Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

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Journal of Experimental Marine Biology and Ecology

j ourna l homepage: www.e lsev ie r.com/ locate / jembe

Habitat use, movements and site fidelity of the gray smooth-hound shark(Mustelus californicus Gill 1863) in a newly restored southern California estuary

Mario Espinoza ⁎, Thomas J. Farrugia 1, Christopher G. Lowe 1

California State University, Long Beach, CA 90840, USA

⁎ Corresponding author at: Present/permanent addPesquera y Acuicultura, Centro de Investigación en CUniversidad de Costa Rica, 2060 San José, Costa Rica. Tefax: +1 562 985 8878.

E-mail addresses:marioespinozamen@gmail.com (M(T.J. Farrugia), clowe@csulb.edu (C.G. Lowe).

1 Tel.: +1 562 985 4918 (office); fax: +562 985 887

0022-0981/$ – see front matter © 2011 Elsevier B.V. Aldoi:10.1016/j.jembe.2011.03.001

a b s t r a c t

a r t i c l e i n f o

Article history:Received 15 November 2010Received in revised form 27 February 2011Accepted 2 March 2011

Keywords:Acoustic telemetryBenthic predatorEcological functionHabitat restorationMustelus californicusSeasonally thermal environmentSouthern California estuary

It is thought that some elasmobranchs use shallow temperate estuaries during warmer months because thesehabitats may provide thermal physiological advantages. However, extensive loss and degradation of southernCalifornia bays and estuaries has reduced coastal species access to estuarine habitats. While restoration ofsouthern California estuaries has increased over the last two decades, little is known about the recovery ofecological function. Top predators are thought to be important indicators of restoration of ecological functionin many ecosystems, including estuarine habitats. In this study, abundance surveys and acoustic telemetrywere employed to examine how gray smooth-hound sharks (GSH) use the newly restored Full Tidal Basin(FTB) of Bolsa Chica. GSH were most abundant inside the FTB during the spring and summer, and numbersdecreased during the winter. Over 83% of all individuals (n=336) caught were immature juveniles and weremost abundant when water temperatures were between 20 and 22 °C. Sharks fitted with acoustictransmitters (n=22) were continuously detected for 6–153 days (August 2008–December 2009). Foraysinto coastal waters were uncommon until individuals left for the season. GSH selected warmer habitats withinthe middle FTB; however, they also exhibited diel movements along the basin. GSH were most often foundassociated with mud and eelgrass at night, presumably for feeding. Since its restoration, population andbehavioral data suggest that the FTB may provide juvenile GSH with a suitable seasonal environment forfeeding and growth.

ress: Unidad de Investigacióniencias del Mar y Limnología,l.: +1 562 985 4918 (office);

. Espinoza), tfarrugi@csulb.edu

8.

l rights reserved.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

The extensive habitat loss and degradation of southern Californiawetlands has reduced coastal species access to estuarine environ-ments (Gillanders et al., 2003). As a result, restoration has become apopular approach to offset loss of estuarine habitats (Zedler, 2005).While restoration of southern California estuaries has increased overthe last two decades, studies measuring the recovery of ecologicalfunction have been limited (Roberts, 1993). Due to the lack of baselineinformation on ecologically mature restored habitats (10 years ormore since restoration), restoration should presently be viewed withcaution, and the ability to assess ecological function remains criticalfor conservation. Top predators such as sharks and rays are thought tobe important indicators of restoration of ecological function in manyecosystems, including bays and estuaries (Berger and Smith, 2005;Sergio et al., 2008). Patterns of abundance and behaviors of predatory

fish inside restored habitats may provide critical information neededto assess their ecological function.

Many coastal elasmobranchs along the Southern California Bight(SCB) use bays and estuaries for feeding, mating and breeding;unfortunately, information on the degree of site fidelity, habitat useand philopatry is often not available (Lowe and Bray, 2006). Thesehighly productive habitats also function as spawning and nurserygrounds (Castro, 1993; Rooper et al., 2006; Conrath and Musick, 2010),migratory pathways (Ray, 2005; Collins et al., 2007), and areas naturallysupporting large fish biomass (Allen et al., 2002). In southern California,long-term abundance data suggest that most elasmobranchs arestrictly marine or marine migrants (Allen et al., 2006). Conversely,recent studies on population composition and elasmobranch behaviorare showing that some of these species (e.g. leopard sharks Triakissemifasciata, round stingrays Urobatis halleri, and brown smooth-houndsharks Mustelus henlei) use estuarine habitats for extended periods oftime and even across years (Jirik, 2009; Carlisle and Starr, 2009; Camposet al., 2009). Therefore, patterns of site fidelity and inter-annualuse remain uncertain for many coastal elasmobranchs due to the lackof quantitative behavioral data.

The gray smooth-hound shark (GSH), Mustelus californicus (Gill1863), is a benthic coastal predator commonly found on continentalshelves, and in shallow muddy bays and estuaries of California (Millerand Lea, 1982). Large numbers of GSH have been observed inside

64 M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

estuarine habitats from southern California during the spring andsummer (Miller and Lea, 1982; Allen et al., 2002). Some elasmobranchsare thought to use shallow temperate estuaries during warmer monthsbecause these habitats may offer thermal physiological advantageswhen animals are foraging (e.g. increased growth, reproduction andgastric evacuation rates) relative to colder coastal areas (Hight andLowe, 2007; Bethea et al., 2007; Jirik, 2009). Therefore, it is possiblethat GSH may be using shallow estuarine habitats on a seasonalbasis for feeding and reproduction. However, it is unclear how longindividuals stay inside estuarine environments, what kind of habitatsthey use, and if they return to the same estuaries every year.

The Full Tidal Basin (FTB) of Bolsa Chica is a newly restored estuarylocated in southern California (Fig. 1). The opening of this new habitatallowed larval dispersal and a supply of invertebrate colonists fromnearshore areas, and thus the establishment of an early benthiccommunity. The FTB is presumed to function as a natural estuary,providing a suitable warmer environment for coastal species,including sharks and rays. Documenting seasonal abundances andbehavioral patterns of GSH inside this new habitat may providecritical information necessary to assess its ecological function. Herewe examined the population composition, habitat use, movementsand site fidelity of GSH inside the FTB. Since access to the FTB hasonly been recently available, this was a unique opportunity to use

Fig. 1. a) Map of the FTB of Bolsa Chica in Huntington Beach, California, USA. Fishing samplinmaps. Black dashed lines indicate the division between inner, middle and outer zone.

a benthic coastal predator as an indicator of recovery of ecologicalfunction. Abundance surveys and acoustic telemetry were employedto test the following predictions: 1) the relative abundance of GSH inthe FTB will be higher during the spring and summer; 2) GSH willexhibit seasonal site fidelity to the FTB during warmer months andacross years; and 3) GSH will use and select mainly warmer habitatsavailable within the FTB.

