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Residency and seasonal movements in Lutjanus argentiventris and Mycteroperca rosacea at Los Islotes Reserve, Gulf of California 

    

Thomas TinHan, Brad Erisman, Octavio Aburto‐Oropeza, Amy Weaver, Daniel Vázquez‐Arce, Christopher G. Lowe. 

             

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MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 501: 191–206, 2014doi: 10.3354/meps10711

Published March 31

INTRODUCTION

Members of the snapper-grouper complex (Lut-janidae; Epinephelidae) play important roles in theorganization of coastal ecosystems via top-down con-trol as predators. To better understand their interac-tions with surrounding marine communities, we needinformation regarding patterns of space use andmovement in these species. These characteristics may

influence the susceptibility of predators to exploita-tion or anthropogenic disturbance (Fahrig 2007), andmay also alter distributions of prey items and com-petitors (Holt 1984). Unfortunately, patterns of move-ment remain poorly understood for a large number ofspecies, many of which are exploited by commercialand recreational fisheries worldwide. Populationdeclines have been reported for a number of thesespecies (e.g. Lutjanus cyanopterus, Epine phelus stri -

© Inter-Research 2014 · www.int-res.com*Corresponding author: t.tinhan@gmail.com

Residency and seasonal movements in Lutjanus argentiventris and Mycteroperca rosacea

at Los Islotes Reserve, Gulf of California

Thomas TinHan1,*, Brad Erisman2, Octavio Aburto-Oropeza2, Amy Weaver3, Daniel Vázquez-Arce3, Christopher G. Lowe1

1Department of Biological Sciences, California State University Long Beach, Long Beach, California 90815, USA2Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego, La Jolla,

California 92093-0202, USA3Sociedad de Historia Natural Niparajá A.C., 23020 La Paz, Baja California Sur, Mexico

ABSTRACT: A detailed understanding of inter- and intraspecific movement patterns is required tounderstand how marine species interact with surrounding ecological communities, their suscepti-bility to anthropogenic disturbance (e.g. fishing pressure), or the feasibility of management strate-gies. Between August 2010 and September 2012, we used acoustic telemetry to continuously mon-itor movements of 31 Lutjanus argentiventris (yellow snapper) and 25 Mycteroperca rosacea(leopard grouper) at Los Islotes, a small no-take reserve and reported spawning site for both spe-cies in the SW Gulf of California. Though the majority of fish from both species exhibited moder-ate levels of site fidelity to Los Islotes (snapper: present 49 ± 30% of days since tagging, grouper:64 ± 30%), cluster analyses revealed multiple patterns of site fidelity within species. Approxi-mately 30% of snapper exhibited decreases in site fidelity during the spawning season, and snap-per did not spawn at the reserve during the study. Grouper spawning aggregations at Los Isloteswere visually observed in 2011 and 2012, though the abundance of fish and the intensity ofcourtship behaviors were reduced in comparison with reported aggregations elsewhere in theGulf. Three snapper and 2 grouper made repeated movements across pelagic waters between LosIslotes and Marisla Seamount, another documented aggregation site in the SW Gulf. The demon-strated variation in movements of these species over multiple temporal and spatial scales warrantsconsideration of movement patterns in assessments of reserve performance, as well as the combi-nation of traditional fisheries regulations (e.g. size limits) with marine reserves throughout the Gulf.

KEY WORDS: Reef fishes · Yellow snapper · Leopard grouper · Marine Protected Areas · MPAs ·Acoustic monitoring · Fish spawning aggregations

Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 501: 191–206, 2014

atus; Huntsman 1996, Sala et al. 2001), and manage-ment efforts have been impeded by the lack of avail-able information regarding the movements of thesespecies.

In the southern Gulf of California, approximatelyhalf of the fish species targeted by coastal fisheriescomprise snappers and groupers, with landings ofthese species generating nearly 78% of annual ex-vessel revenue (i.e. price paid for landings prior toonshore handling) (Erisman et al. 2010). Becausemany reef-associated species in the Gulf, includingsnappers and groupers, form seasonal spawningaggregations at predictable times and locations (Salaet al. 2003), commercial fishing activities often occurin a coincident manner (Sadovy de Mitcheson & Eris-man 2012). However, current management strategiesdo not address the seasonal nature of these fisheries,and instead focus on establishing networks of marinereserves — areas partially or entirely protected fromfishing (Rife et al. 2012). Furthermore, enforcementof reserve areas is sparse, and many of these areasare subject to substantial illegal fishing pressure.Though such reserves are expected to increase bio-mass, organism size and diversity within their bound-aries (Halpern 2003), it is unclear how effective theyare for species that may migrate to seasonally tar-geted aggregation sites.

Species that form spawning aggregations typicallyexhibit resident or transient patterns of behavior, inwhich individuals may remain near their home rangeto spawn in small groups throughout the year (resi-dent), or migrate over varying distances to form largeaggregations in a brief, annual event (transient)(Domeier & Colin 1997). Though resident fish maybenefit most from small marine reserves, transient in-dividuals may be afforded little or no protection if ag-gregations form in unprotected areas. However, spe-cies may also adopt a diversity of behaviors that rangebetween the extremes of resident and transient ag-gregation, and multiple patterns of aggregation be-havior may exist within a species or population (Egli &Babcock 2004, Jarvis et al. 2010, Semmens et al. 2010,Sagarese & Frisk 2011). In order to address such vari-ability in population management stra tegies, oneneeds to determine whether multiple aggregation be-haviors are present within a population, and the pro-portion of individuals exhibiting each behavior(Nemeth 2012).

Yellow snapper Lutjanus argentiventris and leop-ard grouper Mycteroperca rosacea are among themost abundant predatory fishes on rocky reefsthroughout the Gulf of California (Ramírez &Rodríguez 1990, Erisman et al. 2010). Yellow snapper

range from southern California to Peru, whereasleopard grouper are found primarily in the Gulf,ranging from the southwest coast of Baja Californiato Jalisco, Mexico (Allen 1985, Heemstra & Randall1993). Both species aggregate seasonally to spawn(snapper: May to September; grouper: April to May;Sala et al. 2003, Aburto-Oropeza et al. 2009, Piñon etal. 2009), during which time they are heavily ex -ploited by coastal fisheries (Sala et al. 2003, Erismanet al. 2010). There have been no previous studies ofreef fish movements in the Gulf, and it is not knownhow these species utilize coastal habitats, particu-larly with respect to spawning.

