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Fish growth, reproduction, and tissue production on artificial reefs relative to natural reefs

Article in ICES Journal of Marine Science · May 2014 DOI: 10.1093/icesjms/fsu082

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ICES Journal of Marine Science; doi:10.1093/icesjms/fsu082

Fish growth, reproduction, and tissue production on artificial reefs relative to natural reefs

Jennifer E. Granneman*‡ and Mark A. Steele

Department of Biology, California State University, 18111 Nordhoff St., Northridge, CA 91330-8303, USA Downloaded from *Corresponding author: tel: +1 727 452 0127; fax: +1 727 553 1189; e-mail: [email protected] ‡Present address: College of Marine Science, University of South Florida, 140 7th Ave. South, St Petersburg, FL 33701, USA Granneman, J. E., and Steele, M. A. Fish growth, reproduction, and tissue production on artificial reefs relative to natural reefs. – ICES Journal of Marine Science, doi: 10.1093/icesjms/fsu082. http://icesjms.oxfordjournals.org/ Received 12 January 2014; revised 1 April 2014; accepted 13 April 2014.

The extent to which artificial reefs may be useful for mitigation of environmental impacts, fisheries management, and conservation depends in part upon how well the organisms that live on them fare. We tested whether fish living on artificial reefs were in similar condition (weight-at-length), grew, foraged, reproduced, and produced tissue at rates similar to those on natural reefs. We studied five artificial–natural reef pairs spread over .200 km in the Southern California Bight. Underwater visual transects were used to quantify density and size structure of four target species ( clathratus, Paralabrax nebulifer, Semicossyphus pulcher, and Embiotoca jacksoni), which were also collected to measure foraging success, condition, growth, reproductive output, and tissue production. Generally, fish living on artificial reefs fared as well or better than those on natural reefs, with some exceptions. Semicossyphus pulcher fared better on artificial reefs, having higher foraging success, fecundity, densities, and tissue production. Embiotoca jacksoni grew faster on natural reefs, and P. nebulifer was in slightly better condition on natural reefs. Total fish at University of South Florida on June 7, 2014 tissue production tended to be higheron artificial reefsthan on natural reefs, though this pattern was not evident on all reef pairs. Tissue production was positively correlated with the abundance of large boulders, which was higher on artificial reefs than natural reefs. The similar or greater pro- duction of fish tissue per cubic metre on artificial reefs relative to natural reefs indicates that these artificial habitats are valuable in producing fish biomass. Fish living on artificial reefs fared as well as those living on natural reefs, indicating that well-designed artificial reefs can be useful tools for mitigation, conservation, and fisheries management. Keywords: artificial reefs, condition, growth, habitat, mitigation, population density, reef fish, reproduction, tissue production, Southern California Bight.

Introduction organisms be similar to those on natural reefs, but demographic Artificial reefs are widely used, and for some purposes, such as miti- rates such as growth, reproductive output, and mortality must gating environmental impacts (Hueckel et al., 1989; Ambrose, also be similar. These rates have seldom been compared between 1994), these reefs must function similarly to natural reefs. Most artificial and natural reefs, and the few studies that have made studies that evaluate how well artificial reefs work do so by compar- such comparisons have evaluated a single demographic rate in a ing the density or assemblage structure of organisms on these reefs single species (e.g. growth: Love et al., 2007; La Mesa et al., 2010) relative to natural reefs. While such studies provide valuable infor- or on single artificial reefs (e.g. DeMartini et al., 1994; Johnson mation, they cannot answer key questions about how well artificial et al., 1994). Replicated comparisons of several artificial and reefs function. Despite similar densities and identities of organisms natural reefs are necessary to evaluate the functioning of artificial living on artificial and natural reefs, artificial reefs could be demo- reefs (Carr and Hixon, 1997). graphic sinks that do not contribute to or may even reduce regional Here, we compare growth, condition, foraging success, repro- production of marine organisms (Polovina, 1989; Bohnsack et al., ductive potential, density, and tissue production of fish on five 1997; Pickering and Whitmarsh, 1997; Osenberg et al., 2002; large artificial reefs with those on five paired natural reefs. We Powers et al., 2003). studied four ecologically and economically important fish species For artificial reefs to benefit marine organisms by increasing re- on reefs in the Southern California Bight. By studying multiple gional production, not only must densities of resident marine species on several reefs, we were able to evaluate the generality of

