by their histories of exposure (Hughes 1989). Consequently, a single size-frequency distribution represents a snapshot in time that may be misleading, so inferring the eects of disturbance is more reliable when changes in population size-structure and habitat conditions are documented concurrently over time. Recensusing a population through time provides stronger links between changes in size-structure and the eects of disturbance, which are not always immediately evident. The eect of coral bleaching may not be evident in the reduced size (injury) of Porites sp. until months later (Baird and Marshall 2002), while an initial increase in the proportion of small size classes of branching corals following a cyclone will be reversed if the fragments do not survive (Knowlton et al. 1981). In addition to recensusing a population through time, a better understanding of how disturbances cause changes in size-structure can be obtained by dividing the population among relevant life history stages. Life history stages respond dierently to changes in their habitat (Werner 1988), and this response may be independent of size. An increased proportion of smaller size classes following a storm may include attached colonies that were injured and the resulting fragments. Quantifying changes in the proportion of colonies and fragments will provide a relative indication of their mortality rates, and a greater insight into population dynamics. Distinguishing between life history stages is particularly important for sexual and asexual recruits because they have dierent life history traits (Caswell 1989). The frequency of sexual and asexual recruits will vary differently with disturbance, which will have very dierent consequences for population dynamics. Quantifying changes in the size and frequency of life history stages of corals, in response to dierent types and levels of disturbance, can provide much greater insights into population dynamics than a single size-frequency distribution alone. Size-structure analysis of populations of the mushroom coral Fungia fungites Size-structure analysis is best applied to corals whose size is easily measured and whose life cycle can be divided among recognisable stages. The mushroom coral Fungia fungites is a solitary coral with almost-circular polyps, so size can be measured as maximum diameter.

The life cycle of F. fungites can be divided among four main life history stages that are easily recognised: sexual recruits; free-living polyps; parent polyps; and asexual recruits (buds). Sexual recruits are generated after the synchronous spawning of gametes by polyps of separate sexes, and are attached to the substrata via a stalk (Hoeksema 1989; Chadwick-Furman and Loya 1992; Gilmour 2002 a). Sexual recruits grow and detach from their stalk to become free-living polyps, which grow and become sexually mature. Injury to free-living polyps causes the loss of some or all of their living tissue. Injured polyps may become parent polyps if the tissue remaining on their skeleton retracts into the spaces between the septal teeth and costal spines and emerges months later as asexual buds (Boschma 1923; Kramarsky-Winter and Loya 1996; Gilmour 2002 a, b, Gilmour, this issue). The genetically identical asexual buds are attached to the skeleton of the parent polyp by a stalk, and grow and detach from their stalks to become freeliving polyps. Fungiid corals have additional life-history stages, but these are unnecessary for describing the size-structure of Fungia fungites in this study. Additional polyps may regrow from the stalks of sexual and asexual recruits, but the frequency of regrowth can be low (ChadwickFurman et al. 2000), and over two years there was no regrowth from the stalks of 37 sexual recruits, or the many stalks of asexual recruits attached to 34 parent polyps. Additionally, I did not include as a life history stage injured free-living polyps that had both visible tissue on their skeleton and asexual buds in a region of injury, because they occurred rarely (11 compared with 156 parent and 962 free-living polyps) and because an injury usually spread quickly (<6 mo) to the entire surface of the polyp before the buds could emerge (Gilmour 2002 b). Exposure to disturbances, such as storms and sedimentation, should have predictable eects on the size and frequency of sexual recruits, free-living polyps, parent polyps, and asexual recruits. Storms and sedimentation are likely to reduce the maximum size of all stages by increasing rates of injury and mortality, and storm surges will cause sexual and asexual recruits to detach at a smaller size. Disturbances are also likely to decrease the number of free-living polyps and the recruitment of sexual larvae, while increasing the number of asexual recruits and parent polyps. To investigate the extent to which disturbances structure populations of Fungia fungites, two nearby reefs were chosen that clearly diered in their exposure to seasonal storms and levels of sedimentation. The size and frequency of life history stages of polyps was quantied at each reef during four annual censuses, while at the same time their exposure to cyclones, winds, and sedimentation was quantied. Changes in size-structure were correlated with levels of disturbance, leading to inferences about the exposure of each population to disturbance prior to the rst census, and the population dynamics of Fungia fungites.

