Spatial Patterns in Abundance of a Damselfish Reflect Availability of Suitable Habitat

Oecologia (2000) 122:109Ð120 © Springer-Verlag 2000

Sally J. Holbrook á Graham E. Forrester Russell J. Schmitt Spatial patterns in abundance of a damselfish reflect availability of suitable habitat

Received: 18 May 1999 / Accepted: 9 January 1999

Abstract For species with metapopulation structures, evaluating causes of spatial variation in abundance of variation in abundance among patches can arise from reef fishes. variation in the input rate of colonists. For reef fishes, variability in larval supply frequently is invoked as a ma- Key words Habitat availability á Resource limitation á jor determinant of spatial patterns. We examined the ex- Recruitment limitation á Coral reefs á Damselfish tent to which spatial variation in the amount of suitable habitat predicted variation in the abundance of the damselfish Dascyllus aruanus, an abundant planktivore that Introduction occupies live, branched coral throughout the Indo-Pacif- ic. Reef surveys established that size, branching structure Many species have metapopulation structures where the and location (proximity to sand) of the coral colonies to- abundance and dynamics of a sub-population are influ- gether determined the “suitability” of microhabitats for enced by events that occur both within and external to different ontogenetic stages of D. aruanus. Once these the patch. Most marine reef organisms have spatially criteria were known, patterns of habitat use were quanti- sub-divided populations that are linked via planktonic fied within lagoons of five Pacific islands. Availability dispersal of early developmental stages, and the causes of suitable habitat generally was an excellent predictor of spatial variation in local abundance of such species of density, and patterns were qualitatively consistent at have been examined extensively (Connell 1985; Doherty several spatial scales, including among different lagoons and Williams 1988; Mapstone and Fowler 1988; Menge on the same island, among different islands and between 1991; Grosberg and Levitan 1992; Olafsson et al. 1994; the central (French Polynesia and Rarotonga) and west- Booth and Brosnan 1995; Caley et al. 1996; Chesson ern (Great Barrier Reef, Australia) South Pacific. A field 1998a,1998b). It is well appreciated that the abundance experiment that varied the amount of suitable coral in a patch is set by the balance between the externally among local plots indicated that habitat for settlers ac- derived input and subsequent losses (Robertson 1988; counted for almost all of the spatial variation in the num- Underwood and Fairweather 1989; Doherty 1991; Jones ber of D. aruanus that settled at that location, suggesting 1991; Grosberg and Levitan 1992; Doherty and Fowler that spatial patterns of abundance can be established at 1994; Forrester 1995; Schmitt and Holbrook 1996, settlement without spatial variation in larval supply. Sur- 1999a,1999b; Steele 1997). With respect to reef fishes, veys of four other species of reef-associated fish re- considerable debate continues concerning the extent to vealed that a substantial fraction of their spatial variation which post-settlement losses may be density-dependent in density also was explained by availability of suitable (Caley et al. 1996). However, it is widely believed that reef habitat, suggesting that habitat may be a prevalent much of the variation in the input rate among patches, determinant of spatial patterns. The results underscore which often can be large, results from spatial and tempo- the critical need to identify accurately the resource re- ral variability in “larval supply” (Doherty 1991; Doherty quirements of different species and life stages when and Fowler 1994). A substantial body of work has revealed that several S.J. Holbrook (✉) á R.J. Schmitt attributes of reef fish assemblages also can be influenced Department of Ecology, Evolution and Marine Biology, and Coastal Research Center, Marine Science Institute, greatly by variation in habitat features. The distribution University of California, Santa Barbara, CA 93106, USA of species and the composition and diversity of local as- G.E. Forrester semblages can reflect spatial patterns in certain reef attri- Department of Biological Sciences, University of Rhode Island, butes (Hixon and Beets 1989; Holbrook et al. 1990, Kingston, RI 02881, USA 1994; Wellington 1992; Caley and St. John 1996; 110 Munday et al. 1997; Ault and Johnson 1998; Gutierrez aruanus is widespread throughout the Indo-Pacific 1998). Fewer studies have explored the degree to which (Allen 1991), providing an opportunity to examine the patterns of local abundance reflect variation in habitat consistency in habitat relationships among different por- features (Carr 1994; Ault and Johnson 1998), although tions of its geographical range and across several spatial several mechanisms could result in a causal relationship. scales. For example, a larva may need an environmental cue to Our study involved several steps. First, reef surveys settle (Sweatman 1988; Elliott et al. 1995), and spatial were conducted to establish precisely what constituted variation in the intensity of such a cue can alter input “suitable” microhabitat for different ontogenetic stages rates to a patch (Sweatman 1985; Booth and Wellington of D. aruanus. Subsequently, additional survey data were 1998). Early survivorship can be enhanced if appropriate collected to determine the extent to which spatial pat- nursery or shelter habitat is available (Sale and Dybdahl terns in abundance of various life stages could be pre- 1975; Sale et al. 1984; Eckert 1985; Tolimieri 1995; dicted by the amount of microhabitat that was classified Holbrook and Schmitt 1997; Risk 1997; Ohman et al. as suitable. Microhabitat-fish abundance relationships 1998), and the amount of such habitat can vary substan- were explored across several spatial scales (e.g., among tially in space (Carr 1994; Nemeth 1998). Finally, older transects, lagoons, islands, geographic areas). Third, a stages of many species also can exhibit strong habitat field experiment was done to assess whether microha- preferences (Sale 1972; Holbrook et al. 1990; Schmitt bitat-fish abundance relationships could arise from set- and Holbrook 1990; Ault and Johnson 1998), and move- tlement patterns in the absence of substantial spatial ment after settlement can result in positive relationships variation in larval supply. Finally, we conducted comple- between habitat availability and adult abundance. These mentary studies on several other species of reef fish to findings are consistent with the idea that demographic assess the generality of results obtained for D. aruanus. rates can be affected by the availability of suitable habi- Relationships between the availability of preferred sub- tat, which in turn can influence local patterns of abun- strate and spatial patterns in abundance were established dance. for several species with life histories similar to and dif- When examined in survey studies, the amount of vari- ferent from D. aruanus. These included the damselfishes ation in the abundance of fish among patches explained D. flavicaudus (yellow-tail dascyllus), D. trimaculatus by habitat availability has ranged from extremely high (three-spot dascyllus), and Stegastes planifrons (three- (e.g., Carr 1994; Ault and Johnson 1998) to relatively lit- spot damselfish), and the arceye hawkfish Paracirrhites tle (e.g., Ault and Johnson 1998). Drawing inferences arcatus (Family Cirrhitidae). Repeated surveys of D. from the latter outcome can be particularly problematic. aruanus at one location and S. planifrons at another also There are numerous factors (e.g., larval supply, predator allowed us to determine whether observed spatial rela- density) that can decouple a relationship between varia- tionships for these species were temporally consistent. tion in structural aspects of the local environment and abundance, and clearly the factors that set abundance may not involve quantitative variation in a habitat attrib- Methods ute. However, it also could arise if patterns were estimated using incorrect criteria or an inappropriate spatial Study areas scale. For example, reef habitats frequently are classified either into location categories (e.g., fore-reef, reef crest) Sampling of fish and habitats took place in lagoons of five islands in the South Pacific and on the fringing reef of one island in the or into relatively broad microhabitat groupings (e.g., live Caribbean. Three of the islands – Heron Island (23°27’S, coral, rubble, sand). Such classification schemes could 151°55’E), One Tree Island (23°30’S, 152°06’E), and Lady Elliot obscure existing relationships for species with quite spe- Island (24°307’S, 152°43’E) – are on the southern Great Barrier cific microhabitat requirements. Further, it is possible Reef, Australia. The other two Pacific Islands were Rarotonga (21¡14’S, 159°46’W) in the Cook Islands, and Moorea, French that the suitability of a given microhabitat is context-spe- Polynesia (17°30’S, 149°50’W). The Caribbean island was Guana cific, such as when a species inhabits a particular micro- Island, British Virgin Islands (18°29’N, 64°35’W). Water depths habitat only when it occurs in a particular reef area (for were 10 m or less in all areas sampled. examples, see Elliott et al. 1995; Doherty et al. 1996). Here we explore the extent to which spatial variation Spatial patterns of occurrence of D. aruanus: coral morphology, in densities of a damselfish, Dascyllus aruanus (humbug size and location dascyllus), can be explained by availability of suitable habitat. D. aruanus is a reef-associated planktivore in Our own observations and those of other workers (Sale 1972; one of the most speciose families of reef fish (Pomacen- Shpigel 1982; Sweatman 1985; Forrester 1990) indicated that D. aruanus occurs in fairly stable social groups (with up to 80 indi- tridae), which are small-bodied reef fish that have been viduals, but typically less than 10) in coral within shallow, shel- the focus of numerous ecological studies (Sale 1991; re- tered lagoon areas. Occupied corals usually have a branched mor- cent reviews by Booth and Brosnan 1995; Booth and phology or some other shape that provides a network of crevices Wellington 1998; Caley et al. 1996). Like many other within which the fish shelter when threatened. These general observations were not sufficient for the precise assessment of what species of reef fish, D. aruanus inhabits specific types of constitutes suitable habitat for the species, so we conducted sur- microhabitats (live heads of branched coral) that serve as veys at Heron Island to address this issue. A total of 38 band tran- shelter from predators (Sale 1971, 1972). Further, D. sects, each 100×2 m, were established in seven different locations 111 in the lagoon, from nearshore and mid-lagoon (where patch reefs particular morphological type (fine-branched, coarse-branched, were common) to pavement areas behind the reef crest. All corals and so on), and the percent of the colony that was alive was esti- encountered on each transect were categorized by divers according mated. The number (if any) and sizes of D. aruanus occupying to morphology, colony size, presence of D. aruanus, and sur- each coral were determined. The few D. aruanus not clearly rounding substrate. associated with a coral colony were noted. These individuals all In the surveys each coral was examined to determine whether were adults on small patch reefs. Size classes used for analysis it was occupied by D. aruanus. It was then assigned to one of six were recruits (<25 mm standard length, SL), juveniles (25Ð40 mm morphological types, including (1) mound (=massive of Veron SL) and adults (>40 mm SL). Recruits were almost certainly 1986, p. 60), (2) fine-branched (=branching of Veron, with small young-of-the-year (Forrester 1990). spaces between branches), (3) coarse-branched (=branching of In total, 132 transects were included in the analyses (One Tree Veron, with large spaces between branches), (4) lobed (similar to 1987 n=33; One Tree 1993 n=18; Heron n=26; Lady Elliot n=11; columnar of Veron), (5) coarse-branched-lobed (intermediate be- Raratonga n=18; Moorea Teavaro n=13; Moorea Tiahura n=13). tween types 3 and 4), and (6) plate (=laminar of Veron). Colonies Patterns of occupancy of different corals by each of the size class- were categorized according to size along their longest dimension es of D. aruanus were quantified. Relationships between habitat (<10 cm, 10Ð50 cm, 50Ð100 cm, 1Ð5 m, >5 m) as well as sur- features and density of fish were explored with linear multiple re- rounding substrate (on sand, continuous reef pavement, or small gression models (transects as replicates). These models were con- patch reefs). structed to explain the density of a size class of fish using the D. aruanus occupied four of the six morphological types of number of colonies and volume of each of the four morphological corals. To quantify differences in the structure of these four types, types of coral habitat as predictors (fine-branched, coarse- we measured attributes related to overall size of the colony and branched, lobed, coarse-branched-lobed). Analyses reported here quantity of space available for fish to seek refuge between the considered all of the islands with transects as replicates, with loca- branches or lobes. A total of 146 colonies representing the four tion (island or lagoon) as a categorical variable. Since the full types (fine-branched, n=38; coarse-branched, n=73; lobed, n=9; models for all of the Pacific data included some location effects, coarse-branched-lobed, n=26) was measured. The measurements additional regression analyses were performed for each island (or included height, diameter and circumference of the colony, crevice lagoon) separately. Multiple regression models were constructed depth (maximum depth of the crevices between branches or in a forward stepwise fashion to generate the simplest models that lobes), distances between adjacent branch or lobe tips (n=10 mea- could reliably predict fish densities. The insight gained from our surements per colony), and diameter of branches (n=5 per colony). preliminary data on habitat use, and our previous experience with All of the corals were occupied by D. aruanus at the time of mea- this species, were used in the selection of habitat attributes to add surement. Discriminant analysis explored whether the morpholog- to the models, yielding models that were interpretable biological- ical categories we had defined reflected quantifiable differences in ly. shape and branching pattern.

