Daniel J. Pondella, II, Larry G. Allen, Matthew T. Craig, and Brooke Gintert

Transcription

1 BULLETIN OF MARINE SCIENCE, 78(1): , 2006 Evaluation of Eelgrass Mitigation and Fishery Enhancement Structures in San Diego Bay, California Daniel J. Pondella, II, Larry G. Allen, Matthew T. Craig, and Brooke Gintert ABSTRACT To offset habitat loss and increase fishery production, an eelgrass mitigation habitat was completed in San Diego Bay, California in This mitigation effort consisted of the transplantation of eelgrass, Zostera marina L., in the western portion of the bay. In addition to the establishment of a new eelgrass bed, four enhancement reefs made of either quarry rock or concrete rubble were created to further enhance fishery stocks and the area s ecosystem. Two design criteria and a direct comparison between quarry rock and concrete reefs were examined in this 5-yr pilot program. The newly created eelgrass habitat quickly performed at the level of the existing eelgrass bed. The overall analysis found that the mitigation eelgrass habitat was not significantly different from the reference eelgrass habitat in terms of fishes. Neither reef material (quarry rock or concrete rubble) nor original reef design influenced fish utilization. In addition, aspects of fishery enhancement were examined on the enhancement reefs using three target species of Paralabrax (Perciformes: Serranidae). Resource utilization differed among these congeners with differing levels of production. Using enhancement reefs and eelgrass transplantation, enhancement and mitigation goals were achieved in San Diego Bay. Mitigation and enhancement to restore and offset habitat loss in estuaries continues at an increasing pace throughout the world. This is necessary due to the worldwide degradation and loss of these habitats and, in particular, the characteristic seagrasses found in estuaries (Short and Wyllie-Echeverria, 1996). This necessity is acute in southern California where approximately 90% of coastal wetlands have been lost (Zedler et al., 2001). This loss is of great concern since these areas act as important nursery areas for many nearshore fishes (Allen et al., 2002), as they do in other areas of the world (Pollard, 1984). Recently, long-term monitoring programs of finfish in southern California have found that offshore artificial reefs can be productive at or above the levels of natural reefs (Pondella et al., 2002; Stephens and Pondella, 2002). While mitigation continues to be a critical component of various artificial reef programs (Ambrose, 1994), the fisheries production aspect of artificial reefs has been used to offset or mitigate for habitat loss in various estuarine systems (Davis, 1985; Feigenbaum et al., 1989; Bortone et al., 1994; Kennish et al., 2002). Here we assess the combination of these two enhancement techniques in San Diego Bay, California. To offset habitat loss and increase fishery production, an eelgrass mitigation habitat was completed in San Diego Bay, California in This mitigation effort consisted of the transplantation of eelgrass, Zostera marina L., in the lower portion of the bay. In addition to the establishment of a new eelgrass bed, four enhancement reefs made of either quarry rock or concrete rubble were created as a pilot study for enhancement of fishery stocks and the area s ecosystem. In this experiment two types of reef material and two design criteria of the reef modules were examined. For the four reef modules there were two shape designs; two reefs had a mixed boulder Bulletin of Marine Science 2006 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 115