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>32C, and maximum water temperatures coupled with high light intensities have caused recurrent episodes of coral bleaching (Ford 1985; Simpson 1988; Pearce 2003). Summer storms and cyclones have a signicant impact on the coral communities of the archipelago (Ford 1985; Veron and Marsh 1988), and pass within 100 km every few years (Coleman 1971; Lourensz 1981) (Table 1). During storms and cyclones, considerable swell and wave energy can extend through Mermaid Sound, but the wave energy that usually aects the inner-archipelago is generated by local winds rather than swells (Ford 1985; Pearce 2003). Storms and cyclones also move large amounts of sediment, resulting in acute sedimentation over days and chronic sedimentation over weeks (Ford 1985; Simpson 1988; Gilmour 2002 a, b; Pearce 2003). Chronic sedimentation is also a result of resuspension by spring tide cycles of up to 5 m (Semeniuk et al. 1982; Ford 1985; Simpson 1988). Study sites
Fig. 1 Location (d) of the Mainland (ML) and East Lewis (EL) reefs within the Dampier Archipelago (2032S 11638E), northwestern Australia

Methods
The Dampier Archipelago This study was conducted at two inner-reefs in the Dampier Archipelago (2032S 11638E), located o the Pilbara coast of Western Australia (Fig. 1). Water temperatures within the archipelago range from <18 to

Coral reefs within the Dampier Archipelago have different temperature regimes, aspects, substrata, topographies, and turbidities (Marsh 1978; Veron and Marsh 1988). Some reefs are exposed to considerable waves and sedimentation; whereas, others are comparatively sheltered. The two fringing reefs investigated in this study are 5 km apart, and their coral communities are located in similar depths of water (35 m) on a narrow reef at with a slight slope and a small drop o to sandy substrata. Apart from these similarities, they dier in a number of physical attributes that reect their contrasting exposure to disturbances. The Mainland Reef

Table 1 Cyclones that passed within 500 km of Dampier, had a central pressure of <990 hPa, and wind speeds of >25 ms1, between the years 1990 and 2000

Year

Month

Day

Cyclone

Maximum wind speed (m/s) 34 43 31 39 52 48 43 36 39 46 54 18 36 46 25 55 41 52 18 28 31 33

Distance from Dampier (km) 190 196 483 420 394 187 335 445 259 248 194 444 224 207 258 284 226 86 430 303 104 477

Central pressure (hPa) 976 960 975 960 930 940 950 965 960 945 925 995 965 945 990 920 955 930 994 980 975 970

1991 1992 1993 1994 1995 1996

2 3 12 1 12 2 12 2 3 4 12 1 1 12 3 4 12 3 4

1997 1998 1999

2000

23 2 17 12 18 24 10 19 4 12 10 31 7 27 5 22 7 14 16 1 6 18

Daphne Ian Naomi Pearl Annette Bobby Frank Gertie Jacob Kirsty Olivia Phil Rachel Tiany Billy Vance Gwenda John Ilsa Norman Steve Rosita

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(ML) is adjacent to the mainland, has a low prole, and consists primarily of skeletons of fungiid and massive corals with much of its free substrata covered by ne sediment. The Mainland Reef is exposed to the predominately westerly and north-westerly winds and waves produced by summer storms, in addition to swell generated by cyclones that travels through Mermaid Sound (Fig. 1) (Ford 1985; Simpson 1988). The Mainland Reef has a maximum fetch that extends beyond the archipelago to the Indian Ocean, but to produce a conservative estimate of modied eective fetch and exposure (See Howes et al. 1997), fetch distances were limited to the edge of the archipelago. The modied eective fetch for the Mainland Reef is 20 km and the reef is classied as semi-exposed. Because wind speeds and directions are correlated to wave heights and sedimentation, levels of acute and chronic sedimentation are very high at the Mainland Reef (Simpson 1988; Ford 1985; Gilmour 2002 a). In contrast, the East Lewis Reef (EL) has the opposite aspect and is located in a bay on the leeward side of East Lewis Island (Fig. 1). Much of its coral growth occurs on top of thick (1 m) stands of dead or partially dead Pavona decussata that elevate the corals approximately 1 m above a sandy bottom (5 to 7 m depth). The East Lewis Reef is sheltered from the winds and waves resulting from storms and cyclones in summer and is buered from the weaker winds that blow o the mainland in winter (Ford 1985; Simpson 1988). The East Lewis Reef has a modied eective fetch of 6 km and is classied as protected. There is little sediment accumulation at this reef because its rates of sedimentation are comparatively low and because most falls through the many holes in the substrata (Gilmour 2002 a). Disturbances and the frequency of severe weather at the study reefs The eects of cyclones on the corals reefs of the Dampier Archipelago are determined by their severity and trajectory (Ford 1985; Simpson 1988). During this study, Cyclone Vance had a dramatic aect on the corals reefs within the archipelago. It passed within 300 km, and had a central pressure of 925 hPa and wind speeds of 55 ms1. In comparison, there were 22 cyclones between 1990 and 2000 in north Western Australia that passed within 500 km of Dampier, had a central pressure of <990 hPa, and wind speeds of >25 ms1 (Table 1). In addition to cyclone data, local wind speeds and directions provide a good indication of the frequency of severe weather within the archipelago because they are largely responsible for generating waves, which in turn are correlated to levels of sedimentation. Severe winds from the west have previously had the greatest impact on the coral communities (Ford 1985; Simpson 1988). Wind data was available from a weather station adjacent to the Mainland study site from April 1988. Wind speeds

