evaluation of eelgrass mitigation and fishery …

BULLETIN OF MARINE SCIENCE, 78(1): 115–131, 2006

115Bulletin of Marine Science© 2006 Rosenstiel School of Marine and Atmospheric Science of the University of Miami

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

ABSTRACTTo offset habitat loss and increase fishery production, an eelgrass mitigation habi-

tat was completed in San diego Bay, California in 1997. This mitigation effort con-sisted 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: Serra-nidae). 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 contin-ues at an increasing pace throughout the world. This is necessary due to the world-wide 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 impor-tant 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 fin-fish 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 habi-tat was completed in San diego Bay, California in 1997. This mitigation effort con-sisted 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, vOL. 78, NO. 1, 2006116

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 com-parison 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 asso-ciated 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 ad-dress 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 bot-tom 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 arti-ficial reefs (Polovina and Sakai, 1989; Pondella et al., 2002) due to the required syn-thesis 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 Mex-ican 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 re-cycled concrete blocks. Between the channel and the shoreline is the eelgrass transplant area (eelgrass enhancement). Zostera marina was transplanted into this area in fall 1997. 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

PONdELLA, II ET AL.: EELgRASS ANd FIShERy ENhANCEMENT IN SAN dIEgO BAy 117

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 win-ters 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 Panuli-rus 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 1998. The upper bay was also dredged during the winter of 2000–01, precluding sampling during this period. visibility was generally better on flood-ing 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 vis-ibility 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

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.


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 cor-relation 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 pro-gram. 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 correla-tion 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, du = 1.51 and if d > du 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 den-sities 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

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.

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 lengthReef 1 Quarry rock Horseshoe 20 12 39 42Reef 2 Concrete rubble Block 12 18 37 40Reef 3 Quarry rock Block 17 20 38 41Reef 4 Concrete rubble Horseshoe 12 24 41 42


densities by age class were calculated to analyze seasonal utilization. All statistics were com-pleted in STATISTICA (Release 6.1 Stat Soft, Inc.)

Results

Fishes were surveyed regularly from September 1997 to September 2002. We vis-ited the study site 44 times during this period and conducted 1056 transects. visibil-ity 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 enhance-ment 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, 1853. 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, 1854.

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 eel-grass 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 ver-tical 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 16.37 100 m−2, indicating initial attraction, not fishery production. This value increased to 43.19 100 m−2 in the final sampling period. By the end of this study this positive trend


Tabl

e 2.

The

ove

rall

mea

n ad

ult

dens

ity a

nd a

ssoc

iate

d st

anda

rd e

rror

s (S

E)

of fi

shes

for

the

fou

r en

hanc

emen

t re

efs

(Sta

tions

1–4

), t

hree

sof

t bo

ttom

sta

tions

(St

atio

ns 5

–8),

eel

gras

s en

hanc

emen

t are

a (S

tatio

n 8)

, eel

gras

s re

fere

nce

area

(St

atio

n 9)

, and

Zun

iga

Jetty

. For

sta

tion

loca

tions

, ref

er to

Fig

ure

1.

Stat

ion

12

34

56

78

9Z

unig

a

Spec

ies

nam

eC

omm

on n

ame

Fam

ilyM

ean

SEM

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SEM

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SEM

ean

SEM

ean

SEM

ean

SEM

ean

SEM

ean

SEM

ean

SEM

ean

SE

Oxy

lebi

us p

ictu

sPa

inte

d gr

eenl

ing

Hex

agra

mm

idae

0.05

0.05

0.07

0.07

0.01

0.01

0.08

0.04

Het

eros

tichu

s ro

stra

tus

Gia

nt k

elpfi

shC

linid

ae0.

030.

020.

030.

020.

020.

020.

010.

010.

010.

010.

060.

040.

010.

010.

020.

01

Seri

phus

pol

itus

Que

enfis

hSc

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0.19

0.19

Het

erod

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s fr

anci

sci

Hor

n sh

ark

Het

erod

ontid

ae0.

020.

020.

160.

08

Zapt

eryx

exa

sper

ata

Ban

ded

guita

rfish

Rhi

noba

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0.03

0.03

0.02

0.02

0.01

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0.03

0.03

0.02

0.02

0.02

0.02

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pun

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311.

205.

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6810

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2.72

7.49

3.08

0.13

0.09

0.35

0.35

95.2

79.

98

Hyp

sypo

ps r

ubic

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060.

030.

100.

0627

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1.75

Gir

ella

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rica

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pale

yeK

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sida

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280.

852.

070.

556.

701.

186.

751.

140.

310.

260.

050.

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150.

020.

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040.

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70

Em

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ae1.

590.

332.

590.

965.

681.

403.

310.

760.

210.

130.

230.

110.

020.

021.

260.

351.

531.

238.

340.

83

Para

labr

ax m

acul

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asci

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Spot

ted

sand

bas

sSe

rran

idae

2.78

0.48

3.37

0.47

2.63

0.50

3.42

0.56

1.39

0.18

1.34

0.15

1.11

0.20

1.01

0.13

2.10

0.28

0.45

0.10

Para

labr

ax c

lath

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bass

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anid

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360.

231.

710.

294.

070.

762.

670.

460.

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160.

120.

067.

520.

77

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5.48

2.21

2.60

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2.88

0.72

2.75

0.94

0.43

0.10

0.31

0.07

0.38

0.11

0.11

0.04

0.12

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2.85

0.44

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600.

281.

420.

730.

790.

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190.

129.

692.

20

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0.32

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1.58

3.81

0.75

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0.02

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0.02

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0.02

0.01

0.01

0.10

0.04


Tabl

e 2.

Con

tinu

ed.

