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. This electronic reprint is provided by the author(s) to be consulted by fellow scientists. It is not to be used for any purpose other than private study, scholarship, or research. Further reproduction or distribution of this reprint is restricted by copyright laws. If in doubt about fair use of reprints for research purposes, the user should review the copyright notice contained in the original journal from which this electronic reprint was made.
MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser
Vol. 501: 191–206, 2014 doi: 10.3354/meps10711
Published March 31
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 1
Department of Biological Sciences, California State University Long Beach, Long Beach, California 90815, USA Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego, La Jolla, California 92093-0202, USA
Sociedad 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 to understand how marine species interact with surrounding ecological communities, their susceptibility to anthropogenic disturbance (e.g. fishing pressure), or the feasibility of management strategies. Between August 2010 and September 2012, we used acoustic telemetry to continuously monitor 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 species in the SW Gulf of California. Though the majority of fish from both species exhibited moderate 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. Approximately 30% of snapper exhibited decreases in site fidelity during the spawning season, and snapper did not spawn at the reserve during the study. Grouper spawning aggregations at Los Islotes were visually observed in 2011 and 2012, though the abundance of fish and the intensity of courtship behaviors were reduced in comparison with reported aggregations elsewhere in the Gulf. Three snapper and 2 grouper made repeated movements across pelagic waters between Los Islotes and Marisla Seamount, another documented aggregation site in the SW Gulf. The demonstrated variation in movements of these species over multiple temporal and spatial scales warrants consideration of movement patterns in assessments of reserve performance, as well as the combination 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
INTRODUCTION Members of the snapper-grouper complex (Lutjanidae; Epinephelidae) play important roles in the organization of coastal ecosystems via top-down control as predators. To better understand their interactions with surrounding marine communities, we need information regarding patterns of space use and movement in these species. These characteristics may
influence the susceptibility of predators to exploitation or anthropogenic disturbance (Fahrig 2007), and may also alter distributions of prey items and competitors (Holt 1984). Unfortunately, patterns of movement remain poorly understood for a large number of species, many of which are exploited by commercial and recreational fisheries worldwide. Population declines have been reported for a number of these species (e.g. Lutjanus cyanopterus, Epinephelus stri-
*Corresponding author: email@example.com
© Inter-Research 2014 · www.int-res.com
Mar Ecol Prog Ser 501: 191–206, 2014
atus; Huntsman 1996, Sala et al. 2001), and management efforts have been impeded by the lack of available information regarding the movements of these species. In the southern Gulf of California, approximately half of the fish species targeted by coastal fisheries comprise snappers and groupers, with landings of these species generating nearly 78% of annual exvessel revenue (i.e. price paid for landings prior to onshore handling) (Erisman et al. 2010). Because many reef-associated species in the Gulf, including snappers and groupers, form seasonal spawning aggregations at predictable times and locations (Sala et al. 2003), commercial fishing activities often occur in a coincident manner (Sadovy de Mitcheson & Erisman 2012). However, current management strategies do not address the seasonal nature of these fisheries, and instead focus on establishing networks of marine reserves — areas partially or entirely protected from fishing (Rife et al. 2012). Furthermore, enforcement of reserve areas is sparse, and many of these areas are subject to substantial illegal fishing pressure. Though such reserves are expected to increase biomass, organism size and diversity within their boundaries (Halpern 2003), it is unclear how effective they are for species that may migrate to seasonally targeted aggregation sites. Species that form spawning aggregations typically exhibit resident or transient patterns of behavior, in which individuals may remain near their home range to spawn in small groups throughout the year (resident), or migrate over varying distances to form large aggregations in a brief, annual event (transient) (Domeier & Colin 1997). Though resident fish may benefit most from small marine reserves, transient individuals may be afforded little or no protection if aggregations form in unprotected areas. However, species may also adopt a diversity of behaviors that range between the extremes of resident and transient aggregation, and multiple patterns of aggregation behavior 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 variability in population management strategies, one needs to determine whether multiple aggregation behaviors are present within a population, and the proportion of individuals exhibiting each behavior (Nemeth 2012). Yellow snapper Lutjanus argentiventris and leopard grouper Mycteroperca rosacea are among the most abundant predatory fishes on rocky reefs throughout the Gulf of California (Ramírez & Rodríguez 1990, Erisman et al. 2010). Yellow snapper
range from southern California to Peru, whereas leopard grouper are found primarily in the Gulf, ranging from the southwest coast of Baja California to Jalisco, Mexico (Allen 1985, Heemstra & Randall 1993). Both species aggregate seasonally to spawn (snapper: May to September; grouper: April to May; Sala et al. 2003, Aburto-Oropeza et al. 2009, Piñon et al. 2009), during which time they are heavily exploited by coastal fisheries (Sala et al. 2003, Erisman et al. 2010). There have been no previous studies of reef fish movements in the Gulf, and it is not known how these species utilize coastal habitats, particularly with respect to spawning. The Los Islotes Marine Reserve is a small rocky islet in the southwestern Gulf of California, and 1 of 3 no-take reserves (Marine Protected Area, MPA) in the Espíritu Santo Archipelago National Park (ESANP). The ESANP was established in 2007 with the objectives of sustaining natural resources, contributing to regional coastal fisheries, and promoting sustainable tourist activities within the park (CONANP 2011). Though closed to fishing activities, Los Islotes is presumed to be subject to similar levels of illegal fishing as other small protected areas in the region. It is also recognized by regional managers as an aggregation site for several species, including yellow snapper and leopard grouper. Thus, the Los Islotes Marine Reserve represents an ideal location in which to quantify the site fidelity, movement patterns and space use of these 2 commercially important aggregative spawners. A static array of acoustic receivers was used to monitor the long-term movements of yellow snapper and leopard grouper in relation to Los Islotes, and to address the following 4 questions: (1) What is the site fidelity of these species to the reserve? (2) How do these species differ with regard to their temporal movement patterns within the Los Islotes MPA? (3) Do individuals of these species exhibit patterns of site fidelity indicative of resident or transient spawning? (4) What habitat types or depth features do fish associate with at Los Islotes?