2 116 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 and cobble design (small cobble was placed on the upper perimeter between the reefs and eelgrass) versus reefs with only boulders. The second experiment was a comparison between concrete materials and quarry rock reefs. Quarry rock has been the artificial reef building material of choice in California due to its environmental acceptability (Lewis and McKee, 1989; Deysher et al., 2002). The Department of Fish and Game in California has strict guidelines for the use of concrete materials in the marine environment due to environmental concerns. This is the first experiment in California that tests these two substrates against each other in a paired design. The first objective of this multifaceted study was the description of the fishes associated with the eelgrass transplant area, the enhancement structures, and associated habitats. This was necessary not only to understand the dynamics of the target fish species populations on the enhancement reefs and in the eelgrass, but also to address these dynamics on a larger spatial scale, in particular the assemblage structure among the reefs, the eelgrass bed, and surrounding soft bottom habitats. Beginning in September 1997, immediately following reef construction and eelgrass planting, the fish enhancement structures, eelgrass transplant area, and surrounding soft bottom habitats were monitored regularly for 5 yrs by SCUBA divers. Concomitant with this monitoring, two reference sites, the closest naturally occurring eelgrass bed and the nearest rocky-reef, were also surveyed. In development of this mitigation effort, these reef designs had the goal of fisheries enhancement. Few studies have demonstrated localized stock enhancement for artificial reefs (Polovina and Sakai, 1989; Pondella et al., 2002) due to the required synthesis of multiple life history parameters (Bohnsack, 1989; Polovina, 1991; Carr and Hixon, 1997; Osenberg et al., 2002). However, in southern California various aspects of fish production including gonadal and somatic growth (De Martini et al., 1994), larval production (Stephens and Pondella, 2002), and the production of juvenile and adult fishes (Pondella et al., 2002) have been demonstrated. It is with this background that the recruitment, utilization, and production of fishery species were addressed. Materials and Methods Description of the Study Area. San Diego Bay lies a short distance north of the Mexican border and is the largest estuary south of San Francisco Bay in California (Fig. 1; Allen et al., 2002). The study site (Fig. 2) is found at the mouth of the bay and consists of four reef modules (reefs 1 4) set on the slope of the channel (dimensions given in Table 1). The shallow reaches of these reefs are at a depth of 4 m and they slope to a depth of 8 m. Reef height is 1 m with the exception of reef 3 where there is a single 2 m pile of material along the northern portion of the reef. The outer two reefs (reefs 1 and 4) were formed in a horseshoe design, which consisted of cobble added along their upper perimeter in the shape of a horseshoe. Reefs 1 and 3 were constructed of quarry rock while reefs 2 and 4 were constructed with recycled concrete blocks. Between the channel and the shoreline is the eelgrass transplant area (eelgrass enhancement). Zostera marina was transplanted into this area in fall Three sand bottom habitats (sands 5 7) that lie between the four reefs were also surveyed. Directly across the bay proximate to Shelter Island there is a shoal on which a persistent eelgrass bed was found and used as a reference (eelgrass reference). Both eelgrass habitats were at an average depth of 2 m. The other reference in the study was the submerged Zuniga Jetty that borders the outer channel of the harbor directly across from Pt. Loma. Zostera marina was successfully transplanted in the mitigation site at the onset of this study and it quickly developed into a lush eelgrass bed that persisted throughout the 5-yr period. Similarly, the four enhancement reefs were quickly colonized by Laminaria farlowii

3 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 117 Figure 1. Locations of the fishery mitigation site, including the eelgrass transplant area and the fishery enhancement structures. The eelgrass control area proximate to Shelter Island and the rocky reef control, Zuniga Jetty, across the channel from Pt. Loma are also depicted. Setch. (Phaeophyta). This alga was the dominant macrophyte in this system and blanketed the reefs. Other important phaeophytes were Sargassum muticum Yendo, present in the winters creating dense mats and Macrocystis pyrifera (Linnaeus) Agardh, which was present at low densities throughout the study. Macrocystis pyrifera would also intermittently raft into the study site and become snared upon the reefs. The chlorophyte, Codium fragile (Suringar) Hariot, was also present in low numbers. The reefs were also quickly colonized by Panulirus interruptus (J. W. Randall, 1840). Lobsters were the most prevalent macroinvertebrates throughout the study and were routinely observed in high densities on the reefs and they also frequented the eelgrass habitats. Overall, these newly created habitats were quickly colonized and remained healthy for the duration of the study. The location of the study site at the mouth of San Diego Bay precluded sampling during periods of high tidal flow. In addition to having limited visibility during slack tides, there was significant turbidity on numerous occasions, which precluded sampling. The lower bay, including the channel immediately proximate to the study site, was dredged from the fall of 1997 to the beginning of the summer The upper bay was also dredged during the winter of , precluding sampling during this period. Visibility was generally better on flooding tides due to the tidal flooding of offshore waters. However, the offshore water in San Diego can be quite turbid during periods of high runoff and large swells, further complicating visibility problems. Finding appropriate conditions for sampling was problematic. Fish Surveys. The protocols for surveying fishes were modeled after previously described techniques utilized in the southern California bight (Terry and Stephens, 1976; Stephens and Zerba, 1981; Stephens et al., 1984, 1994). Using the belt transect technique fishes observed 1 m to either side of the divers were identified to the lowest taxon possible and counted by age class; adults (A), subadults (S), and young-of-year (YOY). At the reef and sand stations (Fig. 2), divers swum along predetermined isobaths (4, 6, and 8 m) and the length of a transect was fixed by the perimeter of the reefs (Table 1). At the eelgrass enhancement and reference sites we conducted a minimum of three replicate, 5 min, 50 m transects along the 2 3 m isobath depending on tidal phase. At Zuniga Jetty we conducted three replicate, 5 min, 50 m transects

