Spatially and temporally predictable fish communities on coral reefs.

INTRODUCTION

Early ecologists described coral reef fish communities as stable, equilibrial assemblages structured primarily by competitive interactions (Odum and Odum 1955, Hiatt and Strasburg 1960, Smith and Tyler 1972, 1973, Smith 1975, 1978). However, more recent studies have documented a high degree of spatial and temporal variation in the structure of coral reef fish assemblages (e.g., Sale and Dybdahl 1978, Williams 1980, Sale and Douglas 1984, Sale and Steel 1986, 1989, Sale et al. 1994). The apparent randomness in distribution and abundance of fish species has prompted the suggestion that coral reef fish communities are structured by stochastic processes, and in particular, by variation in recruitment (Sale and Dybdahl 1975, 1978, Talbot et al. 1978).

There has been much debate over the relative importance of recruitment and postrecruitment processes in structuring marine assemblages (see reviews by Underwood and Denley 1984, Lewin 1986, Roughgarden et al. 1986, Doherty and Williams 1988, Mapstone and Fowler 1988, Underwood and Fairweather 1989, Sale 1990, Doherty 1991, Fogarty et al. 1991, Jones 1991, Booth and Brosnan 1995). Recruitment of almost all coral reef fish species is by means of a pelagic larval stage, which lasts from weeks to months (Brothers et al. 1983, Thresher 1984). Oceanographic variability coupled with high mortality of pelagic larvae causes considerable spatial and temporal variation in larval recruitment at multiple scales (Eckert 1984, Sale et al. 1984b; Doherty 1987; reviewed by Richards and Lindeman 1987, Doherty and Williams 1988, Doherty 1991). However, it remains to be determined to what extent patterns established by stochastic recruitment are modified by postsettlement processes, such as competition for limiting resources (Smith and Tyler 1972, Thresher 1983a, Jones 1986, 1988, Forrester 1995, Robertson 1996), predation (Shulman et al. 1983, Shulman 1985, Hixon 1991, Hixon and Beets 1993, Carr and Hixon 1995), and migration (Robertson 1988a, b).

The recruitment limitation hypothesis is arguably the most widely accepted demographic model of coral reef fish populations. Its principal tenet is that populations are limited by an undersupply of larval recruits, i.e., there is insufficient recruitment to increase the population beyond the environmental "carrying capacity" at which density-dependent population regulation occurs (Williams 1980, Doherty 1981, 1983, Victor 1983, 1986). Thus, if recruitment patterns are not modified by postsettlement processes, the density of adult populations should reflect spatial and temporal variability in recruitment.

Recruitment of coral reef fishes has been studied using two main techniques. In the first, newly settled individuals are surveyed visually to determine distribution and abundance (e.g., Williams 1980, 1983, Victor 1986, Robertson 1988a, b, Robertson et al. 1993, see also Williams et al. 1994), and in the second, otolith microstructure is examined to indicate the exact time of settlement (e.g., Victor 1982, 1983, 1986). In a recent study, Doherty and Fowler (1994a, b) used both techniques to estimate the extent to which temporal variability in recruitment explains spatial variation in the demography of two damselfish species at a number of sites on the southern Great Barrier Reef. They found that recruitment history explained almost entirely the spatial variation in the population age structure and abundance of both species. These results and those of a number of other studies (reviewed by Doherty and Williams 1988, Doherty 1991) have largely established the paradigm of recruitment limitation as the principal process driving the structure and dynamics of coral reef fish communities.

