Reef fish assemblage structure affected by small-scale spacing and size variations of artificial patch reefs

Journal of Experimental Marine Biology and Ecology 326 (2005) 170 – 186 www.elsevier.com/locate/jembe

Reef fish assemblage structure affected by small-scale spacing and size variations of artificial patch reefs Lance K.B. Jordan a, David S. Gilliam a, Richard E. Spieler a,b,* a

National Coral Reef Institute, Oceanographic Center, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL 33004, USA Guy Harvey Research Institute, Oceanographic Center, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL 33004, USA

b

Received 6 July 2004; received in revised form 18 February 2005; accepted 31 May 2005

Abstract To examine how varying the distance between patch reefs affects reef fish assemblage structure, replicate concrete reef modules (~ 1 m3 each) were deployed on sand bottom at 8 m depth off Ft. Lauderdale, Florida, USA (26807N, 80805W). Modules were positioned at the apices of one of four differently sized equilateral triangles. Triangular configurations had side lengths of: 25 m, 15 m, 5 m, and 0.33 m; each treatment with two replicates. Two additional configurations: (1) a solitary module (Single) and (2) two modules side by side (Double), also with two replicates, were deployed in order to examine the interaction of reef size with fish assemblages. SCUBA divers censused fishes monthly, for 2 years, recording the species present, their abundance and sizes (TL). Fishes were assigned to one of five length categories: b 2 cm, N 2–5 cm, N 5–10 cm, N10–20 cm, and N 20 cm. In general and excluding the smallest three-module spacing treatment (0.33 m treatment), which may have provided unique treatment-specific refuge, total fish abundance and richness were shown to increase when isolation distance increased. However, there were also species-specific and size class differences in response to isolation distance. The second part of this study indicated varying reef size, by doubling and tripling the number of reef modules, increased total fish abundance and species richness. Nevertheless, fish abundance and species richness did not change by an identical multiplier (e.g., doubling modules p double abundance). These results suggest that scientists and marine managers alike should consider reef size and isolation as habitat attributes capable of altering the structure and dynamics of reef fish assemblages. D 2005 Elsevier B.V. All rights reserved. Keywords: Artificial reef; Coral reef; Fishes; Isolation; Patch reef

1. Introduction * Corresponding author. National Coral Reef Institute, Oceanographic Center, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL 33004, USA. Tel.: +1 954 262 3613; fax: +1 954 262 4098. E-mail address: [email protected] (R.E. Spieler). 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.05.023

Artificial reefs are popular tools in experimental marine biology and marine resource management. Their uses include the following: replicate structure for experimental treatments, enhancement of fishing and recreational diving, obstruction of benthic trawl-

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ing, providing breakwaters, and mitigation for nearshore and coral reef damage (Polovina, 1991; Walker et al., 2002; Spieler et al., 2001). Because artificial reefs can be readily replicated, thus eliminating confounding variables of structure (e.g., size, complexity), and can be deployed in an infinite variety of spatial arrangements, they are ideal for the study of fish dynamics on patch reefs. However, both experimental as well as management, deployments of artificial reefs often lack regard for the effects of small-scale (i.e., meters to tens of meters) reef spacing (isolation) and reef size on the resulting fish assemblages. Few studies have examined variability in fish assemblages with regard to reef isolation at scales appropriate to post-recruitment ecological processes. Those that have offered little variation among experimental treatments (i.e., only had two treatments) (Schroeder, 1987; Frazer and Lindberg, 1994) or confounded results by concomitantly varying module structure with module spacing (Walsh, 1985) or had varying module spacing within treatments (Lindberg and Loftin, 1998; Lindberg, 1996). Lindberg (1996), using 16-module configurations at the corners of a hexagonal array, noted a greater abundance of several reef dwelling fish species that forage over the surrounding sand areas (Centropristis striatus: Serranidae, Equetus umbrosus: Scianidae, Balistes capriscus: Balistidae and Haemulon plumierii: Haemulidae) on configurations with 225 m of isolation space when compared to the same configuration with 25 m separating modules. The author ascribed this difference to varying benthic prey densities between the two spacing treatments. Bortone et al. (1998) found a decrease in benthic prey item density closer to artificial reefs. Optimal foraging theory suggests that decreased foraging time will increase net energetic gain (MacArthur and Pianka, 1966; Stephens and Krebs, 1986) as well as reducing the risk of predation (Milinski, 1986). Therefore, it is likely that consumption of prey items closer to a reef, by resident fishes, will occur more rapidly than farther from a reef and, a halo of decreasing density of benthic prey items approaching the reef will result (Randall, 1965; Ogden et al., 1973; Ogden, 1976). For this same reason, the substrate surrounding a patch reef having a greater isolation distance from other reefs may provide a greater density of benthic

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prey items than substrate around reefs in closer proximity to each other. Patch reefs spaced closely could result in overlapping halos with a concomitant decrease in benthic prey density and, in turn, the density of benthic foragers. Benthic carnivores make up a large portion of the fish assemblages on coral reefs, in richness (33–56% in one review; Jones et al., 1991) and abundance, including southeast Florida and the Greater Caribbean, where one of the most abundant families in the region (Haemulidae) (e.g., 72% of the total fish recorded in a recent survey of the inshore fishes of Broward County, Florida, Ferro et al., submitted for publication) forage in sandy areas surrounding reefs (Stark and Davis, 1966; Nagelkerken et al., 2000). Thus, the spacing of reef modules may be a critical component of understanding variations in assemblage structure in patchy environs as well as determining the effectiveness of restoration efforts and artificial reef deployment. The overall size of the reef, measured in volume or footprint, is another component of both natural and artificial reefs that has received attention due to its influence on fish assemblage structure. Assuming other factors are equal (e.g., rugosity, temperature, current, depth), with natural reefs a larger reef can potentially support more individuals and species than a smaller reef, but, depending on spatial scale, a smaller reef may have a higher fish density and a more diverse assemblage per volume (Gladfelter et al., 1980; Chittaro, 2002). Likewise, increases in fish abundance and species richness as a function of reef size have also been demonstrated on artificial reefs (Schroeder, 1987; Molles, 1978). Further, larger fishes and higher biomass values often occur on larger, versus smaller, artificial reefs (Bohnsack et al., 1994). But again, smaller artificial reefs may have greater fish richness and abundance per volume (Bohnsack et al., 1994). This fact becomes an important consideration in surveying natural reefs as well as determining restoration scenarios. Presumably, a reef tract with patchy complexity (patch reefs, natural or artificial) could have higher fish richness and abundance than a much larger reef tract lacking such patchiness (Nanami and Nishihira, 2002). We examined the effects of reef isolation and size on fish assemblages by testing two hypotheses. The first part of this study tested the hypothesis that changing isolation distance among replicate reef mod-