The Los Islotes Marine Reserve is a small rockyislet in the southwestern Gulf of California, and 1 of3 no-take reserves (Marine Protected Area, MPA)in the Espíritu Santo Archipelago National Park(ESANP). The ESANP was established in 2007 withthe objectives of sustaining natural resources, con-tributing to regional coastal fisheries, and promo -ting sustainable tourist activities within the park(CONANP 2011). Though closed to fishing activities,Los Islotes is presumed to be subject to similar levelsof illegal fishing as other small protected areas in theregion. It is also recognized by regional managers asan aggregation site for several species, including yel-low snapper and leopard grouper. Thus, the LosIslotes Marine Reserve represents an ideal location inwhich to quantify the site fidelity, movement patternsand space use of these 2 commercially importantaggregative spawners. A static array of acoustic re -ceivers was used to monitor the long-term move-ments of yellow snapper and leopard grouper in rela-tion to Los Islotes, and to address the following4 questions: (1) What is the site fidelity of these spe-cies to the reserve? (2) How do these species differwith regard to their temporal movement patternswithin the Los Islotes MPA? (3) Do individuals ofthese species exhibit patterns of site fidelity indica-tive of resident or transient spawning? (4) What habi-tat types or depth features do fish associate with atLos Islotes?

MATERIALS AND METHODS

Study site

Los Islotes Marine Reserve is positioned around asmall rocky islet at the northern tip of Isla EspirituSanto, Baja California Sur, Mexico (24° 35’ 54’’ N,110° 24’ 6’’ W) (Fig. 1). It is 1 of 3 zones in the southernGulf fully protected from fishing, and it covers an

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TinHan et al.: Snapper and grouper movement patterns

area of 0.61 km2. The reserve boundaries extend300 m from shore and encompass a reserve area thatcan be broken down into 3 zones by habitat type anddepth: (1) north Los Islotes: a steep boulder fieldextending approximately 100 m from shore anddescending from 10 to 100 m depth; (2) southwest LosIslotes: a narrow, shallow (5 to 20 m), high-relief reefcrest extending approximately 400 m to the south-west (terminating at the ‘Bajito’, a shallow rocky pin-nacle immediately outside of the southwest reserveboundary); and (3) east Los Islotes: a deeper (10 to30 m) flat of unconsolidated seafloor extending 150 msoutheast rapidly descending beyond a depth of 50 m,and a small underwater cave passing in a north-south direction through the easternmost islet of LosIslotes. The bathymetry of Los Islotes was mappedover a 1 × 1 m grid using multibeam sonar (W. Hey-man unpubl. data).

Tagging

Between August 2010 and June 2011, 22 yellowsnapper and 16 leopard grouper were capturedwithin the reserve using baited hook and line, meas-ured, and surgically implanted with small acoustictransmitters (V13-1L, Vemco; 36 × 13 mm, 147 dB).An additional 10 fish from each species were simi-larly captured and implanted with pressure-sensingacoustic transmitters (V13P-1L, Vemco; 45 × 13 mm,150 dB, ±2.5 m accuracy, 0.22 m resolution). Bothtypes of transmitters were programmed to emit a

69 kHz coded pulse-train at 110 to 250 s intervals(180 s nominal range) for an expected battery life of1565 d. With the exception of 1 yellow snapper(29.0 cm total length, TL), all tagged fish were largerthan the reported length-at-maturity for their respec-tive species (yellow snapper: 32.6 cm TL, leopardgrouper: 34.0 cm TL; Erisman et al. 2008, Piñon et al.2009). Neither species exhibits external sexual di -morphism, thus we were unable to determine the sexof tagged individuals in this study. Once captured,fish were anesthetized in 100 mg l−1 tricaine me -thanesulfonate (MS-222) for 3 to 5 min. Transmitterswere implanted into the peritoneum through a smallincision, which was then closed by 2 interruptedabsorbable sutures (Ethicon Chromic-Gut, Johnson &Johnson). Each fish was also externally tagged in thedorsal musculature with a plastic dart tag (FT-1-94,Floy Tag & Mfg) bearing a unique identificationnumber. Fish were then transferred to a fresh seawa-ter bath and allowed to fully recover from anesthesiabefore release at the site of their capture.

Acoustic monitoring

To monitor fish movements in relation to the LosIslotes Reserve, an array of 7 omni-directional under-water acoustic receivers (VR2W, Vemco) was de -ployed on subsurface moorings throughout the re -serve area (Receivers 1 to 7 in Fig. 1). To monitormovements between Los Islotes and other nearbyrocky reefs, 4 additional receivers were positioned at

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Fig. 1. Map of Los Islotes Reserve, Baja California Sur, Mexico. Inset shows location of Los Islotes in the Gulf of California.Dark green shaded rectangle, area protected from fishing; blue dots, VR2W receivers; light green shaded area, the estimated50% detection range. Red borders around each receiver indicate the estimated acoustic detection range of individual re-ceivers. Numbers on contour lines represent isobath depths in meters. Green triangle indicates location of acoustic receiver at

Marisla Seamount

Mar Ecol Prog Ser 501: 191–206, 2014194

prominent locations outside of the reserve. Threereceivers were deployed at the northern tip of Espir-itu Santo Island, approximately 500 m from thereserve boundary (Fig. 1), while the fourth (Receiver8 in Fig. 1) was positioned at the Bahito, a rocky pin-nacle immediately adjacent to the southwest reserveboun dary. Fish movements to Marisla Sea mount, adeep rocky pinnacle and aggregation site located15 km NE of Los Islotes, were also periodically moni-tored (12 June 2011 to 23 October 2012) by anacoustic receiver deployed at this site as part of anunrelated study. Through range testing, the mean50% detection range of receivers at Los Islotes wasestima ted to be approximately 180 m (range: 16 to327 m), providing acoustic coverage for approxi-mately 60% of the designated reserve area. Thoughdetection ranges were highly variable among sites,poor surface conditions (Beaufort 4 to 5) during rangetesting suggest these are highly conservative esti-mates of receiver performance. Visual observationsof both species indicated that fish carrying transmit-ters programmed for a 180 s pulse interval werelikely mobile enough to be detected by receivers atleast twice in a 24 h period (criteria for daily presence).

When within range of a receiver (<300 m), thetransmitter emission is decoded as a unique transmit-ter identification number, and logged with a time anddate stamp as a detection event. Detections of pres-sure-sensing transmitters also contained the instan-taneous depth of the fish at the time of detection.Receiver performance can be influenced by interfer-ence from sources of biological or anthropogenicnoise (e.g. alpheid shrimps, boat traffic) (Heupel etal. 2006). For temporal analyses based on frequencyof detection, detections of a stationary referencetransmitter (V13-IL) were used to calibrate for thiseffect. A correction factor was calculated for eachhour of the day by dividing the mean detection fre-quency of each hour by the overall mean hourlydetection frequency of the reference transmitter.Adjusted detection frequencies were produced bydividing detection frequencies from each hourly binby their respective correction factor (see Payne et al.2010). Only a single reference transmitter was used,because it was assumed that receiving conditionswere consistent among receivers in the array.