were considered severe if they exceeded 9 ms1, which was equivalent to three standard deviations above the mean (3.8 ms1) during this study. Severe winds did not always correspond to the presence of a cyclone in the region. For example, Cyclones Tiany and Norman were not associated with severe winds; whereas, there were many days of severe winds that were not associated with a cyclone (Tables 1, and 2). For this reason, the frequency of severe weather was investigated by considering both cyclone and wind data. Sampling regime Fungia fungites is by far the dominant species of fungiid coral within the Dampier Archipelago (Marsh 1978; Veron and Marsh 1988; Veron 1993). In a random sample of over 50 free-living polyps from around the study area at each reef, ranging in diameter from 3 cm to 21 cm (mean = 10 cm), all were identied taxonomically as F. fungites. Additionally, electrophoretic analysis of a random sample of 120 polyps from the same area at each reef, which included sexual recruits and asexual buds, indicated they were all F. fungites (Gilmour 2002 a). Along the narrow reef at at each study site a permanent transect (150 m) was established parallel to the shore in 3 to 5 m depth, where Fungia fungites were distributed. A single large transect was used, rather than smaller replicate transects, because it sampled the majority of each population along a homogenous area within which there was no dierence in the size-structure of polyps. A quadrat (5050 cm) was laid every 2 m on alternate sides of the permanent transect (n = 75) at each reef. There was no evidence of migration by polyps o the reef at at either study site, with most free-living polyps that had been tagged (>80%, n= 67) moving <30 cm during this study, even following cyclones. Therefore, it can be assumed that the same population was censused through time. Within each quadrat, the maximum diameter and life history stage of F. fungites polyps >0.3 cm was recorded. For parent polyps, the maximum diameter of the skeleton was recorded. Polyps were divided among the following life history stages: sexual recruits that were attached to the substrata via a stalk; free-living polyps that were not attached; parent polyps that had no live tissue other than one or more asexual buds; and asexual recruits that were attached to a parent polyp. Injury to polyps was also recorded, but it was not possible to accurately quantify the number of dead polyps because much of the reef matrix consisted of skeletons of polyps that had died over many years. Image analysis of a range of polyp sizes conrmed a strong polynomial correlation between maximum diameter and area, which was used to calculate area cover (y = 0.442+0.03x + 0.703x2, r2 = 0.990, n= 629). The rst census was conducted in April 1998, and yearly censuses were conducted to April 2001.

497 Table 2 The frequency of cyclones and severe winds within the Dampier Archipelago during the study period. Winds were considered severe if their mean hourly speeds exceeded 9 ms1, which was more than three standard deviations above the mean wind Cyclone Census interval 12 Year Month Day speed of 3.8 ms1 h1. Cyclones passed within 500 km of the Dampier Archipelago at times of protracted severe winds within the Archipelago # Hours d1 mean winds 9 ms1 h-1 1 1 3 1 2 2 11 3 2 1 1 1 1 1 1 1 9 19 1 1 4 1 1 19 24 12 6 1 1 2 2 3 4 1 4 1 5 3 1 1 1 Mean speed (ms1 h1) when winds 9 ms1 h1 9 9.1 9.2 9 9.1 9.2 10.7 15.3 9.2 13.1 15.5 14.7 11.1 9.1 9.4 9.8 11 13.3 9.1 9.5 9.5 10.4 9 12.2 14 10.7 9.1 9.2 9.4 9.3 9.15 10.2 9.6 9.7 9.6 9.7 10.1 9.5 9.6 9.2 11.9 Mean wind direction h1 (deg due N) 30 289 299 283 302 19 53 49 148 294 124 230 255 275 278 64 155 230 8 266 266 58 271 255 339 350 335 102 53 267 259 37 265 268 279 48 29 5 266 266 144