# International Council for the Exploration of the Sea 2014. All rights reserved. For Permissions, please email: [email protected] Page 2 of 11 J. E. Granneman and M. A. Steele any differences between artificial and natural reefs, and evaluate Each fish was weighed, total length measured, and the sagittal which attributes of reefs were associated with any differences otoliths, gonads, and digestive tracts were removed and stored. between the two reef types. To our knowledge, this study is the Before storage, gonads were examined macroscopically to deter- first to compare reproductive potential and tissue production on mine sex and stage of maturity, and were classified as follows: F1 artificial and natural reefs. (immature female), F2 (inactive mature female), F3 (active mature female), F4 (ripe mature female), F5 (hydrated female), Methods M1 (immature/inactive male), M2 (active mature male), and M3 Study sites and study species (ripe flowing male). This study was conducted between June and August 2009 on ten Fish growth and condition reefs that spanned 225 km of coastline within the Southern Somatic growth over the year before collection was estimated by California Bight. Five artificial reefs and the five natural reefs otolith back-calculation (details in Granneman, 2011). We limited closest to them were sampled. The artificial reefs studied were our growth estimate to only the preceding year to maximize the Topanga, Wheeler J. North, Pendleton, Torrey Pines 2, and Pacific likelihood that the fish collected had resided on the reef they were Beach. These artificial reefs spanned a broad range of sizes collected from for the whole duration of the growth increment. (924–704 000 m2; median ¼ 5600 m2), ages (10–34 year), relief Based on what is known about the movement patterns of the four Downloaded from (,1–4.9 m), and configurations (1–74 modules); but they were study species (Hixon, 1981; Lowe et al., 2003; Topping et al., 2005; all composed primarily of quarry rock (the Wheeler J. North reef Mason and Lowe, 2010), we think it is likely that the vast major- had a small proportion of concrete). The natural reefs surveyed ity of the fish collected had resided on the reef they were collected were large, contiguous reefs (87 700–11 333 000 m2; median ¼ 3 from for the whole duration of the growth increment. Back- 512 000 m2) with low relief (,1 m). The average reef depth calculation of growth was possible because the otoliths had annual ranged from 7 to 16 m, with pairs having no more than a 2.3 m http://icesjms.oxfordjournals.org/ rings (Love et al., 1996; Baca-Hovey et al., 2002; Froeschke et al., ¼ depth difference (median difference 0.5 m). Artificial and 2007) and there is a tight relationship between otolith size and , natural reef pairs were 7.5 km apart and thus experienced body size in the study species (JEG, unpublished data). We deter- similar oceanographic conditions. mined the equations defining the linear relationship between fish We studied four fish species: bass (Paralabrax clathratus), total length and otolith radius for each species. These equations (Paralabrax nebulifer), were calculated after excluding outliers outside of 95% confidence (Semicossyphus pulcher), and black perch (Embiotoca jacksoni). intervals. The relationship between fish weight and total length These species are some of the most abundant, and ecologically for each species was used to calculate weight change during the and economically important nearshore species inhabiting the preceding year. The estimates of fish growth obtained from otolith rocky reefs of Southern California (Cowen, 1983; Tegner and