Data analysis

Analyses of telemetry data were performed using Rv. 2.15.0 (R Development Core Team 2012), Statisticav. 10.0 (Statsoft), and PRIMER v. 6.1.7 (PRIMER-E,

Plymouth). Overall site fidelity of fish to Los Isloteswas calculated as the proportion of days tagged indi-viduals were present within the array since date oftagging. An individual was considered to be presentwithin the array if it was detected at least twice in a24 hr period. Fish were assigned to 3 groups based ontheir degree of site fidelity, or the proportion of daysat liberty that a fish was present in the reserve, withgroups being arbitrarily defined as low (<33%), moderate (33−66%), or high (>66%). To determinewhether there were any distinct behavioral modes inpatterns of presence at Los Islotes, a hierarchicalcluster analysis was applied to a Simple MatchingSimilarity matrix generated from the presence-ab -sence of individual fish on each day of the studyperiod. Because fish were tagged over the span ofseveral months, presence-absence data used in clus-ter analyses were truncated to begin on the earliestdate on which the majority of individuals had beentagged (snapper, n = 22; grouper, n = 25). Individualstagged after this date were omitted from clusteranalyses.

To determine whether site fidelity to Los Islotesvaried with fish size, overall site fidelity was re -gressed against fish total length. Individual patternsof movement in relation to Los Islotes were sporadicthrough both spawning and non-spawning periods;thus we did not use ‘streaks’ (consecutive days) ofpresence-absence to examine temporal trends inpresence. To identify long-term patterns in the pres-ence of tagged fish at the population level, the pro-portion of tagged individuals present, or probabilityof detecting a randomly selected fish, was calculatedfor each day and analyzed using the Seasonal TrendLoess (STL) procedure as described in Clevelandet al. (1990). The STL procedure decomposes timeseries data into long-term, seasonal, and remaindercomponents. This approach was primarily used todistinguish long-term tag losses from the reserve (viaemigration, predation or fishing mortality) and po -tentially spawning-related changes in presence toLos Islotes (seasonal trends). The remainder compo-nent represented residual variation in daily fish pres-ence remaining after the fitting of both seasonal andlong-term trends. The STL cannot be used to exam-ine annual patterns in time series shorter than 2 yr,thus only snapper tagged in 2010 (n = 25) were con-sidered in this analysis. Diel patterns of movement inrelation to Los Islotes as a whole were examined bypooling detection data for all receivers and all fishinto hourly bins (following standardization of detec-tion frequencies described above), applying a FastFourier Transform to these frequencies, and plotting

TinHan et al.: Snapper and grouper movement patterns

a spectrogram. Dominant peaks emerging in thepower spectra indicated the interval of cyclical pat-terns in presence at Los Islotes. Time-series of detec-tions were used to identify the movements of alltagged fish among receivers at the study site. A hori-zontal movement was defined as any detection of asingle fish at a different receiver than that of the pre-vious detection. Depth data from individuals carryingdepth transmitters were examined to identify verticalmovements, based on the changes in depth betweensubsequent detections of individuals. Mean hourlyrates of movement (ROM) were calculated by indi-vidual for both the horizontal and vertical axes. Hor-izontal ROM was calculated as the number of move-ments per detection in hourly bins, while verticalROM was determined by taking the mean of theabsolute differences in depth between consecutivedepth detections in each hour.

Site attachment was estimated by calculating theevenness of detections among receivers for eachindividual, using a diversity index of space useadapted from Pielou’s evenness index (Pielou 1966):

where R is the number of receivers in the array and ρi

is the relative number of detections at the i th receiver.Spatial evenness (se) values can range from zero toone, with values approaching one indicating evenuse of all areas. Spatial evenness for each specieswas calculated by taking the mean of the spatialevenness values calculated for each tagged individ-ual. The relationship between spatial evenness andfish size was examined in a linear regression of spa-tial evenness values calculated for individual fish andfish total length. Overall patterns in space use withinLos Islotes Reserve were compared by determiningthe proportion of detections occurring at each re -ceiver for individual fish, then calculating the meanfor each receiver.

Spawning observations

Diver observations were made from 21 to 23 Apriland 28 to 30 September 2012, during the peakmonths of spawning for yellow snapper and leopardgrouper, respectively, to determine the presence andextent of spawning or aggregation behavior at LosIslotes. Teams of divers swam the circumference ofthe reserve area to monitor spawning and estimate

the total abundance of yellow snapper and leopardgrouper during their respective spawning periods.Dives were made in the late afternoon and duskhours, and divers recorded observations of direct(gamete release) or indirect (courtship or chasingbehaviors, color change, swollen abdomens) indica-tions of spawning (detailed in Colin et al. 2003).Dives were made to depths between 5 and 20 m, andvisibility ranged from 3 to 15 m.

RESULTS

Site fidelity

A total of 32 yellow snapper and 26 leopardgrouper were tagged between August 2010 and June2011. In 2010, 25 snapper were tagged, though only3 grouper were tagged at this time due to the diffi-culty of capturing individuals of this species outsideof the peak spawning months of April and May. Theremaining 7 snapper and 23 grouper were tagged inApril and May 2011 (Fig. 2a,b). Two snapper wereomitted from the data set as they were presumed tohave died within the array shortly after tagging. Athird snapper (Larg22) was caught by fishers at theBajito in March 2011 and was thus omitted fromanalyses of site fidelity or long-term temporal trends.Grouper exhibited the greatest overall site fidelity toLos Islotes, being detected on 64 ± 30% of days at liberty (mean ± SD). Thirteen grouper (50% of indi-viduals) exhibited high site fidelity, 8 (30%) showedmoderate site fidelity and 5 (19%) showed low sitefidelity. Overall, snapper displayed moderate sitefidelity (49 ± 30% of days at liberty). Eight snapper(25% of individuals) exhibited high site fidelity, 12(38%) showed moderate site fidelity and 9 (28%)showed low site fidelity.