MATERIALS AND METHODS Study site Los Islotes Marine Reserve is positioned around a small rocky islet at the northern tip of Isla Espiritu Santo, Baja California Sur, Mexico (24° 35’ 54’’ N, 110° 24’ 6’’ W) (Fig. 1). It is 1 of 3 zones in the southern Gulf fully protected from fishing, and it covers an
TinHan et al.: Snapper and grouper movement patterns
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 estimated 50% detection range. Red borders around each receiver indicate the estimated acoustic detection range of individual receivers. Numbers on contour lines represent isobath depths in meters. Green triangle indicates location of acoustic receiver at Marisla Seamount
area of 0.61 km2. The reserve boundaries extend 300 m from shore and encompass a reserve area that can be broken down into 3 zones by habitat type and depth: (1) north Los Islotes: a steep boulder field extending approximately 100 m from shore and descending from 10 to 100 m depth; (2) southwest Los Islotes: a narrow, shallow (5 to 20 m), high-relief reef crest extending approximately 400 m to the southwest (terminating at the ‘Bajito’, a shallow rocky pinnacle immediately outside of the southwest reserve boundary); and (3) east Los Islotes: a deeper (10 to 30 m) flat of unconsolidated seafloor extending 150 m southeast rapidly descending beyond a depth of 50 m, and a small underwater cave passing in a northsouth direction through the easternmost islet of Los Islotes. The bathymetry of Los Islotes was mapped over a 1 × 1 m grid using multibeam sonar (W. Heyman unpubl. data).
Tagging Between August 2010 and June 2011, 22 yellow snapper and 16 leopard grouper were captured within the reserve using baited hook and line, measured, and surgically implanted with small acoustic transmitters (V13-1L, Vemco; 36 × 13 mm, 147 dB). An additional 10 fish from each species were similarly captured and implanted with pressure-sensing acoustic transmitters (V13P-1L, Vemco; 45 × 13 mm, 150 dB, ± 2.5 m accuracy, 0.22 m resolution). Both types 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 of 1565 d. With the exception of 1 yellow snapper (29.0 cm total length, TL), all tagged fish were larger than the reported length-at-maturity for their respective species (yellow snapper: 32.6 cm TL, leopard grouper: 34.0 cm TL; Erisman et al. 2008, Piñon et al. 2009). Neither species exhibits external sexual dimorphism, thus we were unable to determine the sex of tagged individuals in this study. Once captured, fish were anesthetized in 100 mg l−1 tricaine methanesulfonate (MS-222) for 3 to 5 min. Transmitters were implanted into the peritoneum through a small incision, which was then closed by 2 interrupted absorbable sutures (Ethicon Chromic-Gut, Johnson & Johnson). Each fish was also externally tagged in the dorsal musculature with a plastic dart tag (FT-1-94, Floy Tag & Mfg) bearing a unique identification number. Fish were then transferred to a fresh seawater bath and allowed to fully recover from anesthesia before release at the site of their capture.
Acoustic monitoring To monitor fish movements in relation to the Los Islotes Reserve, an array of 7 omni-directional underwater acoustic receivers (VR2W, Vemco) was deployed on subsurface moorings throughout the reserve area (Receivers 1 to 7 in Fig. 1). To monitor movements between Los Islotes and other nearby rocky reefs, 4 additional receivers were positioned at
Mar Ecol Prog Ser 501: 191–206, 2014
prominent locations outside of the reserve. Three receivers were deployed at the northern tip of Espiritu Santo Island, approximately 500 m from the reserve boundary (Fig. 1), while the fourth (Receiver 8 in Fig. 1) was positioned at the Bahito, a rocky pinnacle immediately adjacent to the southwest reserve boundary. Fish movements to Marisla Seamount, a deep rocky pinnacle and aggregation site located 15 km NE of Los Islotes, were also periodically monitored (12 June 2011 to 23 October 2012) by an acoustic receiver deployed at this site as part of an unrelated study. Through range testing, the mean 50% detection range of receivers at Los Islotes was estimated to be approximately 180 m (range: 16 to 327 m), providing acoustic coverage for approximately 60% of the designated reserve area. Though detection ranges were highly variable among sites, poor surface conditions (Beaufort 4 to 5) during range testing suggest these are highly conservative estimates of receiver performance. Visual observations of both species indicated that fish carrying transmitters programmed for a 180 s pulse interval were likely mobile enough to be detected by receivers at least twice in a 24 h period (criteria for daily presence). When within range of a receiver (< 300 m), the transmitter emission is decoded as a unique transmitter identification number, and logged with a time and date stamp as a detection event. Detections of pressure-sensing transmitters also contained the instantaneous depth of the fish at the time of detection. Receiver performance can be influenced by interference from sources of biological or anthropogenic noise (e.g. alpheid shrimps, boat traffic) (Heupel et al. 2006). For temporal analyses based on frequency of detection, detections of a stationary reference transmitter (V13-IL) were used to calibrate for this effect. A correction factor was calculated for each hour of the day by dividing the mean detection frequency of each hour by the overall mean hourly detection frequency of the reference transmitter. Adjusted detection frequencies were produced by dividing detection frequencies from each hourly bin by their respective correction factor (see Payne et al. 2010). Only a single reference transmitter was used, because it was assumed that receiving conditions were consistent among receivers in the array.