1998

12

1999 Cyclone Vance 23 1999

1 2 3 4 8 9 11

Cyclone John and Ilsa

12

2000

Cyclone Steve 34 2000

1 1 2 2 3 3 3 3 7 10 11 12

2001

1 2 3

6 16 17 25 10 2 21 22 7 2 16 25 27 5 6 12 14 15 17 15 23 5 19 6 7 8 9 26 18 7 17 5 9 10 11 12 17 19 16 17 30

Results
The size-structure of each population at the rst census At the rst census the Mainland and East Lewis populations of Fungia fungites had very dierent sizestructures (Fig. 2). There were 2,288 polyps at the Mainland Reef that covered 92% of the area sampled (Table 3). Many polyps were piled on top of each other and the mean number of free-living polyps alone was 10.5 ( 8.2 SD) per quadrat (0.25m2) (Table 3). The East Lewis population was much smaller, having 411 polyps that covered 11% of the area sampled (Table 3). The mean number of free-living polyps per quadrat was 0.8 ( 1.0 SD).

There was also a dramatic dierence in the proportion of dierent life history stages in each population at the rst census (Fig. 2, Table 3). Most obviously, asexual buds and their parent polyps were only found at the Mainland population, where they composed 63% and 5% of the polyps, respectively. Free-living polyps were common (28%), while sexual recruits were rare (4%) (Table 3). The substrata at the Mainland population were composed of, and covered by, skeletons of fungiid polyps spanning all sizes, and 13 free-living polyps had injuries. In contrast, at the East Lewis Reef sexual recruits were by far the most abundant life history stage, composing 86% of the population, and all the remaining polyps were freeliving (Table 3). There were only a few polyp skeletons observed at East Lewis, which were outside the sample

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larger than any at the Mainland Reef at between 23 and 35 cm (Fig. 2). The mean diameter of free-living polyps at the Mainland Reef was 9.8 cm ( 3.8 SD), which was slightly less than for its parent polyps (12.1 cm 4.2 SD) and polyps with injury (13.1 cm 1.9 SD).

Exposure of the populations to disturbances during this study During this study the Mainland Reef experienced more frequent and intense disturbances than the East Lewis Reef, the most obvious of which were seasonal storms and cyclones, and chronic and acute sedimentation. Over three years (1998 2001) four cyclones passed within 500 km of Dampier at times of severe winds within the archipelago (Table 2). In the rst year there were at least 24 h of severe winds, of which Cyclone Vance produced at least 14 h. During Cyclone Vance there were > 24 h when winds speeds were probably at their highest but were not recorded. In the second year there were frequent and protracted periods of severe winds totalling 109 h, of which 72 h were produced by cyclones John, Ilsa, and Steve. In the nal year there were 30 h of severe winds that were not associated with cyclone activity. The Mainland Reef is exposed to winds that blow from between approximately 290 and 70, and there were at least 82 h of severe winds from this direction (Table 2), with >30 h in which severe winds were probably blowing from this direction but were not recorded. The maximum fetch for the Mainland Reef extends to the Indian Ocean, and the reef was exposed to the swell and waves generated by recurrent storms and cyclones. In contrast, the East Lewis Reef has a maximum fetch of approximately 6 km and is exposed to winds blowing from between approximately 110 and 250, but was buered by the mainland and other Islands from the 52 h of severe winds from this direction (Table 2). Storms and cyclones elevated levels of sedimentation within the inner-archipelago, and the movement, resuspension, and deposition of sediment at the Mainland Reef was particularly high at these times. During this study, the levels of sedimentation at the Mainland Reef (mean = 301 g m2 d1) were between three and ve times higher than at the East Lewis Reef (mean = 121 g m2 d1) (Gilmour 2002 a). Reecting the higher levels of disturbance at the Mainland Reef, and possibly higher water temperatures, were the incidences of polyp bleaching. Bleaching was only obvious in polyps >2 cm, and in the rst and second censuses 70% and 28% of these polyps showed some sign of bleaching. In total, >70% of free-living polyps and asexual buds larger than 2 cm had bleached, compared with 33% of the sexual recruits. There was no evidence of bleaching of polyps at the East Lewis Reef.