2. Materials and methods

2.1. Study site

Historically, Bolsa Chica used to be part of an extensive tidal marshwetland, with associated tidal embayments, sloughs, mudflats anddirect access to the ocean. During the last century the site was alteredby filling, oil extraction activities, flood control operations, andhydrologic modifications (U.S. Fish and Wildlife Service, 2001). InAugust 2006, a new tidal inlet (20 m×100 m long channel) restoredcoastal access from the Pacific Ocean (Fig. 1). Prior to thismodification,the only access to the wetlands was through Anaheim Bay andHuntingtonHarbor (Carlberg, 2009). The newly restored FTB is a small,shallow embayment (approx. 1.48 km2)with a deeper central channel(b4 m depth; 1.3 m tidal range) and intertidal mudflats (Fig. 1). The

g locations recorded during b) long-lines, and c) and beach seines are shown in smaller

65M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

FTB is not connected to the Bolsa Chica Ecological Reserve, andthere are no freshwater inputs, which is typical of many southernCalifornia estuaries (Carlberg, 2009). Hyper-spectral data of the FTBwere obtained from the WeoGeo Spatial Library (WeoGeo, 2007).Qualitative information on substrates available was complementedwithmulti-beam sonar surveys performed byMerkel & Assoc., Inc., andthe bathymetry was mapped over a 50×50 m grid. This informationallowed us to estimate the percentage of depth and habitats availablein the FTB.

2.2. Abundance and population composition

Between June 2008 and September 2009, abundance surveys wereemployed to examine spatial and temporal changes in abundances,and characterize size and sex composition of the population of GSH.The FTB was divided into three similar sized zones (inner, middle, andouter) and GSH were captured during daylight hrs using long-linesand beach seines (Fig. 1). Date/time, substratum, depth, and fishinglocations were recorded during each set. A datalogger (StowAwayTidbit; accuracy±0.2 °C) was attached to the fishing gear and set torecord sea-floor temperatures at 30 s intervals.

A large beach seine (26 m×2.5 m) fitted with a 2.8×2.8×2.8 mbag (5.0 cm mesh in wings; 1.0 cm mesh in bag) and a small seine(20 m×1.2 m; 3 mm mesh) were used to capture fish and inverte-brates at low tides in shallow intertidal habitats. Additionally, a 100 mlong polyethylene long-line was used to target GSH in the deeperchannel duringhigh and incoming tides. Long-lines had 10 interspacedgangions, each with a 3 m long monofilament line (36 kg test) and abarbless circle hook (Mustad #4/0-5/0) baited with fresh squid. Beachseine Catch Per Unit Effort (CPUE) was defined as the number ofindividuals caught per net set (individual×net set−1), while long-lineCPUE was expressed as the number of sharks caught per hook×time(sharks×hook h−1). The number of hooks×h was calculated bymultiplying the number of hooks deployed in each set by the soak time(time from first hook in the water to first hook out).

GSH caught in the FTB were measured, weighed and externallyfitted with a Peterson disc tag in their first dorsal fin for identification.Estimated size at maturity for females was based on reproductive dataobtained from Yudin and Cailliet (1990). Length and calcification ofclaspers were used to assess male maturity. Males over 65 cm StretchTotal Length (STL) with calcified claspers, and females over 70 cm STLwere considered sexually mature. Males between 60 and 65 cm STLand females between 65 and 70 cm STL were considered sub-adults,while males between 40 and 60 cm STL and females between 40 and65 STL were categorized as juveniles. GSH less than 40 cm STL withopen yolk scars (ageb3 week) were categorized as newborns.

GSH captured during long-lines and beach seines were analyzedto examine size and sexual segregation patterns. Temporal changesof abundance were examined over monthly periods. Long-line CPUEwas also pooled and analyzed over seasons and zones. Seasonswere defined as 1) summer 2008 (Jun–Aug), 2) fall 2008 (Sep–Nov),3) winter 2008–09 (Dec–Feb), 4) spring 2009 (Mar–May), and5) summer 2009 (Jun–Aug). Differences in long-line CPUE amongseasons (fixed effect) and zones (random factor) were tested usinga mixed GLM model (SAS System). Post-hoc multiple comparisons(Tukey's HSD, α=0.05) were used to determine which seasonsand zones were significantly different from each other. Data werelog-transformed [(log(x+1)] for normality and equality of variances(Zar, 1999).

2.3. Site fidelity and seasonal residency

Twenty-two sharks were internally fitted with a coded tag (VemcoV13-1L-R64k, 69 kHz) with nominal code transmission delay of 60 s(40–80 s range) and a battery life of approximately 700 day. Sharkswere placed into a tub filled with fresh seawater and quickly inverted

to achieve a state of tonic immobility (Henningsen, 1994). A 1 cmincision was made in the ventral midline and a small transmitter wasplaced into the peritoneal cavity. The incision was closed with 2interrupted surgical sutures (Ethicon Chromic Gut 2–0) and sharkswere kept in fresh seawater until they exhibited clear signs of smoothswimming behavior (CSULB IACUC Protocol #254).

The presence and movements of acoustically tagged individualswere monitored using a gridded array of 16 VR2W omnidirectionalacoustic receivers (Vemco Ltd, Nova Scotia) with overlapping detectionranges deployed throughout the entire embayment (Fig. 1). Receiverswere deployed at similar depths (approx. 2.0 m) and secured to a lineanchored to the bottom. Temperature loggers were attached to eachreceiver to monitor thermal gradients (5 min intervals) throughoutthe FTB (Fig. 2a). An additional logger was secured to a piling of thebridge to monitor temperatures in the ocean inlet. Daily temperaturedata from adjacent coastal waters were obtained from the SouthernCalifornia Coastal Ocean Observing System. These data allowed forcomparison of water temperatures inside and outside the FTB.

Range tests were conducted prior to tagging and deployment oftelemetry equipment to determine the acoustic range and detectionefficiency of each receiver (Simpfendorfer et al., 2008). A single codedtransmitter (Vemco V13-1L-R64k, 69 kHz) was placed at 10 fixedlocations for approximately 2 h. Acoustic range varied between 350and 900 m (N85% detection efficiency); however, a conservative250 m range was used to increase the area of overlapping detectionsby three or more receivers.