4 118 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Figure 2. The four enhancement reefs (1 4), the sand transects (5 7), and the eelgrass transplant area (8) in relation to NAS North Island. The reefs are on the slope of the channel. along the 6 and 8 m isobaths. We originally attempted transects along the 4 m isobath, but these were prevented by surge. Fish abundances were converted to densities by dividing the abundance by the area sampled on each transect. Analyses. All habitats were first compared by cluster analysis using the Pearson s R correlation coefficient. Further, Euclidean distances were calculated and used for non-metric multi-dimensional scaling (MDS). Comparisons among the enhancement reef designs were made using adult fish densities with a one-way analysis of variance (ANOVA). In this analysis the three transects (along the 4, 6, and 8 m isobaths) were treated as replicates and were not tested against each other. We sampled each reef on 34 sampling days during the 5-yr program. The mean adult fish density for each sampling period for each reef was calculated. Daily mean densities were used to avoid autocorrelation between replicates. These densities were transformed using the natural log to satisfy the assumption of normality, which was tested using Shapiro-Wilks w statistic. To address the potential autocorrelation between temporally concordant replicates, we examined first order serial correlation using the Durbin Watson d statistic from the residual analysis of the linear regression model (Studenmund, 1992). The results of this analysis produce values that range between 0 and 4: for positive serial correlation d = 0; for negative serial correlation d 4; and, no serial correlation d 2. This can be tested against the critical values of the Durbin Watson Test Statistic where k = 34, d u = 1.51 and if d > d u there is no positive serial correlation. Levene s test for homogeneity of variance was used to examine the final ANOVA assumption of homoscedasticity. The total mean densities of adult fishes in the eelgrass habitats were compared using a Mann Whitney U Test. A comparison of the entire fish assemblages between the two eelgrass habitats was completed using a Kendall s τ correlation. For fishery species, annual mean densities were calculated per reef and habitat by age class. When all age classes were present, the mean annual density for each age per reef was calculated. These densities were then correlated with the subsequent year class in a lagged analysis. Parametric data were correlated with Pearson s R statistic and Spearman s correlation coefficients were used for nonparametric data sets. Monthly mean Table 1. Dimensions and design for the four enhancement reefs. All reefs run in a north to south direction. The horizontal distance of Stations 5 7 are 58, 71, and 33 m, respectively. Enhancement reef dimensions (m) Material Design Northerly width Southerly width Shallow length Deep length Reef 1 Quarry rock Horseshoe Reef 2 Concrete rubble Block Reef 3 Quarry rock Block Reef 4 Concrete rubble Horseshoe

5 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 119 densities by age class were calculated to analyze seasonal utilization. All statistics were completed in STATISTICA (Release 6.1 Stat Soft, Inc.) Results Fishes were surveyed regularly from September 1997 to September We visited the study site 44 times during this period and conducted 1056 transects. Visibility was a significant problem for sampling. On four occasions visibility precluded all surveys. Visibility intermittently precluded surveys at various stations throughout the 5-yr study. The reef and sand stations were surveyed 34 times and on one of those occasions visibility precluded the surveys of the adjacent eelgrass enhancement area. Conditions allowed the eelgrass references area to be surveyed 29 times and Zuniga Jetty was surveyed on 22 occasions. On six occasions Zuniga jetty was workable while the other stations were not. We were never able to complete a survey on any site during May. Fifty-nine species of fishes from 27 families were observed during the 5-yr study period. The overall mean density (fish 100 m 2 ) and standard error of adult fishes by station is listed in Table 2. Table 2 also lists species richness and Shannon-Weiner Diversity (H ) values for each station. Xenistius californiensis (Steindachner, 1876) were observed only as YOY. The enhancement reefs (reefs 1 4) were comprised of a typical southern Californian rocky-reef fauna. The most commonly encountered fishes were Chromis punctipinnis (Cooper, 1863), Paralabrax clathratus (Girard, 1854), Paralabrax nebulifer (Girard, 1854), Girella nigricans (Ayres, 1860), and black perch Embiotoca jacksoni Agassiz, The main difference in ranks of abundance between these reefs and Zuniga Jetty was for Oxyjulis californica (Günther, 1861) and Hypsypops rubicundus (Girard, 1854). These two species were more abundant at Zuniga Jetty, most likely due to the differences in reef relief and maturity. Species richness for the eelgrass enhancement and reference was 32 and 28, respectively, and was similar to what was observed on the reefs (24 29 for reefs 1 4 and 30 at Zuniga Jetty). In the eelgrass habitats the most abundant species were Atherinops affinis (Ayres, 1860), Urobatis halleri (Cooper, 1863), Paralabrax maculatofasciatus (Steindachner, 1868), Embiotoca jacksoni Agassiz, 1853, and Cymatogaster aggregata Gibbons, The relationship of these habitats with regard to fish densities was examined using Pearson s correlation coefficients and MDS (Fig. 3). Zuniga Jetty was distinct from the eelgrass, sand, and enhancement reefs. Within the bay, two major clusters were delineated by habitat type. The four reefs formed one cluster and reefs 3 and 4 were most similar. The soft bottom stations formed the other grouping, with the two eelgrass stations found to be more similar to each other than to the sand stations. These relationships were further examined in the MDS plot. The first dimension separated the rocky reef habitats from the two soft bottom habitats, eelgrass, and sand. The second dimension distributed stations by relief. Eelgrass obviously offers greater vertical relief than sand, and the amount of vertical relief separates five rocky reefs with the exception of reef 4, which was closely related to reef 3. For adult fishes there was an overall increase in abundance throughout the 5-yr study (Fig. 4). In the first sampling period the mean density of adult fishes was m 2, indicating initial attraction, not fishery production. This value increased to m 2 in the final sampling period. By the end of this study this positive trend