Fig. 2 Stacked bar graphs illustrating changes in the size and frequency of life history stages of Fungia fungites polyps at the Mainland and East Lewis reefs

area, and no asexual recruits, parent polyps, or injured polyps. The size-frequency distribution of polyps at both populations was positively skewed around a mean diameter of 4 cm, but polyps were larger at the East Lewis Reef (Fig. 2, Table 3). At East Lewis, 3% of polyps were between 25 cm and 30 cm, and these were larger than any at the Mainland Reef. Consequently, the size-frequency distribution of polyps at East Lewis was more skewed, despite the percentages (60 65%) of small (<4 cm) polyps at both populations being similar. At the Mainland Reef, 96% of the polyps smaller than 3 cm were asexual recruits, and their mean diameter of 1.1 cm ( 1.1 SD) was smaller than the 3.2 cm ( 1.6 SD) for the sexual recruits. The sexual recruits at East Lewis had a similar mean diameter of 3.5 cm ( 2.8 SD), but 6% were between 8 and 20 cm, which were larger than any at the Mainland (Fig. 2). Free-living polyps were much larger at the East Lewis Reef, having a mean diameter of 18.6 cm ( 10.5 SD), none being smaller than 3 cm, and almost 40% being

Table 3 Descriptive statistics for the life history stages of Fungia fungites polyps at the Mainland and East Lewis populations. Sexual recruits are attached to the substrata via a stalk, asexual recruits are attached to the skeleton of a parent polyp via a stalk, free-living polyps are not attached, parent polyps have one or more asexual recruits attached to their skeleton and no other live tissue. Censuses were conducted in April of each year and numbers are for polyps of all life history stages that were recorded within 75 quadrats (0.25 m2) along a permanent transect EAST LEWIS Free-living polyps 650 46289 9.8 3.8 0.9 22.4 (28) (74) 116 121867 12.1 4.2 3.6 24.7 (5) (20) 1442 2944 1.1 1.1 0.3 10.8 (63) (5) 2288 171796 4.2 4.9 0.3 24.7 1.2 402 13559 5.4 4.9 0.3 20.4 0.9 280 6902 3.8 4.7 0.3 16.5 1.0 (70) (6) 208 5224 3.4 4.8 0.3 22.8 1.5 (100) (100) (100) (100) 355 4570 3.5 2.8 0.3 20.0 (86) (21) Parent polyps Asexual recruits Total for population Sexual recruits Free-living polyps Total for population 56 16808 18.6 10.5 3.7 34.2 (14) (79) 411 21378 4.6 5.6 0.3 34.2 3.1 324 2024 2.3 1.8 0.3 10.1 (83) (23) 66 13415 15.0 6.9 7.1 34.5 (17) (87) 390 15439 4.1 5.2 0.3 34.5 3.0 (100) (100) 292 1832 4.2 3.5 0.3 18.7 (95) (28) 32 8360 13.9 9.4 3.9 34.0 (5) (82) 324 10192 4.7 4.6 0.3 34.0 2.6 (100) (100) 262 2033 4.0 4.1 0.3 16.5 (87) (27) 39 5634 13.7 9.5 3.3 34.0 (13) (73) 301 7667 5.0 5.7 0.3 34.0 2.8 (100) (100)

Census

MAINLAND

Descriptive statistic

Sexual recruits

80 696 3.2 1.6 0.9 7.8

(4) (1)

42 306 3.0 1.4 0.5 6.5

(10) (2)

202 11523 8.4 4.2 1.9 20.4

(50) (85)

14 1554 13.0 1.8 10.2 15.0

(4) (12)

144 176 1.0 0.4 0.3 2.6

(36) (1)

(100) (100)

20 339 4.4 2.3 0.9 8.8

(8) (5)

76 5444 10.0 3.0 4.0 16.5

(27) (79)

12 1026 11.2 2.2 8.2 15.4

(4) (15)

172 93 0.5 0.5 0.3 2.9

(61) (1)

(100) (100)

1998 Number (%) Area cover (cm2) (%) Mean diam. SD (cm) Min. - max. diam. (cm) Size-frequency distribution skewness 1999 Number (%) Area cover (cm2) (%) Mean diam. SD (cm) Min. - max. diam. (cm) Size-frequency distribution skewness 2000 Number (%) Area cover (cm2) (%) Mean diam. SD (cm) Min. - max. diam. (cm) Size-frequency distribution skewness 2001 Number (%) Area cover (cm2) (%) Mean diam. SD (cm) Min. - max. diam. (cm) Size-frequency distribution skewness (7) (5) 34 3156 10.8 3.9 4.8 18.8 (16) (60) 14 1508 11.6 4.5 7.2 22.8 (7) (29) 145 336 0.9 1.3 0.3 11.5