Experimental test of the effect of habitat availability on settlement Patterns of occupancy of branched corals by D. aruanus A field experiment tested the effect of habitat abundance on settle- The coral surveys revealed the sizes, morphologies and locations ment in the absence of substantial spatial variation in larval flux. of coral used by D. aruanus and yielded an explicit, operational Habitat availability was manipulated by transplanting colonies of definition of suitable habitat. This information enabled us to ex- branched coral (Pocillopora sp.) to six 5×5 m reef areas that plore patterns of occupancy of branched corals. First, the propor- lacked coral in Viapahu Lagoon, Moorea. Between 1 and 14 live tion of all (live) branched corals on each transect (each 200 m2 in coral heads were transplanted during July 1995 to each plot by at- area) occupied by D. aruanus was determined, and these values taching them with marine epoxy to cinder blocks. Corals were were regressed against the proportion of corals on each transect measured and their volumes calculated; the range in volume mir- deemed suitable by size and location criteria. Second, the propor- rored that obtained among the transects in the Tiahura lagoon at tion of suitable habitat occupied on each transect was regressed Moorea. Six additional sites served as controls; these lacked coral against the number of suitable corals on the transect to determine (natural or transplanted). The plots were arranged in a two by six whether the intensity of occupation varied with habitat availabili- grid with 5 m spacing between adjacent plots. The highly local- ty. Proportions were angular transformed for statistical analyses. ized configuration of this experiment was intended to minimize the likelihood of gross spatial differences in larval supply. Groups of D. aruanus (as well as several other species of coral-dwelling Relationships between habitat availability and abundance fish including D. flavicaudus) became established on the outplant- of D. aruanus by life stage ed corals via settlement from the plankton. One year after the plots were established, daily settlement of D. aruanus was assessed Ontogenetic patterns of habitat use in six lagoons were quantified each morning during a settlement pulse. After the week-long set- in 1993 at two lagoon areas in Moorea (Tiahura on the west coast tlement event, the total number of settlers to each coral and plot and Teavaro on the east coast), and one lagoon on each of four was calculated and plotwise data were regressed against total vol- other islands (Heron, One Tree, Lady Elliot, and Rarotonga). One ume of live coral. Tree Island was sampled in 1987 and 1993. Up to 13 sites were selected within the lagoon(s) of each island and within each site counts were made on two to six transects. Studies of variation in abundance of other species Transects were rectangular, but were variable in size due to re- strictions imposed by lagoon topography. Most transects were The relationship between habitat availability and abundance for 10 m wide (range 5Ð15 m) and 85 m long (range 37Ð85 m). After four additional species of reef-associated fish was explored. Two marking the perimeter of the transect, it was searched systemati- were congeners of D. aruanus (D. trimaculatus and D. flav- cally. All corals that were suitable habitat for D. aruanus, based icaudus) and so are relatively similar in several facets of their life- on the criteria established in the previous surveys, were counted history and ecology. Notably, both are planktivorous and live in and measured. Volumes of corals were determined by assigning stable social groups for at least part of their lifespan. By contrast, the coral to a shape (sphere, cylinder, ellipsoid, rectangle) at the Stegastes planifrons (Family Pomacentridae) is an aggressive ter- time of sampling, and making measurements that allowed later ritorial herbivore, and Paracirrhites arcatus (Family Cirrhitidae) calculation of volume with standard formulas. Corals were identi- is a benthic sit-and-wait predator. fied to genus. Commonly-occupied genera included Pocillopora, S. planifrons was studied on Guana Island and the other three Acropora, Porites, and Seriatopora. Each coral was assigned to a species were investigated in lagoons on Moorea. For each species, 112 band transects were established at a range of sites, and fish and Table 1 Classification of corals to determine usable habitat. Giv- their habitats were enumerated. en are the percent (and number) of coral colonies occupied by Da- D. trimaculatus settles to sea anemones and associates with scyllus aruanus on Heron Island when corals were categorized by them until adulthood, at which point it becomes more mobile. morphology. Total number of corals in the survey was 3675 (FB Anemones were counted and measured on each transect (n=19 lo- fine-branched, CB coarse-branched, CB-L coarse-branched-lobed) cations, four 40 m×2 m transects per location), to estimate habitat availability as anemone cover per square meter. D. flavicaudus oc- Coral morphology cupies fine- and coarse-branched coral, and P. arcatus lives in Po- cillopora sp. and Acropora sp.. The volume and number of these Massive Plate FB CB CB-L Lobed corals on each 10 m×5 m transect (n=22 for D. flavicaudus and n=13 for P. arcatus) were quantified as described previously. %Occupied 0 0 5.6 38.6 8.8 0.2 S. planifrons recruits are positively associated with colonies of n 482 266 936 422 1063 503 Montastrea annularis, a massive coral with crevices that provide shelter (Tolimieri 1995; Booth and Beretta 1994), and they may also favor other live corals (Booth and Beretta 1994). As adults their microhabitat associations are less distinct, but in some areas Table 2 Classification of corals to determine usable habitat. Giv- adult territories are common on coral rubble or colonies of Acro- en are the percent (and number) of coral colonies occupied by D. pora cervicornis or A. palmata (Itzkowitz 1977; Williams 1978). aruanus on Heron Island when corals were categorized by loca- S. planifrons and reef attributes were enumerated each July from tion. Total number of corals in the survey was 3675 (FB fine- 1992 to 1996 at eight sites around Guana Island. All sites consist- branched, CB coarse-branched, CB-L coarse-branched-lobed) ed of fringing reef with continuous hard substrate at 8Ð10 m × depth. Counts were made on three to six replicate 1.5 m 30 m Location of corals transects per site. S. planifrons were recorded as recruits if <20 mm SL and adults if >40 mm SL. Percent cover of taxa of Patch reef Pavement Sand live coral plus other types of substrates were estimated on transects by line intercept. The type of coral, substrate or organism >5 m <5 m Center Edge Open Edge (sand, coral pavement, dead coral, coral rubble, algae, sponge, soft diameter diameter area of reef coral, hard coral, anemone) under a tape placed in the middle of the band transect was recorded every 0.25 m (120 points per tran- %Occupied 2.9 15.1 0 50 24.2 0 sect) to give an estimate of cover of different habitat categories. n 34 1237 1929 2 463 10 Linear regression analyses explored the relationship between habitat availability and abundance of each species. For D. trimaculatus, D. flavicaudus and P. arcatus, we generated models predicting spatial patterns in the density of adult fishes using transects (or locations in the case of D. trimaculatus) as replicates. For Table 3 Classification of corals to determine usable habitat. Giv- S. planifrons, we had temporal as well as spatial information on en are the percent (and number) of coral colonies occupied by patterns of abundance of fish and habitat features. These data Dascyllus aruanus on Heron Island when corals were categorized spanned at least one generation (K. Clifton, personal communica- by size. Total number of corals in the survey was 3675 (FB fine- tion), allowing a test of whether time-averaged density of recruits branched, CB coarse-branched, CB-L coarse-branched-lobed) at each site was related to time-averaged cover of M. annularis. We also tested the relationships between density of adult S. plani- Coral diameter (m) frons in 1996 and the history of recruitment to the site (1992 to 1996) or the availability of preferred habitat (M. annularis). For <0.1 0.1Ð0.5 0.5Ð1.0 1.0Ð5.0 >5.0 these, transects at each site were pooled, and site means were used as replicates. %Occupied 0.2 7.8 20.1 53.0 0 n 1144 1991 402 134 4