6 120 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Table 2. The overall mean adult density and associated standard errors (SE) of fishes for the four enhancement reefs (Stations 1 4), three soft bottom stations (Stations 5 8), eelgrass enhancement area (Station 8), eelgrass reference area (Station 9), and Zuniga Jetty. For station locations, refer to Figure 1. Station Zuniga Species name Common name Family Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Oxylebius pictus Painted greenling Hexagrammidae Heterostichus rostratus Giant kelpfish Clinidae Seriphus politus Queenfish Sciaenidae Heterodontus francisci Horn shark Heterodontidae Zapteryx exasperata Banded guitarfish Rhinobatidae Chromis punctipinnis Blacksmith Pomacentridae Hypsypops rubicundus Garibaldi Pomacentridae Girella nigricans Opaleye Kyphosidae Embiotoca jacksoni Back perch Embiotocidae Paralabrax maculatofasciatus Spotted sand bass Serranidae Paralabrax clathratus Kelp bass Serranidae Paralabrax nebulifer Barred sand bass Serranidae Oxyjulis californica Senorita Labridae Urolophus halleri Round stingray Urolophidae Atherinops affinis Topsmelt Atherinopsidae Halichoeres semicinctus Rock wrasse Labridae Cymatogaster aggregata Shiner perch Embiotocidae Engraulis mordax Northern anchovy Engraulidae Cheilotrema saturnum Black croaker Sciaenidae Atherinopsis californiensis Jacksmelt Atherinopsidae Anisotremus davidsonii Sargo Haemulidae Rhacochilus vacca Pile perch Embiotocidae Rhacochilus toxotes Rubberlip seaperch Embiotocidae Semicossyphus pulcher California sheephead Labridae Ilypnus gilberti Cheekspot goby Gobiidae Gobiidae* Unidentified goby Gobiidae Phanerodon furcatus White seaperch Embiotocidae Hypsurus caryi Rainbow seaperch Embiotocidae Scorpaena guttata California scorpionfish Scorpaenidae

7 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 121 Table 2. Continued. Station Zuniga Species name Common name Family Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Umbrina roncador Yellowfin croaker Sciaenidae Hermosilla azurea Zebraperch Kyphosidae Alloclinus holderi Island kelpfish Clinidae Medialuna californiensis Halfmoon Kyphosidae Paralichthys californicus California halibut Paralichthyidae Gibbonsia elegans Spotted kelpfish Clinidae Scorpaenichthys marmoratus Cabezon Cottidae Rhinobatos productus Guitarfish Rhinobatidae Hypsopsetta guttulata Diamond turbot Pleuronectidae Pleuronichthys ritteri Spotted turbot Pleuronectidae Hypsoblennius jenkinsi Mussel blenny Blenniidae Myliobatis californica Bat ray Myliobatidae Micrometrus minimus Dwarf perch Embiotocidae Clevelandia ios Arrow goby Gobiidae Trachurus symmetricus Jack mackerel Carangidae Platyrhinoidis triseriata Thornback Rhinobatidae Syngnathus sp. Pipefish Syngnathidae Pleuronichthys verticalis Hornyhead turbot Pleuronectidae Pleuronectidae Unidentified turbot Pleuronectidae Hypsoblennius gentilis Bay blenny Blenniidae Sardinops sagax Pacific sardine Clupeidae Mugil cephalus Striped mullet Mugilidae Hyperprosopon argenteum Walleye surfperch Embiotocidae Pleuronichthys coenosus C-0 sole Pleuronectidae Caulolatilus princeps Ocean whitefish Malacanthidae Sebastes serranoides Olive rockfish Scorpaenidae Atractoscion nobilis White seabass Sciaenidae Mustelus sp.** Unid. smoothhound Charcharinidae Xenistius californiensis*** Salema Haemulidae Species Richness Shannon Wiener Diversity (H ) *These unidentified gobies were one of three species, Clevelandia ios (arrow goby) Ilypnus gilberti (cheekspot goby), or Quietula y-cauda (shadow goby). **This unidentified smoothhound was either a Mustelus californicus (gray smoothhound) or Mustelus henlei (brown smoothhound). ***Only observed as YOY.