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ules affects the associated fish assemblages by manipulating the spacing among reef modules in a fixed configuration. The second part of the study tested the hypothesis that reef size affects fish abundance and species richness by manipulating the number of replicate modules within a treatment.

2. Materials and methods 2.1. Experimental design This study was performed using replicate concrete reef modules (~ 1 m3) (Fig. 1). This module has four horizontal levels separated by nine support blocks, which create overhangs and refuge space. Modules were constructed using waste concrete block (unused and leftover from construction projects) to form an interlocking block structure amalgamated by poured concrete and rebar. Once completed, a module weighed approximately 1.5 tons and, at the study site, was stable in varying weather conditions (Gilliam, 1999). 2.2. Description of study site The study site was located offshore Fort Lauderdale, Florida, USA (26807N, 80805W) in 8 m water depth (Fig. 2). Reef modules were positioned on a sandy bottom between two natural hardbottom tracts.

Fig. 1. An artificial reef module used in the present study.

Fig. 2. Laser Airborne Depth Sounder (LADS) image of Broward Co. Florida coastline. Cross marks center of the study site.

For the first portion of the study (i.e., testing the effects of module isolation), modules were placed at the apices of four differently sized equilateral triangular configurations. The configurations had side lengths of 25 m, 15 m, 5 m, or 0.33 m, each with two replicates (Fig. 3). For the second part of the study (testing the effects of increasing reef material on fish assemblages), two treatments represented by a solitary module (Single) and two modules separated by 0.33 m (Double), also with two replicates, were compared to the 0.33 m triangular treatment (Fig. 3). The precise location of the modules in the planned configurations was achieved using differential global positioning system (DGPS). The modules were used in another study (Gilliam, 1999) and thus seasoned in the marine environment for 4 years prior to use in this study. They were lifted from the previous study site to the surface using a 2-ton lift bag and positioned to within 10% of the desired side length of the treatment configuration (e.g., b 2.5 m of a 25 m side) and N 35 m away from substantial hardbottom substrate or any module from a different configuration (see Fig. 3).

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25m

N

Single

Double

15m

0.33m

5m 5m

35m

15m

0.33m Hardbottom Double

25m

Single

Fig. 3. Drawing of module configurations in the study site. Not to scale.

Upon completion of positioning all modules in their final configuration, the modules were tagged for visual identification and cleaned of all fish using rotenone, effectively creating a starting point for the study (4 September 1998). Data were collected using visual census. One diver, on SCUBA recorded, on PVC slates using pencils, the abundance of all species present on and within 1 m proximity of the module. Because adult fishes may display different distribution patterns to newly settled individuals, each fish was assigned into one of five size categories [0–2 cm, 2–5 cm, 5–10 cm, 10–20 cm, and N 20 cm total length (TL)]. Certain species are wary in the presence of divers. Thus, divers stopped when the module(s) became visible (N 5 m away) making it possible to record the presence of wary species before they fled. As the divers slowly approached the module they continued to record the fleeing fishes. Once those fishes were recorded, the diver moved closer to the module and recorded the abundance of fishes that demonstrated greater site fidelity. The final step in the census involved counting the smaller, cryptic species. This was achieved by visually scanning all surfaces including those within

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the interior of the module. All fish counters were highly experienced in visual counting techniques including extensive experience with the modules used in this study, the species, and the study site. Although some inter-diver differences in size estimation no doubt added to the total variation within the data, it is unlikely this variation would produce a Type I statistical error (Sherman et al., 1999). In two instances fish were only identified to genus. This occurred for all fishes belonging to the genus Acanthemblemaria (Chaenopsidae) and juveniles (b5 cm TL) of the genus Haemulon (Haemulidae). Although not identified to species due to time constraints, subsampling leads us to believe that nearly all Acanthemblemaria encountered were Acanthemblemaria aspera. A variety of juvenile (0–5 cm) grunt species were seen throughout the duration of the study. Multispecies schools occurred frequently and identifying and enumerating individual species would have been error prone and highly time consuming. Previous work on these modules in Broward County indicates the majority of the grunts were H. aurolineatum, H. flavolineatum, and H. plumierii (authors, unpublished data). Because of the close proximity of the modules in the 0.33 m treatments, the modules could not be counted individually and were treated as one large module. Special attention was given to minimize bdouble countingQ fish and to avoid problems inherent to a visual fish census under poor visibility conditions; fish surveys were not performed unless horizontal visibility was N 5 m. On a few days, horizontal visibility exceeded 15 m. The study duration was 24 months. Data were collected monthly with counts of all modules completed on the same day. The first data collection occurred 1 October 1998 and the final data set was collected 25 September 2000. For the September and October 1999 sampling intervals, data were not collected due to rough sea conditions. 2.3. Data analysis We tested for statistical differences in fish abundance and species richness among and between treatments for all sizes and by size class. The abundance data were heteroscedastic and log(x + 1) transformation was performed to homogenize variances (Zar, 1974).