Data analysis Analyses of telemetry data were performed using R v. 2.15.0 (R Development Core Team 2012), Statistica v. 10.0 (Statsoft), and PRIMER v. 6.1.7 (PRIMER-E,
Plymouth). Overall site fidelity of fish to Los Islotes was calculated as the proportion of days tagged individuals were present within the array since date of tagging. An individual was considered to be present within the array if it was detected at least twice in a 24 hr period. Fish were assigned to 3 groups based on their degree of site fidelity, or the proportion of days at liberty that a fish was present in the reserve, with groups being arbitrarily defined as low (< 33%), moderate (33−66%), or high (> 66%). To determine whether there were any distinct behavioral modes in patterns of presence at Los Islotes, a hierarchical cluster analysis was applied to a Simple Matching Similarity matrix generated from the presence-absence of individual fish on each day of the study period. Because fish were tagged over the span of several months, presence-absence data used in cluster analyses were truncated to begin on the earliest date on which the majority of individuals had been tagged (snapper, n = 22; grouper, n = 25). Individuals tagged after this date were omitted from cluster analyses. To determine whether site fidelity to Los Islotes varied with fish size, overall site fidelity was regressed against fish total length. Individual patterns of movement in relation to Los Islotes were sporadic through both spawning and non-spawning periods; thus we did not use ‘streaks’ (consecutive days) of presence-absence to examine temporal trends in presence. To identify long-term patterns in the presence of tagged fish at the population level, the proportion of tagged individuals present, or probability of detecting a randomly selected fish, was calculated for each day and analyzed using the Seasonal Trend Loess (STL) procedure as described in Cleveland et al. (1990). The STL procedure decomposes time series data into long-term, seasonal, and remainder components. This approach was primarily used to distinguish long-term tag losses from the reserve (via emigration, predation or fishing mortality) and potentially spawning-related changes in presence to Los Islotes (seasonal trends). The remainder component represented residual variation in daily fish presence remaining after the fitting of both seasonal and long-term trends. The STL cannot be used to examine annual patterns in time series shorter than 2 yr, thus only snapper tagged in 2010 (n = 25) were considered in this analysis. Diel patterns of movement in relation to Los Islotes as a whole were examined by pooling detection data for all receivers and all fish into hourly bins (following standardization of detection frequencies described above), applying a Fast Fourier Transform to these frequencies, and plotting
TinHan et al.: Snapper and grouper movement patterns
a spectrogram. Dominant peaks emerging in the power spectra indicated the interval of cyclical patterns in presence at Los Islotes. Time-series of detections were used to identify the movements of all tagged fish among receivers at the study site. A horizontal movement was defined as any detection of a single fish at a different receiver than that of the previous detection. Depth data from individuals carrying depth transmitters were examined to identify vertical movements, based on the changes in depth between subsequent detections of individuals. Mean hourly rates of movement (ROM) were calculated by individual for both the horizontal and vertical axes. Horizontal ROM was calculated as the number of movements per detection in hourly bins, while vertical ROM was determined by taking the mean of the absolute differences in depth between consecutive depth detections in each hour. Site attachment was estimated by calculating the evenness of detections among receivers for each individual, using a diversity index of space use adapted from Pielou’s evenness index (Pielou 1966): R
– Spatial evenness =
ln ( R )
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 to one, with values approaching one indicating even use of all areas. Spatial evenness for each species was calculated by taking the mean of the spatial evenness values calculated for each tagged individual. The relationship between spatial evenness and fish size was examined in a linear regression of spatial evenness values calculated for individual fish and fish total length. Overall patterns in space use within Los Islotes Reserve were compared by determining the proportion of detections occurring at each receiver for individual fish, then calculating the mean for each receiver.
Spawning observations Diver observations were made from 21 to 23 April and 28 to 30 September 2012, during the peak months of spawning for yellow snapper and leopard grouper, respectively, to determine the presence and extent of spawning or aggregation behavior at Los Islotes. Teams of divers swam the circumference of the reserve area to monitor spawning and estimate
the total abundance of yellow snapper and leopard grouper during their respective spawning periods. Dives were made in the late afternoon and dusk hours, and divers recorded observations of direct (gamete release) or indirect (courtship or chasing behaviors, color change, swollen abdomens) indications of spawning (detailed in Colin et al. 2003). Dives were made to depths between 5 and 20 m, and visibility ranged from 3 to 15 m.