Results habitat availability should take into account the fact that Spatial patterns of occurrence of D. aruanus: not all branched corals offer suitable living space. coral morphology, size, and location Coral colonies of four different morphologies were occupied (fine-branched, coarse-branched, coarse-branched- The surveys conducted to define usable habitat for D. lobed, and lobed), whereas corals with massive or plate aruanus revealed strong patterns of occurrence among growth forms were not (Table 1). Corals in the branched corals of differing morphology, location and size. In all, and lobed categories differed in several attributes that could 3675 live coral colonies were encountered on the tran- influence ontogenetic patterns of habitat use (Table 4). For sects. D. aruanus occurred on corals with a branched instance, fine-branched corals have smaller and less vari- morphology (Table 1). Underlying substrate also was able distances between branch tips than all the other critically important in that fish rarely occupied branched morphs, and they have shallower crevices between the corals on continuous reef pavement or on large (>5 m) branches (i.e., smaller branch depth). Coarse-branched cor- patch reefs. Rather, they occurred mainly on corals locat- als have deeper crevices between branches than other types; ed on or immediately adjacent to sand (Table 2). Further, lobed corals have thicker branches than the others. The re- the size of the coral colony mattered. Small corals (di- sults of the discriminant analysis indicated that the morpho- ameter <0.1 m) were almost never occupied despite their logical categories we defined did reflect statistically defin- great abundance (Table 3). These findings indicate that able features of branching morphology. The analysis re- suitability of coral as habitat is determined by several vealed highly significant differences among categories factors (shape, size and location), and that estimates of (Pillai Trace F=26.1, df=15,414; P<0.0001). The model 113 Table 4 Summary of morphological attributes of branching cor- tance between adjacent branch tips, and diameter of branches of als. Given are the mean (top row for each morphological type) and the four morphological types (CB-L coarse-branched-lobed mor- SE (bottom row for each morphological type) of branch depth, dis- phology)