8 122 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Figure 3. (A) MDS ordination of adult fish densities at all stations with Euclidean distances and cluster analysis (B) with Pearson s R correlation coefficient. (Pearson s R = 0.784) was continuing to increase, indicating that fish densities had not reached a plateau. Comparisons Between Various Enhancement Reef Types. To examine potential autocorrelation between temporally concordant surveys at reefs 1 4, a series of Durbin Watson d statistics were calculated. These were 2.18, 1.84, 2.01, and 1.60 for reefs 1 4, respectively; there was no positive or negative serial correlation. The variances were homogeneous (Levene s test; F 3, 132 = 1.11, P = 0.346). There was a significant difference between the four replicated reefs in terms of adult fish abundance (One-way ANOVA; F (3, 132) = 6.522, P < 0.001; Table 3). Reef 3 was significantly different from reefs 1 and 2, but not reef 4 (Tukey s HSD, Table 3, Fig. 5). Reef 3 had the highest vertical relief of the four modules and supported the highest density of adult fishes. The horseshoe vs non-horseshoe design was not significantly different (F 1, 134 = 0.69, P = 0.418) nor was the concrete vs rock comparison (F 1, 134 = 1.798, P = 0.182; Table 3). While there were slight differences in the mean densities in both of

9 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 123 Figure 4. Overall mean density of (A) adult and (B) YOY fishes for reefs 1 4. Error bars are 1 SE. these comparisons, this variance can be explained by the influence of reef 3 on the results (Fig. 5). Other than this unplanned high relief effect, the reefs were indistinguishable. The recruitment of YOY fishes to these reefs was seasonal and peaked in September for all years (Fig. 6). The overall density of juvenile fishes was lower for reefs 1 and 4 (8.33 and m 2, respectively) than reefs 2 and 3 (13.94 and 14.95/100 m 2, respectively; Fig. 4). These densities were not significantly different from each other (Mann Whitney U = 1.188, P = 0.234) due to the relatively high variance associated with these estimates. However, the overall density of first year fishes was increasing throughout the study period following the pattern shown for adult fishes (Fig. 5). Indicating continual and increasing recruitment to support the conclusion that the reefs were increasing localized fishery resources. Utilization by Fishery Species. Spotted sand bass, P. maculatofasciatus, utilized the study primarily as adults. For the entire study only five YOYs were observed in the entire study area. The utilization of the study site by adults was seasonal (Fig. 7). Their density was highest in the winter and lowest in spring. Their overall density was higher on the fishery enhancement structures than either of the eelgrass habitats indicating that these fishes preferred this habitat (Fig. 7). In fact, it appeared that there was an interaction or attraction effect between the reefs and the eelgrass mitigation site. The eelgrass enhancement habitat supported a significantly lower density of spotted sand bass when compared to the eelgrass reference suggesting at-

10 124 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Table 3. ANOVA tables and associated analyses for interstation comparisons. * = significant value. df MS F P Reef <0.0001* Error Concrete vs rock Error Horseshoe design Error Tukey s HSD test, MS = 0.933, df = 132 Reef * * * * Figure 5. Mean densities of (A) adult and (B) YOY fishes for the enhancement reefs by sampling period. Error bars are 1 SE.

11 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 125 Figure 6. Monthly mean density (100 m 2 ) of YOY fishes. Error bars are 1 SE and no transects were conducted during May. Figure 7. Mean density of spotted sand bass, Paralabrax maculatofasciatus, (A) by month for all reef sites, and (B) for each reef (1 4) and the eelgrass enhancement and reference sites. No observations were made in May. Error bars are 1 SE.