RESULTS Site fidelity A total of 32 yellow snapper and 26 leopard grouper were tagged between August 2010 and June 2011. In 2010, 25 snapper were tagged, though only 3 grouper were tagged at this time due to the difficulty of capturing individuals of this species outside of the peak spawning months of April and May. The remaining 7 snapper and 23 grouper were tagged in April and May 2011 (Fig. 2a,b). Two snapper were omitted from the data set as they were presumed to have died within the array shortly after tagging. A third snapper (Larg22) was caught by fishers at the Bajito in March 2011 and was thus omitted from analyses of site fidelity or long-term temporal trends. Grouper exhibited the greatest overall site fidelity to Los Islotes, being detected on 64 ± 30% of days at liberty (mean ± SD). Thirteen grouper (50% of individuals) exhibited high site fidelity, 8 (30%) showed moderate site fidelity and 5 (19%) showed low site fidelity. Overall, snapper displayed moderate site fidelity (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 of fish at Los Islotes revealed 3 significant groups for yellow snapper, and 2 groups for leopard grouper (Fig. 2c,d). These distinct groups were considered to represent individuals exhibiting resident, transient or mixed patterns of presence to the reserve. For yellow snapper, the largest group of individuals (~30%) exhibited moderate to high levels of site fidelity during non-spawning months, but sustained periods of absence during the months of spawning. Approximately 80% of grouper displayed continuous patterns of residence at the reserve, and though the remaining individuals showed low overall site fidelity, these individuals also exhibited high site fidelity over short time scales (i.e. weeks). A significant rela-
Mar Ecol Prog Ser 501: 191â€“206, 2014
Fig. 2. Lutjanus argentiventris, Mycteroperca rosacea. (a,b) Detection plots of individual daily presence-absence at Los Islotes Reserve 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 detected at Los Islotes; black triangles represent detections at Marisla Seamount. Shaded areas (a,b) indicate spawning seasons for the species shown; rows are arranged in order of similarity between individuals. Short, vertical gray lines in (a) indicate individuals not included in nMDS analyses. Overlaid contour lines (in c,d) from hierarchical cluster analysis represent groups showing different residency patterns (corresponding group membership represented by red, blue, and green lines in detection plots)
tionship was found between site fidelity and body size for grouper (F1, 23 = 8.637, r2 = 0.273, p = 0.007; Fig. 3). However, the significance and strength of this relationship were greatly improved (F1, 22 = 21.71, r2 = 0.49, p = 0.0001) when grouper Mros17 was omitted from analysis as an outlier (Fig. 3). No such relationship between size and site fidelity was observed for snapper (F1, 27 = 1.934, r2 = 0.06, p = 0.175).
Temporal patterns STL decomposition of the daily proportion of tagged yellow snapper present over the course of the study revealed long-term declines in fish presence
and seasonal fluctuations corresponding with the spawning season (May to September) (Fig. 4). The proportion of tagged snapper present at Los Islotes declined steadily over a 2 yr period at a mean rate of 35.5% per year (Fig. 4c). Cyclical changes in snapper presence to Los Islotes were also identified, with the probability of detecting a tagged fish decreasing by approximately 30% during the months of peak spawning. In each year, the probability of detection increased rapidly between the months of November and January, shortly after the end of the reported spawning season (Fig. 4b). However, there remained substantial daily fluctuations in snapper presence (approx. Âą10%) that could not be explained by the identified seasonal or long-term trends (Fig. 4d). As
TinHan et al.: Snapper and grouper movement patterns
Fig. 3. Lutjanus argentiventris, Mycteroperca rosacea. Natural-log relationship between fish length and site fidelity of (a) yellow snapper and (b) leopard grouper at the Los Islotes Reserve. Reported regression statistics for leopard grouper omit an outlier (Mros17) shown as ‘×’ in lower right corner of plot (b)
data for leopard grouper were limited to a period of 1 yr, STL analysis could not be used to identify annual cycles for this species. However, similar longterm declines (72%) in fish presence to Los Islotes were also identified for this species (data not shown). No size difference was found between yellow snapper that disappeared from the array and those remaining at Los Islotes at the end of the study period (September 2012) (t-test, t = −0.243, p = 0.980). However, 18 grouper were no longer detected at Los Islotes at the end of the study, and these were significantly smaller than those that remained in the array (t-test, t = −4.377, p = 0.0002). Of the 18 ind. that disappeared from the array, 7 (36%) showed declines in site fidelity in the weeks prior to their disappearance (Fig. 2b; e.g. Mros08). Spectral analysis of adjusted hourly detection frequencies revealed 2 dominant peaks at periods of 12 and 24 h for yellow snapper and a single large peak at 24 h for leopard grouper (Fig. 5). Detection frequency did not vary significantly with tide height, tidal phase, or lunar phase. The frequency of movements made among receivers, or level of horizontal
activity, also peaked during the crepuscular hours for both species, although these increases did not correspond to any particular area of the reserve. Snapper activity levels became more variable during the night, though there was no clear overall increase in activity during this period (Fig. 6a). Grouper maintained an increased level of activity throughout the day before becoming more quiescent at night (Fig. 6b). Examination of vertical activity patterns for individuals tagged with depth-sensing transmitters (yellow snapper: n = 9; leopard grouper: n = 10) revealed temporal patterns similar to those in the horizontal axis, with both species increasing in activity during the crepuscular hours. However, snapper sustained their levels of vertical activity throughout the night, while grouper showed an overall pattern of increased crepuscular and diurnal vertical activity (Fig. 6c,d). Between June 2011 and October 2012, 3 yellow snapper (Larg12, Larg20, Larg26) and 2 leopard grouper (Mros07, Mros11) were detected by acoustic receivers at the Marisla Seamount, approximately 15 km to the northeast of Los Islotes (Fig. 1). Marisla Seamount comprises 3 submerged rocky pinnacles that rise from a depth of 1000 m to within 15 m of the surface. All 3 snapper were first detected at Marisla Seamount between July and September — the months of peak spawning for yellow snapper. Two snapper (Larg12, Larg20) remained at this site for extended periods (> 6 mo), while the third (Larg26) was only detected on 9 non-consecutive days over the subsequent 8 mo. Of these 3, only 1 snapper (Larg12) returned to Los Islotes from Marisla Seamount. In contrast, leopard grouper movements to Marisla Seamount did not coincide with the spawning season and tended to be brief, with all fish traveling to Marisla Seamount and back to Los Islotes within 24 h. Transit times between the 2 sites for yellow snapper ranged from 3 h to 8 d, while the shortest transit time for leopard grouper was 102 min at an estimated swimming speed of 2.5 m s−1 or 2.9 body lengths s−1.