The degree of seasonal site fidelity of GSH to the FTB (% of timeanimals spent within the estuary) was determined by dividing thetotal number of days an individual was detected inside the basin bythe monitoring period of the study during the 2008 and 2009 seasons.Site fidelity indices were also calculated for each shark, and wereaveraged across weeks and months. For this analysis, the number ofdays an individual shark was detected inside the basin was divided bynumber of days per week/month during each monitoring period.

2.4. Movements and habitat use

Eight synchronizing transmitters or “sync tags” (Vemco 16-5H-R64k, 69 kHz)with a nominal code transmission delay of 300 s (range:200–400 s) were also deployed within the array to synchronize theinternal clocks of the receivers (Fig. 1). Sync tags were positionedb150 m from each receiver to ensure that they were detectedconsistently, which was necessary for the best possible timesynchronization. Differences in arrival times of detections to three ormore receivers were used to triangulate an individual shark's position.This new Vemco VR2W Positioning System (VPS) of acoustic receiversand sync tagswas used to quantify longer-term, fine-scalemovementsand habitat use ofmultiple GSH simultaneously (Espinoza et al., 2011).

VPS data and horizontal position error (HPE) were analyzed usingVemco VPS Software (Vemco Ltd, Nova Scotia) before positions wererendered. HPEwas based on the error sensitivity of the receiver layoutemployed, calibrated to local environmental conditions. Data wereclassified according to tides (low slack, high slack, incoming, outgoing)and diel stage (day, night, crepuscular). Tide and sunset/sunrise datawere obtained from NOAA (www.ndba.noaa.gov). High and low tideswere assumed to occur 1 h before and after high and low tide times,respectively. Crepuscular periods were defined as 1 h before and 1 hafter sunrise and sunset. Only VPS estimates with b15 m HPE wereincluded in the analyses. Additionally, sample locations wererandomly selected from each shark using a bootstrapping approachin order to correct for autocorrelation in time-series data (Politis,2003; Rogers and White, 2007). Three sharks had consistently lowerVPS positions compared to the rest so they were eliminated fromfurther analyses.

Shark movements among zones were examined using ArcMap9.2® (ESRI, Redlands, California) were used to examine. Mixed GLM

Fig. 2. a) Daily water temperature difference (minimum, maximum and running average) between the FTB and coastal waters. Warmer temperatures recorded inside the FTB areindicated by positive values. Black arrow indicates the shift in the temperature regime at which coastal waters became warmer than the FTB; b) mean monthly Catch per Unit Effort(CPUE±SE) of gray smooth-hounds captured with long-lines and beach seines. Gray solid line indicates mean daily water temperature for the FTB of Bolsa Chica.

66 M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

models were performed to determine the effect of sex, tides and dielstage on horizontal distance traveled. Data were log-transformed[(log(x+1)] prior to analyses for normality and equality of variances.Rate of movements (ROMs) were also used to examine diel and tidalpatterns. ROMs were calculated by dividing distance traveledbetween successive positions by the time interval between positionreadings. However, data could not be effectively transformed to fit anormal distribution. Therefore, a Kruskall–Wallis non-parametric test,followed by Dunn's pairwise comparisons was employed.

The center of activity (COA) and home ranges for each shark weredetermined to examine shark distribution and activity space. Thegeometric COAwas calculated by dividing themean of all X coordinatelocations by the mean of all Y coordinate locations from a particularshark. A test of homogeneity (χ2) was used to compare the distri-bution of shark locations from the mean COA (at 50 m increments)during day and nighttimes. Minimum convex polygon (MCP) andkernel utilization distribution (KUD) were used as estimates of ashark's home range. MCP is the smallest convex polygon that includesall individuals' locations, while KUD is a probability distributionapproach of finding an individual location within an area. The AnimalMovement Analyst Extension from ArcView 3.3® (Hooge andEichenlaub, 1997) was used to calculate MCP and KUD. KUD wereestimated using bivariate normal density kernel to determine thearea of use. The 95% KUD is considered a measure of the overall homerange of an animal (b5% excursions), while the 50% KUD is morerepresentative of the area of core use. Uninhabitable areas (i.e., land)were excluded from the analysis to prevent an overestimation ofthe true size of the activity space (ArcMap 9.2®). Mixed GLM modelsusing individuals as a random factor were performed to examine the

effect of sex and diel stage (day and night) on the size of activity space(MCP, 50% and 95% KUD).

Natural neighbor interpolations were employed to create depthand habitat layers of the FTB (ArcMap 9.2®; Johnston et al., 2001).Subsamples were randomly selected from each shark, and individual'slocations were classified according to habitats and depths. MCP areasfrom each shark were used to quantify habitat utilization. A 10 meelgrass buffer was defined as the edge between soft-mud andeelgrass habitats. Two log-likelihood tests (χ2) were performed usingSAS System 9.0 to examine heterogeneity and habitat selection duringday and night hrs (Manly et al., 2002; Rogers and White, 2007). Thefirst log-likelihood test (χL1

2 ) was used to determine if GSHwere usingthe various habitat types in a similar way,

χ2L1 = 2∑n

j−1∑li=1uij loge

uij�E uijð Þ

h i;

where E(uij)=ui+u+ j/u++, uij is the amount of habitat type i used byshark j; ui+ is the amount of habitat type i used by all sharks; u+ j is thetotal amount of habitat units used by shark j; and u++ is the totalnumber of habitat units used by all sharks. Large values indicateheterogeneity among habitat types. Habitat selectionwas investigatedusing a second log-likelihood test(χL2

2 ),

χ2L2 = 2∑n

j−1∑li=1uij loge

uij�E uijð Þ

h i;

where E(uij)=πi+u+ j, and πij is the proportion of availableresource units that are in category i. Selection is indicated withvalues greater than one, while avoidance is indicated with ratios

Table 1Number of gray smooth-hounds (GSH) captured, size ranges, and sex ratio. STL =stretch total length. Monthly sex ratios (ratio of females to males) different from a 1:1ratio are indicated by * (α=0.05).