Morphology n Branch depth Distance between branch tips (cm) Branch diameter (cm) (cm) Mean of 10 SD of 10 Mean of 5 SD of 5 measurements/ measurements/ measurements/ measurements coral coral coral coral

Fine-branched 38 9.7 1.3 0.4 0.9 0.2 0.7 0.2 0.1 0.1 0.03 Coarse-branched 71 20.4 3.1 0.7 0.8 0.2 0.5 0.1 0.04 0.06 0.02 CB-L 26 16.8 3.3 0.9 2.5 0.6 0.9 0.2 0.07 0.1 0.04 Lobed 9 14.6 2.9 1.3 3.2 0.9 1.5 0.3 0.1 0.2 0.07 was able to successfully separate the corals into morphological types (126 of 146 corals correctly assigned).

Patterns of occupancy of branched corals

The analyses above indicate that D. aruanus inhabit live, branched corals, but only those that are above a threshold size that are located on sand or small patch reefs. Both the number and proportion of branched corals that satisfied these criteria varied considerably among the transects at Heron Island. The proportion of branched corals in a transect that was deemed suitable by the size and location criteria was an excellent predictor of the proportion of all branched corals actually occupied by D. aruanus (Fig. 1, r2=0.97; P<0.001), indicating that spatial variation in the frequency of coral occupation was tightly coupled to the proportion of branched corals classified as appropriate. However, not all of the branched corals that were catego- Fig. 1 Relationship between the proportion of all branching corals occupied by Dascyllus aruanus and the proportion of habitat rized by our criteria as suitable were occupied. On aver- judged to be suitable for occupancy at Heron Island. Each point age, ~78% of corals we deemed suitable contained D. aru- represents a transect. The dashed line represents equality in the anus. That objectively classified corals were not all occu- proportions of each variable pied could have been due to the local availability of usable habitat exceeding demand (i.e., available habitat was greatly unsaturated), and/or our failure to identify some enumerating fish and suitable corals (i.e., of the appro- other factor(s) that diminished the suitability of unoccu- priate sizes, morphologies, and location). This was done pied corals. If the former hypothesis were the explanation, on 132 band transects in lagoons of several islands. the proportion of suitable habitat that was unoccupied There were marked ontogenetic differences in the types might increase as amount of usable habitat increased (i.e., of coral utilized. For all lagoons combined, the majority as habitat availability outstrips demand). This was not of recruits (81%) surveyed occurred in fine-branched supported by the data as the proportion of suitable corals corals, and they occupied fine-branched corals more fre- that was occupied remained constant and independent of quently than any other type (Table 5). By contrast, the variation in the absolute amount of such habitat among the majority of adult humbugs (67%) were in coarse- transects (slope=Ð0.004: statistically indistinguishable branched corals, and they occupied proportionately more from 0; t20=1.47; P>0.15). of that coral type than any other (Table 5). Subadults dis- played an intermediate pattern in that both fine-branched and coarse-branched habitats were used about equally Relationships between habitat availability (Table 5). and abundance of D. aruanus by life stage Availability of suitable habitat was an excellent predictor of density of D. aruanus. In the stepwise regres- Once suitable habitat for D. aruanus was defined, pat- sion models that considered all of the islands (with tran- terns of ontogenetic habitat use could be quantified by sects as replicates), up to 79% of the among-transect 114 Table 5 Ontogenetic patterns of coral occupancy based on tran- of D. aruanus, and the number (and proportion in parentheses) of sect surveys on five islands (Heron, One Tree, Lady Elliot, Raro- fish of each ontogenetic stage found in the corals (n=3335 corals, tonga, Moorea). Given are the number of corals of each morpho- CB-L coarse-branched-lobed morphology) logical type and the percent occupied by three ontogenetic stages

Coral morphology Fine-branched Coarse-branched CB-L Lobed

No. corals 1711 860 394 370 %Corals occupied Recruits 22.0 10.9 4.6 3.5 Sub-adults 21.2 33.8 8.6 5.7 Adults 13.6 53.7 22.1 10.3 No. fish occupying each type Recruits 987 (0.81) 183 (0.15) 23 (0.02) 27 (0.02) Sub-adults 751 (0.53) 580 (0.41) 41 (0.03) 43 (0.03) Adults 589 (0.22) 1718 (0.67) 150 (0.06) 118 (0.05)

Fig. 2 Relationships between the abundance (number per 1000 m2 of reef) of recruits of D. aruanus and volume (m3 per 1000 m2 of reef) of fine-branched corals on transects in six locations. Each point represents a transect. Numbers of transects sampled and regression statistics are given in Table 7

variation in density was explained by independent vari- was the volume of fine-branched corals on a transect. ables that described amount of habitat offered by coarse- For adults, the number of coarse-branched corals ex- branched and fine-branched corals, as well as the loca- plained large amounts of variance among transects. tion (lagoon) of the sampling (Table 6). For recruits and However, the combined availability of both juvenile subadults, the main habitat feature to enter the model (fine-branched) and adult (coarse-branched) explained 115 Fig. 3 Relationships between the abundance (number per 1000 m2 of reef) of adults of D. aruanus and number (per 1000 m2 of reef) of coarse- branched corals on transects in six locations. Each point represents a transect. Numbers of transects sampled and regression statistics are given in Table 7