15 222 3.8 2.4 0.9 7.9

(100) (100)

499

500

Changes in the size-structure of each population Over three years the Mainland population decreased dramatically in size, compared with the East Lewis population (Fig. 2). At the nal census of the Mainland population there were 208 polyps, with their number and area cover having declined to 9% and 3% of the initial values, respectively (Table 3). Its rate of decline was greatest in the rst year, followed by smaller but similar rates of decline in the second and third years (Fig. 3). The East Lewis population at the nal census had 301 polyps, having decreased in number and area cover to 73% and 36% of the initial values respectively (Table 3). Its yearly rates of decline were small but consistent (Fig. 3). There was more variation in the abundance of life history stages at the Mainland population (Fig. 2). The asexual recruits were the most variable, decreasing by 1,298 (90%) polyps in the rst year, increasing by 28 (28%) in the second year, and decreasing again by 27 (16%) in the nal year (Fig. 3). The numbers of parent polyps displayed a similar pattern of change, although their absolute changes in number were far smaller, decreasing by 102 in the rst year and changing little over subsequent years. The free-living polyps decreased by 448, 126, and 42 polyps each year, resulting in large and consistent annual rates of decline of between 55 and 66% (Fig. 3). The sexual recruits had similar rates of decline, decreasing by 38 (48%), 22 (52%), and 5 (25%) polyps over consecutive years (Fig. 3). At East Lewis, the small decreases in population size were driven by changes in the number of sexual recruits. They decreased by between 30 and 32 polyps each year, producing small but consistent yearly rates of decline of 9 to 10% (Fig. 3). The numbers of free-living polyps were more variable, increasing by 10 (17%), decreasing by 34 (52%), and increasing by 7 (21%) polyps over the three years (Fig. 3). The proportions of dierent life history stages at the Mainland population were similar for all but the second census, and changed little over the course of the study at the East Lewis population (Table 3, Fig. 2). The asexual
Fig. 3 Rates of change for the dierent life history stages of Fungia fungites at the Mainland and East Lewis reefs

recruits were the dominant life history stage at the Mainland population, comprising between 60% and 70% of its polyps, apart from their decrease to 36% at the second census when the 50% of free-living polyps were the dominant stage (Table 3). At the East Lewis population the sexual recruits were consistently the dominant life history stage, comprising 83 to 95% of the polyps (Table 3, Fig. 2). The variation in the numbers of free-living polyps had little eect on the population structure overall. The decreases in the abundance of life history stages at both populations were largely independent of their polyp sizes (Fig. 2, Table 3). There was a signicant dierence in the size of asexual recruits and free-living polyps at the Mainland, and sexual recruits at East Lewis, through time (Table 4), but there was little change in the skewness of the population size-frequency distributions and no clear pattern of increasing or decreasing polyp sizes within each of the life history stages (Table 3). Nor was there any evidence that the small or large polyps at the Mainland Reef were disproportionately aected by repeated disturbances, with the exception of perhaps the loss of most large asexual buds. At the rst census there were 107 asexual buds larger than 3 cm, compared with 0, 0, and 9 over consecutive censuses. Within all of the other life history stages at both populations, there were similar decreases across size classes each year, reected by little change in their mean polyp sizes or the percentage of polyps in each size class (Table 3, Fig. 2).

Discussion
Population size-structures at the rst census and their histories of disturbance At the rst census, the size and frequency of dierent life history stages of polyps at both populations provided evidence of their habitat conditions and histories of disturbance. At the East Lewis Reef, there were few

501 Table 4 ANOVA. Planned comparisons between the size of polyps within each life history stage, for each annual census, at each reef. Data were transformed (ln x+1) and planned comparisons using deviation contrasts were used because the data were unbalanced Mainland Reef Life history stage Sexual recruits Error Free-living polyps Error Parent polyps Error Asexual recruits Error Sum of squares 1.184 24.207 5.607 167.948 0.217 14.392 9.332 300.331 df 3 153 3 958 3 152 3 1899 Mean square 0.395 0.158 1.869 0.175 0.072 0.095 3.111 0.158 F 2.494 10.661 0.764 19.668 P-level 0.062 <0.001 0.516 <0.001 East Lewis Reef Sum of squares 90.136 427.926 1.835 64.688 df 3 1230 3 189 Mean square 30.045 0.348 0.612 0.342 F 86.360 1.787 P-level <0.001 0.151