Month No. GSHcaptured

Size rangeSTL (cm)

Sex ratio(% females)

(sex ratio 1:1)P-value

June 2008 34 45.2–70.7 41.2 0.303July 2008 45 44.1–69.8 62.2 0.101August 2008 64 45.9–71.1 57.8 0.211September 2008 40 51–73.9 50.0 –

October 2008 16 51.4–107.4 68.8 0.134November 2008 7 50–74.4 42.9 0.705December 2008 1 61.5 0.0 0.317January 2009 4 47.6–71 50.0 –

February 2009 3 52.3–54.2 33.3 0.564March 2009 14 42.5–66.1 57.1 0.593April 2009 32 47.2–101.4 18.8 b0.0001⁎

May 2009 57 40.6–85.5 54.4 0.508June 2009 24 42.9–94.8 70.8 0.041⁎

July 2009 34 49.1–76.6 67.6 0.040⁎

August 2009 16 46.5–81.3 31.3 0.134September 2009 29 49–87.2 75.9 0.005⁎

Total 420 40.6–107.4 54.3 0.079

67M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

less than one. Confidence intervals (CI) were calculated using thestandard error (SE):

SE wi

� �=

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffin

n−1ð Þ u++� �∑n

j=1

uij

πi−wi u+ j

� �� 2:

s

A spline with barrier interpolation approach (ArcMap 9.2®) wasused to create thermal raster layers of the FTB. Thermal layers werethen overlaid with VPS data on a 50×50 m grid. This allowed us toquantify the frequency of temperatures use and available (χ2) at30 min intervals over the entire study period. A paired t-test was alsoemployed to calculate individual differences in temperatures usedand available inside and outside the FTB.

Teleost fish and invertebrates from beach seines were used toestimate potential prey available. Only taxonomic groups previouslyidentified in the diet of GSH were included as potential prey in theanalysis (San Filippo, 1995). Seasonal and spatial patterns wereexamined using an ANOVA followed by post-hoc multiple comparisons

Fig. 3. Mean seasonal Catch per Unit Effort (CPUE±SE) of gray smooth-houn

tests (Tukey's HSD, α=0.05). Data were log-transformed [(log(x+1)]for normality and equality of variances.

3. Results

3.1. Abundance and population composition

A total of 224 long-line sets and 156 beach seines were deployedthroughout the FTB. Overall, 420 GSH were captured and externallytagged between June 2008 and September 2009. More GSH werecaught using long-lines (n=298; 69.6%) than beach seines (n=130;30.4%). GSH abundance increased during spring and summer anddecreased during fall and winter months. Despite comparable fishingefforts across months, more sharks were captured in the summer of2008 (n=188; 44.9%) than 2009 (n=109; 22.2%).

Greater proportions of females than males were observed duringJune, July and September 2009. Conversely, males were significantlymore abundant than females in April 2009 (Table 1). Size range ofmales (46–79 cmSTL) and females (44–107.4 cmSTL)was statisticallysimilar (t=−0.26, df=401, p=0.798). Newborns or individualssmaller than 40 cm STL were absent during the study period. Juveniles(73.2%; n=295) and sub-adults (11.8%; n=45) made up 84% of thetotal catch, while only 16% (n=63) of the sharks found inside the FTBwere mature. GSH larger than 80 cm STL (b3%) were uncommon andonly represented by females.

Although GSH were captured throughout the FTB, a greaterproportion occurred in the middle (48.9%; n=206) and inner zones(31.6%; n=133). Less than 20% of all individuals were captured in theouter zone (χ2=55.3, df=2, pb0.001). Water temperatures rangedfrom 8.6 to 29.6 °C, withmost individuals captured in waters between18 and 22 °C (60%). Long-line (F15, 207=4.28, pb0.0001) and beachseine CPUE varied significantly among months (F15, 140=2.17,p=0.009). Post-hoc comparison tests revealed a significant decreasein shark CPUE between December and February (Fig. 2b). Seasonallong-line CPUE increased during the spring and summer, anddecreased during winter months (F4, 208=11.34, pb0.0001). Signif-icant differences in GSH catch rates were also observed betweensummer seasons, with higher long-line CPUE in 2008 than 2009(t=3.024, p=0.0233). Conversely, based on beach seine data, CPUEincreased in the inner zone during the summer of 2009 (Fig. 3).Long-line CPUE was also higher in the middle zone (F2, 208=4.73,

ds captured with beach seines and long-lines in the FTB of Bolsa Chica.

Table 2Summary of acoustic telemetry data for gray smooth-hound tracked in the FTB. STL: stretch total length; maturity stage: I—immature, M—mature; S: apparent survival; D:transmitter became stationary (death or shed).

Tag No. STL(cm)

Weight(g)

Sex MaturityStage

Date released(mm/dd/yyyy)

Date last detection(mm/dd/yyyy)

Overall monitoringperiod (d)

Number of daysdetected

VPS trackingduration (d)

Distance traveledday1 (km d−1)

Status

GSH #1 69.8 1100 F I 08/05/2008 08/29/2008 493 25 25 3.4 SGSH #2 71.1 1150 M M 08/12/2008 09/06/2008 486 25 25 2.7 DGSH #3 60.7 810 M I 08/12/2008 08/23/2008 486 12 12 3.9 SGSH #4 61 655 F I 08/21/2008 08/26/2008 477 6 6 5.3 SGSH #5 62.7 765 M I 08/21/2008 10/22/2008 477 56 56 3.4 SGSH #6 68.7 1000 M M 08/21/2008 09/05/2008 477 14 14 3.5 SGSH #7 61.8 780 F I 08/26/2008 09/05/2008 472 16 16 4.8 SGSH #8 67 920 F I 08/26/2008 09/01/2008 472 7 7 3.0 SGSH #9 60.8 750 F I 08/26/2008 09/01/2008 472 7 7 3.7 SGSH #10 66.1 1000 F I 03/17/2009 03/30/2009 269 13 13 2.1 SGSH #11 60.2 650 F I 03/17/2009 03/31/2009 269 14 14 2.7 SGSH #12 72 1050 M M 04/21/2009 05/04/2009 234 14 14 1.7 SGSH #13 65.4 850 F I 04/21/2009 05/12/2009 234 19 19 1.6 SGSH #14 67.9 950 M M 04/21/2009 05/06/2009 234 14 14 2.7 SGSH #15 68 1000 M M 04/21/2009 05/06/2009 234 15 14 2.5 DGSH #16 71 1200 M M 04/21/2009 05/04/2009 234 13 13 1.9 DGSH #17 101.4 3800 F M 04/21/2009 09/19/2009 234 6 5 2.1 SGSH #18 68.5 920 M M 05/04/2009 05/26/2009 221 22 21 1.7 SGSH #19 73.9 1150 M M 05/04/2009 12/7/2009 221 153 145 3.6 SGSH #20 63.1 840 F I 05/08/2009 05/15/2009 217 7 7 1.5 SGSH #21 75.2 1650 F M 05/08/2009 05/14/2009 217 6 5 1.4 SGSH #22 70.2 950 M M 07/07/2009 07/24/2009 157 16 14 1.2 S

68 M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

p=0.0098), and there was a significant interaction between seasonsand zones, with higher catch rates in the middle zone during thespring and summer seasons (F2, 208=2.24, p=0.026; Fig. 3).