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Using statistical software (SAS 9.1, SAS Institute Inc., Cary, NC, USA), a repeated measures analysis was accomplished with a mixed linear model (Proc MIXED) that isolated the fixed treatment effects (spacing distance or reef size) from the random within subject effects (interaction between counts within a treatment). Post hoc analyses between means were done with a Tukey–Kramer Multiple Comparisons test (T–K); a p b 0.05, was selected as a significant difference. In addition to examining differences in reef isolation among triangular treatments as complete units, fish abundance and richness of individual modules were also analyzed. This analysis included the Single treatment, acting as an individual module from a hypothetical triangular treatment with a side length of N35 m (as previously mentioned, all modules were placed N35 m away from any module of a different configuration). Because the three modules of the 0.33 m treatment were not counted individually, it was excluded from individual module analysis. Multivariate statistical analyses were performed using the Plymouth Routines in Multivariate Ecological Research statistical package (PRIMER v5) including multidimensional scaling (MDS) plots of Bray-Curtis similarity indices, analysis of similarity (ANOSIM) tests, and similarity percentages (SIMPER). These multivariate analyses normally allow for examination of assemblage structure as a whole by including all species and treating them separately. However, the high numbers of juvenile haemulons across treatments (see Results) overwhelmed any assemblage differences and made the results similar to mixed linear model results of abundance alone. Therefore, only the mixed linear model and T–K results were included in this paper.

3. Results 3.1. General results A total of 38,047 fish from 102 taxa, belonging to 31 families, was recorded over the 2-year period (22 monthly surveys). Table 1 lists all species recorded during the study. For all treatments, the mean number of fish present per monthly census was 1729.4 F 223.8 (mean F S.E.M.) with 47 F 1.17 spe-

cies. Intra-annual variations in fish abundance and species richness were evident throughout the study duration. Mean fish abundance, after pooling all treatments, showed significant differences over the duration of the study (Fig. 4). Fish abundance had seasonal fluctuations but generally increased throughout the study duration with a seasonal pattern of abundance increasing as summer approached and peaking during summer months (i.e., June, July, and August) (Fig. 4). Species richness, also showing significant differences over time, followed a pattern similar to abundance (Fig. 5). Fishes in the 2–5 cm size class comprised over 55% of the total abundance. The 0–2 cm size class contained more than 16% while the 10–20 cm size class constituted over 12%. Just over 9% of the total abundance was assigned to the 5–10 cm size class. The least abundant size class was the N20 cm size class, contributing only about 6%. Juvenile Haemulon spp. (0–5 cm TL) represented the most abundant taxon comprising more than 62% of the total abundance in this study. Excluding juvenile Haemulon spp., the nine next most abundant taxa were: Acanthurus bahianus (Acanthuridae), Acanthemblemaria spp. (Chaenopsidae), Thalassoma bifasciatum (Labridae), Anisotremes virginicus (Haemulidae), H. plumierii (Haemulidae), Halichoeres bivittatus (Labridae), Acanthurus chirurgus (Acanthuridae), Equetus acuminatus (Scianidae), and Parablennius marmoratus (Bleniidae). After excluding juvenile Haemulon spp., these nine taxa made up 73.7% of the remaining total abundance of the entire study. 3.2. Reef spacing effects Statistically significant differences in fish abundance and species richness occurred among the triangular isolation treatments varying in isolation distance (reef spacing). Total fish abundance (including all size classes) was significantly different among the four treatments (Fig. 6). Both the largest and smallest triangular spacing treatments (25 m and 0.33 m) had statistically higher mean abundance values than the 5 m and 15 m treatments. Mean species richness provided a pattern similar to that of total abundance but only the 5 m treatment had significantly fewer species than the other three triangular treatments (Fig. 7).

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Table 1 List of species and total numbers recorded in study with trophic group of family (herbivore, piscivore, non-piscivorous carnivore)a Common name

Scientific name

Family: Nurse shark Nurse shark Family: Round stingray Yellow stingray Family: Stingray Southern stingray Family: Moray eels Purplemouth moray Family: Squirrelfishes Squirrelfish Blackbar soldierfish Family: Trumpetfishes Trumpetfish Family: Sea basses Red grouper Sand perch Harlequin bass Family: Cardinalfishes Flamefish Twospot cardinalfish Family: Remoras Sharksucker Family: Jacks Amberjack Blue runner Bar jack Yellow jack Family: Snappers Yellowtail snapper Grey snapper Lane snapper Mutton snapper Family: Grunts Cottonwick White grunt Tomtates Juvenile grunts Margate French grunt Spanish grunt Bluestripe grunt Sailors choice Black margate Porkfish Pigfish Smallmouth grunt Ceasar grunt Family: Porgies Pinfish Saucereye porgy Sheepshead porgy Family: Drums

Ginglymostomatitidae Ginglymostoma cirratum Urolophidae Urobatis jamaicensis Dasyatidae Dasyatis americana Muraenidae Gymnothorax vicinus Holocentridae Holocentrus adsensionis Myripristis jacobus Aulostomidae Aulostomus maculatus Serranidae Epinephelus morio Diplectrum formosum Serranus tigrinus Apogonidae Apogon maculatus Apogon pseudomaculatus Echeneididae Echeneis naucrates Carangidae Seriola dumerili Caranx crysos Carangoides ruber Carangoides bartholomaei Lutjanidae Ocyurus chrysurus Lutjanus griseus Lutjanus synagris Lutjanus analis Haemulidae Haemulon melanurum Haemulon plumierii Haemulon aurolineatum Haemulon juveniles Haemulon album Haemulon flavolineatum Haemulon macrostomum Haemulon sciurus Haemulon parra Anisotremus surinamensis Anisotremus virginicus Orthopristis chrysoptera Haemulon chrysargyreum Haemulon carbonarium Sparidae Lagodon rhomboides Calamus calamus Calamus penna Sciaenidae