back-calculation should be interpreted with some caution given at University of South Florida on June 7, 2014 Dayton, 2000; Erisman et al., 2011). Kelp bass and barred sand that otolith growth is an imperfect predictor of somatic growth bass are generalist carnivores that feed on fish and invertebrates (e.g. Wright et al., 1990; Booth, 2014). We defined condition as (Hobson and Chess, 1976; Eschmeyer et al., 1983), California sheep- weight at length, and thus fish with high body weights for their head feed on macroinvertebrates (Cowen, 1986), and black perch length were in good condition, as might occur if food resources feed on microinvertebrates (Ellison et al., 1979). Home ranges of were abundant. the study species are smaller than the distances that separated artifi- cial reefs from natural reefs (Hixon, 1981; Lowe et al., 2003; Topping Foraging success et al., 2005; Mason and Lowe, 2010; details in Supplementary data). To compare foraging success of fish on artificial and natural reefs, we Although no tagging studies were conducted to quantify fish move- compared the relationship between total gut weight (tract and con- ment on these reefs, given the large sizes of the artificial reefs we tents) and body weight (excluding total gut weight) between artifi- studied relative to many other artificial reefs, combined with the cial and natural reefs. These tests were done only for black perch and known or suspected home ranges of local reef fish and documented California sheephead because they feed primarily on reef-dwelling persistence of tagged fish on artificial reefs in the study area invertebrates (Johnson et al., 1994), whereas the other two study (DeMartini et al., 1994), it is likely the fish we collected were long- species sometimes feed extensively on organisms from off-reef term residents of the reefs on which they were captured. sources (e.g. coastal pelagic fish). Sheephead and black perch are diurnal foragers, and they were collected during a relatively Fish collection and processing narrow time frame (8:30 a.m. to 12:00 p.m.), which ensured that We collected the four target fish species to compare growth, condi- they had at least 2 h of daylight to forage before they were collected. tion, foraging success, reproductive output, and tissue production Collecting activities typically spanned the majority of this 3.5 h on the reefs. Fish were collected at haphazardly selected reef period at all reefs and did not differ between reef types. modules on the artificial reefs and fairly evenly throughout the natural reefs. Collections of fish were made in the middle of the Reproductive potential spawning seasons of three of four species (details in Supplementary We evaluated reproductive potential with two methods for kelp Table S1), from 11 June 2009 to 21 August 2009. Fish were collected bass, barred sand bass, and California sheephead. We could not es- between 8:30 a.m. and 12:00 p.m., before most spawning occurred. timate reproductive potential for black perch because none of the Collections were made primarily by divers using spears, and second- individuals collected was reproductively active because collections arily by hook and line fishing. Fish were pithed or placed in an ice were made after their seasonal parturition. For California sheep- and seawater slurry to euthanize them and then kept on ice until head, we estimated batch fecundity of females with hydrated eggs dissected. The Institutional Care and Use Committee of in their ovaries (F5 stage) using a modified version of the hydrated California State University Northridge approved the protocols used. oocyte method developed by Hunter et al. (1985). This is the Fish performance on artificial reefs Page 3 of 11 preferred method for estimating fecundity in batch spawning fish by draping a 4-m-long chain directly on the substrate, parallel with and we were able to use it with California sheephead because most the transect line. Rugosity was calculated as one minus the ratio of adult females collected were in the F5 stage. For this method to the draped chain to the stretched chain length. Substrate give an accurate estimate of batch fecundity, the hydrated oocytes [sand; cobble (,10 cm); small (10–30 cm), medium (30–75 cm), must be distributed uniformly throughout the two lobes of the and large boulder (.75 cm)] was also recorded every metre. The ovaries. This is known to be true for California sheephead, provided density of giant kelp (), which can occur on they have not ovulated (Wang, 2010). To ensure that ovulation had both reef types, was measured as the number of stipes within 1 m not commenced histological sections of the ovaries were examined on each side of the transect along the length of the entire transect. for evidence of ovulation and fish that had newly formed postovu- Divers measured reef depth and height above the sand at the shal- latory follicles were not used in the fecundity analysis. lowest point using their dive computers. To estimate the density Most adult female kelp bass and barred sand bass were in the F4 of reef-associated invertebrates that could be prey for some fish stage (ripe, mature), not the F5 stage. For them, we used the “mature species, conspicuous invertebrates in major categories (barnacles, egg” method to estimate reproductive potential. This method is a sea cucumbers, gorgonians, mussels, sea snails, sea stars, urchins, modified version of the size frequency method of Hunter et al. worms, crabs, nudibranchs, limpets, lobsters, and sea hares) were (1985) that was developed by Wang (2010). We counted the identified and counted within 0.5-m2 quadrats placed every 2 m number of eggs .0.4 mm in diameter in ovarian subsamples and along each benthic transect. Downloaded from extrapolated from these subsamples to get an estimate of the total number of these mature eggs within the ovaries of each F4 female. Data summary and statistical analysis Wang (2010) concluded that these mature eggs would form the All statistical analyses were done using SYSTAT 13. We used analysis next two to three batches to be spawned. of variance (ANOVA) to test for differences in growth rate (g year21), density (number of fish m23), and tissue production http://icesjms.oxfordjournals.org/ of each species between artificial and natural reef types (hereafter Tissue production referred to as “reef types”), among the five regions (Pacific Beach, We estimated the production of fish tissue over the preceding year Pendleton, Topanga, Torrey Pines, and San Clemente). Two-way by adding the somatic and gonadal production of fish tissue in ANOVA was used to test for differences in the average growth of a manner similar to that used by DeMartini et al. (1994), but each species between reef types and among regions. Reef type was with differences in the estimation of key parameters (details in treated as a fixed factor and region as a random factor. Individual Supplementary data). In brief, the annual per-capita rates of fish were treated as replicates. Because preliminary analyses revealed somatic and gonadal tissue production (i.e. somatic growth and no relationship between growth rate and body size, size was not gamete production in grammes per fish) were multiplied by the included as a covariate in these analyses. To test for differences in density of each species on each transect surveyed by scuba divers. density and tissue production between natural and artificial reefs, at University of South Florida on June 7, 2014 The production of fish tissue per cubic metre was calculated separ- transects were treated as replicates, and the model included block ately for each species collected. (a random factor) nested within the reef type × region interaction. All variables were transformed as necessary to meet the assumptions Reef surveys of ANOVA. At each reef, scuba divers sampled the density and size structure Analysis of covariance (ANCOVA) was used to test for differ- of the four study species. Additionally, the abundance of reef- ences in condition, foraging success, andfecundity betweenartificial associated invertebrates was measured to assess the similarity in po- and natural reefs while factoring out the effect of body size (length) tential food sources on the two reef types. Physical characteristics of on these response variables. All ANCOVA models included the the reefs and the surrounding environment were also measured to factor “reef type” and the covariate body length (TL). Individual determine how closely the artificial reefs physically mimicked the fish were treated as replicates, and because at some reefs we were nearby natural reefs. unable to collect large numbers of fish, we pooled fish into the Fish, invertebrates, and habitat attributes were surveyed along two categories artificial reef or natural reef. For condition, length 99 band transects. Natural reefs were divided into ten blocks of ap- and weight were log-transformed for each species for the analysis proximately equal size, and five to six of these were randomly to linearize the relationship between the two. For foraging success, chosen to be surveyed. Within each block, two haphazardly to meet the assumptions of ANCOVA, the data for black perch gut placed 30-m long transects were sampled. Because the artificial weight and body weight were log-transformed, whereas California reefs sampled consisted of spatially discrete modules (1–74) of sheephead gut weight was square-root transformed and body varying shape and area, these reefs were surveyed in a slightly differ- weight was log-transformed. For fecundity, egg number was log- ent manner than the natural reefs. Artificial reef modules were transformed for all species to ensure the linearity of the relationships treated as blocks and 1–12 of them were sampled. The maximum and to meet the other assumptions of ANCOVA. transect length sampled was 30 m; however, transect length was We used Pearson’s correlations to test for reef-scale associations reduced in some cases when artificial reef modules were ,30 m between the three summed measures of tissue production (somatic, in length. gonadal, and total) and six reef characteristics (substrate PC1, ru- Along the transects, fish were surveyed within a 2 × 2 m window gosity, depth, reef size, invertebrate density, and giant kelp and the size of each fish encountered was estimated by eye. Transects density). (Multiple regression was not used because of the large were sampled in two habitat types: the benthos and the water number of predictor variables relative to the number of replicates, column 3 m above the benthos. Reefs were sampled only when 10 reefs.) Substrate PC1 was derived from a principal components underwater visibility was .3 m. Physical and biological measure- analysisthat provideda multivariate summary of substrate variation ments were made along the same benthic transects used for the as measured by the per cent cover of the five substrate variables fish surveys. Rugosity was measured every 10 m along each transect (sand; cobble; small, medium, and large boulders). Page 4 of 11 J. E. Granneman and M. A. Steele