Cluster analysis of patterns in presence-absence offish at Los Islotes revealed 3 significant groups foryellow snapper, and 2 groups for leopard grou per(Fig. 2c,d). These distinct groups were considered torepresent individuals exhibiting resident, transientor mixed patterns of presence to the reserve. For yel-low snapper, the largest group of individuals (~30%)exhibited moderate to high levels of site fidelity dur-ing non-spawning months, but sustained periods ofabsence during the months of spawning. Approxi-mately 80% of grouper displayed continuous pat-terns of residence at the reserve, and though theremaining individuals showed low overall site fide -lity, these individuals also exhibited high site fidelityover short time scales (i.e. weeks). A significant rela-

R

i ii

R

Spatial evenness– ln

ln1̈

( )( )=

W W¬® ¼¾=

195

Mar Ecol Prog Ser 501: 191–206, 2014

tionship was found between site fidelity and bodysize for grouper (F1,23 = 8.637, r2 = 0.273, p = 0.007;Fig. 3). However, the significance and strength of thisrelationship were greatly improved (F1,22 = 21.71, r2 =0.49, p = 0.0001) when grouper Mros17 was omittedfrom analysis as an outlier (Fig. 3). No such relation-ship between size and site fidelity was observed forsnapper (F1,27 = 1.934, r2 = 0.06, p = 0.175).

Temporal patterns

STL decomposition of the daily proportion oftagged yellow snapper present over the course of thestudy revealed long-term declines in fish presence

and seasonal fluctuations corresponding with thespawning season (May to September) (Fig. 4). Theproportion of tagged snapper present at Los Islotesdeclined steadily over a 2 yr period at a mean rate of35.5% per year (Fig. 4c). Cyclical changes in snapperpresence to Los Islotes were also identified, with theprobability of detecting a tagged fish decreasing byapproximately 30% during the months of peakspawning. In each year, the proba bility of detectionincreased rapidly between the months of Novemberand January, shortly after the end of the reportedspawning season (Fig. 4b). However, there remainedsubstantial daily fluctuations in snapper presence(approx. ±10%) that could not be ex plained by theidentified seasonal or long-term trends (Fig. 4d). As

196

Fig. 2. Lutjanus argentiventris, Mycteroperca rosacea. (a,b) Detection plots of individual daily presence-absence at Los IslotesReserve and (c,d) non-metric multi-dimensional scaling (nMDS) plots of individual patterns of residence at the reserve for (a,c)yellow snapper and (b,d) leopard grouper. Short, vertical coloured lines in detection plots indicate days on which fish were de-tected at Los Islotes; black triangles represent detections at Marisla Seamount. Shaded areas (a,b) indicate spawning seasonsfor the species shown; rows are arranged in order of similarity between individuals. Short, vertical gray lines in (a) indicate in-dividuals not included in nMDS analyses. Overlaid contour lines (in c,d) from hierarchical cluster analysis represent groupsshowing different residency patterns (corresponding group membership represented by red, blue, and green lines in

detection plots)

TinHan et al.: Snapper and grouper movement patterns

data for leopard grouper were limited to a period of1 yr, STL analysis could not be used to identifyannual cycles for this species. However, similar long-term declines (72%) in fish presence to Los Isloteswere also identified for this species (data not shown).No size difference was found between yellow snap-per that disappeared from the array and those re -maining at Los Islotes at the end of the study period(September 2012) (t-test, t = −0.243, p = 0.980). How-ever, 18 grouper were no longer detected at LosIslotes at the end of the study, and these were signif-icantly smaller than those that remained in the array(t-test, t = −4.377, p = 0.0002). Of the 18 ind. that dis-appeared from the array, 7 (36%) showed declines insite fidelity in the weeks prior to their disappearance(Fig. 2b; e.g. Mros08).

Spectral analysis of adjusted hourly detection fre-quencies revealed 2 dominant peaks at periods of 12and 24 h for yellow snapper and a single large peakat 24 h for leopard grouper (Fig. 5). Detection fre-quency did not vary significantly with tide height,tidal phase, or lunar phase. The frequency of move-ments made among receivers, or level of horizontal

activity, also peaked during the crepuscular hours forboth species, although these increases did not corre-spond to any particular area of the reserve. Snapperactivity levels became more variable during thenight, though there was no clear overall increase inactivity during this period (Fig. 6a). Grouper main-tained an increased level of activity throughout theday before becoming more quiescent at night(Fig. 6b). Examination of vertical activity patterns forindividuals tagged with depth-sensing transmitters(yellow snapper: n = 9; leopard grouper: n = 10)revealed temporal patterns similar to those in thehorizontal axis, with both species increasing in activ-ity during the crepuscular hours. However, snappersustained their levels of vertical activity throughoutthe night, while grouper showed an overall pattern ofincreased crepuscular and diurnal vertical activity(Fig. 6c,d).

Between June 2011 and October 2012, 3 yellowsnapper (Larg12, Larg20, Larg26) and 2 leopardgrouper (Mros07, Mros11) were detected by acousticreceivers at the Marisla Seamount, approximately15 km to the northeast of Los Islotes (Fig. 1). MarislaSeamount comprises 3 submerged rocky pinnaclesthat rise from a depth of 1000 m to within 15 m of thesurface. All 3 snapper were first detected at Mar -isla Seamount between July and September — themonths of peak spawning for yellow snapper. Twosnapper (Larg12, Larg20) remained at this site forextended periods (>6 mo), while the third (Larg26)was only detected on 9 non-consecutive days overthe subsequent 8 mo. Of these 3, only 1 snapper(Larg12) returned to Los Islotes from Marisla Sea -mount. In contrast, leopard grouper movements toMarisla Seamount did not coincide with the spawn-ing season and tended to be brief, with all fish travel-ing to Marisla Seamount and back to Los Isloteswithin 24 h. Transit times between the 2 sites for yel-low snapper ranged from 3 h to 8 d, while the shortesttransit time for leopard grouper was 102 min at anestimated swimming speed of 2.5 m s−1 or 2.9 bodylengths s−1.

Spawning observations

We confirmed the presence of at least 1, and pos -sibly 2, small spawning aggregations of leopardgrouper at Los Islotes during underwater surveys conducted in the afternoon (13:00 to 20:00 h) on 21 to23 April 2012. Throughout this period, we observed agroup of approx. 80 adult leopard groupers looselyaggregated off the east point of the island. Fish were

197

Fig. 3. Lutjanus argentiventris, Mycteroperca rosacea. Natural-log relationship between fish length and site fidelityof (a) yellow snapper and (b) leopard grouper at the Los Is-lotes Reserve. Reported regression statistics for leopardgrouper omit an outlier (Mros17) shown as ‘×’ in lower right

corner of plot (b)

Mar Ecol Prog Ser 501: 191–206, 2014

present both in the water columnabove the thermocline (depth range =5 to 10 m) or on the reef itself (depthrange = 10 to 20 m). Indirect evidenceof spawning via the presence of nu me -rous females with enlar ged (swollen)abdomens was observed on all dives.We also observed direct evidence ofspawning during visual surveys con-ducted the hour before sunset (i.e.18:45 to 19:45 h) on 22 and 23 April atthe easternmost point of the island, onboth the north and south side of thepoint. During these dives, we re -corded nearly the en tire repertoire ofbehaviors asso ciated with courtshipand spawning in leopard grouper:courtship color change, following,courtship chase, mobbing, femaledarting, rubbing, bumping, lateral dis-