Number recorded

Trophic group N–P carnivorea

1 3 N–P carnivore 1 Piscivore 111 N–P carnivore 36 7 N–P carnivore 4 Piscivore 49 153 3 N–P carnivore 107 157 N–P carnivore 2 Piscivore 7 101 107 64 Piscivore 10 140 13 15 N–P carnivore 145 928 24 23,920 12 66 7 198 83 2 959 72 2 10 N–P carnivore 3 24 6 N–P carnivore (continued on next page)

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Table 1 (continued) Common name

Scientific name

Highhat Jacknifefish Family: Goatfishes Spotted goatfish Family: Butterflyfishes Reef butterflyfish Spotfin butterflyfish Family: Angelfishes Queen angelfish Blue angelfish French angelfish Grey angelfish Family: Damselfishes Sergeant major Dusky damselfish Cocoa damselfish Beaugregory Bicolor damselfish Brown chromis Family: Wrasses Hogfish Spanish hogfish Creole wrasse Clown wrasse Slippery dick Yellowhead wrasse Puddingwife Rainbow wrasse Bluehead wrasse Family: Parrotfishes Unidentified parrotfish Redtail parrotfish Redfin parrotfish Stoplight parrotfish Redband parrotfish Striped parrotfish Bucktooth parrotfish Greenblotch parrotfish Family: Stargazer Southern stargazer Family: Labrisomids Hairy blenny Marbled blenny Saddled blenny Family: Chaenopsids Roughhead blenny Sailfin blenny Family: Combtooth blennies Unidentified blenny Molly miller Barred blenny Seaweed blenny Family: Gobies Unidentified goby

Pareques acuminatus Equetus lanceolatus Mullidae Pseudupeneus maculatus Chaetodontidae Chaetodon sedentarius Chaetodon ocellatus Pomacanthidae Holocanthus ciliaris Holocanthus bermudensis Pomacanthus paru Pomacanthus arcuatus Pomacentridae Abudefduf saxatilis Stegastes adustus Stegastes variabilis Stegastes leucostictus Stegates partitus Chromis multilineata Labridae Lachnolaimus maximus Bodianus rufus Clepticus parrae Halichoeres maculipinna Halichoeres bivittatus Halichoeres garnoti Halichoeres radiatus Halichoeres pictus Thalassoma bifasciatum Scaridae Scaridae Sparisoma chrysopterum Sparisoma rubripinne Sparisoma virride Sparisoma aurofrenatum Scarus croicensis Sparisoma radians Sparisoma atomarium Dactyloscopidae Astroscopus y-graecum Labrisomidae Labrisomus nuchipinnis Paraclinus marmoratus Malacoctenus triangulatus Chaenopsidae Acantheblemaria spp. Emblemaria pandionis Blenniidae Blenniidae Scartella cristata Hypleurochilus bermudensis Parablennius marmoreus Gobiidae Gobiidae

Number recorded

Trophic group

463 8 N–P carnivore 19 N–P carnivore 9 4 N–P carnivore 14 5 52 54 19 11 62 22 5 1

N–P carnivore Herbivore Herbivore Herbivore Herbivore Herbivore N–P carnivore

35 79 5 17 838 3 45 9 1329 Herbivore 12 26 22 148 215 6 5 2 Piscivore 1 N–P carnivore 1 1 2 N–P carnivore 1677 32 N–P carnivore 17 2 11 371 N–P carnivore 1

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Table 1 (continued) Common name

Scientific name

Neon goby Bridled goby Goldspot goby Blue goby Family: Surgeonfishes Ocean surgeon Doctorfish Blue tang Family: Scorpionfish Spotted scorpionfish Family: Lefteye flounders Unidentified flounder Family: Leatherjackets Scrawled filefish Orangespotted filefish Planehead filefish Family: Triggerfish Grey trigger Family: Boxfishes Scrawled cowfish Spotted trunkfish Smooth trunkfish Family: Puffers Sharpnose puffer Bandtail puffer Family: Spiny puffers Porcupinefish Balloonfish

Elacatinus oceanops Coryphopterus glaucofraenum Gnatholepis thompsoni Ptereleotris calliurus Acanthuridae Acanthurus bahianus Acanthurus chirurgus Acanthurus coeruleus Scorpaenidae Scorpaena plumieri Bothidae Bothidae Monocanthidae Aluterus scriptus Cantherhines pullus Stephanolepis hispidus Balistidae Balistes capriscus Ostraciidae Acanthostracion quadricornis Lactophrys trigonus Lactophrys triqueter Tetraodontidae Canthigaster rostrata Sphoeroides spengleri Diodontidae Diodon hystrix Diodon holocanthus

Number recorded

Trophic group

269 48 1 4 Herbivore 3180 674 71 Piscivore 14 Piscivore 1 N–P carnivore 12 54 29 N–P carnivore 152 N–P carnivore 17 1 8 N–P carnivore 150 1 N–P carnivore 16 132

a The trophic group was assigned by family based on the predominant food, with the exception of the pomacentrids which were assigned to tropic groups by species.

In general, the abundance of the individual size classes mirrored mean total fish abundance with a trend of increasing numbers from the 5 m to 15 m to 25 m

treatments with the 25 m treatment and the 0.33 m treatment having similar values (Table 2). In contrast, the abundance patterns of the two most common

Mean Total Abundance (+/- 1SEM)

400 350 300 250 200 150 100 50

Oct-98 Nov-98 Dec-98 Jan-99 Feb-99 Mar-99 Apr-99 May-99 Jun-99 Jul-99 Aug-99 Sep-99 Oct-99 Nov-99 Dec-99 Jan-00 Feb-00 Mar-00 Apr-00 May-00 Jun-00 Jul-00 Aug-00 Sep-00

0

Fig. 4. Mean total fish abundance (F1 S.E.M.) for each sampling month pooling all treatment replicates.

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Mean Species Richness (+/- 1SEM)

25

20

15

10

5

Oct-98 Nov-98 Dec-98 Jan-99 Feb-99 Mar-99 Apr-99 May-99 Jun-99 Jul-99 Aug-99 Sep-99 Oct-99 Nov-99 Dec-99 Jan-00 Feb-00 Mar-00 Apr-00 May-00 Jun-00 Jul-00 Aug-00 Sep-00

0

Fig. 5. Mean species richness (F1 S.E.M.) for each sampling month pooling all treatment replicates.