3.2. Site fidelity and residency

Twenty-two GSH (60.2–101.4 cm STL) were passively trackedbetween August 2008 and December 2009 (Table 2). Acousticallytagged individuals had similar body sizes (t=0.07, df=20,p=0.945). Three of the sharks fitted with acoustic transmitters diedor shed transmitters after a few weeks of release. Although the causeof death was not apparent, detailed examination of tracking datarevealed that these sharks exhibited similar natural behaviors to othersharks prior to transmitters becoming stationary.

Fig. 4. Acoustic monitoring data of gray smooth-hound tagged inside the FTB. Dotted-line indwater temperature. Individuals are ordered by sex and STL (stretch total length; cm).

In 2008, GSH were detected for an average of 18 days (6–56 days),while in 2009 they were detected for an average of 24 days (6–153 days) inside the FTB (Table 2). Mean site fidelity index (SFI) forindividuals tagged in 2008 was 12.9% d (range: 4.5–36.8% d), whilein 2009 the mean SFI was 10.8% d (range: 2.6–69.2% d) detectedinside the basin. SFI did not differ between years (t=1.37, df=20,p=0.185). Most GSH acoustically tagged in August 2008 left the basinduring September 2008. Only one shark (GSH #5) stayed until lateOctober 2008 (Fig. 4). In 2009, most sharks were tagged early in thespring, and they stayed for approximately 3–4 weeks (Table 2). GSH#19 exhibited a higher degree of site fidelity than other individualsmonitored, and was present in the FTB for approximately 8 months(Fig. 4). Overall, GSH tracked in the FTB showed relatively shortresidency times, and none of the sharks tagged in 2008 returned thefollowing year. Mean weekly and monthly estimates of site fidelity

icates the division between year 2008 and 2009 and solid gray line indicates mean daily

69M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

revealed that most sharks spend over 60% of their time inside theFTB (Table 3). Based on the absence of detections, movements outsidethe basin to other adjacent coastal habitats were uncommon whileanimals were using the FTB. The only exception was GSH #17 (apresumed pregnant female) that left for 5 months and returned foronly two days (Fig. 4). Other sharks like GSH #5 and GSH #19 leftthe FTB during colder periods and returned after a few days (Fig. 4).

3.3. Movements and habitat use

A total of 68,637 positions were estimated using VPS tracking.Sharks were tracked for periods of 5–145 days (Table 2). ROMwere significantly higher at night (range=63.14 mmin−1; median=3.95 mmin−1) and decreased during the day (range=92.58 mmin−1;median=5.88 mmin−1; Kruskall–Wallis χ2=10.64, df=1, pb0.001).There was no relationship between ROM and tidal cycles (Kruskall–Wallis χ2=6.28, df=3, p=0.099) or sex (Kruskall–Wallis χ2=0.01,df=1, p=0.921); however, ROM were significantly higher inthe outermost areas of the FTB (range=63.14 mmin−1; median=6.9 mmin−1) than in the inner (range=51.28 mmin−1; median=5.2 mmin−1) and middle zone (range=92.6 mmin−1; median=4.5 mmin−1) (Kruskall–Wallis χ2=18.66, df=3, pb0.0001).

All sharks tracked displayed distinct diel movements. From 06:00to 12:00 h, GSH moved towards the inner zone, and from 15:00 to20:00 h they moved back to the middle and outer zone. Distancetraveled to the inner zone decreased during the day (732.1±309.6 m)relative to night (948.2±411.7 m) and crepuscular hours (884.1±336.5 m; F3, 919=7.53, pb0.0001). Additionally, there was a signifi-cant interaction between diel and tidal cycles. Most sharks moved tothe outer zone at night, particularly during outgoing and high tides(F9, 916=2.42, p=0.010).

Sharks were found using the entire FTB; however, most individualsutilized a small portion of the basin (Fig. 5a). VPS estimates from 19GSH were determined and distances to their COA were compared foreach year. No significant differences in the mean COA were foundbetween 2008 and 2009 (t=−1.57, df=20, p=0.132), revealingthat in both years sharks were commonly found in the middle zone(Fig. 5b). The maximum distance from the COA was constrained bythe acoustic coverage of the array. As a result, the mean distance fromthe COA for all sharks was 297.3±244.7 m (1.7–1467.5 m) (Fig. 5b).

Table 3Site fidelity index (% of d inside the basin), Minimum Convex Polygon (MCP) and Kernel U

Tag no. Mean weekly sitefidelity (% d)

Mean monthly sitefidelity (% d)

MCP area(km2)

GSH #1 96.4 96.0 0.70GSH #2 96.4 60.7 0.56GSH #3 100.0 63.2 0.57GSH #4 71.4 60.0 0.54GSH #5 85.7 88.1 0.69GSH #6 85.7 57.1 0.58GSH #7 76.2 53.6 0.54GSH #8 64.3 53.6 0.58GSH #9 64.3 53.6 0.69GSH #10 71.4 48.0 0.57GSH #11 76.2 52.0 0.42GSH #12 81.0 55.4 0.78GSH #13 85.7 69.6 0.54GSH #14 81.0 53.6 0.67GSH #15 81.0 55.4 0.59GSH #16 76.2 53.6 0.51GSH #17 47.6 21.8 0.47GSH #18 85.7 84.6 0.56GSH #19 94.6 94.6 0.90GSH #20 92.9 31.8 0.54GSH #21 85.7 27.3 0.26GSH #22 90.5 88.2 0.42Mean±SD 81.4±12.5 60.1±20.2 0.58±0.13

Over 54% of all locations were recorded less than 300 m away fromtheir COA, while only 20% were recorded at distances greater than700 m. Distances from the mean COA differed between day and nighthours (χ2=485.5, df=18, pb0.0001), and between males andfemales (χ2=200.7, df=18, pb0.0001). At night, there was anoverall expansion in the movement of male sharks to the middle andoutermost habitats of the FTB. MCP home range areas varied between0.26 and 0.90 km2 (0.6±0.1 km2). GSH used approximately 51% ofthe total area available in the FTB; however, 95% KUD showed smallerhome ranges (0.06–0.78 km2). Sharks typically utilized a small corearea of their home range (50% KUD: 0.006–0.13 km2), which waslocated in the middle zone. Both MCP and KUD activity spaceincreased significantly during nighttimes (Tables 3 and 4, Fig. 5a).