An important limitation of the majority of studies examining the ecology and dynamics of coral reef fish assemblages is that they have been conducted on patch reefs, i.e., outcrops of reef surrounded entirely by sand. In most studies, experimental patches have been small (area of patch reefs [less than]30 [m.sup.2]; e.g., Sale and Dybdahl 1975, 1978, Williams 1980, Sale and Douglas 1984, Clarke 1988, Jones 1990), isolated ([greater than]8 m from neighboring patches; e.g., Williams 1980, Doherty 1983, Victor 1986, Clarke 1988, Jones 1990), and located in sheltered lagoons (e.g., Doherty 1983, Thresher 1983a, b, Sale and Douglas 1984, Clarke 1988, Doherty and Fowler 1994a,b). Furthermore, many researchers have focused exclusively on highly site-attached and/or territorial species (e.g., Williams 1980, Doherty 1981, Doherty 1983, Doherty and Fowler 1994a, b). Visual censusing is easier for species with small home ranges than for wide-ranging, highly vagile species, and small sedentary species are easy to capture and are ideal for experiments that involve manipulation of population density (e.g., Sweatman 1985, Jones 1987a, 1988, Forrester 1990). Similar advantages are gained by studying fish assemblages on small, isolated patch reefs (Sale 1984). These advantages underpin the paucity of studies examining populations of vagile species and fish assemblages on contiguous coral reef.

While there is good data on the population dynamics of site-attached species on isolated patch reefs, an understanding of the processes affecting patch-reef assemblages cannot necessarily be extrapolated to those inhabiting large, well-connected reef mosaics (Walsh 1985, Jones 1987b, 1988, Robertson 1988a, Sale 1991, Sale and Guy 1992, Sale et al. 1994). Here, we argue that assemblages of site-attached species inhabiting small, isolated patch reefs represent a special case with respect to the ecology and dynamics of coral reef fish communities. Moreover, we suggest that conclusions arising from the study of these systems do not necessarily apply to populations of vagile species or to fish assemblages inhabiting large sections of contiguous coral reef.

The primary aim of our research was to quantify the degree of spatial and temporal variability in the structure of fish communities (species composition and relative abundances) and the density of fish populations on sections of contiguous reef and on patch reefs varying in size and isolation from neighboring patches. The study can be categorized conveniently into two parts (Study 1 and Study 2), namely examination of spatial and temporal variability in the distribution and abundance of coral reef fish species.

In Study 1, we investigated the degree to which spatial variation in fish community structure and population density is related to habitat characteristics (e.g., substratum characteristics, shelter availability). Specifically, we addressed the following questions: (1) How much spatial variation in fish community structure and population density is explained by variation in habitat structure alone? and (2) Does predictability in fish community structure and population density differ for fish species varying in vagility among sites on contiguous and patchy reef?

Previous studies of spatial variation in the structure of coral reef fish communities have been criticized for lacking a temporal component (Doherty 1983). Thus, to reduce ambiguity in our results, we conducted a concordant study assessing temporal variability in community structure and population density at sites varying in size and connectivity (Study 2). Over a 2-yr period, we repeatedly surveyed a range of sites from contiguous and patchy reef, with an aim to answering three main questions. (1) Is there any evidence that fish communities vary through time in a predictable direction (i.e., community succession) or fluctuate around a stable configuration? (2) Is the overall magnitude of temporal variability of a particular fish assemblage related to the size and connectivity of the survey patch and/or the vagility of the species comprising the assemblage? (3) Is there any evidence that recruitment events are primarily responsible for temporal variation in fish community structure?

METHODS

Study sites

Research was conducted at adjacent Heron and Wistari reefs (23 [degrees] 21[minutes] S, 151 [degrees] 55 [minutes] E) in the Capricorn Group, southern Great Barrier Reef. Both are platform reefs, consisting of a shallow lagoon surrounded by a continuous rim of coral comprising distinctive reef flat, crest, and slope habitats. All sampling was conducted on the outer reef slope, within a depth range of 4-15 m. On most sides of Heron and Wistari reefs, the reef slope consists of large tracts of contiguous coral reef. However, in a number of areas along the north side of both reefs, the slope is formed primarily by patch reefs that vary widely in size and in isolation from neighboring reef habitat.

Experimental design

In the examination of spatial variability in the structure of fish communities (Study 1), 36 sites on contiguous reef and 39 sites on patch reefs were surveyed once for fish community and habitat structure between October 1992 and October 1993. Locations of sites were varied as widely as practicable to minimize the possibility that local effects may mask general trends in community structure [ILLUSTRATION FOR FIGURE 1 OMITTED]. Patch-reef sites were chosen to vary along gradients of patch size and isolation from neighboring patches (connectivity).