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Fig. 4. Lutjanus argentiventris. Time series of proportion of tagged yellow snapper present at Los Islotes (a) over the durationof the study, and decomposed into (b) seasonal, (c) trend and (d) remainder components. Gray shading represents spawning

seasons. The sign of y-values in (b,d) represents changes in relation to the trend component in (c)

Fig. 5. Lutjanus argentiventris, Mycteroperca rosacea. Spectral analyses ofFast Fourier Transformed (FFT) hourly detection frequencies at Los Islotes

for (a) yellow snapper and (b) leopard grouper

TinHan et al.: Snapper and grouper movement patterns

play, gaping, burst rise, head shake, and spawningrush (Erisman & Allen 2006, Erisman et al. 2007).Courtship occurred within subgroups of 3 to 6 ind.that, led by a gravid female with a swollen abdomen,would engage in bouts of chasing behavior and mob-bing of the female, followed by rapid ascents off thereef up into the water column. While rushing behav-ior of subgroups was observed, ga mete release couldnot be confirmed due to the poor visibility and strongcurrents. A second aggregation of approx. 60 leopardgrouper was observed at the west point of the island,which included gravid fe males with enlarged ab -

domens. However, court ship or spawning was notob served. Several small groups of 10 to 20 adult leop-ard grouper were documented on reefs on the northside of the island, indicating the presence of ap -prox. 180 to 200 adult leopard grou per at Los Islotesduring the April spawning period. Total abundanceof yellow snapper at Los Islotes was estimated to beno more than 100 ind. in September 2012. Weobserved an aggregation of 50 to 100 adult yellowsnapper within the cave at Los Islotes during all sur-vey months; however, we found no direct evidencethat this aggregation represented a spaw ning aggre-gation. Though small groups of snapper (<5 ind.)were observed loosely swimming together, therewere no definitive signs of aggregation, and no ob -servations were made that indicated spawning activ-ity in yellow snapper at this site.

Space use

Yellow snapper exhibited significantly lower spa-tial evenness index values (0.60 ± 0.17, mean ± SD)than leopard grouper (0.71 ± 0.14) (Kruskal-Wallisχ2 = 5.13, df = 1, p = 0.024). Though grouper werefound to make greater use of the available reservearea, both species were most frequently detected byreceivers along the east point and northern side ofthe islet — locations composed primarily of steepboulder fields and wall habitat fringed by sand bot-tom habitat (Table 1). There was no relationshipbetween spatial evenness and body length for eitherspecies (snapper: r2 = 0.009, p = 0.394; grouper: r2 =0.063, p = 0.119). However, both species were foundto occupy a similar distribution of depths (F = 3.40,df = 1, p = 0.085). Though no correlation was foundbetween body length and mean depth for snapper(r2 = 0.06, p = 0.247), a significant positive relation-

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Fig. 6. Lutjanus argentiventris, Mycteroperca rosacea. Ac-tivity levels by time of day (hourly): rate of (a,b) horizontalmovement and (c,d) vertical movement for yellow snapperand leopard grouper. Grey shaded areas indicate nighttime.

Note differences in scale along vertical axes

Station Yellow snapper Leopard grouperMean ± SD Mean ± SD

1 0.205 ± 0.212 0.160 ± 0.1472 0.087 ± 0.153 0.143 ± 0.1443 0.311 ± 0.215 0.174 ± 0.1834 0.125 ± 0.153 0.145 ± 0.1455 0.201 ± 0.209 0.090 ± 0.1396 0.025 ± 0.027 0.058 ± 0.0747 0.014 ± 0.030 0.120 ± 0.1678 0.029 ± 0.087 0.105 ± 0.186

Table 1. Lutjanus argentiventris, Mycteroperca rosacea. Re -la tive proportion of detections calculated across individuals

at each acoustic receiver at Los Islotes Reserve

Mar Ecol Prog Ser 501: 191–206, 2014

ship was found for grouper (r2 = 0.47, p = 0.017)(Fig. 7), with the largest individuals being detected atmean depths of 16 to 18 m.

DISCUSSION

Site fidelity

Overall, yellow snapper and leopard groupertagged in this study exhibited site fidelity to the LosIslotes Reserve. However, species differed in theirpatterns of presence to the reserve, as well as theiroverall degrees of site fidelity. The majority of leop-ard grouper (80%) were detected on at least 50% ofdays, whereas less than half (48%) of yellow snapperwere detected on at least 50% of days (Fig. 3). Exam-ination of long-term changes in site fidelity for bothspecies revealed an overall decline in the presence oftagged fish at Los Islotes over the course of the study.Over a 2 yr period (789 d), approximately 70% ofsnapper were no longer detected at Los Islotes, whilea similar proportion of leopard grouper were unde-tected in the reserve after 515 d. Similar patternshave been reported in previous studies of reef fishmovements, although residence times are variableamong studies. Topping & Szedlmayer (2011) ob -served comparable declines in red snapper Lutjanuscampechanus presence on reefs in the Gulf of Mex-ico, with 20 to 25% of tagged fish remaining at studysites after a period of ~750 d, while a study of snapperand grouper in the Florida Keys reported residencetimes of <1 yr (Lindholm et al. 2005). While LosIslotes is a no-take marine reserve, enforcement issporadic due to the re mote location of the reserve inrelation to the nearest coastal city (La Paz; distance =50 km). Illegal fishing at night by hookah divers isknown to occur at this site (B. Erisman, O. Aburto-

Oropeza & A. Weaver unpubl. data; pers. comm. withpark guards and CONANP officials), and it is there-fore unknown whether declines in the presence oftagged fish at Los Islotes are the result of long-termemigration, natural mortality by predation, or fishingmortality. Another possibility for fish disappearanceis tag failure, though unpublished data from otherstudies indicate extremely low failure rates (<3%) forsimilar tags produced by the manufacturer (e.g. M.A. Dance et al. unpubl., B. W. Wolfe et al. unpubl.).Nevertheless, estimates of site fidelity for fish at thislocation should be viewed as conservative.