far more variance in adult abundance than did coarse- tion among locations in the absolute abundance of corals branched alone. We re-sampled one lagoon (One Tree Is- and fish. The single exception was for recruits in the land) 6 years after the initial survey and found slight Teavaro lagoon of Moorea, where the volume of suitable quantitative but no qualitative difference in the relation- fine-branched corals explained none of the spatial varia- ships between variation in abundance of various corals tion in density (Fig. 2; Table 7). Variation in subadults and age classes of D. aruanus (Figs. 2,3; Table 7), sug- and adults in the Teavaro lagoon, however, were gesting that the underlying relationships with habitat well predicted by the amount of suitable habitat (Fig. 3; availability may be relatively unvarying through time. Table 7). In general, availability of suitable habitats ex- Overall, these findings corroborated the patterns seen for plained more variance for adults and subadults than for coral occupancy (Table 5) and indicate that the positive recruits (Table 7). relationship between availability of suitable habitats and The existence of location effects in the full models density of each size class on transects was robust over a for all Pacific data combined indicated that there was wide geographical area of the Pacific. not a single relationship between variation in availabili- The full models for all of the Pacific data combined ty of suitable habitats and variation in abundance of the also included some location effects, that is the lagoon of various age classes of D. aruanus among the lagoons. sampling (Table 6). When the transect data were ana- The slope of the relationship between fine-branched lyzed separately for each of the six lagoons, strong posi- corals and recruits tended to be similar among the three tive relationships between coral availability and fish den- lagoons on the Great Barrier Reef and at Rarotonga, and sity still were found (Table 7; Figs. 2,3), despite varia- steeper than at Moorea (Fig. 2). For adults and coarse- 116 Table 6 Summaries of forward stepwise regression models Independent variables predicting fish density r2 predicting density of D. aruanus. Each transect is a repli- Recruits cate (n=132), and location FB corals (vol.) 0.14 (lagoon) was a categorical vari- FB corals (vol.)+Lagoon 0.37 able in the analyses (FB fine- FB corals (vol.)+Lagoon+FB corals×Lagoon 0.49 branched corals, CB coarse- branched corals, vol. volume of Sub-adults coral on a transect, no. number FB corals (vol.) 0.52 of colonies on a transect) FB corals (vol.)+CB corals (no.) 0.58 FB corals (vol.)+CB corals (no.)+Lagoon 0.66 FB corals (vol.)+CB corals (no.)+Lagoon+FB corals×Lagoon+CB corals×Lagoon 0.79 Adults CB corals (no.) 0.24 CB corals (no.)+FB corals (vol.) 0.40 CB corals (no.)+FB corals (vol.)+Lagoon 0.53 FB corals (vol.)+CB corals (no.)+Lagoon+FB corals×Lagoon+CB corals×Lagoon 0.75 CB corals (no.)+Lagoon 0.38 CB corals (no.)+Lagoon+CB corals×Lagoon 0.57 CB corals (no.)+FB corals (vol.)+Lagoon+CB corals×Lagoon 0.72

Table 7 Summaries of forward stepwise regression models pre- als, FB fine-branched corals, vol. volume of coral on a transect, dicting density of D. aruanus. Locations (lagoons) were analyzed no. number of colonies on a transect). In each case the r2 value is separately and transects are replicates (CB coarse-branched cor- given Site One Tree Heron Lady Elliot Rarotonga Moorea Moorea Teavaro Tiahura 1987 1993

No. transects 33 18 26 11 18 13 13 Recruits FB corals (vol.) 0.70*** 0.31* 0.47*** 0.49*** 0.52*** 0.00 0.70*** Sub-adults FB corals (vol.) 0.73*** 0.63*** 0.0 0.31 0.03 0.00 0.91*** CB corals (no.) 0.00 0.02 0.54*** 0.45* 0.00 0.47** 0.15 CB corals (no.)+FB corals (vol.) 0.74*** 0.64*** 0.56*** 0.50 0.13 0.48* 0.91*** Adults CB corals (no.) 0.56*** 0.55*** 0.78*** 0.73*** 0.53*** 0.41* 0.25* CB corals (no.)+FB corals (vol.) 0.56*** 0.63*** 0.77*** 0.70*** 0.52*** 0.39* 0.88***

*P<0.05, **P<0.01, ***P<0.001

branched corals, there also was qualitative similarity in the slope of the relationships for the three Great Barrier Reef islands and Rarotonga, but the slopes were less steep than at the two lagoons on Moorea (Fig. 3). These differences account for the added variance explained in the full models by an interaction term involving location (Table 6).

Experimental test of microhabitat availability on settlement

The field settlement experiment revealed that D. aruanus settled to live heads of Pocillopora on sand, and that the volume of this coral available per area of reef was an excellent predictor of spatial variation in the abundance of Fig. 4 Relationship between the number of settlers of D. aruanus during a 1-week settlement pulse and the volume (m3 per plot) of new settlers (Fig. 4). For the settlement event examined, live fine-branched coral in Viapahu Lagoon, Moorea. Each point most of the among-plot variation in number of settlers represents a 5 m×5 m experimental plot was explained statistically by the amount of suitable 117