Results species we measured (Figure 3). Gut fullness (digestive tract + con- Growth rates of three of four studyspecies were similar between arti- tents weightvs. body weight) of California sheephead increased with ficial andnaturalreefs (Figure 1).The exception, black perch, grewat body weight at a greater rate on artificial reefs than on natural reefs higher rates on natural reefs than on artificial reefs (81.8 vs. 61.9 g such that small sheephead on the two reef types had similar gut year21 based on otolith back-calculation; F ¼ 86.2, p , 0.001). weights, whereas large sheephead had heavier guts on artificial 1,4 × Averaged over all regions, growth rates of the other three species reefs (reef type body weight: F1,172 ¼ 5.2, p ¼ 0.01). Black (kelp bass, barred sand bass, and California sheephead) did not perch gut fullness did not differ between the reef types (slope: ¼ ¼ ¼ ¼ differ between reef types (F1,4 ¼ 0.4, p ¼ 0.55; F1,4 ¼ 1.2, p ¼ F1,292 3.0, p 0.08; elevation: F1,293 2.5, p 0.12). 0.33; F1,4 ¼ 0.002, p ¼ 0.97, respectively), although this pattern The reproductive potential of females on artificial reefs was was not consistent among all reef pairs. Barred sand bass grew similar or higher than that of females on natural reefs (Figure 4). faster on Pacific Beach and Topanga artificial reefs than on Batch fecundity of California sheephead was higher on artificial the paired natural reefs, but at similar rates on the reefs in the reefs than on natural reefs (reef type: F1,100 ¼ 6.9, p ¼ 0.01; × ¼ other three regions (reef type × region: F4,150 ¼ 2.7, p ¼ 0.03). type length: F1,99 , 0.1, p 0.95). There were no statistically sig- California sheephead grew faster on the Pendleton natural reef nificant differences in reproductive potential at size between reef than on the paired artificial reef, but grew slightly faster on the arti- types for barred sand bass (reef type: F1,55 ¼ 0.1, p ¼ 0.70; reef × Downloaded from ficial reefs in the other reef pairs (reef type × region: F3,140 ¼ 5.9, type length: F1,54 ¼ 3.1, p ¼ 0.09) or kelp bass (reef type: × p , 0.001). F1,81 ¼ 2.4, p ¼ 0.12; reef type length: F1,80 ¼ 1.4, p ¼ 0.24). Condition of fish (weight-at-length) was similar for fish living on Densities of three of four study species did not differ consistently artificial and natural reefs (Figure 2). Condition did not differ sig- between artificial reefs and natural reefs (Figure 5). The exception nificantly for three species, California sheephead, black perch, and was California sheephead, which was significantly more abundant × kelp bass (ANCOVA: reef type: all p . 0.08; reef type body on artificial reefs than natural reefs (reef type: F1,4.1 ¼ 12.3, http://icesjms.oxfordjournals.org/ length: all p . 0.09). For barred sand bass, however, condition p ¼ 0.02), a pattern that was consistent among five reef pairs (reef was significantly higher on natural reefs than artificial reefs (reef type × region: F4,43.1 ¼ 1.8, p ¼ 0.15). The other three species type: F1,204 ¼ 6.3, p ¼ 0.01), but the difference appeared biologically had inconsistent differences in density between artificial and trivial (a 1.7% difference in weight; Figure 2). natural reef pairs in the five regions (reef type × region: black Foraging success was higher on artificial reefs than natural reefs perch: F4,43.0 ¼ 3.2, p ¼ 0.02; kelp bass: F4,43.8 ¼ 6.8, p , 0.001; for one species, but did not differ significantly for the other barred sand bass: F4,42.5 ¼ 5.7, p , 0.001), such that averaged at University of South Florida on June 7, 2014

Figure 1. Annual growth of fish in body weight (mean + s.e.) on artificial and natural reefs in five regions for the following species: (a) black perch (n ¼ 278); (b) kelp bass (n ¼ 229); (c) barred sand bass (n ¼ 160); and (d) California sheephead (n ¼ 148). Growth of black perch was significantly faster on natural reefs than on artificial reefs, but growth rates did not differ between reef types for the other three species (see the Results section). Fish performance on artificial reefs Page 5 of 11 Downloaded from http://icesjms.oxfordjournals.org/ at University of South Florida on June 7, 2014

Figure 2. Relationships between body weight (g) and total length (mm) on artificial and natural reefs of the following species: (a) black perch (n ¼ 298); (b) kelp bass (n ¼ 271); (c) barred sand bass (n ¼ 207); and (d) California sheephead (n ¼ 177). These relationships did not differ in slope or elevation between artificial and natural reefs, except for barred sand bass (see the Results section).