Spawning observations We confirmed the presence of at least 1, and possibly 2, small spawning aggregations of leopard grouper at Los Islotes during underwater surveys conducted in the afternoon (13:00 to 20:00 h) on 21 to 23 April 2012. Throughout this period, we observed a group of approx. 80 adult leopard groupers loosely aggregated off the east point of the island. Fish were
Mar Ecol Prog Ser 501: 191â€“206, 2014
Fig. 4. Lutjanus argentiventris. Time series of proportion of tagged yellow snapper present at Los Islotes (a) over the duration of 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 of Fast Fourier Transformed (FFT) hourly detection frequencies at Los Islotes for (a) yellow snapper and (b) leopard grouper
present both in the water column above the thermocline (depth range = 5 to 10 m) or on the reef itself (depth range = 10 to 20 m). Indirect evidence of spawning via the presence of numerous females with enlarged (swollen) abdomens was observed on all dives. We also observed direct evidence of spawning during visual surveys conducted the hour before sunset (i.e. 18:45 to 19:45 h) on 22 and 23 April at the easternmost point of the island, on both the north and south side of the point. During these dives, we recorded nearly the entire repertoire of behaviors associated with courtship and spawning in leopard grouper: courtship color change, following, courtship chase, mobbing, female darting, rubbing, bumping, lateral dis-
TinHan et al.: Snapper and grouper movement patterns
domens. However, courtship or spawning was not observed. Several small groups of 10 to 20 adult leopard grouper were documented on reefs on the north side of the island, indicating the presence of approx. 180 to 200 adult leopard grouper at Los Islotes during the April spawning period. Total abundance of yellow snapper at Los Islotes was estimated to be no more than 100 ind. in September 2012. We observed an aggregation of 50 to 100 adult yellow snapper within the cave at Los Islotes during all survey months; however, we found no direct evidence that this aggregation represented a spawning aggregation. Though small groups of snapper (< 5 ind.) were observed loosely swimming together, there were no definitive signs of aggregation, and no observations were made that indicated spawning activity in yellow snapper at this site.
Fig. 6. Lutjanus argentiventris, Mycteroperca rosacea. Activity levels by time of day (hourly): rate of (a,b) horizontal movement and (c,d) vertical movement for yellow snapper and leopard grouper. Grey shaded areas indicate nighttime. Note differences in scale along vertical axes
play, gaping, burst rise, head shake, and spawning rush (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 mobbing of the female, followed by rapid ascents off the reef up into the water column. While rushing behavior of subgroups was observed, gamete release could not be confirmed due to the poor visibility and strong currents. A second aggregation of approx. 60 leopard grouper was observed at the west point of the island, which included gravid females with enlarged ab-
Yellow snapper exhibited significantly lower spatial evenness index values (0.60 ± 0.17, mean ± SD) than leopard grouper (0.71 ± 0.14) (Kruskal-Wallis χ2 = 5.13, df = 1, p = 0.024). Though grouper were found to make greater use of the available reserve area, both species were most frequently detected by receivers along the east point and northern side of the islet — locations composed primarily of steep boulder fields and wall habitat fringed by sand bottom habitat (Table 1). There was no relationship between spatial evenness and body length for either species (snapper: r2 = 0.009, p = 0.394; grouper: r2 = 0.063, p = 0.119). However, both species were found to occupy a similar distribution of depths (F = 3.40, df = 1, p = 0.085). Though no correlation was found between body length and mean depth for snapper (r2 = 0.06, p = 0.247), a significant positive relationTable 1. Lutjanus argentiventris, Mycteroperca rosacea. Relative proportion of detections calculated across individuals at each acoustic receiver at Los Islotes Reserve Station 1 2 3 4 5 6 7 8
Yellow snapper Mean ± SD
Leopard grouper Mean ± SD
0.205 ± 0.212 0.087 ± 0.153 0.311 ± 0.215 0.125 ± 0.153 0.201 ± 0.209 0.025 ± 0.027 0.014 ± 0.030 0.029 ± 0.087
0.160 ± 0.147 0.143 ± 0.144 0.174 ± 0.183 0.145 ± 0.145 0.090 ± 0.139 0.058 ± 0.074 0.120 ± 0.167 0.105 ± 0.186
Mar Ecol Prog Ser 501: 191â€“206, 2014
ship was found for grouper (r2 = 0.47, p = 0.017) (Fig. 7), with the largest individuals being detected at mean depths of 16 to 18 m.