polyp skeletons and no asexual buds; whereas, their abundance at the Mainland Reef indicated a history of disturbance over long and short time scales. A long history of disturbance was evident in the abundance of fungiid skeletons that had been integrated into the reef matrix and the numerous skeletons on the reef that were colonised by encrusting and boring organisms (see Littler et al. 1997; Chadwick-Furman et al. 2000). A more recent history of disturbance was evident in the abundance of parent polyps and asexual recruits, which result from the injury of free-living polyps due to processes such as physical damage (Boschma 1923; Kramarsky-Winter and Loya 1996), freshwater runo (Krupp et al. 1992), or sedimentation (Gilmour 2002 b). The production and growth of buds to a size of around 0.5 cm takes approximately 6 mo at the Mainland Reef (Gilmour 2002 b), and there were numerous small and large (>2 cm) buds resulting from disturbance events that had occurred over a time scale of months to years. The smaller size of sexual recruits and free-living polyps at the Mainland Reef also provided evidence of its exposure to disturbances. Physical disturbances are likely to cause sexual recruits to detach from their stalks at a smaller size, and corals at sites that are exposed to disturbances are more likely to be injured and consequently smaller (Hughes and Jackson 1980; Hoeksema 1991). Most (69%) free-living polyps at the Mainland were <12 cm, whereas most (64%) at East Lewis were >12 cm. The average diameter of free-living polyps at the Mainland was 10 cm, compared with 13 cm for injured polyps and 12 cm for parent polyps, suggesting that above 11 cm the chances of injury are high. Despite the history of disturbance at the Mainland population, it had far more free-living polyps at the rst census than the East Lewis population. Genetic data indicated that most of these free-living polyps were sexual recruits that were produced locally (Gilmour 2002 a). Therefore, sexual recruitment had previously been high, but the lack of sexual recruits at the rst census indicated a recent decline despite the abundance of adult polyps. Sexual recruitment during this period may have been reduced by elevated levels of sedimentation, which can dramatically reduce rates of fertilisation, larval survival, settlement, and post-settlement survival in corals (Hodgson 1990; Babcock and Davies 1991;

Gilmour 1999). Alternately, locally produced propagules may have been carried o the reef. In contrast, at the East Lewis Reef there were few free-living polyps but an abundance of sexual recruits that were locally produced (Gilmour 2002 a). The number of sexual recruits produced by the adult polyps at East Lewis may be proportionally higher because of the lower levels of disturbance, particularly sedimentation. Most (74%) of the sexual recruits were < 4 cm, indicating that they have either died or detached by this size, yet only 25% of the free-living polyps were < 7 cm and there was a relatively even number across the larger size classes. Therefore, the sexual recruits at East Lewis apparently have high mortalities following their detachment, which has been suggested for a number of other fungiids (Chadwick-Furman and Loya 1992; Goredo and Chadwick-Furman 2000). The reef matrix at East Lewis is elevated (1 to 2 m) above a sandy bottom and has many holes through which newly detached polyps may fall and die, which may be why the abundance of sexual recruits did not reect that of the free-living polyps at a site with comparatively low levels of disturbance. Disturbances and the variability in the size-structure of populations during this study During the three years of this study the Mainland Reef was exposed to the strongest winds and waves produced by four cyclones that physically altered parts of its reef. Levels of sedimentation were up to ve times higher than at the East Lewis Reef, and during the rst two summers many of the polyps of the Mainland Reef had bleached. Over that time, the East Lewis population had remained comparatively stable; whereas, the Mainland population had undergone considerable variation in size-structure. These changes were certainly associated with the Mainland Reefs exposure to storms and cyclones, chronic and acute sedimentation, and their synergistic eect, as it is the combination of concurrent or successive disturbances that most aect populations (Dayton et al. 1992; Connell 1997; Hughes and Connell 1999). Severe storms and cyclones alter the size-structure of coral populations, typically reducing the number of corals and increasing the proportion of small individuals