12 126 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Figure 8. Monthly mean densities of adult, subadult and YOY kelp bass, Paralabrax clathratus, for all reef sites. No observations were made in May. Error bars are 1 SE. traction to the adjacent enhancement reefs (Mann Whitney U = 4371, Z = 2.95, P = 0.003). Kelp bass, P. clathratus, utilized the study site throughout their ontogeny (Fig. 8). The utilization of these habitats by kelp bass was not seasonal. There was no significant relationship between various age classes between years. There was no significant correlation between first year fish versus subadult fish in a 1 yr lag (r 2 = 0.05, P = figure not shown). The relationship between subadult kelp bass and adults was slightly more predictive, but still not significant (r 2 = 0.13, P = 0.17; figure not shown). We observed more YOY kelp bass on the enhancement reefs than in any other habitat. For barred sand bass, P. nebulifer, the enhancement structures significantly increased their density compared to the eelgrass stations (Fig. 9). They were observed in very low densities in both eelgrass habitats. Utilization of the enhancement reefs by adult, subadult, and YOY barred sand bass were observed throughout the entire study period. The density of YOY positively predicted the density of subadult fishes the following year on the same reef (Spearman s R = 0.54, P = 0.03; Fig. 9). Similarly, the density of subadult fishes positively predicted the density of adult fishes in the lagged analysis (R = 0.67, P = 0.004; Fig. 9). Comparison of the Eelgrass Restoration Area to the Eelgrass Reference Area. The mean density at the eelgrass enhancement site was 22.4 adult fish 100 m 2 (SE = 5.7) and 10.6 adult fish 100 m 2 (SE = 2.2) at the eelgrass reference. The adult fish density within these two eelgrass habitats was not significantly different (Mann-Whitney U, Z = 0.300, P = 0.76; Fig. 10). The density of adult fishes in these two habitats was nearly indistinguishable for all years of the study except for the sampling season. Schools of jacksmelt and topsmelt were observed at the eelgrass enhancement area during these surveys. The influence of these schooling fishes caused the mean density of adult fishes to increase to 71.4 ind m 2 during this period, with an associated greater error in estimate of the mean. Otherwise the error estimates were quite low. Species richness and Shannon Wiener diversity were similar between the two eelgrass habitats. In the enhancement eelgrass habitat 32 species were observed versus 28 in the reference habitat (Table 2). Shannon-Wiener

13 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 127 Figure 9. (A) Mean density of adult barred sand bass, Paralabrax nebulifer, for each reef (1 4) and the eelgrass enhancement and reference sites. Error bars are 1 SE. Positive correlations between (B) YOY and subadult, and (C) subadult and adult barred sand bass with a 1 yr lag. diversity was slightly higher in the reference habitat (H = 2.23 vs 2.11). The species assemblages were significantly correlated (Kendall s τ = ; P = 0.147). Discussion The main objective of this study was to describe the fish utilization of newly created eelgrass beds, fisheries enhancement structures, and associated habitats. In addition to this assessment, we examined the potential for these novel structures in San Diego Bay to enhance fisheries in this region. Using the density of adult fishes we were able to describe the relationship between the eelgrass habitats, enhancement reefs,

14 128 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Figure 10. Annual mean densities of adult fishes in the enhancement eelgrass habitat and the reference eelgrass habitat. Error bars are 1 SE. soft bottom habitats, and Zuniga Jetty. The assemblages of these habitats clustered tightly by habitat type and relief. The fish assemblage at Zuniga Jetty was least similar to the remaining habitats. Zuniga Jetty was a mature high relief submerged jetty located at the entrance of the bay. However, its inclusion in this study helped illustrate the importance of three dimensional complexity or relief in the characterization of these fish assemblages. This factor somewhat confounded our enhancement reef experimental design. While we were able to detect significant differences between the replicated enhancement reefs, a result of the unplanned high relief component of reef 3 that had significantly higher density of adult reef fishes than reefs 1 and 2 but not reef 4. This complex result was most likely due to an interaction effect between reef 3 and 4. The distance between the two reefs is 33 m. Interestingly, this is the exact distance used to describe a halo effect around artificial reefs in southern California (Johnson et al., 1994). This halo effect is the primary area that fishes in southern California travel away from a reef module to forage. Thus, we hypothesize that reefs 3 and 4 are a linked system and the relatively short distance between the reefs explains this interaction. The implications of this interaction are significant for further reef module designs in this area. This interaction did not, however, completely obfuscate the experimental comparisons of concrete versus rock and horseshoe cobble versus no cobble design. The horseshoe design of reefs 1 and 4 did not increase the densities of juvenile fishes as was originally intended. In fact, while not statistically significant, the lower densities are the opposite of what these reefs were theoretically designed to do. The reason this happened was twofold. The cobble on the shallow perimeter of these reefs was not large enough to provide a sufficient amount of shelter for juvenile fishes minimizing its effectiveness. At the same time, this design excluded the eelgrass from growing proximate to reefs 1 and 4. This was not the case for reefs 2 and 3 where eelgrass grew close to their upper edge. There were no significant differences in overall fish utilization of these reef substrates or designs. Either type of reef material, concrete or rock, performed similarly throughout the experiment. While variation in reef type did not significantly affect fish utilization, overall reef performance with respect to fishery production of the three target species studied was also documented at various levels. Both the density of YOY and adult fishes increased throughout the study period. This trend was expected as a response to reef