Sta

tion

12

34

56

78

9Z

unig

aS

peci

es n

ame

Com

mon

nam

eF

amil

yM

ean

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ean

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ean

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Mea

nS

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ean

SE

Mea

nS

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ean

SE

Mea

nS

EU

mbr

ina

ronc

ador

Yel

low

fin

croa

ker

Sci

aeni

dae

0.12

0.12

0.02

0.02

Her

mos

illa

azu

rea

Zeb

rape

rch

Kyp

hosi

dae

0.01

0.01

0.11

0.08

All

ocli

nus

hold

eri

Isla

nd k

elpfi

shC

lini

dae

0.01

0.01

0.08

0.04

Med

ialu

na c

alif

orni

ensi

sH

alfm

oon

Kyp

hosi

dae

0.01

0.01

0.07

0.03

Par

alic

hthy

s ca

lifo

rnic

usC

alif

orni

a ha

libu

tP

aral

icht

hyid

ae0.

010.

010.

010.

010.

020.

010.

020.

020.

010.

01G

ibbo

nsia

ele

gans

Spo

tted

kel

pfish

Cli

nida

e0.

010.

010.

020.

020.

010.

010.

020.

02Sc

orpa

enic

hthy

s m

arm

orat

usC

abez

onC

otti

dae

0.02

0.02

0.05

0.02

Rhi

noba

tos

prod

uctu

sG

uita

rfish

Rhi

noba

tida

e0.

030.

030.

020.

02H

ypso

pset

ta g

uttu

lata

Dia

mon

d tu

rbot

Ple

uron

ecti

dae

0.01

0.01

0.04

0.02

Ple

uron

icht

hys

ritt

eri

Spo

tted

turb

otP

leur

onec

tida

e0.

020.

020.

010.

010.

020.

02H

ypso

blen

nius

jen

kins

iM

usse

l ble

nny

Ble

nnii

dae

0.01

0.01

0.02

0.02

0.01

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(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 po-tential 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; F3, 132 = 1.11, P = 0.346). There was a significant difference between the four replicated reefs in terms of adult fish abun-dance (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 (F1, 134 = 0.69, P = 0.418) nor was the concrete vs rock comparison (F1, 134 = 1.798, P = 0.182; Table 3). While there were slight differences in the mean densities in both of

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.


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 indistin-guishable.

The recruitment of yOy fishes to these reefs was seasonal and peaked in Septem-ber for all years (Fig. 6). The overall density of juvenile fishes was lower for reefs 1 and 4 (8.33 and 6.99⁄100 m2, respectively) than reefs 2 and 3 (13.94 and 14.95/100 m2, 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, uti-lized 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 den-sity 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-

Figure 4. Overall mean density of (A) adult and (B) YOY fishes for reefs 1–4. Error bars are 1 SE.


Table 3. ANOVA tables and associated analyses for interstation comparisons. * = significant value.

df MS F PReef 3 6.082 6.522 <0.0001*Error 132 0.933

Concrete vs rock 1 0.691 0.659 0.4185Error 134 1.050

Horseshoe design 1 1.871 1.798 0.1822Error 134 1.041Tukey’s HSD test, MS = 0.933, df = 132Reef 1 2 3 41 0.9794 0.0006* 0.10012 0.9795 0.0026* 0.22883 0.0006* 0.0026* 0.37274 0.1001 0.2288 0.3727

Figure 5. Mean densities of (A) adult and (B) YOY fishes for the enhancement reefs by sampling period. Error bars are 1 SE.


Figure 6. Monthly mean density (100 m2) 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.


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 (r2 = 0.05, P = 0.405 figure not shown). The relationship between subadult kelp bass and adults was slightly more predictive, but still not significant (r2 = 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 signifi-cantly increased their density compared to the eelgrass stations (Fig. 9). They were observed in very low densities in both eelgrass habitats. Utilization of the enhance-ment 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 sub-adult 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 Refer-ence 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 1999–2000 sampling season. Schools of jacksmelt and topsmelt were observed at the eelgrass enhancement area during these surveys. The influence of these school-ing 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

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.


diversity was slightly higher in the reference habitat (h´ = 2.23 vs 2.11). The species assemblages were significantly correlated (Kendall’s τ = 0.0289; 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 di-ego 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,

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 be-tween (B) YOY and subadult, and (C) subadult and adult barred sand bass with a 1 yr lag.


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 lo-cated 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 ex-perimental 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 Califor-nia (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 eel-grass 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 mate-rial, 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 in-creased throughout the study period. This trend was expected as a response to reef

Figure 10. Annual mean densities of adult fishes in the enhancement eelgrass habitat and the reference eelgrass habitat. Error bars are 1 SE.


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 indi-cates 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 hypoth-esis 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 habi-tats 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 de-veloping 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 through-out this study period.

The final aspect of this program was to use fish abundance to characterize the per-formance 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 enhance-ment 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 abun-dance 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.


Acknowledgements

This project would not have been possible without the support and assistance of M. Perdue, Southwest division, Naval Facilities Engineering Command and B. hoff-man 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.

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Addresses: (d.J.P.) Vantuna Research Group, Moore Laboratory of Zoology, Occidental Col-lege, 1600 Campus Rd., Los Angeles, California 90041. E-mail: <[email protected]>. (L.g.A.) Department of Biology, California State University, Northridge, Northridge, California 91330-8303. (M.T.C.) Scripps Institution of Oceanography, 9500 Gilman Drive, Mail Code 0208, La Jolla, California 92093-0208. (B.g.) University of Miami, Rosenstiel School of Marine and Atmospheric Science, Division of Marine Biology and Fisheries, 4600 Rickenbacker Causeway, Miami, Florida 33149.

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