300 250

a a

200

b

b

150 100 50 0

0.33m

5m

15m

25m

Treatment

Fig. 6. Mean abundance values (F 1 S.E.M.) for triangular isolation treatments when pooling over all sampling intervals. Differing letters indicate significant differences between treatments using log transformed data [log(x + 1)] (T–K, p b 0.05).

This occurrence was likely the result of the large proportion of haemulons b 5 cm in this study (composing 69% of non-piscivorous carnivorous species). Examination of piscivorous fishes rendered a result with a similar trend in means to those found for fishes N 20 cm (Table 2). Individual modules from the triangular treatments (excluding the 0.33 m treatment) were also examined (Table 3). The Single treatment (primarily intended to test the effects of reef size on fish assemblage structure) hypothetically acted as an individual module from a N 35 m triangle and, therefore, we compared the Single treatment with individual modules of 5 m, 15 m, and 25 m treatments. For total fish over all size classes on individual reef modules, the

Species Richness (+/- 1SEM)

Mean Total Abundance (+/- 1SEM)

labrids that resulted from spacing variability among treatments did not appear to follow the patterns described above. For bluehead wrasse, T. bifasciatum, the 5 m treatment had the highest abundance. Slippery dick, H. bivittatus, abundance was highest on the 15 m treatment (Table 2). Analysis of trophic group (see Table 1 for family assignments to trophic groups) abundance values revealed no significant differences among spacing treatments for herbivores (Table 2). This group was primarily composed of acanthurids, which also lacked differences among treatments. The pattern of nonpiscivorous carnivore abundance was similar to that of total abundance for all species (Table 2; Fig. 6).

25 20

a

a

a

15m

25m

b

15 10 5 0 0.33m

5m Treatment

Fig. 7. Mean species richness values (F1 S.E.M.) for triangular isolation treatments when pooling over all sampling intervals. Differing letters indicate significant differences between treatments (T– K, p b 0.05).

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Table 2 Comparisons of triangular isolation treatments, data are in Mean F S.E.M. per count across the 24-month study duration Isolation distances

0–2 cm (total length) 0–5 cm 2–5 cm 5–10 cm 10–20 cm N20 cm Juvenile Haemulon spp. (0–5 cm) Abund w/o juvenile grunts Abund w/o all grunts Abundance w/o acanthurids Blue head Slippery dick Herbivore Non-piscivorous carnivores Piscivores

0.33 m

5m

15 m

25 m

16.95 F 6.18b,c 123.05 F 21.39a 106.09 F 20.34a 24.27 F 4.86a 23.20 F 3.32a,b 18.07 F 3.38a 114.89 F 21.8a 73.70 F 4.98a 55.64 F 3.67a 170.73 F 22.83a 6.59 F 0.50b 3.18 F 0.40c,d 20.50 F 2.77a 162.16 F 22.74a 5.93 F 1.41a

12.64 F 4.83b 90.66 F 23.57a 78.02 F 23.23a 10.50 F 2.28a 18.82 F 2.56b 10.68 F 1.92b 74.75 F 23.66a 55.91 F 3.08c 47.25 F 3.05a 113.68 F 23.28c 8.64 F 0.56a 2.48 F 0.34d 18.80 F 2.48a 109.11 F 23.28b 2.75 F 0.31a

18.14 F 4.58a,c 101.23 F 17.58a 83.09 F 17.39a 20.57 F 6.60a 19.02 F 3.09b 6.98 F 0.75b 85.27 F 20.84a 62.55 F 4.88b,c 55.23 F 4.63a 130.16 F 21.45b,c 6.36 F 0.38b 6.80 F 0.72a,b 20.39 F 3.25a 124.91 F 21.34b,c 2.50 F 0.38a

43.30 F 12.26a 165.36 F 28.19a 122.07 F 23.88a 13.39 F 2.45a 25.36 F 2.27a 9.93 F 1.23b 147.02 F 27.42a 67.02 F 3.92a,b 55.86 F 3.75a 193.50 F 28.46a,b 4.98 F 0.45b 4.30 F 0.39b,c 23.34 F 2.78a 188.32 F 28.16a,c 2.39 F 0.31a

Differing letters indicate significant differences between treatments by row using log transformed data (logx + 1) (T–K, p b 0.05).

Single and 25 m treatments contained significantly more fish than the 5 m and 15 m treatments (Fig. 8). Analysis of species richness on individual reefs showed that the 5 m and 15 m treatments had significantly less species than the 25 m and Single treatments, which did not differ (Fig. 9). Examination of fish abundance on individual reefs of the two smallest size classes (i.e., 0–2 cm and 2–5 cm) also revealed significant differences. For the 0–2 cm fishes, the Single treatment had the highest abundance. Individual reefs from the 25 m treatment were significantly greater than the 5 m treatment but not than the 15 m treatment modules (Table 3). Fish abundance of the 5–10 cm and N20 cm size classes lacked significant differences for individual reefs. The 10–20 cm size class, however, had a significantly

higher abundance value on the 25 m treatment (Table 3). 3.3. Reef size effects Significant differences among treatments varying in reef size (number of modules) were found for total abundance and species richness. For both of these assemblage structure attributes, the three module reef (0.33 m treatment) had statistically higher values than either the Double and Single treatments, with the Double treatment being also statistically greater than the Single treatment (Figs. 10 and 11). By size class, fishes from the 0–2 cm size class appeared to exhibit no preference towards individual treatments. The 0.33 m treatment had significantly more 2–5 cm

Table 3 Comparisons of individual modules within isolation treatments, data are in Mean F S.E.M. per count across the 24-month study duration Individual modules from triangular treatments