across the five reef pairs, densities were not significantly different reef type × region: F4,42 ¼ 1.8, p ¼ 0.14; Figure 7). Averaged across between the two reef types (reef type: black perch: F1,4.1 ¼ 5.8, reefs, each species had similar gonadal production on artificial reefs p ¼ 0.07; kelp bass: F1,4.0 ¼ 0.006, p ¼ 0.94; barred sand bass: relative to natural reefs (California sheephead: F1,3 ¼ 6.1, p ¼ 0.09; F1,4.0 ¼ 0.03, p ¼ 0.86). kelp bass: F1,4 ¼ 0.04, p ¼ 0.9; barred sand bass: F1,4 ¼ 0.06, Somatic tissue production was similar or higher on artificial reefs p ¼ 0.8). These patterns were statistically consistent among relative to natural reefs (Figure 6). Somatic production of California regions for California sheephead (reef type × region: F3,36 ¼ 2.2, sheephead and black perch was 2 times greater on artificial reefs p ¼ 0.10), but not for kelp bass or barred sand bass (F4,42 ¼ 8.6, than on natural reefs, a difference that was consistent among p , 0.001, and F4,42 ¼ 5.9, p , 0.001, respectively). regions in sheephead (reef type × region: F3,36 ¼ 1.6, p ¼ 0.21; Total tissue production (gonadal + somatic) of all species com- reef type: F1,3 ¼ 10.4, p ¼ 0.048), but inconsistent in black perch bined tended to be greater on artificial reefs than natural reefs, but (reef type × region: F4,42 ¼ 2.9, p ¼ 0.03; reef type: F1,4 ¼ 4.5, this pattern was not exhibited by all reef pairs (reef type × region: p ¼ 0.10). Somatic production of kelp bass and barred sand bass F4,42 ¼ 3.7, p ¼ 0.01; Figure 8) and thus, this difference wasnot stat- was similar on the reef types when averaged across reefs (F1,4 ¼ istically significant (reef type: F1,4 ¼ 2.1, p ¼ 0.22). Gonadal pro- 0.01, p ¼ 0.9; F1,4 ¼ 0.1, p ¼ 0.8, respectively), but the pattern duction accounted for 35% and somatic production for 65% of between the two reef types was inconsistent among regions (reef the total. Total production of the four target species combined 23 23 type × region: kelp bass: F4,42 ¼ 7.9, p , 0.001; barred sand bass: was 12.1 g m on artificial reefs and 8.3 g m on natural reefs. F4,42 ¼ 6.2, p , 0.001). Summed across all four species, somatic California sheephead exhibited significantly greater total tissue pro- production was 1.3 times higher on average on artificial than on duction on artificial reefs (F1,3 ¼ 11.6, p ¼ 0.04) and this trend was natural reefs, but this pattern was not statistically significant consistent among regions (reef type × region: F3,36 ¼ 1.4, p ¼ (F1,4 ¼ 1.2, p ¼ 0.3) because it was not evident at every reef pair 0.27). Total production of kelp bass and barred sand bass did not (reef type × region: F4,42 ¼ 3.9, p ¼ 0.009). differ between reef types (F1,4 ¼ 0.003, p ¼ 0.96; F1,42 ¼ 0.3, p ¼ 0.6), Gonadal tissue production summed across the target species was but again, there were inconsistent differences between pairs of 2 × greater on artificial reefs than on natural reefs, but this differ- reefs in different regions (reef type × region: kelp bass: F4,42 ¼ ence was not statistically significant (reef type: F4,4 ¼ 5.5, p ¼ 0.08; 8.0, p ¼ 0.002; barred sand bass: F4,42 ¼ 5.3, p , 0.001). Page 6 of 11 J. E. Granneman and M. A. Steele Downloaded from http://icesjms.oxfordjournals.org/ at University of South Florida on June 7, 2014

Figure3. Relationships between gut weight (g) and body weight (g) on artificial and natural reefs for (a) black perch (n ¼ 253) and (b) California sheephead (n ¼ 176). These relationships did not differ significantly between artificial and natural reefs for black perch, but did for California sheephead (see the Results section).

All three summed measures of tissue production (gonadal, somatic, and total) were correlated with the physical structure of the reefs. Principal component 1 (PC1) summarized 59% of the variation in substrate composition and was positively related to the per cent cover of large boulders (r ¼ 0.57), and negatively related to sand (r ¼ 20.37), cobble (r ¼ 20.50), and small boulders (r ¼ 20.49). All three measures of tissue production were positively correlated with substrate PC1 (r ¼ 0.63–0.71; p , 0.05; n ¼ 10; Table 1), which differed between reef types (paired t-test: t4 ¼ 4.71, p ¼ 0.01). Two of the three measures of production were negatively correlated with giant kelp density Figure 4. Relationships between reproductive potential of females (total: r ¼ 20.65; gonadal: r ¼ 20.70; both p , 0.05), which dif- (number of eggs in ovaries) and total length (mm) on artificial and fered between reef types (paired t-test: t4 ¼ 2.85, p ¼ 0.046). natural reefs for (a) California sheephead (n ¼ 103), (b) barred sand Summed gonadal production was also negatively correlated with bass (n ¼ 58), and (c) kelp bass (n ¼ 84). Reproductive potential was reef area (r ¼ 20.67, p , 0.05), which differed between reef types significantly higher on artificial reefs than natural reefs for California (t4 ¼ 3.86, p ¼ 0.02). The negative correlations between measures sheephead but did not differ between reef types for the other two of tissue production and giant kelp density and reef area may in species (see the Results section). fact be driven by substrate, because both area and kelp density were negatively correlated (collinear) with PC1 (r ¼ 20.86 and reef types: t4 ¼ 0.98, p ¼ 0.40), rugosity (which differed between 20.77, respectively, p , 0.05). Tissue production was not signifi- reef types: t4 ¼ 4.34, p ¼ 0.01), or invertebrate density (which cantly correlated with reef depth (which did not differ between tended to be higher on artificial reefs: t4 ¼ 2.52, p ¼ 0.065; Table 1). Fish performance on artificial reefs Page 7 of 11 Downloaded from http://icesjms.oxfordjournals.org/

Figure 5. Density (number m23) of fish on artificial and natural reefs in five regions of the following species: (a) black perch, (b) kelp bass, (c) barred sand bass, and (d) California sheephead. Values shown are means + s.e. at University of South Florida on June 7, 2014