As data on spatial variability were collected over a 1-yr period, it is possible that temporal variability in the structure of fish communities (e.g., seasonal effects) may have weakened overall relationships between community structure and habitat characteristics. Thus, analyses of spatial variation are likely to be conservative. To investigate the degree of temporal variability in the structure of fish communities, a number of permanent sites were surveyed for fish community structure on multiple occasions over a 2-yr period (Study 2). In February 1993, three contiguous-reef sites and nine patch-reef sites were set up on the north side of Heron Reef. In May 1993, three more contiguous-reef sites were set up on the south side of Heron Reef, and in October 1993, seven more patch-reef sites were set up on the north side of Heron Reef. In general, surveys of fish community structure were conducted at [approximately]3-mo intervals although additional surveys were conducted in the early stages of the study (Table 1).

 
TABLE 1. Months during which surveys of temporal variation in fish 
community structure were conducted (Study 2). 
 
Survey no.                 Survey date 
 
1                         Feb 1993 
2                         Mar 1993 
3                         May 1993(*) 
4a                        Aug 1993 
4b                        Oct 1993(**) 
5                         Nov 1993 
6                         Jan/Feb 1994 
7                         May 1994 
8                         Aug 1994 
9                         Nov/Dec 1994 
10                        Feb/Mar 1995 
 
* First survey for three additional contiguous-reef sites (see 
Methods: Experimental design). 
 
** First additional survey for seven additional patch-reef sites, no 
other sites surveyed (see Methods: Experimental design). 

Surveying of fish communities

At each contiguous-reef site, fish species abundance was recorded on a 10 x 10 m grid of 25 quadrats (each 4 [m.sup.2]) marked out by cords laid over the substratum. Each quadrat was surveyed for 2 min by a single diver on scuba (T. R. Ault throughout the study). All fish that were present or that entered the quadrat during the 2-min period were recorded, with the exception of small cryptic species (e.g., blennies and gobies), nocturnal species (e.g., cardinal fishes or soldierfishes), and semipelagic species not usually associated closely with the substratum (e.g., fusiliers and trevallies). Species that were usually present in large polarized schools (e.g., Chromis atripectoralis, C. nitida, Cirrhilabrus punctatus) were also excluded from statistical analyses.

During surveying of fish communities, the observer remained stationary or moved slowly, thereby reducing the likelihood of "herding" or frightening fish into or out of the grid. Although little diver-induced migration was observed, larger mobile species were recorded first as these were more likely to be disturbed than smaller site-attached species. Individuals that moved between quadrats during surveying were recorded once only.

The same method was used for sites located on patch reefs except that smaller grids of 4-[m.sup.2] quadrats were used as the area of each patch reef was [less than] 100 [m.sup.2]. Unlike the patch reefs commonly found in shallow lagoonal habitats, the patch reefs examined on the reef slopes of Heron and Wistari reefs were generally low in vertical relief relative to area and did not present a problem with the placement of quadrats.

Evaluation of surveying method

Surveying precision was evaluated by surveying a single site on contiguous reef (site 1; [ILLUSTRATION FOR FIGURE 1 OMITTED]) three times in 3 h. Results were compared to surveys of all other contiguous-reef sites investigated in Study 1 (sites 236, [ILLUSTRATION FOR FIGURE 1 OMITTED]) to determine if surveying precision was sufficient to resolve differences in community structure among sites. Similarity among surveys was estimated using the Bray-Curtis (BC) index of similarity on data that had been transformed to log(X + 1) (see Wolda 1981). Logarithmic transformation of the data ensured that BC scores were not dominated by abundant species. A cluster dendrogram summarizing similarity among sites was constructed using the unweighted pair-group method with arithmetic averaging (UPGMA).

Habitat measurements

At each site investigated during Study 1, several habitat parameters were measured, including water current velocity, mean depth, topographic complexity, substratum composition, and availability of shelter. Water current velocity was measured immediately after each survey by timing the movement of …