Males and females used waters of similar depths (χ2=11.1, df=5,p=0.05). Over 60% of VPS locations were recorded at depths N2.0 m,while only 11% were observed in shallower waters b1.6 m (Fig. 6b).Depth utilization did not differ between day and night (χ2=2.5,df=5, p=0.769); however, there was a significant heterogeneity anda strong selection for deeper over shallower habitats (χ2=259.1,df=90, pb0.0001). Although there was some evidence of inshoremovements at night, there was no selection for shallow habitats(Fig. 6c).

VPS tracking revealed that GSH used primarily soft-mud habitats.These habitats represented 31.5% of all habitats available in the FTB(Fig. 7a). Habitat use differed during day and night hrs (χ2=867.7,df=6, pb0.0001), and between males and females (χ2=147.9,df=6, pb0.0001). At night, males spent more time using lowerintertidal and the outermost habitats of the basin (sand, sand-mudand eelgrass) than females. GSH selected mainly soft-muddy habitatswithin the FTB (χ2=2259.28, df=108, pb0.0001; Fig. 7c). Addition-ally, sharks usedmud and eelgrass disproportionally to its availability,but it was less than expected. Use of eelgrass edges changed fromavoidance during the day to random use at night.

Most of the year water temperatures inside the FTB were warmerthan adjacent coastal waters; however, during a portion of the wintermonths, the FTBwas actually colder thanwater along the coast (Fig. 2).During the summer, the inner zone was on average 3 °C warmerthan coastal waters, with daily fluctuations ranging between 5 and15 °C. Overall, mean summer temperatures for 2008 (22.5±0.6 °C)were significantly higher than in 2009 (21.3±0.1 °C; t=4.62, df=60,

tilization Distribution (KUD) for gray smooth-hounds tracked in the FTB.

50% dayKUD (km2)

95% dayKUD (km2)

50% nightKUD (km2)

95% nightKUD (km2)

0.03 0.20 0.05 0.410.03 0.23 0.02 0.230.01 0.15 0.01 0.080.01 0.10 0.01 0.120.00 0.04 0.00 0.040.03 0.17 0.02 0.210.01 0.12 0.03 0.320.07 0.30 0.07 0.470.02 0.13 0.01 0.190.02 0.19 0.03 0.280.01 0.14 0.03 0.270.02 0.30 0.04 0.300.03 0.24 0.03 0.280.02 0.20 0.15 0.930.03 0.17 0.13 0.640.03 0.38 0.03 0.350.02 0.11 0.16 0.780.01 0.07 0.02 0.160.01 0.17 0.02 0.480.01 0.09 0.17 0.680.00 0.04 0.09 0.400.03 0.12 0.02 0.150.02±0.01 0.17±0.09 0.05±0.05 0.35±0.23

Fig. 5. Spatial distribution and center of activity (COA) for gray smooth-hounds tracked in the FTB. a) Number of tagged individuals observed in 50×50 m grids. Solid and dotted linesrepresent the 50 and 95% kernel utilization distribution (KUD) for day and nighttimes. b) Distance of VPS positions (filled circles) from the mean COA (target circle).

70 M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

pb0.0001). Conversely, temperatures in fall 2008 were colder than in2009 (t=−3.18; df=60; p=0.002). GSH used more intensivelywarmer temperatures available inside the FTB than in adjacent coastalwaters (t=286.4, df=21,710, pb0.0001). Less than 5% of all locationswere found at temperatures b18 °C, while over 68% occurred between18 and 22 °C (χ2=26781.3, df=198, pb0.0001). Overall, sharks spentmost of their time in warmer waters (21.6±1.7 °C), selecting similartemperature profiles from the middle and inner zone (Fig. 8).

During the course of beach seine sampling, 16,868 epibenthicinvertebrates (54.5%) and 14,102 teleost fish (45.5%) were collected.Snails (Bulla gouldiana) and bay scallops (Argopecten ventricosa)represented over 90% of individual invertebrate catch,while topsmelts(Atherinops affinis) and California killifish (Fundulus parvipinnis)dominated teleost fish catches (60%) (Farrugia et al., unpubl. data).Seasonal (F4, 81=13.31, pb0.0001) and spatial differences (F2, 81=9.66, pb0.0001) in potential prey abundance were found. Higherabundances of potential prey were recorded during summer months,particularly in the middle zone. Additionally, yearly differences inpotential prey abundance were observed, with higher abundancesduring the 2008 summer season than in 2009 (t=6.58, pb0.0001).

Table 4GLM model of the effect of sex and diel stage (day and night) on the size of activityspace (MCP, 50% and 95% KUD area) of gray smooth-hounds tracked in the FTB of BolsaChica.

Factor DF F P-value

MCP areaMales vs. Females 578 0.04 0.8485Day vs. Night 578 514.1 b0.0001

50% KUD areaMales vs. Females 578 0.05 0.8152Day vs. Night 578 144.1 b0.0001

50% KUD areaMales vs. Females 577 0.07 0.7955Day vs. Night 577 278.4 b0.0001

A significant positive correlation was also found between monthlyshark CPUE and potential prey abundance (r=0.340, p=0.001).

4. Discussion

4.1. Site fidelity, seasonal patterns and population composition

The use of bays and estuaries by coastal sharks may be related toforaging in highly productive habitats, mating or breeding (Betheaet al., 2004; Hueter et al., 2005; Chapman et al., 2009). Since itsrestoration, the establishment of a benthic community inside the FTBhas likely shaped the fish community, as has been seen in the UpperWhite River restoration wetland (Leao et al., 2004). However, it is stillunknown how long it will take for this benthic community to developinto a more mature community capable of supporting higher fishbiomass (Larkin et al., 2008). Evidence of GSH using the newlyrestored FTB for extended periods of time and across years may bea promising sign of recovery of ecological function. During the twoyear tracking study, GSH did not return to the FTB and only a smallpercentage of acoustically tagged individuals (10%) stayed forN2 months. However, the continuous presence (6–153 days) ofacoustically tagged individuals inside the basin suggests that onceGSH entered, forays into adjacent coastal waters were uncommonuntil they left for the season. Similar patterns have been observed inother coastal elasmobranchs such as leopard sharks (Carlisle andStarr, 2009), bonnetheads Sphyrna tiburo (Heupel et al., 2006),blacktips Carcharhinus limbatus (Heupel and Simpfendorfer, 2005),and cownose rays Rhinoptera bonanus (Collins et al., 2007). Thesestudies reported longer residency times (N45 day), and at least a smallportion of the population exhibited some degree of philopatry totheir estuary. Conversely, the FTB is smaller (1.48 km2) and shallowerthan these estuaries, which may also have influenced patterns of sitefidelity, residency and inter-annual use.

The results from this study support the hypothesis that GSH areseasonally abundant, and most individuals leave the FTB during the

Fig. 6. a) Depth distribution layers of the FTB. Graphs show b) depth use, and c) depth selection index (ŵi) for gray smooth-hounds tracked during day and nighttimes.