DISCUSSION Site fidelity Overall, yellow snapper and leopard grouper tagged in this study exhibited site fidelity to the Los Islotes Reserve. However, species differed in their patterns of presence to the reserve, as well as their overall degrees of site fidelity. The majority of leopard grouper (80%) were detected on at least 50% of days, whereas less than half (48%) of yellow snapper were detected on at least 50% of days (Fig. 3). Examination of long-term changes in site fidelity for both species revealed an overall decline in the presence of tagged fish at Los Islotes over the course of the study. Over a 2 yr period (789 d), approximately 70% of snapper were no longer detected at Los Islotes, while a similar proportion of leopard grouper were undetected in the reserve after 515 d. Similar patterns have been reported in previous studies of reef fish movements, although residence times are variable among studies. Topping & Szedlmayer (2011) observed comparable declines in red snapper Lutjanus campechanus presence on reefs in the Gulf of Mexico, with 20 to 25% of tagged fish remaining at study sites after a period of ~750 d, while a study of snapper and grouper in the Florida Keys reported residence times of <1 yr (Lindholm et al. 2005). While Los Islotes is a no-take marine reserve, enforcement is sporadic due to the remote location of the reserve in relation to the nearest coastal city (La Paz; distance = 50 km). Illegal fishing at night by hookah divers is known to occur at this site (B. Erisman, O. Aburto-
Fig. 7. Mycteroperca rosacea. Relationship between fish total length and mean depth for leopard grouper at Los Islotes Reserve (r2 = 0.47, p = 0.017)
Oropeza & A. Weaver unpubl. data; pers. comm. with park guards and CONANP officials), and it is therefore unknown whether declines in the presence of tagged fish at Los Islotes are the result of long-term emigration, natural mortality by predation, or fishing mortality. Another possibility for fish disappearance is tag failure, though unpublished data from other studies indicate extremely low failure rates (< 3%) for similar 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 this location should be viewed as conservative. Though the majority of grouper exhibited moderate to high levels of site fidelity to Los Islotes, periods of absence were often prolonged, and many individuals did not return to the reserve prior to completion of the study (Fig. 2b). There was considerable variation in site fidelity among individuals, and a small percentage (16%) exhibited low site fidelity to the reserve. It was found that much of this variation was explained by body size, with smaller individuals exhibiting lower site fidelity to the reserve than larger grouper (Fig. 3b). At the end of the study, the majority of tagged grouper had disappeared from Los Islotes, and these fish were also found to be significantly smaller than those remaining in the reserve. Ontogenetic habitat shifts have been described in at least one other species of Mycteroperca (gag grouper; M. microlepis), where individuals move from shallow to deeper reef habitats with maturity, presumably to exploit larger or more abundant prey items found in habitats presenting a greater predation risk to smaller individuals (Bullock & Smith 1991, Dahlgren & Eggleston 2000). Shapiro et al. (1994) also observed an increase in home range size with body size for red hind Epinephelus guttatus, as well as the disappearance of approximately 44% of tagged individuals from a small fore reef in Puerto Rico over a 5 mo period. However, if Los Islotes was abandoned by maturing individuals in favor of habitat more suitable to larger fish, this does not explain why large grouper are encountered in any substantial number at Los Islotes. In fact, fish tagged in the present study were at least as large (53 cm mean SL) as mature leopard grouper captured in spawning aggregations near Loreto, Mexico (47 cm mean SL) (Erisman et al. 2007). Illegal fishing has been reported to occur at Los Islotes at night, when enforcement levels are lowest, and the abrupt disappearance of some individuals (Fig 2b; e.g. Mros03) from the array may have resulted from their capture by fishers within the reserve. However, some individuals lost from the array showed declines in site
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 these particular losses resulted from illegal fishing within the Los Islotes Reserve. Though the fate of leopard grouper after leaving the reserve remains unknown, these declines in site fidelity may represent periods in which grouper began exploring new habitats before eventually emigrating from Los Islotes. We saw no indication that individuals departed from, or returned to, the array via any particular part of the reserve, but we suspect that fish might have been capable of traversing the range of one or more receivers between transmitter pulses, obscuring any directional pattern of emigration. If indeed these disappearances were the result of emigration, there are 2 potential explanations for the size difference seen. Firstly, smaller grouper may have been competitively excluded from Los Islotes by larger individuals and were thus forced to visit sites elsewhere in order to satisfy their energetic requirements. Secondly, the abundance of sea lions Zalophus californianus at Los Islotes (~400 ind.; CONANP 2011) might have posed enough of a disturbance or predation risk to smaller grouper to merit emigration to habitats with fewer potential predators. On several occasions, divers in the present study observed sea lions harassing both yellow snapper and leopard grouper, and interrupting spawning behaviors in the latter (B. Erisman & A. Weaver pers. obs.), though studies of sea lion diet have not explicitly identified these species as prey items (e.g. GarcĂa-RodrĂguez & Aurioles-Gamboa 2004). Snapper were detected consistently over the course of the study but were frequently absent for short periods (Fig. 2a). The brief yet common nature of absences for snapper suggests individuals utilized other nearby areas in addition to habitat at Los Islotes. Though it is possible that these absences resulted from fish moving into areas of the reserve outside of the detection range of receivers, it is unlikely fish would remain in these locations for the multi-day periods observed. Previous studies of snapper movement have found fish to make repeated forays among multiple areas and habitat types separated by small or intermediate distances (Meyer et al. 2007, Luo et al. 2009). Los Islotes is separated from the nearest rocky reef (northern Isla Espiritu Santo) by waters ranging in depth from 80 to 100 m, and a distance of approx. 700 m. However, on only one occasion was a snapper detected by the array at northern Espiritu Santo. Because of the relatively long pulse interval of the transmitters used in this study (110 to 250 s), it is possible that fish were able
to transit this area undetected while making directed movements. It is also plausible that fish venturing away from Los Islotes simply did not orient to the nearest available habitat, and instead traveled along routes outside of the detection range of these receivers until reaching more preferable sites further along Espiritu Santo. Site fidelity in yellow snapper was also variable among individuals, but size could not explain the variation in site fidelity in this species (Fig. 3a). Cluster analysis of patterns in presence-absence also produced groups indicating fish from both species exhibited differential patterns in movement and site fidelity in relation to Los Islotes. Such patterns have also been reported for other species inhabiting coastal waters, and it is presumed that multiple patterns in movement or space use may provide individuals with a means of minimizing intraspecific competition for resources such as food or space. For example, a study of movements of juvenile Atlantic sharpnose shark Rhizoprionodon terraenovae identified multiple peaks in the distribution of site fidelity and home range values (Carlson et al. 2008). Similar results were obtained from another study of sparid snapper Pagrus auratus movements in a New Zealand MPA, where 2 distinct groups of fish were identified as exhibiting either low or high degrees of site fidelity (Egli & Babcock 2004). Two possible interpretations of the apparent differences in site fidelity seen among individuals are that (1) snapper with low site fidelity to Los Islotes exhibit high site fidelity to another area, or (2) snapper with low site fidelity to Los Islotes are simply more transient than those displaying high degrees of site fidelity. Snapper movements among different activity spaces in the Gulf remain unclear, and future studies using active tracking may be successful in identifying the scale and frequency of these movements, as well as the influence of environmental factors.