Fig. 5 Relationships between A the abundance of D. flavicaudus [n=22 transects, number of fish and volume (m3) of Pocillopora per 25 m2 of reef], B D. trimaculatus [n=19 locations, number of fish and area (m2) of anemones per 320 m2 of reef] and C Para- Fig. 6 Relationships between the time-averaged (1992Ð1996) cirrhites arcatus [n=13 transects, number of fish and volume (m3) abundance of A recruits and B 1996 adults of Stegastes planifrons of Pocillopora and Acropora per 50 m2 of reef] and usable sub- and time-averaged (1992Ð1996) percent cover of preferred substrate on reefs at Moorea strate (Montastrea annularis) on reefs at Guana Island. C The relationship between density of adults in 1996 and time-averaged density of recruits. Each point represents a transect habitat available. No settlement occurred at the six con- Discussion trol sites that lacked coral. Local populations of marine reef organisms often show great spatial variation in abundance, and understanding Studies of spatial variation in abundance of other species the causes of these patterns has been a central focus in marine ecology. Variation in abundance has been argued A substantial amount of spatial variation in density of to arise from a combination of variation in the supply of older stages of four additional species was explained by young from the plankton and in factors that influence availability of reef habitats. Synoptic surveys of adult D. post-settlement losses (Robertson 1988; Doherty 1991; trimaculatus, D. flavicaudus and P. arcatus revealed that Jones 1991; Schmitt and Holbrook 1996, 1999a,1999b; the abundance of adult fishes was positively and appar- Schmitt et al. 1999; Steele 1997). Variation in the input ently linearly associated with availability of the particu- to a patch of reef frequently is assumed to result primari- lar coral type or anemone inhabited by each species ly from variability in larval supply (Doherty 1991), yet (Fig. 5). Long-term surveys of S. planifrons and the hab- habitat features can greatly affect the likelihood of settle- itat it uses showed that the density of recruits at the 8 ment because many species require settlement cues sites, averaged over 5 years, was strongly related to the (Sweatman 1988; Elliott et al. 1995) or particular micro- percent cover of M. annularis (Fig. 6). Both the long- habitats (Sale and Dybdahl 1975; Sale et al. 1984; Eckert term recruitment level, and the availability of preferred 1985; Tolimieri 1995; Holbrook and Schmitt 1997; habitat for recruits (M. annularis) were very good pre- Booth and Wellington 1998). As both larval supply and dictors of among-site variation in the 1996 density of availability of suitable habitat can vary substantially and adults (Fig. 6). with differing degrees of covariation, careful studies are 118 needed that assess their joint contributions in determin- settlement mortality. To compare the extent to which the ing spatial patterns of abundance. Elucidating the contri- density of adults is related to recruitment levels or habi- bution of habitat can be challenging as requirements of- tat attributes, it is necessary to monitor recruitment over ten change with age or size of a reef fish (e.g., Holbrook long time periods (at least the generation time of the spe- et al. 1990; Carr 1994), and the attractiveness of a partic- cies), as well as understand the effects of habitat avail- ular patch can be context-specific (Elliott et al. 1995; ability on different ontogenetic stages. For D. aruanus, Doherty et al. 1996). abundance of both recruits and adults is correlated with Surprisingly few attempts have been made to deter- the availability of suitable habitat for each life-history mine the quantitative relationship between microhabitat stage, and these qualitative patterns held between two availability and abundance of reef fishes in a patch (e.g., sets of surveys 6 years apart. As expected, settlement in Ault and Johnson 1998). Our finding that local abun- our experiment varied tremendously among neighboring dance of D. aruanus was well predicted by spatial varia- plots, and the pattern was adequately explained by variation in specific habitats highlights both the need to con- tion in the abundance of suitable juvenile habitat among sider explicitly the contribution of habitat and some of the plots (Fig. 4). However, our lack of temporal data on the challenges this involves. One is the need to identify recruitment prevents us from testing whether abundance precisely what constitutes suitable habitat. Prior to this of adult humbugs might also be related to long-term re- study, it was well known that D. aruanus inhabits live cruitment levels. The supplementary study of S. plani- heads of branched corals that serve as shelter (Sale 1972; frons allowed us to address this issue because we had Forrester 1990), yet a previous survey study of this spe- temporal data on both recruitment and availability of cies at Heron Island by Sale (1972) failed to detect a preferred habitat. Differences in adult abundance among strong relationship between spatial variation in the abun- sites were indeed strongly related to prior levels of re- dance of branching corals and fish. We found that sever- cruitment. However, they were also strongly related to al features operated together to determine the suitability the availability of preferred habitat (Montastrea annul- of a coral head to this species Ð size, morphology, and aris). Importantly, the availability of habitat for recruits location of the coral, and in some areas a sizeable frac- was also a very good predictor of adult density, suggest- tion of branched corals did not meet these criteria. For ing that patterns in availability of habitat at the recruit- example, about one-third of the otherwise appropriate ment stage may set up patterns in abundance of adults of corals at Heron Island were below the minimum size oc- this species. cupied by D. aruanus. Further, almost no corals were oc- While the survey data presented here indicate that cupied (regardless of coral size) unless they were situat- microhabitat availability can be an important determi- ed on or adjacent to sandy bottom; this feature could nant of spatial variation in local abundance of reef fish- arise from larval preference at settlement, patterns of es, they cannot be used to infer the extent to