Though the majority of grouper exhibited moder-ate to high levels of site fidelity to Los Islotes, periodsof absence were often prolonged, and many individ-uals did not return to the reserve prior to completionof the study (Fig. 2b). There was considerable varia-tion in site fidelity among individuals, and a smallpercentage (16%) exhibited low site fidelity to thereserve. It was found that much of this variation wasexplained by body size, with smaller individualsexhibiting lower site fidelity to the reserve thanlarger grouper (Fig. 3b). At the end of the study,the majority of tagged grouper had disappearedfrom Los Islotes, and these fish were also found tobe significantly smaller than those remaining in thereserve. Ontogenetic habitat shifts have been de -scribed in at least one other species of Mycterop-erca (gag grou per; M. microlepis), where individualsmove from shallow to deeper reef habitats withmaturity, presumably to exploit larger or more abun-dant prey items found in habitats presenting agreater predation risk to smaller individuals (Bullock& Smith 1991, Dahlgren & Eggleston 2000). Shapiroet al. (1994) also observed an increase in home rangesize with body size for red hind Epinephelus gutta-tus, as well as the disappearance of approximately44% of tagged individuals from a small fore reef inPuerto Rico over a 5 mo period. However, if LosIslotes was abandoned by maturing individuals infavor of habitat more suitable to larger fish, this doesnot explain why large grouper are encountered inany substantial number at Los Islotes. In fact, fishtagged in the present study were at least as large(53 cm mean SL) as mature leopard grouper capturedin spawning aggregations near Loreto, Mexico (47 cmmean SL) (Erisman et al. 2007). Illegal fishing hasbeen re ported to occur at Los Islotes at night, whenenforcement levels are lowest, and the abrupt disap-pearance of some individuals (Fig 2b; e.g. Mros03)from the array may have resulted from their captureby fishers within the reserve. However, some individ-uals lost from the array showed declines in site

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Fig. 7. Mycteroperca rosacea. Relationship between fish to-tal length and mean depth for leopard grouper at Los Islotes

Reserve (r2 = 0.47, p = 0.017)

TinHan et al.: Snapper and grouper movement patterns

fidelity in the weeks prior to their disappearance(Fig. 2b; e.g. Mros08), and it is unlikely that theseparticular losses resulted from illegal fishing withinthe Los Islotes Reserve.

Though the fate of leopard grouper after leavingthe reserve remains unknown, these declines in sitefidelity may represent periods in which grouperbegan exploring new habitats before eventually emi-grating from Los Islotes. We saw no indication thatindividuals departed from, or returned to, the arrayvia any particular part of the reserve, but we suspectthat fish might have been capable of traversing therange of one or more receivers between transmitterpulses, obscuring any directional pattern of emigra-tion. If indeed these disappearances were the resultof emigration, there are 2 potential explanations forthe size difference seen. Firstly, smaller grouper mayhave been competitively excluded from Los Islotesby larger individuals and were thus forced to visitsites elsewhere in order to satisfy their energeticrequirements. Secondly, the abundance of sea lionsZalophus californianus at Los Islotes (~400 ind.;CONANP 2011) might have posed enough of a dis-turbance or predation risk to smaller grouper to meritemigration to habitats with fewer potential predators.On several occasions, divers in the present studyobserved sea lions harassing both yellow snapperand leopard grouper, and interrupting spawningbehaviors in the latter (B. Erisman & A. Weaver pers.obs.), though studies of sea lion diet have not explic-itly identified these species as prey items (e.g. Gar-cía-Rodríguez & Aurioles-Gamboa 2004).

Snapper were detected consistently over thecourse of the study but were frequently absent forshort periods (Fig. 2a). The brief yet common natureof absences for snapper suggests individuals utilizedother nearby areas in addition to habitat at LosIslotes. Though it is possible that these absencesresulted from fish moving into areas of the reserveoutside of the detection range of receivers, it isunlikely fish would remain in these locations for themulti-day periods observed. Previous studies ofsnapper movement have found fish to make repeatedforays among multiple areas and habitat types sepa-rated by small or intermediate distances (Meyer et al.2007, Luo et al. 2009). Los Islotes is separated fromthe nearest rocky reef (northern Isla Espiritu Santo)by waters ranging in depth from 80 to 100 m, and adistance of approx. 700 m. However, on only oneoccasion was a snapper detected by the array atnorthern Espiritu Santo. Because of the relativelylong pulse interval of the transmitters used in thisstudy (110 to 250 s), it is possible that fish were able

to transit this area undetected while making directedmovements. It is also plausible that fish venturingaway from Los Islotes simply did not orient to thenearest available habitat, and instead traveled alongroutes outside of the detection range of thesereceivers until reaching more preferable sites furtheralong Espiritu Santo.

Site fidelity in yellow snapper was also variableamong individuals, but size could not explain thevariation in site fidelity in this species (Fig. 3a). Clus-ter analysis of patterns in presence-absence also pro-duced groups indicating fish from both speciesexhibited differential patterns in movement and sitefidelity in relation to Los Islotes. Such patterns havealso been reported for other species inhabiting coas -tal waters, and it is presumed that multiple patternsin movement or space use may provide individualswith a means of minimizing intraspecific competitionfor resources such as food or space. For example, astudy of movements of juvenile Atlantic sharpnoseshark Rhizoprionodon terraenovae identified multi-ple peaks in the distribution of site fidelity and homerange values (Carlson et al. 2008). Similar resultswere obtained from another study of sparid snapperPagrus auratus movements in a New Zealand MPA,where 2 distinct groups of fish were identified asexhibiting either low or high degrees of site fidelity(Egli & Babcock 2004). Two possible interpretationsof the apparent differences in site fidelity seenamong individuals are that (1) snapper with low sitefidelity to Los Islotes exhibit high site fidelity toanother area, or (2) snapper with low site fidelity toLos Islotes are simply more transient than those dis-playing high degrees of site fidelity. Snapper move-ments among different activity spaces in the Gulfremain unclear, and future studies using activetracking may be successful in identifying the scaleand frequency of these movements, as well as theinfluence of environmental factors.

Temporal patterns

A moderate seasonal component was also identi-fied in patterns of presence of tagged yellow snapperat Los Islotes. The greatest proportion of tagged fishwas detected between February and April, followedby a steady decline through the summer and earlyfall (Fig. 4b). Yellow snapper in the Gulf of Californiahave been found to spawn throughout the summermonths (May to Sept) (Sala et al. 2003, Aburto-Oropeza et al. 2009), though local fishers report thatspawning activity and aggregative be haviors peak in

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August and September. However, many fish thatwere less likely to be detected during spawning peri-ods did not simply leave Los Islotes for extendedperiods, but instead made multiple trips away fromthe reserve throughout the spawning season (Fig 2a).Yellow snapper are serial spaw ners, and these re -peated short-term migrations may therefore repre-sent movements to other spawning sites in the Gulf.In this regard, yellow snapper appear to exhibit sim-ilar spawning patterns to those identified in earlierstudies of lutjanid reproduction, where species tendto spawn throughout an ex tended spawning seasoncontaining multiple peaks in spawning activity (Jo -hannes 1981, Grimes 1987, Collins et al. 1996).