Temporal patterns A moderate seasonal component was also identified in patterns of presence of tagged yellow snapper at Los Islotes. The greatest proportion of tagged fish was detected between February and April, followed by a steady decline through the summer and early fall (Fig. 4b). Yellow snapper in the Gulf of California have been found to spawn throughout the summer months (May to Sept) (Sala et al. 2003, AburtoOropeza et al. 2009), though local fishers report that spawning activity and aggregative behaviors peak in
Mar Ecol Prog Ser 501: 191â€“206, 2014
August and September. However, many fish that were less likely to be detected during spawning periods did not simply leave Los Islotes for extended periods, but instead made multiple trips away from the reserve throughout the spawning season (Fig 2a). Yellow snapper are serial spawners, and these repeated short-term migrations may therefore represent movements to other spawning sites in the Gulf. In this regard, yellow snapper appear to exhibit similar spawning patterns to those identified in earlier studies of lutjanid reproduction, where species tend to spawn throughout an extended spawning season containing multiple peaks in spawning activity (Johannes 1981, Grimes 1987, Collins et al. 1996). Though the repeated seasonal declines in presence to a home range seen in the present study are characteristic of transient aggregation behavior, it is important to note that the proportion of tagged fish present at Los Islotes fluctuated by ~30% between spawning and non-spawning periods (Fig. 4b). It is unknown what proportion of the adult population spawns each year, so the possibility remains that some individuals simply did not engage in spawning during this study. Local divers and tour operators have reported seeing yellow snapper spawn at Los Islotes, though dive surveys performed in the present study provided little evidence of spawning or aggregation behavior at this site. On several occasions, snapper were seen to form small groups and engage in chasing behaviors that are typically followed by courtship displays and spawning, but these groups were often interrupted by rushes from sea lions that inhabit Los Islotes, and no direct observations of gamete release or spawning rushes were made. However, yellow snapper have also been observed to form large spawning aggregations at sites elsewhere in the Gulf, such as Isla Las Animas, Cabo Pulmo National Park and Marisla Seamount (B. Erisman pers. obs.). Interestingly, 3 tagged snapper (Larg12, Larg20, Larg26) made a synchronized migration from Los Islotes at the end of July 2011 and were detected shortly afterwards on acoustic receivers deployed at Marisla Seamount. Because these migrations coincided with the beginning of what are thought to be the months of peak spawning for yellow snapper, we speculate that they may have been related to reproduction, though further study is needed to understand the nature and degree of connectivity between these 2 sites. Erisman et al. (2007) reported seasonal shifts in leopard grouper abundance among a number of sites near Loreto, Mexico, and suggested that individuals migrate over significant distances to specific sites in order to spawn. Though 2 grouper in the present
study made migrations over a distance of 15 km to Marisla Seamount, these movements did not correspond with spawning periods and were thus not believed to be spawning migrations. We observed the synchronous disappearance of 7 grouper from Los Islotes at the start of the 2012 spawning season (27 April to 13 May 2012) (Fig. 2b), and though the possibility of fishing mortality could not be eliminated (landings peak between March and May; Erisman et al. 2010), we speculate these movements were related to spawning. Dive surveys also provided evidence of leopard grouper spawning at Los Islotes during the months of April and May, suggesting grouper at this site may instead represent a subpopulation of both resident and transient spawners. There is evidence that aggregating species may exhibit partial migration, where a single population contains both resident and transient spawners (Jarvis et al. 2010, Semmens et al. 2010). Partial migration in fish may represent a suite of strategies within a population whereby individuals may maximize their fitness under a combination of environmental and genetic factors (e.g. food availability, sex, maturation or growth rates) (Jonsson & Jonsson 1993). Previous studies have shown that the distribution and availability of resources, such as food or habitat, can impact social structures and reproductive behaviors (e.g. Travis & Slobodchikoff 1993), and it is possible that differences in habitat quality are influencing the differences in aggregation behavior seen between Los Islotes and sites sampled near Loreto. For example, Marsh et al. (2000) report decreased aggregation behavior and increased site fidelity in male tungara frogs as the distance between ponds (breeding habitat) increased. In contrast to coastal areas like Loreto, where fish may be able to move easily among aggregation sites via contiguous coastal habitat, Los Islotes may instead represent one of several insular, patchily distributed aggregation sites, where it is adaptive for individuals to form resident spawning aggregations. Spectral analyses revealed a diel pattern in the hourly detection frequencies of a stationary reference transmitter, indicating that diel rhythms in background noise interfered, to some degree, with detection efficiencies of receivers. These results are broadly consistent with the findings of Payne et al. (2010), in which predictable diel fluctuations in receiver performance were identified and attributed to interference from external noise sources (e.g. soniferous fishes or invertebrates). However, in contrast to the opposing diel patterns shown in Payne et al. (2010), the similarity of patterns seen between corrected and uncorrected detection frequencies at Los
TinHan et al.: Snapper and grouper movement patterns