15 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 129 community development and maturation. The most intriguing data were found in relation to the three fishery species. First, spotted bay bass, P. maculatofasciatus, were observed foraging over the entire enhancement area. Thus, while these reefs certainly attract spotted sand bass, the seasonal aspect of their utilization indicates that they are exploiting these habitats while alternative habitat sites were less available to them (i.e., in the winter) in San Diego Bay (Allen et al., 2002). Allen et al. (2002) found that the lowest abundances of fishes including spotted sand bass were in January (they sampled quarterly for five years). In addition, the absence of spotted bay bass from the artificial reef area during the spring and summer period is concomitant with their reproductive period. They have been reported to spawn from June through August (Allen et al., 1995). This analysis supports their hypothesis that spotted bay bass moves towards the mouth of the bay during the winter, which is consistent with the observed decreased density in the upper portions of the bay. These reefs appeared to be acting as a winter foraging area for spotted sand bass. All age classes of kelp bass, P. clathratus, were abundant on these reefs at all times of the year during this study, indicating that these reefs were able to attract both adults and recruits. There was not a significant correlation between age classes in the lagged analysis, suggesting that by kelp bass were transient and/or not exhibiting fidelity to a particular reef. This was not what we found for P. nebulifer, barred sand bass. YOY fishes were seasonally present on the four enhancement structures predominantly in the fall and winter. This timing was consistent with their settlement and juvenile development periods. Like kelp bass, subadult and adult fishes utilized these habitats consistently throughout the year. Further, in August 1999 large aggregations of barred sand bass were observed on the reefs. Whether or not these were spawning aggregations is unknown, however, this timing was concomitant with their spawning season. The seasonal use by YOY barred sand bass suggests that this species is developing on these reefs throughout their life history. This conclusion was supported by the 1-yr lagged correlation analyses between the three age classes. It appears that these enhancement reefs were able to attract and produce barred sand bass throughout this study period. The final aspect of this program was to use fish abundance to characterize the performance of the newly created eelgrass bed. This 5-yr time series showed that adult fishes quickly colonized the new eelgrass habitat, and within a year, the enhancement eelgrass bed was performing at a level almost identical to the reference eelgrass bed. Over the course of this study, the enhancement and reference eelgrass beds were similar in terms of species richness and Shannon-Wiener Diversity. Adult fish abundance and species composition were significantly comparable as well. Other than the influence of schooling fishes, fish utilization of this habitat was relatively constant, based upon the small error estimates, and colonization was rapid at the onset of the study; an indication that eelgrass habitat may be limiting in this system. Integrating enhancement reefs with eelgrass restoration in a southern California estuary was a unique and innovative design. These enhancement reefs can be built with either quarry rock or concrete rubble and the distance between reef modules may be an important concern for future projects. Our results demonstrated that, in addition to creating a vibrant and complex enhancement fish habitat, enhancement reefs increased localized fishery production in terms of both eelgrass restoration and production of our target species.