Discussion California sheephead allocating extra energy from increased Our results indicate that fish living on artificial reefs generally fare as feeding to reproduction rather than somatic growth. well or better than those on natural reefs, although therewere excep- Black perch was the only species for which growth rates consist- tions to this pattern for certain species. California sheephead were ently differed between artificial and natural reefs, with faster growth more abundant and appeared to perform better on artificial reefs on natural reefs. Curiously, this faster growth was not mirrored by than on natural reefs. The only other differences that were relatively increased foraging success. Our estimate of foraging success (gut consistent across the five pairs of artificial and natural reefs were content + digestive tract weight relative to body weight) may have higher growth rates of black perch on natural reefs, which was been too coarse to detect important differences in diet that would offset by higher densities on artificial reefs, and very slightly be evident from detailed analysis of the gut contents. Prey preferred higher condition (weight-at-length) of barred sand bass on by black perch are closely tied to certain species of understory algae natural reefs. (Holbrook and Schmitt, 1992), which are less dense on artificial California sheephead fared better on artificial reefs than on reefs (R. Ambrose, D. Reed, and S. Schroeter, unpublished data). natural reefs most likely because the habitat on the artificial reefs Although neither the microinvertebrates consumed by black studied is more suitable for this species. California sheephead rely perch nor understory algae they inhabit were measured in this on cracks and crevices in rocky reefs for night-time shelter study, our unquantified observations indicated the understory (Topping et al., 2005). These were more abundant in the artificial algae was less abundant on the five artificial reefs we studied than reefs in our study, which were mostly composed of large boulders, on the five natural reefs (Granneman, personal observations). whereas the natural reefs were primarily composed of small Despite lower per-capita growth rates on artificial reefs, the produc- cobble (Granneman, 2011). In addition to providing more suitable tion of somatic tissue per cubic metre by black perch did not differ habitat for shelter, the artificial reefs also harboured denser assem- between the two reef types because densities of this species averaged blages of invertebrates (Granneman, 2011) upon which sheephead 2.5-fold higher on artificial reefs than on natural reefs. The higher feed (Johnson et al., 1994). This difference in food abundance was abundance of refuge in the form of cracks and crevices on artificial reflected in the higher foraging success of California sheephead on reefs may reduce the riskof predation relative to natural reefs. Fish in artificial reefs. Yet, higher foraging success on artificial reefs did these denser populations of black perch on artificial reefs may suffer not result in higher growth rates or condition, but was reflected in lower per-capita performance, both in terms of growth and repro- higher reproductive output. This result is consistent with ductive output (not measured in this study), due to lower food Page 8 of 11 J. E. Granneman and M. A. Steele Downloaded from http://icesjms.oxfordjournals.org/ at University of South Florida on June 7, 2014

Figure 6. Somatic tissue production (g m23) on artificial and natural reefs in five regions of the following species: (a) black perch, (b) kelp bass, (c) barred sand bass, (d) California sheephead, and (e) all species combined. Values shown are means + s.e.

density from sparse understory algae on artificial reefs as well as pos- present on four out of five reef pairs, but not the fifth pair. This sible density-dependent effects of crowding. fifth pair, the Wheeler J. North Artificial Reef and the San Mateo Condition (weight-at-length) of barred sand bass was statistical- natural reef, is informative. This artificial reef is physically most ly higher on natural reefs than artificial reefs, but we consider this similar to the natural reefs, being much larger than the other artifi- difference to be biologically trivial for two reasons. First, the magni- cial reefs, relatively low relief, low rugosity, and composed of smaller tude of the difference was very small, a 1.7% difference. Second, it boulders than the other artificial reefs (Granneman, 2011). The im- was not reflected in growth rate, nor was there an impact on repro- plication is that fish living on artificial reefs that most closely mimic ductive output. natural reefs physically will perform most like those on natural reefs, Fish tissue production per cubic metre summed across our though it would be worthwhile to evaluate more artificial reefs that study species tended to be higher on artificial reefs than on natural closely mimic natural reefs, given that we studied only a single reef reefs, though not statistically significantly because this pattern was that met that criterion. Fish performance on artificial reefs Page 9 of 11 Downloaded from http://icesjms.oxfordjournals.org/

Figure7. Gonadal tissue production (g m23) on artificial and natural reefs in five regions of the following species: (a) kelp bass, (b) barred sand bass,

(c) California sheephead, and (d) all species combined (excluding black perch). Values shown are means + s.e. at University of South Florida on June 7, 2014

We found that patterns of tissue production were driven mainly reproductive output, and tissue production are similar to those on by densities of the target species. In our system, this is because per- natural habitats. While our study addresses several relatively unex- capita somatic growth rates and reproductive output were generally plored aspects of fish performance on artificial reefs, it does not similar between reef types, as were size structures of the populations provide a comprehensive answer to the attraction–production (Granneman, 2011). In other systems, differences between size issue (Polovina, 1989; Bohnsack et al., 1997). To do so, we would structure or growth rates may exist between artificial and natural have had to measure mortality rates and recruitment rates in add- reefs, as La Mesa et al. (2010) found for Scorpaena porcus in the ition to the rates we measured, and we would have had to demon- Adriatic Sea, such that tissue production estimates might not strate that regional fish production increased when artificial reefs closely match population densities. Given the strong influence of were added. No study yet has quantified all of these parameters. size on reproductive output (e.g. Figure 4) and the relatively large Mortality rates, in particular, deserve further study because some proportion of total tissue production due to reproductive tissues studies have revealed that fish on artificial reefs die at higher rates (also noted by DeMartini et al., 1994), differences in size structure than on natural reefs due to increased fishing pressure (Matthews, between populations on artificial and natural reefs might be 1985; Solonsky, 1985). The densely aggregated fish on small artificial expected to strongly affect rates of tissue production on these two reefs may suffer high rates of mortality because they are more easily habitat types. targeted by fishers. The solution may be to create larger artificial Reef substrate composition, notably the abundance of large reefs to dilute targeted fishing effort. Although we did not quantify boulders (as summarized by PC1), was the best predictor of fish fishing pressure during this study, we observed higher concentra- tissue production. Most measures of fish tissue production were tions of fishing boats on the natural reefs than on the artificial positively related to this aspect of substrate composition. Tissue reefs. Fishing on reefs in the study region is often focused on the production was also negatively related to giant kelp density and edges of kelp beds, and the scarcity of kelp on the artificial reefs reef size. But here, collinearity among the predictor variables we studied may at least partly explain the apparently lower fishing makes it difficult to separate the roles of all the measured attributes pressure on them. of reefs. Studies that include more artificial reefs and that avoid con- This study provides evidence that artificial reefs can be useful in founding reef attributes (e.g. substrate composition and size) are mitigating impacts to natural reefs. Based on the indicators of fish needed to disentangle the roles that various attributes of artificial performance that we measured, artificial reefs in the Southern reefs play in setting fish tissue production. California Bight appear to meet the criteria stated by Carr et al. The results of our study indicate that artificial reefs can provide (2003) that, “if species perform equivalently or better on artificial good quality habitat for reef fish where critical rates such as growth, reefs than they do on natural reefs, it is most likely that the presence Page 10 of 11 J. E. Granneman and M. A. Steele Downloaded from http://icesjms.oxfordjournals.org/