71M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

winter. Seasonal changes in the abundance of GSH were likely relatedto warmer water temperatures and changes in prey availabilitybetween 2008 and 2009. Although these changes are potentially dueto inter-annual variability, the arrival of El Niño during 2009may havedisrupted the temperature regime off the coast of southern California,diminishing ocean productivity and nutrient circulation (Furnas,2007). Despite inter-annual differences in GSH abundance, similarseasonal patterns have been observed in other studies. For example,

Fig. 7. a) Habitat layers of the FTB. Graphs show b) habitat use, and c) habitat sele

GSH left Anaheim Bay (a neighboring natural estuary in southernCalifornia) during thewinter as water temperature decreased, movingto their southern distribution range, or alternatively to warmercoastal areas (Lane and Hill, 1975). Additionally, changes in watertemperature influenced seasonal abundances of brown smooth-hounds (BSH), bat rays Myliobatis californica and leopard sharksin Tomales Bay, northern California (Hopkins and Cech, 2003). Mostindividuals left Tomales Bay during the winter, after temperatures

ction index (ŵi) for gray smooth-hounds tracked during day and nighttimes.

Fig. 8. a) Frequency of water temperatures use by gray smooth-hounds andtemperatures available in the inner, middle and outer zone, and b) temperatureselection index for males and females tracked in the FTB. Shading rectangle showsthe range of temperatures selected by male and female GSH.

72 M. Espinoza et al. / Journal of Experimental Marine Biology and Ecology 401 (2011) 63–74

decreased b10–12 °C. Hopkins and Cech (2003) hypothesized thatwinter emigrations are less common in bays and estuaries of southernCalifornia, since these habitats experience warmer temperatures andsalinities are less variable. Conversely, summer water temperaturesinside the FTB were elevated, particularly in the innermost areas ofthe basin, while these same areas were colder during the winter. Asa result, the FTB offers GSH a seasonally warmer environment forfeeding and growth. There is correlative support for this hypothesis,since GSH were more abundant in warmer habitats during the springand summer, and acoustically tagged individuals were only detectedduring warmer periods. However, it is unclear if GSH were usingwarmer habitats for some thermal physiological advantage, or ifsharkswere simply taking advantage of potential prey available insidethe FTB during summer months.

Previous diet studies and estimates of daily ration showed thatGSH feed continuously on small benthic prey (Lane and Hill, 1975;San Filippo, 1995). Although it is unknown if GSH are using the FTBfor feeding, our movement data suggest that some sharks may beforaging at night. Additionally, a few individuals captured duringlong-lines regurgitated fragments of crabs, shrimps, scallops, andghost shrimps. Potential prey available in the FTB increased duringwarmer months, and was unequally distributed along the basin. As aresult, GSH may be using the middle and outer FTB more intensivelyat night, possibly because these habitats may offer more resourcesthan other areas of the basin. Alternatively, sharks may be exploitingprey that is coming in from the ocean (opportunistic foraging). Theinfluence of prey on shark abundance and distribution have beenpreviously documented; however, most studies suggest that preyalone is not the only factor influencing seasonal and spatial patternsof elasmobranchs (Heupel and Hueter, 2002; Torres et al., 2006).Conversely, intense competition (intra and inter-specific) may limit

access to resources, population densities and residency times of GSHinside this small, shallow embayment (Papastamatiou et al., 2006).

Immature individuals dominated GSH abundances inside the FTB.Lane and Hill (1975) found that 48% of GSH captured in AnaheimBay were adults (N70 cm STL), while only 9% of the individuals fromthis study were larger than 70 cm STL. Although it is unclear if thepopulation composition of GSH in southern California has changedover time, it is likely that larger, mature estuaries may support agreater proportion of adults. Mature females were also more commoninside the FTB in the fall, while mature males were mainly presentfrom February through May (Lane and Hill, 1975). The highproportion of immature individuals observed inside the FTB suggeststhat this new habitat could be ecologically important for early stagesof GSH (Heupel and Hueter, 2002; Conrath and Musick, 2010).Although the concept of shark nurseries is widely used, distinctcriteria for defining a nursery have been lacking until recently. Heupelet al. (2007) proposed that a shark nursery will likely have: 1) higherdensities of sharks compared to other areas, 2) sharks would displaystrong site fidelity and residency, and 3) natal homing and philopatricbehavior would be more likely to occur. Based on these criteria, weshowed that GSH are seasonal residents of the FTB, with higherabundances during the summer. It is still unclear if GSH abundanceinside the FTB is greater than in natural estuaries or other adjacentcoastal habitats, and if GSH will exhibit philopatry to the FTB. Theabsence of newborns and lownumbers of adults indicate that althoughthe FTB may be important for juveniles, at this early restorationstage, this habitat is not functioning directly as a pupping, nursery ormating ground.

4.2. Movements and distribution

Long-term movement data revealed that GSH used primarily asmall portion of the FTB. A similar study on BSH in Tomales Bayshowed that tidal cycles influenced larger distribution patterns,whereas both diel and tidal cycles affected their short-term move-ments (Campos et al., 2009). BSH are thought to move towards innerTomales Bay during incoming and high tides to feed on benthic preyavailable in flooded mudflats, as previously documented on leopardsharks (Ackerman et al., 2000). Campos et al. (2009) also suggestedthat their behavior may reflect predator avoidance since sevengillsharks Notorynchus cepedianus are known to use Tomales Bay.Movements of GSH to the outer FTB were common during outgoingand high tides; however, they were at least partially driven by dielcycles. GSH also spent the majority of time in the deeper channel withvery few excursions to shallow intertidal mudflats. Additionally, sincethe FTB is smaller and shallower than Tomales Bay and none of thespecies observed in the FTB are potential predators, GSH are likely toexperience low predation risk. Behavioral patterns of sharks insidesmall, shallow embayments may differ from bays and estuaries withdifferent size, topography and geological age.