16 130 BULLETIN OF MARINE SCIENCE, VOL. 78, NO. 1, 2006 Acknowledgements This project would not have been possible without the support and assistance of M. Perdue, Southwest Division, Naval Facilities Engineering Command and B. Hoffman of the National Marine Fisheries Service. Funding was from the U.S. Navy. We would also like to thank M. Love, J. Stephens, Jr., and T. Maher for their critical reviews of this manuscript. Literature Cited Allen, L. G., A. M. Findlay, and C. M. Phalen Structure and standing stock of the fish assemblages of San Diego Bay, California from 1994 to Bull. S. Calif. Acad. Sci. 101: , T. E. Hovey, M. S. Love, and J. T. W. Smith The life history of the spotted sand bass (Paralabrax maculatofasciatus) within the southern California Bight. CalCOFI Rep. 36: Ambrose, R. F Mitigating the effects of a coastal power plant on a kelp forest community: rationale and requirements for an artificial reef. Bull. Mar. Sci. 55: Bohnsack, J. A Are high densities of fishes at artificial reefs the result of habitat limitation or behavioral preference? Bull. Mar. Sci. 44: Bortone, S. A., T. Martin, and C. M. Bundrick Factors affecting fish assemblage development on a modular artificial reef in a northern Gulf of Mexico estuary. Bull. Mar. Sci. 55: Carr, M. H. and M. A. Hixon Artificial reefs: the importance of comparisons with natural reefs. Fisheries 22: Davis, G Artificial structures to mitigate marina construction impacts on spiny lobster, Panulirus argus. Bull. Mar. Sci. 37: DeMartini, E. E., A. M. Barnett, T. D. Johnson, and R. F. Ambrose Growth and production estimates for biomass-dominant fishes on a southern California artificial reef. Bull. Mar. Sci. 55: Deysher, L. E., T. A. Dean, R. S. Grove, and A. Jahn Design considerations for an artificial reef to grow giant kelp (Macrocystis pyrifera) in Southern California. ICES J. Mar. Sci. 59: S201 S207. Feignebaum, D., M. Bushing, J. Woodward, and A. Friedlander Artificial reefs in Chesapeake Bay and nearby coastal waters. Bull. Mar. Sci. 44: Johnson, T. D., A. M. Barnett, E. E. DeMartini, L. L. Craft, R. F. Ambrose, and L. J. Purcell Fish production and habitat utilization on a southern California artificial reef. Bull. Mar. Sci. 55: Kennish, R., K. D. P. Wilson, J. Lo, S. C. Clarke, and S. Laister Selecting sites for largescale deployment of artificial reefs in Hong Kong: constraint mapping and prioritization techniques. ICES J. Mar. Sci. 59: S164 S170. Lewis, R. D. and K. K. McKee A guide to the artificial reefs of southern California. State of California, the Resources Agency, Department of Fish and Game, Sacramento. 73 p. Osenberg, C. W., C. M. St. Mary, J. A. Wilson, and W. J. Lindberg A quantitative framework to evaluate the attraction-production controversy. ICES J. Mar. Sci. 59: S214 S221. Pollard. D. A A review of ecological studies on seagrass-fish communities, with particular reference to recent studies in Australia. Aquat. Bot. 18: Polovina, J. J Fisheries applications and biological impacts of artificial habitats. Pages in W. Seaman, Jr. and L. M. Sprague, eds. Artificial habitats for marine and freshwater fisheries. Academic Press, Inc., San Diego. and I. Sakai Impacts of artificial reefs on fishery production in Shimamaki, Japan. Bull. Mar. Sci. 44:

17 PONDELLA, II ET AL.: EELGRASS AND FISHERY ENHANCEMENT IN SAN DIEGO BAY 131 Pondella, D. J., II, J. S. Stephens, Jr., and M. T. Craig Fish production of a temperate artificial reef based upon the density of embiotocids (Teleostei: Perciformes). ICES J. Mar. Sci. 59: S Short, F. T. and S. Wyllie-Echeverria Natural and human-induced disturbance of seagrasses. Env. Conserv. 23: Stephens, J. S., Jr. and D. J. Pondella, II Larval productivity of a mature artificial reef: the ichthyoplankton of King Harbor, California, ICES J. Mar. Sci. 59: S and K. E. Zerba Factors affecting fish diversity on a temperate reef. Env. Biol. Fish. 6: , P. A. Morris, K. Zerba, and M. Love Factors affecting fish diversity on a temperate reef: the fish assemblage of Palos Verdes Point, Env. Biol. Fish. 11: ,, D. J. Pondella, T. A. Koonce, and G. A. Jordan Overview of the dynamics of an urban artificial reef assemblage at King Harbor, California, USA, : a recruitment driven system. Bull. Mar. Sci. 55: Studenmund, A. H Using econometrics: a practical guide, 2 nd ed. HarperCollins Publishers, Inc., New York. 662 p. Terry, C. B. and J. S. Stephens, Jr A study of the orientation of selected environmental fishes to depth and shifting seasonal vertical temperature gradients. Bull. S. Calif. Acad. Sci. 57: Zedler, J. B., J. C. Callaway, and G. Sullivan Declining biodiversity: why species matter and how their functions might be restored in Californian tidal marshes. BioSci. 51: Addresses: (D.J.P.) Vantuna Research Group, Moore Laboratory of Zoology, Occidental College, 1600 Campus Rd., Los Angeles, California <pondella@oxy.edu>. (L.G.A.) Department of Biology, California State University, Northridge, Northridge, California (M.T.C.) Scripps Institution of Oceanography, 9500 Gilman Drive, Mail Code 0208, La Jolla, California (B.G.) University of Miami, Rosenstiel School of Marine and Atmospheric Science, Division of Marine Biology and Fisheries, 4600 Rickenbacker Causeway, Miami, Florida

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