Figure 8. Total tissue production (somatic + gonadal; g m23) on artificial and natural reefs in five regions of the following species: (a) kelp bass, (b)

barred sand bass, (c) California sheephead, and (d) all species combined. Values shown are means + s.e. at University of South Florida on June 7, 2014

Table 1. Correlations between three measures of fish tissue Supplementary data production and physical and biological attributes of reefs, tested Supplementary material describing biological attributes of the using reefs as replicates, including both artificial and natural reefs target species in this study and how tissue production was calculated (n ¼ 10). is available at ICESJMS online. Total Somatic Gonadal production production production Substrate 0.71 0.63 0.70 Acknowledgements PC1 Thanks to A. Bagdasaryan, without whose extensive help in the field Rugosity 0.58 0.51 0.59 and laboratory this work would not have been possible. We also ap- Depth 0.18 0.26 0.00 preciate the efforts of E. Leung, G. Salazar, M. Schram, and D. Bailey, Reef area 20.58 20.46 20.67 who helped with laboratory work. We thank L. Allen, S. Dudgeon, Invert. 0.61 0.55 0.58 and P. Edmunds for providing helpful comments, which greatly density improved this manuscript. This research was supported by Kelp density 20.65 20.54 20.70 funding from the following sources: COAST Graduate Student Pearson’s correlation coefficients (r) are given. Bold values represent Award for Marine Science Research, Graduate Fellowship for significant correlations at a ¼ 0.05. Outstanding Research Promise in Science and Mathematics, California State University Northridge’s Graduate Studies, and the Association of Retired Faculty Memorial Award. of an artificial habitat will benefit the regional population of that species ”. Our results support the commonsense view that artificial habitats that are most similar in physical structure to natural habi- References tats will function most like them; but also that relatively unnatural Ambrose, R. F. 1994. Mitigating the effects of a coastal power plant on a kelp forest community: rationale and requirements for an artificial (or at least unusual) habitat configurations (e.g. high relief, high reef. Bulletin of Marine Science, 55: 694–708. complexity) can function better than natural habitats from the per- Baca-Hovey, C., Allen, L. G., and Hovey, T. E. 2002. The reproductive spective of certain taxa. Whether intentionally designing artificial pattern of barred sand bass (Paralabrax nebulifer) from Southern habitats with unnaturalfeaturesto benefit certain species is desirable California. California Cooperative Oceanic Fisheries Investigations or wise will depend on the goals of the project. Reports 43. Fish performance on artificial reefs Page 11 of 11