Behavioral diel changes are generally a trade-off among opportu-nistic foraging, predator or competitor avoidance, and bioenergeticefficiency (Andrews et al., 2009; Tiffan et al., 2009). GSH are presumedto move to warmer habitats during the day and to exploit foodresources at night. Evidence for this hypothesis is supported by anincrease in ROM at dusk and an expansion of their activity space atnight. Most elasmobranchs regulate their body temperature behav-iorally by increasing their activity where abiotic conditions arephysiologically favorable (Lowe and Goldman, 2001; Carlson et al.,2004). Although the innermost areas of the FTB were warmer duringsummermonths, a combination of physical factors (e.g., sun exposure,heat retention and longer daylight hours) and the shallow nature ofthe basin resulted in higher temperatures between 16:00 and 18:00 h.Female leopard sharks aggregated during the day in a warm, shallowembayment in southern California, but moved away from their“thermal refuge” at night (Hight and Lowe, 2007). Elevated core body

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temperatures recorded in leopard sharks at dusk (17:00–20:00 h) isthought to augment metabolic and physiological functions such asgastric evacuation rates, somatic growth, and possibly reproduction.Similar diel movements have been reported in bat rays, which arethought to be related to behavioral thermoregulation (Matern et al.,2000). Since bat rays have a high temperature sensitivity (Q10=6.81),this behavior may be the result of bat rays efficiently feeding inwarmer waters and digesting in colder waters. Although the Q10 ofGSH has not been previously reported, it is likely that dailytemperature fluctuations in the FTB could have a substantial effecton their physiology. Further conclusions will require a thermal choiceexperiment or the use of respirometry.

Water temperature and potential prey availability were twoimportant factors that influenced spatial patterns of GSH in the FTB.However, our data also showed that GSH spent most of their time inthemiddle zone rather than the innermost, warmer habitats available.Dissolved oxygen (DO) levels in the inner (1.3±0.4 mg l−1) werelower than in the middle zone (5.1±2.4 mg l−1) (Merkel & Assoc.Inc., unpubl. data). Seasonal and diel dissolved oxygen (DO)depressions (hypoxia) are common events in shallow bays andestuaries (Breitburg, 1992). Low levels of DO are known to influencespatial and temporal patterns of fish in estuarine environments(Hasler et al., 2009; Heithaus et al., 2009). Additionally, some studieshave found low activity levels in costal sharks under hypoxicconditions (2.5–3.4 mg l−1) (Carlson and Parsons, 2001). Theseresults suggest that extreme summer temperatures coupled withreduced DOmay have limited the use of the warmest, innermost areasof the FTB, as well as reducing shark activity levels.

4.3. Habitat use

A small area of eelgrass (b1% of the FTB) was initially transplantedto the basin in August 2007 (Merkel & Assoc. Inc., unpubl. data). Sincethen, eelgrass has expanded covering approximately 18% of subtidalhabitats. Dissolved oxygen can also influence eelgrass seedling,distribution and growth (Holmer and Bondgaard, 2001). As a result,eelgrass was mainly found in areas of the basin with high water flownear the inlet. Eelgrass has increased the structural complexity of thebasin, providing essential habitat for many coastal species (Allen et al.,2002). GSH spent most of their time in the deeper channel, using soft-muddy habitats. Some studies suggest that shallow mudflats may beessential habitats for sharks and rays in estuarine environments(Ackerman et al., 2000; Campos et al., 2009; Carlisle and Starr, 2009).However, most GSH avoided shallow intertidal habitats, possiblybecause these are typically exposed at low tide, may have been toowarm, and had low DO levels. Leopard sharks tracked in ElkhornSlough used primarily lower intertidal mudflats when available, andselected subtidal habitats in areas with only upper mudflats available(Carlisle and Starr, 2009). Benthic core sampling in the FTB's intertidalmudflats revealed low densities of epibenthic fauna. While this doesnot indicate that GSH will never use or forage in these habitats,GSH use of mudflats is limited compared to other subtidal areas thatmay have abundant food resources. Alternatively, GSH may be moreeffective at foraging in subtidal habitats than other benthic predators,and therefore have little need to forage on mudflats during floodingtides. Although it is unlikely that GSH are using primarily eelgrass,sharks may be foraging along the edges (periphery) at night, wherethere is a higher chance of finding prey in the mud. An increase ineelgrass habitat may also increase edge habitat and therefore foragingopportunities. Conversely, reducing access to mud substrata withdense eelgrass coverage may reduce shark densities.

Restoration of bays and estuaries has become a popular approachin southern California; however, most studies evaluating its effec-tiveness and success have mainly examined the community structure(species richness and composition) and not the ecological function(Zedler, 2005). Lack of ecological data on restoration and maturation

process has also limited our ability to make comparisons with naturalhabitats. Recent studies have shown that some elasmobranchs usehabitats that vary in their degree of ecological function. For example,female leopard sharks exhibited high degrees of site fidelity to ElkhornSlough, which have changed greatly over the last century (Van Dykeand Wasson, 2005; Carlisle and Starr, 2009). Jirik (2009) found thatpregnant round stingrays spent more time inside warm man-madeponds than in natural habitats from the Seal Beach National WildlifeRefuge. Large summer aggregations of round stingrays have also beenobserved near a heated effluent outfall at Seal Beach (Hoisington andLowe, 2005; Vaudo and Lowe, 2006). Here we found high estimatesof biomass for GSH (1.20 gm−2 or 1655 kg for the entire FTB), whichare comparable to those of numerically abundant fishes in San DiegoBay (Allen et al., 2002). Additionally, since its restoration the fishassemblage in the FTB has been dominated by many coastalelasmobranchs, which may be shaping the FTB's benthic community(Farrugia et al., in press). Therefore, altered and restored nearshorehabitats with different degrees of ecological function can providesuitable estuarine-like environments for many coastal elasmobranchs.

Coastal species' access to newly restored habitats can also increasethe degree of spatial connectivity between estuarine and nearshoreareas; however, it remains necessary to measure the recovery ofecological function (Ray, 2005; Berger and Smith, 2005). Bycombining population and behavioral data on GSH we were able todetermine how a coastal benthic predator uses a newly restoredhabitat that was not accessible for over 80 years. VPS tracking alsoprovided a novel approach to quantify fine-scale, long-term move-ments of multiple individuals simultaneously. This new approachhas the potential for becoming a valuable tool in aquatic monitoringstudies. It may also enable us to measure the recovery of ecologicalfunction in aquatic environments, and where a restored habitat is inits ecological succession.

Acknowledgements

This research would not have been possible without thecollaboration and support of Kelly O'Reilly (California DFG), reservemanager of Bolsa Chica. We would like to thank Drs. B. Pernet andB. Allen for their comments and also acknowledge F. Smith andD. Webber from Vemco Ltd. for their technical assistance. Volunteerwork was an integral part of this project and we are thankful for thefieldwork assistance of many extraordinary volunteers that helped uscompleting this research. Last, we would like to thank the anonymousreviewers for all their valuable comments. Financial support wasgenerously provided by PADI Foundation, Project AWARE Foundation,SCTC Marine Biology Foundation, CSULB, USC SeaGrant and VemcoLtd. [RH]

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