which local early post-settlement mortality (Shpigel 1982) and/or densities of the fish may have been limited by larval sup- movement after settlement. Whatever the mechanism(s), ply, density-independent mortality, and/or density-depen- our findings reveal the potential for error that is intro- dent mortality. Linear relationships between spatial vari- duced when microhabitats are classified into gross cate- ation in the abundance of microhabitats and fish (i.e., gories or when more subtle features (e.g., size, underly- amount per area of reef) can result if local fish popula- ing substrate) that define suitability to a fish are over- tions either were only recruitment limited (i.e., no densi- looked. ty-dependence) or were completely habitat limited (mi- Our results also illustrate the need to understand age- crohabitats saturated such that further increases in settle- or size-specific habitat requirements. Like many species, ment produces no increase in density of older stages). ontogenetic differences in use of habitats were marked There is growing evidence that local densities of reef for D. aruanus. Juveniles primarily occupied corals with fishes often can be constrained simultaneously by re- small spaces between branches (e.g., Pocillopora spp.), cruitment limitation and resource limitation (Forrester whereas older stages lived in coarse-branched corals 1995; Steele 1997; Chesson 1998a; Schmitt and Hol- (e.g., staghorn Acropora) with larger shelter spaces. This brook 1999a, 1999b; Schmitt et al. 1999). In this context, difference possibly reflects the efficacy of various sizes analytical protocols that are coupled with appropriate of shelter relative to body size of the fish in protection field data are needed to quantify the relative importance from predators (Hixon and Beets 1989; Beukers and of the multiple processes that set local densities (for an Jones 1997). The importance of understanding ontoge- example, see Schmitt et al. 1999). netic patterns in habitat use is demonstrated by the con- In sum, this study underscores the critical need to ac- siderable improvement in amount of explained variance curately identify resource requirements of reef fishes and in abundance of adult D. aruanus in regression models to consider the role of resource availability in determin- that included the availability of both juvenile (fine- ing patterns of abundance of reef organisms with open branched corals) and adult (coarse-branched corals) mi- populations. Larval supply and availability of suitable crohabitats compared with only appropriate adult microhabitat must be considered together as the nature of their habitat (Table 6). covariation is critical in shaping patterns of abundance In long-lived species, adult densities will be the prod- and in determining which processes most strongly limit uct of numerous settlement events tempered by post- local densities. Because input to a patch is determined by 119 both the number of potential colonists and the availabili- Elliott JK, Elliott JM, Mariscal RN (1995) Host selection, loca- ty of critical resources, and because of the interaction be- tion, and association behaviors of anemonefishes in field settlement experiments. Mar Biol 122:377Ð389 tween input and density dependence, advancing our un- Forrester GE (1990) Factors influencing the juvenile demography derstanding of the abundance and dynamics of species of a coral reef fish. Ecology 71:1666Ð1681 with metapopulation structures requires that local re- Forrester GE (1995) Strong density-dependent survival and resources are identified and measured appropriately. cruitment regulate the abundance of a coral reef fish. Oecolo- gia 103:275Ð282 Acknowledgements We thank Sean Connell, Elizabeth Kintzing, Grosberg RK, Levitan DR (1992) For adults only Ð supply-side Linda O’Bryan, Craig Osenberg, Colette St. Mary, Sue Swarbrick ecology and the history of larval biology. Trends Ecol Evol 7: and Bonnie Williamson for assistance in the field, Lianna Jarecki 130Ð133 and Bonnie Williamson for logistic help, and Mike Kingsford for Gutierrez L (1998) Habitat selection by recruits establishes local insightful discussions. We appreciate the hospitality of the UC patterns of adult distrubution in two species of damselfishes: Berkeley Richard Gump South Pacific Biological Station on Stegastes dorsopunicans and S. planifrons. Oceologia 115: Moorea, Heron Island Research Station, One Tree Island Research 268Ð277 Station and the staff at Guana Island, the help of Greg Wilson of Hixon MA, Beets JP (1989) Shelter characteristics and Caribbean Cook Island Divers, and the warm welcome extended to us by so fish assemblages: experiments with artificial reefs. Bull Mar many people in Australia, the Cook Islands, French Polynesia, and Sci 44:666Ð680 the British Virgin Islands. The research was supported by the Na- Holbrook SJ, Schmitt RJ (1997) Settlement patterns and process tional Science Foundation (U.S.-Australia International Program in a coral reef damselfish: in situ nocturnal observations using supplement to OCE 91-02191, and OCE 95-03305 to RJS and infrared video. Proc 8th Int Coral Reef Symp 2:1143Ð1148 SJH), The Falconwood Corporation (to GEF) and the Guana Is- Holbrook SJ, Carr MH, Schmitt RJ, Coyer JA (1990) Effect of gi- land Wildlife Sanctuary (to GEF). This paper is Contribution No. ant kelp on local abundance of reef fishes: the importance of 62 of the Richard Gump South Pacific Biological Station. ontogenetic resource requirements. Bull Mar Sci 47:104Ð 114 Holbrook SJ, Kingsford MJ, Schmitt RJ, Stephens JS Jr (1994) Spatial and temporal patterns in assemblages of temperate reef References fish. Am Zool 34:463Ð475 Itzkowitz M (1977) Spatial organization of the Jamaican damself- Allen GR (1991) Damselfishes of the world. Mergus Baensch, ish community. J Exp Mar Biol Ecol 28:217Ð242 Melle Jones GP (1991) Postrecruitment processes in the ecology of coral Ault TR, Johnson CR (1998) Spatially and temporally predictable reef fish populations: a multifactorial perspective. In: Sale PF fish communities on coral reefs. Ecol Monogr 68:25Ð50 (ed) The ecology of fish on coral reefs. Academic Press, San Beukers JS, Jones GP (1997) Habitat complexity modifies the Diego, pp 293Ð330 impact of piscivores on a coral reef fish population. 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