502

due to injury and fragmentation, particularly if sexual recruitment persists (e.g. Done and Potts 1992; Hunter 1993; Coroth and Lasker 1998). Sedimentation also structures coral populations by aecting individual patterns of growth, reproduction, and survival (e.g. Rogers 1990; Obura 1995; Bell and Turner 2000; Gilmour 2002 b). However, the eect of sedimentation on the size-structure of corals varies and can increase the proportion of small massive corals (Brown et al. 2002), or large Porites sp. (Done and Potts 1992), depending on size-specic rates of injury, mortality and recruitment. Fungiid corals are particularly good at removing sediment, but chronic or acute sedimentation is likely to decrease the proportion of small Fungia fungites polyps because their ability to remove sediment increases with size (Schuhmacher 1977; Staord-Smith 1993; Gilmour 2002 b). Together, sediment and storms combine to physically abrade and bury corals, but their eect on size-structure is likely to vary among species (Bak and Engle 1979; Fadlallah 1983; Chadwick-Furman and Loya 1992). The exposure of the Mainland Reef to these disturbances was evident in the smaller size of its sexual recruits and free-living polyps, but during this study there was no obvious change in the proportion of polyps of dierent sizes within each of the life history stages. Scouring and burial of polyps during and after storms probably caused injury and mortality across size classes, particularly because even the largest polyps were unable to maintain an injury which usually spread to the entire polyp within months (Gilmour 2002 b). Most of the decrease in the size of the Mainland population occurred during the rst year, despite there being recurrent disturbances during the second year. This decrease was largely due to the death of many asexual recruits, which were the most abundant and most susceptible of the life history stages. When the most susceptible individuals have already been removed from a population, then the impact of consecutive disturbances may be less apparent (Hughes 1989; Gleason 1993; Dayton et al. 1998). Importantly, the constant decline of free-living polyps at the Mainland Reef was not reected by an increased abundance of parent polyps or asexual buds. Asexual buds are produced from the tissue remaining on a polyp following its injury, and if disturbances cause the death of most of this tissue, or are so frequent as to act on the emerging buds, asexual recruitment will be low. Recurrent disturbances at the Mainland population resulted in a constant rate of decline in sexual recruits and free-living polyps, and limited the recruitment of asexual buds that could potentially restock the population if the intensity or frequency of disturbances were relaxed. Future demography based on the observed variation in population size-structures The East Lewis population was comparatively stable during this investigation despite the frequency of storms

and cyclones, and the abundance of small sexual recruits at each census indicated an ongoing supply and settlement of larvae. In contrast, the observed changes in the size-structure of polyps at the Mainland Reef suggest that it will not return to a size similar to that at the start of this study for many years. Genetic data indicated that the Mainland population is routinely maintained by sexual recruits that are generated from within the population (Gilmour 2002 a), yet the number of free-living polyps of reproductive size (>9 cm) decreased from 389 to 21 during this study. At the nal census almost half the free-living polyps were larger than 12 cm, at which size the chances of injury and mortality are probably high. Also, the abundance of sexual recruits and small free-living polyps was low, and many of these are likely to die if it is assumed that small polyps have high mortality rates, as is common in corals (Hughes and Jackson 1980; Babcock 1991; Chadwick-Furman et al. 2000). Populations of corals are likely to have cycles of destruction and recovery that are far longer than the usual period of investigation (Karlson and Hurd 1993; Connell 1997; Hughes and Connell 1999; Cox et al. 2000). Recovery of sites following disturbance can take between approximately 5 and 15 years, and potentially much longer depending on the scale of disturbance, rates of recruitment, and whether the physical environment has been altered (Myers 1995; Connell 1997). Cyclone Vance had a dramatic aect on the coral communities at the Mainland Reef, and the Dampier Archipelago has not been impacted by a cyclone of similar magnitude since at least 1975 (Ford 1985; Simpson 1988). Further compounding the aects of Cyclone Vance were repeated storm and cyclone disturbances during the following years. The population of Fungia fungites at the Mainland Reef may return to a size similar to that at the start of this study within a decade, but only if there is successful recruitment and survival of larvae, and increased survival of free-living polyps and asexual buds. Clearly, this can only occur if the frequency and intensity of disturbances over the period of recovery is less than was observed during this investigation.
Acknowledgements I thank K. Smith from the Australian Bureau of Meteorology and A. Grieco from the Department of Environmental Protection (Western Australia) for providing weather information. The Australian Institute of Marine Science (WA operations) and Hamersley Iron Pty Limited, have provided continued equipment and infrastructure support. R. Black assisted in all aspects of this research. L. Beesley, L. Smith, and two anonymous reviewers greatly improved the manuscript. This research was supported by Sigma Xi grants in-aid-of research, and the University of Western Australia.

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