Bohnsack, J. A., Ecklund, A. M., and Szmant, A. M. 1997. Artificial reef Northern Anchovy, Engraulis mordax, pp. 67–77. Ed. by R. L. research: is there more than the attraction–production issue? Lasker. Department of Commerce, NOAA Technical Report NMFS Fisheries, 22: 14–23. 36. Booth, D. J. 2014. Do otolith increments allow correct inferences about Johnson, T. D., Barnett, A. M., DeMartini, E. E., Craft, L. L., Ambrose, age and growth of coral reef fishes? Coral Reefs, 33: 255–258. R. F., and Purcell, L. J. 1994. Fish production and habitat utilization Carr, M. H., and Hixon, M. A. 1997. Artificial reefs: the importance of on a Southern California artificial reef. Bulletin of Marine Science, comparisons with natural reefs. Artificial Reef Management, 22: 55: 709–723. 28–33. La Mesa, M., Scarcella, G., Grati, F., and Fabi, G. 2010. Age and growth of Carr, M. H., McGinnis, V., Forrester, G. F., Harding, J. A., and the blackscorpionfish, Scorpaena porcus (Pisces: Scorpaenidae) from Raimondi, P. T. 2003. Consequences of Alternative artificial structures and natural reefs in the Adriatic Sea. Scientia Decommissioning Options to Reef Fish Assemblages and Marina, 74: 677–685. Implications for Decommissioning Policy. MMS OCS Study Love, M. S., Brooks, A., Busatto,D., Stephens, J.,and Gregory, P.A. 1996. 2003-053. Coastal Research Center, Marine Science Institute, Aspects of the life histories of the kelp bass, Paralabrax clathratus, University of California, Santa Barbara, California. MMS and barred sand bass, P. nebulifer, from the Southern California Cooperative Agreement Number 14-35-0001-30758. Bight. Fishery Bulletin, 94: 472–481. Cowen, R. K. 1983. The effect of sheephead (Semicossyphus pulcher) pre- Love, M. S., Brothers, E., Schroeder, D. M., and Lenarz, W. H. 2007. dation on red sea urchin (Strongylocentrotus franciscanus) popula- Ecological performance of young-of-the-year blue rockfish tions—an experimental analysis. Oecologia, 58: 249–255. (Sebastes mystinus) associated with oil platforms and natural reefs Downloaded from Cowen, R. K. 1986. Site-specific differences in the feeding ecology of the in California as measured by daily growth rates. Bulletin of Marine California sheephead, Semicossyphus pulcher (Labridae). Science, 80: 147–157. Environmental Biology of Fishes, 16: 193–203. Lowe, C. G., Topping, D. T., Cartamil, D. P., and Papastamatiou, Y. P. DeMartini, E. E., Barnett, A. M., Johnson, T. D., and Ambrose, R. F. 2003. Movement patterns, home range, and habitat utilization of 1994. Growth and production estimates for biomass-dominant adult kelp bass Paralabrax clathratus in a temperate no-take fishes on a Southern California artificial reef. Bulletin of Marine marine reserve. Marine Ecology Progress Series, 256: 206–216. http://icesjms.oxfordjournals.org/ Science, 55: 484–500. Mason, T. J., and Lowe, C. G. 2010. Home range, habitat use, and site Ellison, J. P., Terry, C., and Stephens, J. S., Jr. 1979. Food resource util- fidelity of barred sand bass within a Southern California marine pro- ization among five species of Embiotocids at King Harbor, tected area. Fisheries Research, 1: 93–101. California, with preliminary estimates of caloric intake. Marine Matthews, K. R. 1985. Species similarity and movement of fishes on Biology, 52: 161–169. natural and artificial reefs in Monterey Bay, California. Bulletin of Erisman, B. E., Allen, L. G., Claisse, J. T., Pondella, D. J., Miller, E. F., and Marine Science, 37: 252–270. Murray, J. H. 2011. The illusion of plenty: hyperstability masks col- Osenberg, C. W., St Mary, C. M., Wilson, J. A., and Lindberg, W. J. 2002. lapses in two recreational fisheries that target fish spawning aggrega- A quantitative framework to evaluate the attraction–production tions. Canadian Journal of Fisheries and Aquatic Sciences, 68: controversy. ICES Journal of Marine Science, 59: S214–S221. 1705–1716. Pickering, H., and Whitmarsh, D. 1997. Artificial reefs and fisheries ex- Eschmeyer, W. N., Herald, E. S., and Hammann, H. 1983. A Field Guide ploitation: a review of the “attraction versus production” debate, the at University of South Florida on June 7, 2014 to Pacific Coast Fishes of North America. Houghton Mifflin influence of design and its significance for policy. Fisheries Research, Company, Boston, USA. 336 pp. 31: 39–59. Froeschke, B., Allen, L. G., and Pondella, D. J. II. 2007. Life history and Polovina, J. J.1989. Artificial reefs: nothing more than benthic fish aggre- courtship behavior of black perch, Embiotoca jacksoni (Teleostomi: gators. California Cooperative Oceanic Fisheries Investigations Embiotocidae), from Southern California. Pacific Science, 61: Reports, 30: 37–39. 521–538. Powers, S. P.,Grabowski, J.H., Peterson, C. H., and Lindberg, W. J. 2003. Granneman, J. E. 2011. A comparison of fish production on artificial Estimating enhancement of fish production by offshore artificial and natural reefs in southern California. MS thesis. California reefs: uncertainty exhibited by divergent scenarios. Marine State University, Northridge. Ecology Progress Series, 264: 265–277. Hixon, M. A. 1981. An experimental analysis of territoriality in the Solonsky, A. C. 1985. Fish colonization and the effect of fishing activities California reef fish Embiotoca jacksoni (Embiotocidae). Copeia, on two artificial reefs in Monterey Bay, California. Bulletin of Marine 1981: 653–665. Science, 37: 336–347. Hobson, E. S., and Chess, J. R. 1976. Trophic interactions among fishes Tegner, M. J., and Dayton, P. K. 2000. Ecosystem effects of fishing in kelp and zooplankters near shore at Santa Catalina Island, California. forest communities. ICES Journal of Marine Science, 57: 579–589. Fishery Bulletin US, 74: 567–598. Topping, D. T., Lowe, C. G., and Caselle, J. E. 2005. Home range and Holbrook, S. J., and Schmitt, R. J. 1992. Causes and consequences of habitat utilization of adult California sheephead, Semicossyphus dietary specialization in surfperches: patch choice and intraspecific pulcher (Labridae), in a temperate no-take marine reserve. Marine competition. Ecology, 73: 402–412. Biology, 147: 301–311. Hueckel, G. J., Buckley, R. M., and Benson, B. L. 1989. Mitigating rocky Wang, D. 2010. Reproductive potential of temperate marine fishes on habitat loss using artificial reefs. Bulletin of Marine Science, 44: natural and artificial reefs. MS thesis. California State University, 913–922. Northridge. Hunter, J. R., Lo, N. C. H., and Leong, R. J. H. 1985. Batch fecundity in Wright, P. J., Metcalfe, N. B., and Thorpe, J. E. 1990. Otolith and somatic multiple spawning fishes. In An Egg Production Method for growth rates in Atlantic salmon parr, Salmo salar L: evidence against Estimating Spawning Biomass of Pelagic Fish: Application to the coupling. Journal of Fish Biology, 36: 241–249.

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