0–2 cm (total length) 0–5 cm 2–5 cm 5–10 cm 10–20 cm N20 cm

5m

15 m

25 m

Single (N35 m)

4.21 F1.48c 30.22 F 4.87c 26.01 F 4.68a 3.50 F 0.57a 6.27 F 0.92b 3.56 F 0.42a

6.05 F 1.42b 33.73 F 4.29b,c 27.68 F 4.11a 6.83 F 1.99a 6.32 F 0.76b 2.34 F 0.22a

14.43 F 3.99b 55.12 F 7.09a,b 40.69 F 5.60a 4.46 F 0.80a 8.45 F 0.65a 3.31 F 0.38a

24.16 F 6.43a 62.36 F 9.90a 38.20 F 7.16a 3.50 F 1.16a 6.59 F 1.00a,b 3.00 F 0.68a

Differing letters indicate significant differences between treatments by row using log transformed data [log(x + 1)] (T–K, p b 0.05).

100 90 80 70 60 50 40 30 20 10 0

a a b

5m

b

15m 25m Treatment

Single

Fig. 8. Mean total abundance (F 1 S.E.M.) for individual modules of the 5 m, 15 m, 25 m, and Single treatments (Single acting as a single module from a N35 m triangular treatment). Differing letters indicate significant differences between treatments using log transformed data [log(x + 1)] (T–K, p b 0.05).

Species Richness (+/- 1SEM)

TL fishes than the Double and Single treatments (which did not differ) (Table 4). For the remaining size classes (i.e., 5–10 cm, 10–20 cm, and N 20 cm TL), significance levels paralleled those of total abundance and species richness (Figs. 10 and 11; Table 4). Although mean fish abundance values for total abundance and all size classes (except the 0–2 cm size class) increased with increasing reef size, the assemblage variables did not change as an identical multiple of reef size. That is, when doubling and tripling effective reef size, total fish abundance or richness increased but did not double and triple as a result. In contrast, for fish abundance in the three largest size classes (i.e., 5–10 cm, 10–20 cm, and N20 cm) and total biomass, doubling and tripling

12 10

a

a

8 6 4 2 0 15m

25m

250

a 200 150

b c

100 50 0

Single

Double Treatment

0.33m

Fig. 10. Mean total fish abundance (F 1 S.E.M.) for reef size treatments. Differing letters indicate significant differences between treatments using log transformed data [log(x + 1)] (T–K, p b 0.05).

reef size more than doubled and tripled the magnitude of these values (Table 4).

4. Discussion 4.1. Reef spacing The results of this study indicate variable isolation distance among small artificial reef modules can alter the structure (i.e., abundance and species richness) of the associated fish assemblages, with specific responses for different species, trophic groups, and size classes. When triangular treatments were examined as a whole, rather than as individual modules, the results were somewhat confounded by the smallest triangular treatment (0.33 m). Excluding the 0.33 m treatment there was a trend for total abundance to increase with increasing isolation distance among modules. Walsh (1985) also reported increasing abun-

a

b

5m

Mean Total Abundance (+/- 1SEM)

L.K.B. Jordan et al. / J. Exp. Mar. Biol. Ecol. 326 (2005) 170–186

Single

Treatment

Fig. 9. Mean species richness (F1 S.E.M.) for individual modules of the 5 m, 15 m, 25 m, and Single treatments (acting as a single module from a N35 m triangular treatment. Differing letters indicate significant differences between treatments (T–K, p b 0.05).

Species Richness (+/- 1SEM)

Mean Total Abundance (+/- 1SEM)

180

25

a

20

b

15

c 10 5 0 Single

Double Treatment

0.33m

Fig. 11. Mean species richness values (F1 S.E.M.) for reef size treatments. Differing letters indicate significant differences between treatments (T–K, p b 0.05).

L.K.B. Jordan et al. / J. Exp. Mar. Biol. Ecol. 326 (2005) 170–186 Table 4 Comparisons of different sized reefs with one to three modules, data are in Mean F S.E.M. per count across the 24-month study duration Size treatments Single 0–2 cm (total length) 2–5 cm 5–10 cm 10–20 cm N20 cm

Double a

Triple a

24.16 F 6.43

25.43 F 10.93

16.95 F 6.18a

38.20 F 7.16b 3.50 F 1.16b 6.59 F 1.00c 3.00 + 0.68c

53.98 F 11.33b 7.02 F 1.34b 13.75 F 1.62b 7.97 F 1.50b

106.09 F 20.34a 24.27 F 4.86a 23.20 F 3.32a 18.07 F 3.38a

Differing letters indicate significant differences in log transformed data [log(x + 1)] between treatments by row (T–K, p b 0.05).

dance when isolating artificial reefs from natural reefs. Higher juvenile fish abundance was also found on isolated habitat when compared to a continuous reef habitat in Okinawa (Nanami and Nishihira, 2002). However, the 0.33 m treatment was not significantly different in mean abundance than the 25 m treatment and in one instance, the N20 cm size class, the 0.33 m treatment demonstrated a greater fish abundance than any other treatment. Our study was designed only to determine if and where differences among treatments existed, and not to explain why differences occurred. Nevertheless, from our observations, it is likely that fishes present on the 0.33 m treatment were able to utilize the internal space separating the three modules, as they would a crevice, so that it essentially performed as a larger (N 3 m3), individual reef rather than three closely spaced, but individual modules. This additional and unique space may have provided refuge for larger fishes not available on other treatments. It is also possible that the larger reef was able to harbor more prey species and/or increased prey availability (Hixon and Beets, 1989). As a result, more N 20 cm and piscivorous fish were present on the 0.33 m treatment than on any other treatment. While the 0.33 m treatment had the most individuals from the largest size class, when all fish (including all size classes and species) were analyzed, some degree of preference or enhanced survivorship was shown toward this particular amount of separation between modules. Again, the most logical explanation for this apparent preference is utilization of the separating space by the resident population. The reason for utilization of the unique separating space may be due to either habitat preference (see Bohnsack, 1989), predatory exclusion