Though the repeated seasonal declines in presenceto a home range seen in the present study are charac-teristic of transient aggregation behavior, it is impor-tant to note that the proportion of tagged fish presentat Los Islotes fluctuated by ~30% between spawningand non-spawning periods (Fig. 4b). It is unknownwhat proportion of the adult population spawns eachyear, so the possibility remains that some individualssimply did not engage in spawning during this study.Local divers and tour operators have reported seeingyellow snapper spawn at Los Islotes, though dive sur-veys performed in the present study provided littleevidence of spawning or aggregation behavior at thissite. On several occasions, snapper were seen to formsmall groups and engage in chasing behaviors thatare typically followed by courtship displays andspawning, but these groups were often interruptedby rushes from sea lions that inhabit Los Islotes, andno direct observations of gamete release or spawningrushes were made. However, yellow snapper havealso been observed to form large spawning aggrega-tions at sites elsewhere in the Gulf, such as Isla LasAnimas, Cabo Pulmo National Park and Marisla Sea -mount (B. Erisman pers. obs.). Interestingly, 3 taggedsnapper (Larg12, Larg20, Larg26) made a synchro-nized migration from Los Islotes at the end of July2011 and were detected shortly afterwards on acous -tic receivers deployed at Marisla Seamount. Becausethese migrations coincided with the beginning ofwhat are thought to be the months of peak spawningfor yellow snapper, we speculate that they may havebeen related to reproduction, though further study isneeded to understand the nature and degree of con-nectivity between these 2 sites.

Erisman et al. (2007) reported seasonal shifts inleopard grouper abundance among a number of sitesnear Loreto, Mexico, and suggested that individualsmigrate over significant distances to specific sites inorder to spawn. Though 2 grouper in the present

study made migrations over a distance of 15 km toMarisla Seamount, these movements did not corre-spond with spawning periods and were thus not be -lieved to be spawning migrations. We observed thesynchronous disappearance of 7 grouper from LosIslotes at the start of the 2012 spawning season(27 April to 13 May 2012) (Fig. 2b), and though thepossibility of fishing mortality could not be elimi-nated (landings peak between March and May; Eris-man et al. 2010), we speculate these movementswere related to spawning. Dive surveys also pro-vided evidence of leopard grouper spawning at LosIslotes during the months of April and May, suggest-ing grouper at this site may instead represent a sub-population of both resident and transient spawners.

There is evidence that aggregating species mayexhibit partial migration, where a single populationcontains both resident and transient spawners (Jarviset al. 2010, Semmens et al. 2010). Partial migration infish may represent a suite of strategies within a pop-ulation whereby individuals may maximize their fit-ness under a combination of environmental andgenetic factors (e.g. food availability, sex, maturationor growth rates) (Jonsson & Jonsson 1993). Previousstudies have shown that the distribution and avail-ability of resources, such as food or habitat, canimpact social structures and reproductive behaviors(e.g. Travis & Slobodchikoff 1993), and it is possiblethat differences in habitat quality are influencing thedifferences in aggregation behavior seen betweenLos Islotes and sites sampled near Loreto. For exam-ple, Marsh et al. (2000) report decreased aggregationbehavior and increased site fidelity in male tungarafrogs as the distance between ponds (breeding habi-tat) increased. In contrast to coastal areas like Loreto,where fish may be able to move easily among aggre-gation sites via contiguous coastal habitat, Los Islotesmay instead represent one of several insular, patchilydistributed aggregation sites, where it is adaptive forindividuals to form resident spawning aggregations.

Spectral analyses revealed a diel pattern in thehourly detection frequencies of a stationary refer-ence transmitter, indicating that diel rhythms inbackground noise interfered, to some degree, withdetection efficiencies of receivers. These results arebroadly consistent with the findings of Payne et al.(2010), in which predictable diel fluctuations inreceiver performance were identified and attributedto interference from external noise sources (e.g.soniferous fishes or invertebrates). However, in con-trast to the opposing diel patterns shown in Payne etal. (2010), the similarity of patterns seen between cor-rected and uncorrected detection frequencies at Los

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Islotes suggest environmental noise did not funda-mentally alter observations of fish movement at thissite. Spectrograms of hourly detection frequencies atLos Islotes revealed a dominant 24 h period in activ-ity, indicating clear patterns of diel movement forboth species. A secondary peak in activity occurringat 12 h intervals was observed in snapper, but pat-terns of fish presence to the reserve were not foundto correspond with tidal height or phase, so this peakmost likely represents the 12 h interval between cre-puscular periods of activity in this species (Fig. 5a).Examination of levels of horizontal and verticalmovement in snapper also revealed peaks in activityduring the crepuscular periods (Fig. 6a,c). This isconsistent with previous observations of yellow snap-per movements in the Gulf of California made byHobson (1965), who found snapper to be most activewhen foraging at dusk and at night, and least activewhen seeking refuge in rock crevices during the day.Because of the low probability of detecting fish whensheltered in rock crevices, it is likely that the 24 hinterval between periods of presence and absence tothe reserve observed in spectral analyses for bothspecies are the result of diurnal refuging behavior,rather than diurnal movements away from the re -serve area.

While no substantive secondary peak was ob -served in spectral analysis of leopard grouper move-ments in relation to Los Islotes (Fig. 5b), small in -creases in activity within the reserve were observedduring crepuscular periods (Fig. 6b,d). This indicatesthat while grouper become more active during thecrepuscular hours, they show no shift in their overallpresence at the reserve during these periods. Theseperiods of activity are most likely foraging-related asleopard grouper are thought to be primarily crepus-cular foragers (Hobson 1965).

Space use

Crepuscular and nocturnal foraging behaviors arecommon among predatory fishes, where low lightlevels probably allow predators to increase their like-lihood of capturing small, fast-moving prey items(Hobson et al. 1981, Helfman 1986, Parrish 1992),such as schools of flat-iron herring Harengula thris -sina that frequent Los Islotes. Flat-iron herring are aprincipal prey item of adult yellow snapper and leop-ard grouper, but both species also show ontogeneticshifts in diet: Juveniles primarily consume benthicinvertebrates (and fish eggs, for snapper), whileadults are increasingly piscivorous (Hobson 1965,

Vázquez et al. 2008). Hobson (1965) observed thatleopard grouper typically utilized sand bottom habi-tats to ambush schooling baitfish near the surface,and larger grouper in the present study were de -tected most commonly at depths >15 m, coincidingwith sand bottom/rock edge habitat surrounding LosIslotes. Larger grouper might simply occupy deeperwaters irrespective of habitat type, but another possi-bility is that larger, more piscivorous individuals areseeking out deeper sand bottom habitats to betterprey on small schooling fish as described in Hobson(1965).