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(Gilliam, 1999) or some combination of the two. Further, although the presence of resident predators (e.g., serranids, lujanids, scorpaenids, etc.) was commonly recorded, Gilliam et al. (1998), using the same reef modules in the same general locale, noted the importance of transient predators. Predatory passes by schools of transient predators (jacks: Carangidae) were seen frequently in the present study, as well as in other studies examining artificial reefs (Carr and Hixon, 1995; Gilliam, 1999). Although the fast-moving and agile carangids were capable of maneuvering within the separating space of the 0.33 m treatment, it is likely the predators were only able to do so as individuals (or small groups of individuals) and not as a school, possibly decreasing their attack effectiveness (Radakov, 1965; Major, 1978). This type of interaction, between interstructural space, predator size, and predation has been determined for other species (Hixon and Beets, 1989; Bartholomew et al., 2000). It appears that the three modules separated by only 0.33 m effectively functioned as a single, larger (N 3 m3) reef rather than three individual modules (as the other spacing treatments). We believe the somewhat confounding results demonstrated by the 0.33 m treatment in this study (i.e., it did not significantly differ from the 25 m treatment and appeared to break a trend of increasing abundance with increasing isolation distance among modules) are the consequence of fish utilization of the unique separating space. Module isolation appeared to differentially influence the abundance of individual species. Several species deviated from the trend found for total fish abundance. For example, Thalassoma bifasciatum abundance revealed a pattern somewhat opposite that of total fish abundance. Despite the 5 m treatment having the highest abundance for T. bifasciatum, rather than the 0.33 m treatment, there appears to be a trend of decreasing abundance with increasing module spacing. Halichoeres bivittatus abundance also exhibited significant differences among spacing treatments, but lacked a discernable trend with spacing variability, with the 15 m and 25 m treatments representing the first and second highest significance levels, respectively. H. bivittatus exhibits a haremic population organization, usually with several initial phase females following a terminal phase male defending a territory from other terminal males (Thresher, 1984). Terminal phase T. bifasciatum defends a daily spawn-

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ing site where they also feed but, unlike slippery dick, are not believed to form harems (Choat and Bellwood, 1998). These behaviors may help explain their atypical preference toward intermediate isolation treatments (i.e., 5 m and 15 m treatments). Perhaps the intermediate spacing treatments may have been optimally isolated to defend a territory or reduce conspecific competition. Examination of individual modules from triangular treatments allowed us to eliminate the 0.33 m treatment, and its confounding effects, from analysis while including an additional treatment (Single treatment, acting as an individual module from a N 35 m triangular treatment). When these individual modules were analyzed, the results indicated total abundance as well as the abundance of fishes from the two smallest size classes (i.e., 0–2 cm and 2–5 cm size classes) increased as isolation distance increased. Although the individual modules of the two treatments with the greatest amounts of separation (i.e., 25 m and Single) lacked significant difference from one another for total fish abundance, a trend of increasing species richness with increasing isolation distance appeared to be present. The examination of individual modules also allowed for comparison with other studies. The results of the Frazer and Lindberg (1994) and Lindberg and Loftin (1998) studies were consistent with the findings of the present study: increasing isolation among reefs caused an increase in the abundance of several species. The authors ascribed these changes in abundance to differing benthic prey densities surrounding the varying spacing treatments. Other studies have indicated similar results for infaunal and epifaunal organisms surrounding hardbottom areas (Ogden et al., 1973; Ambrose and Anderson, 1990; Posey and Ambrose, 1994; Lindquist et al., 1994; Dahlgren et al., 1999). The authors of those studies have found infaunal prey density gradients (halos), in which infaunal abundance and diversity increased with increasing distance from adjacent hardbottom communities. The gradients are the result of a variety of biological and physical processes. Benthic feeding fish (intermediate predators), which utilize the reef for refuge, often forage on adjacent sandy bottom areas (Stark and Davis, 1966). Since it is generally believed that fish utilize (but not solely) the refuge provided by reefs to avoid predation, the

assumption could be made: when fish spend time away from the reef for the purpose of foraging, exposure to an increased probability of encountering a higher-level predator may occur (Milinski, 1986; Hobson, 1991). Therefore, reducing the distance away from the reef during benthic foraging decreases the time spent away from the reef and also allows for a quicker return to the shelter of the reef should a predator decide to strike. If benthic foragers used this predator avoidance technique, then it would be likely for an infaunal prey density gradient to occur with prey concentrations increasing with distance from the reef module. Close spacing of reefs could result in overlapping halos with an additive decrease in benthic prey density. In contrast, at some specific spacing there should be no overlap of halos. Presumably, all else equal, the larger food resource should be able to support larger populations of predators. This may explain the higher total abundance found on the largest isolation treatments [i.e., 25 m and Single (N 35 m)] in the present study. It is possible that hydrodynamic variability directly caused differences in the fish assemblage structure. Currents have been shown to affect the distribution of certain fishes, mainly planktivores (Lindquist and Pietrafesa, 1989). Artificial reefs can disrupt current flow and different sections of the reef may also have varying hydrodynamics (Bray, 1981; Baynes and Szmant, 1989). Hydrodynamics may have caused surrounding sediment characteristics and infaunal community to vary or had a direct effect on the fish assemblage (Seaman, 2000). Differently sized and shaped module configurations would likely have varying hydrodynamic properties (Sato, 1985). However, with regard to the present study, it is likely that the 5 m, 15 m and 25 m treatments had similar hydrodynamic properties that differed only to that of the 0.33 m treatment. Although we have stressed the potential importance of post-settlement ecological processes, recruitment variability must be addressed. Schroeder (1987) found that increasing spacing among modules in an array increased daily settlement on experimental artificial structures. This appeared to hold true for the present study as there were more 0–2 cm juvenile haemulons on the 25 m treatment than on 5 m treatment. Settling recruits to the fish assemblages in this study were almost certainly not from residents of