Yellow snapper exhibited spatial evenness valueslower than those calculated for leopard grouper, indi-cating a greater degree of site attachment to specificareas of the reserve. Diver observations indicate thatlarge numbers of snapper would congregate in asmall underwater cave passing in a north-southdirection through the easternmost islet of Los Islotes.A large proportion of detections at eastern Los Islotesmay be attributed to the aggregation of tagged snap-per within this feature, as 2 out of the 3 receivers hav-ing the greatest number of yellow snapper detectionshad an unimpeded ‘line-of-sight’ into this cave.Detections of yellow snapper along the western pointof Los Islotes were infrequent. Though range testsindicated receiver performance to be poor in thisarea, detection frequencies of grouper at this sitewere comparable to those in other parts of the re -serve, suggesting receiver performance might havebeen adequate for detection of fish movementsthrough this area. Leopard grouper were detectedmore evenly across all receivers in the array, but sim-ilar to snapper, detection frequencies were greatestalong the easternmost point and north side of LosIslotes. However, grouper were not observed to con-gregate in the eastern islet cave, indicating detec-tions at these receivers were of fish moving alongdeeper boulder and rocky wall habitats present inthis area. These results are consistent with diverobservations of fish habitat associations by Aburto-Oropeza & Balart (2001), in which the highest densi-ties of both species were found in association withthe wall habitats along the eastern and westernpoints of the islets.

Implications for management

The objectives of the establishment of Los IslotesMarine Reserve as a part of the larger Espiritu SantoArchipelago National Park (ESANP) were primarilyto conserve biodiversity, ecosystem function, and

Mar Ecol Prog Ser 501: 191–206, 2014

genetic diversity among populations, and to promotesustainable use of commercial species in the region.Since there exist no studies assessing such endpointsas biodiversity, abundance, genetic diversity or fish-eries contribution prior to Los Islotes’ establishmentas a marine reserve, it is difficult to ascertain whetherit has succeeded under the original objectives of theESANP. However, the findings of the present studymay be used to assess the potential contribution offuture reserve design and management approaches.

The moderate levels of site fidelity seen for themajority of fish suggest that the protection affordedto individual fish by Los Islotes is limited over bothdaily and annual time scales, and reserve benefitsmight be improved if future reserves are designed toencompass larger areas than Los Islotes. Buffer zonesaround such reserve boundaries may also be instru-mental in protecting individuals that utilize habitatsnearing the boundaries of the reserve area, particu-larly if these may be the largest and oldest individu-als as seen for leopard grouper at Los Islotes (Nemethet al. 2007). Furthermore, there currently exist nofisheries regulations for these species in the Gulf ofCalifornia. The demonstrated high level of vulnera-bility of fish at Los Islotes due to their daily and sea-sonal movements (coincident with the times of peakexp loitation) across reserve boundaries indicates thatmanagement efforts should be complemented bythe incorporation of traditional regulations (e.g.catch, size limits, time/area closures). Observationsof spaw ning at this site did not compare with themagnitude of snapper and grouper aggregationsreported at other locations in the Gulf, and due to thelack of spawning observations for yellow snapper,this is likely not an important spawning site for thisspecies. Samoilys (1997) and Zeller (1998) foundcoral trout Plectropomus leopardus to aggregate lesspredictably and in smaller numbers at a number ofsites on the Great Barrier Reef and suggested thesewere secondary spawning sites. Los Islotes may bean example of one such site in the Gulf of California,though an alternate possibility is that heavy fishingpressure at this site prior to its closure (or as a resultof poaching) has reduced the number of participantsand level of spawning activity seen at this site. It isimportant that future studies examine the relation-ship between habitat quality and aggregation behav-ior with the aim of understanding determinant char-acteristics of which sites become primary spawningsites. Though boulder, wall and sand bottom/rockedge habitats appear to be the most important habi-tats at Los Islotes, it is also crucial to determinewhether fish encountered in other areas of the Gulf

exhibit similar patterns of site fidelity and seasonalmovement in relation to these habitats.

Frisk et al. (2013) emphasized the importance ofadult movement — in contrast to larval dispersal — inthe connectivity, structuring and recruitment of pop-ulations. To assess the success of small marine re -serves in meeting their objectives of maintaininggenetic diversity or fisheries contribution will requirean understanding of the connectivity between puta-tive secondary spawning sites such as Los Islotes andother aggregation sites (e.g. Marisla Seamount).Nevertheless, the intraspecific behavioral differ-ences seen for yellow snapper and leopard grouperat Los Islotes suggest that mixed management strate-gies affording protection to the full diversity ofaggregation and movement behaviors within a popu-lation may be the most appropriate approach forthese species.

Acknowledgements. We thank 3 anonymous reviewers fortheir help in improving the manuscript. We also thank D.Hernandez, the CMBC team in La Paz, and most impor-tantly, the entire Niparajá team for their logistic and scien-tific support in the field: Dani, Pollo, Pelón, Tito, and Zorro.We thank the La Paz CONANP office for allowance of thisproject within a protected area, as well as J. Rivera, F. León,Javier, Jorge, Cachas and A. Garcia and the fishers of SCPPPescadores del Esterito, Baja Pirata Fleet and Baja Expedi-tions for assistance capturing fish for tagging. Thank you toJ. Ketchum for kindly sharing detection data from acousticreceivers at Marisla Seamount. We are grateful to B. Allenfor comments on an early draft of the manuscript. B. Allen, J.Archie and B. Wolfe provided in valuable assistance withstatistical analyses. Thanks to W. Heyman and S. Kobara forproviding bathymetry maps of Los Islotes. This project wasfunded by the Walton Family Foundation, the David andLucile Packard Foundation, along with support from theCalifornia State University (CSU) Long Beach College ofNatural Sciences and Mathematics, CSU COAST, the AAUSKevin Gurr Scholarship, and the SCTC Marine BiologyFoundation. All work was carried out in accordance withanimal use protocols of the University of California, SanDiego (protocol S09323) and conducted under permit fromthe National Commissions of Fisheries and Aquaculture(CONAPESCA) (permit #DGOPA-05356-140710-3457).

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Editorial responsibility: Nicholas Tolimieri, Seattle, Washington, USA

Submitted: July 31, 2013; Accepted: January 3, 2014Proofs received from author(s): March 13, 2014