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these particular artificial reefs, as reef fish eggs and larvae tend to disperse from parental populations (Leis, 1991; but see Jones et al., 1999; Leis et al., 1998). Even if the residents were able to successfully spawn, the likelihood of their offspring recruiting to the same modules is very low, especially with the predominately longshore currents that exist along the southern Broward coastline (Soloviev et al., 2001). Reef isolation may have affected recruitment from the plankton. One of the basic premises behind the theory of island biogeography is that a larger island has a greater chance to receive more propagules than a smaller one because a larger island is effectively a larger target (MacArthur and Wilson, 1967). The theory is equally applicable to artificial reefs. Larvae are patchily distributed, occurring in highdensity aggregations that are often several miles wide (Williams and English, 1992; Victor, 1984). Settlement normally occurs when larvae, capable of undergoing metamorphosis to the sedentary life phase, find their way back to a reef. This process usually occurs at high densities, not as solitary individuals (Victor, 1991). A large patch of larvae, ready to settle onto a reef, passing over the study site, would, presumably, be most likely to settle on the largest target (due to increased probability of discovery) (Bohnsack, 1991). While three-module reefs separated by several meters would not seem like an single entity (though we treat it as such for this study), the increased isolation could offer a larger target than the same three modules separated by less than 1 m. The larger numbers of new recruits (0–2 cm fishes) on the 15 m and 25 m treatments may support this hypothesis. Nonetheless, for a large patch of settling fish it is likely that the entire study site would act as a large target and variations in recruit densities among treatments were the result of stochastic processes. In this case, post-settlement processes would primarily drive differences among treatments.

and tripling the amount of reef material by doubling and tripling the number of modules did not double and triple the number of fish or species present on the reefs. Similarly to the isolation portion of the study, certain size classes appeared to be affected differently by variations in reef size. Fish from the 0–2 cm size class demonstrated no significant difference in abundance among the three reef-size treatments. The abundance of 2–5 cm size class fish was significantly highest on the largest reef (0.33 m treatment). In contrast, fish abundance from the three remaining size classes (i.e., 5–10 cm, 10–20 cm, and N 20 cm) paralleled significance levels of total abundance. The results of this study suggest that a greater density of fish can exist on smaller reefs than larger reefs and several smaller reefs will have a greater abundance than a larger one of equal volume. Bohnsack et al. (1994) suggested that the nonlinear increase in abundance with increasing reef size was likely the result of smaller reefs having a greater edge effect (i.e., a greater percentage of sand/reef interface area); smaller reefs have a greater edge to area ratio than larger reefs. A larger edge to area ratio implies a greater supply of benthic prey items as well as more surface area for demersal fish species occupation. Although total abundance increased substantially with the number of modules, the abundance of fishes in the N20 cm size class more than doubled and tripled when the number of modules was increased. Essentially, in addition to increased refugia, (created by the close module proximity of the Double and 0.33 m treatments) more N 20 cm fish may have been present on the larger reefs because more prey was available (note that there were more b 5 cm juveniles on the 0.33 m treatments than Double or Single treatments).

4.2. Reef size effects

The results of this two-part study suggest that varying reef module isolation distance and size can alter fish assemblage structure at a variety of levels. Total fish abundance was shown to increase when isolation distance increased, even though the smallest three-module spacing treatment (0.33 m treatment), presumably due to the unique treatment-specific refuge, confounded the results. However, there were also

The results of the effects of reef size variability are consistent with the findings of other studies (Sale and Douglas, 1984; Schroeder, 1987; Bohnsack et al., 1994, Chittaro, 2002). An increase in the amount of reef material increased fish abundance and species richness but not as an identical multiple; doubling

5. Conclusions

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species-specific and size class differences in response to isolation distance. Some species followed the trend of increased abundance with increasing isolation distance while others showed preference or perhaps reduced mortality towards decreased isolation, and in some cases increased abundance on intermediate treatments. The second part of this study indicated varying reef size, by doubling and tripling the number of reef modules, increased total fish abundance and species richness. Nevertheless, fish abundance and species richness did not double and triple. These results suggest that scientists and marine managers alike should consider reef size and isolation as habitat attributes capable of altering the structure and dynamics of reef fish assemblages. This study may help answer an important pragmatic question regarding artificial reefs. What is the best way to configure artificial reef modules to attract the most abundant and diverse fish assemblage? The results of this study, and others, imply that increased spacing may increase total abundance and species richness of a multi-module configuration. Increasing reef size by adding more modules may also yield a more abundant and diverse fish assemblage, however, the increase is likely to be less than the module multiplier (e.g., module  3 p abundance  3). The combined results from the reef spacing and reef size portions of the study suggest that smaller, widely spaced modules may support the most abundant and diverse fish assemblages. However, larger fishes may be able to utilize the unique refuge created by closely spaced modules and be more abundant in such a configuration. Therefore, we caution: module design, relative to refuge (Gilliam, 1999); management objectives, regarding species and life stage (Spieler et al., 2001); as well as knowledge of the local ecology of fish assemblages (Sherman et al., 2001) are all also critical considerations in module configuration.

Acknowledgements Broward County Department of Planning and Environmental Protection personnel: Kenneth Banks, Pamela Fletcher, Louis Fisher, Joseph Ligas, and David Stout provided extensive technical assistance. Many Oceanographic Center, Nova Southeastern University graduate students aided this project with reef

deployment and diving chores; Paul Arena, Dan Fahy and Brian Walker are especially noteworthy. Two anonymous reviewers offered extensive, discerning and constructive comments to the initially submitted manuscript of this paper. This research was funded in part by grant, OFMAS-132, from the Florida Department of Environmental Protection, Division of Marine Resources and by the National Oceanic and Atmospheric Administration Coastal Ocean Program under awards NA96OP0205 and NA06OA0390 to Nova Southeastern University for the National Coral Reef Institute (NCRI). This is NCRI contribution No. 71. [AU]

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