Islotes suggest environmental noise did not fundamentally alter observations of fish movement at this site. Spectrograms of hourly detection frequencies at Los Islotes revealed a dominant 24 h period in activity, indicating clear patterns of diel movement for both species. A secondary peak in activity occurring at 12 h intervals was observed in snapper, but patterns of fish presence to the reserve were not found to correspond with tidal height or phase, so this peak most likely represents the 12 h interval between crepuscular periods of activity in this species (Fig. 5a). Examination of levels of horizontal and vertical movement in snapper also revealed peaks in activity during the crepuscular periods (Fig. 6a,c). This is consistent with previous observations of yellow snapper movements in the Gulf of California made by Hobson (1965), who found snapper to be most active when foraging at dusk and at night, and least active when seeking refuge in rock crevices during the day. Because of the low probability of detecting fish when sheltered in rock crevices, it is likely that the 24 h interval between periods of presence and absence to the reserve observed in spectral analyses for both species are the result of diurnal refuging behavior, rather than diurnal movements away from the reserve area. While no substantive secondary peak was observed in spectral analysis of leopard grouper movements in relation to Los Islotes (Fig. 5b), small increases in activity within the reserve were observed during crepuscular periods (Fig. 6b,d). This indicates that while grouper become more active during the crepuscular hours, they show no shift in their overall presence at the reserve during these periods. These periods of activity are most likely foraging-related as leopard grouper are thought to be primarily crepuscular foragers (Hobson 1965).
Space use Crepuscular and nocturnal foraging behaviors are common among predatory fishes, where low light levels probably allow predators to increase their likelihood of capturing small, fast-moving prey items (Hobson et al. 1981, Helfman 1986, Parrish 1992), such as schools of flat-iron herring Harengula thrissina that frequent Los Islotes. Flat-iron herring are a principal prey item of adult yellow snapper and leopard grouper, but both species also show ontogenetic shifts in diet: Juveniles primarily consume benthic invertebrates (and fish eggs, for snapper), while adults are increasingly piscivorous (Hobson 1965,
VĂĄzquez et al. 2008). Hobson (1965) observed that leopard grouper typically utilized sand bottom habitats to ambush schooling baitfish near the surface, and larger grouper in the present study were detected most commonly at depths >15 m, coinciding with sand bottom/rock edge habitat surrounding Los Islotes. Larger grouper might simply occupy deeper waters irrespective of habitat type, but another possibility is that larger, more piscivorous individuals are seeking out deeper sand bottom habitats to better prey on small schooling fish as described in Hobson (1965). Yellow snapper exhibited spatial evenness values lower than those calculated for leopard grouper, indicating a greater degree of site attachment to specific areas of the reserve. Diver observations indicate that large numbers of snapper would congregate in a small underwater cave passing in a north-south direction through the easternmost islet of Los Islotes. A large proportion of detections at eastern Los Islotes may be attributed to the aggregation of tagged snapper within this feature, as 2 out of the 3 receivers having the greatest number of yellow snapper detections had an unimpeded â€˜line-of-sightâ€™ into this cave. Detections of yellow snapper along the western point of Los Islotes were infrequent. Though range tests indicated receiver performance to be poor in this area, detection frequencies of grouper at this site were comparable to those in other parts of the reserve, suggesting receiver performance might have been adequate for detection of fish movements through this area. Leopard grouper were detected more evenly across all receivers in the array, but similar to snapper, detection frequencies were greatest along the easternmost point and north side of Los Islotes. However, grouper were not observed to congregate in the eastern islet cave, indicating detections at these receivers were of fish moving along deeper boulder and rocky wall habitats present in this area. These results are consistent with diver observations of fish habitat associations by AburtoOropeza & Balart (2001), in which the highest densities of both species were found in association with the wall habitats along the eastern and western points of the islets.
Implications for management The objectives of the establishment of Los Islotes Marine Reserve as a part of the larger Espiritu Santo Archipelago National Park (ESANP) were primarily to conserve biodiversity, ecosystem function, and
Mar Ecol Prog Ser 501: 191–206, 2014
genetic diversity among populations, and to promote sustainable use of commercial species in the region. Since there exist no studies assessing such endpoints as biodiversity, abundance, genetic diversity or fisheries contribution prior to Los Islotes’ establishment as a marine reserve, it is difficult to ascertain whether it has succeeded under the original objectives of the ESANP. However, the findings of the present study may be used to assess the potential contribution of future reserve design and management approaches. The moderate levels of site fidelity seen for the majority of fish suggest that the protection afforded to individual fish by Los Islotes is limited over both daily and annual time scales, and reserve benefits might be improved if future reserves are designed to encompass larger areas than Los Islotes. Buffer zones around such reserve boundaries may also be instrumental in protecting individuals that utilize habitats nearing the boundaries of the reserve area, particularly if these may be the largest and oldest individuals as seen for leopard grouper at Los Islotes (Nemeth et al. 2007). Furthermore, there currently exist no fisheries regulations for these species in the Gulf of California. The demonstrated high level of vulnerability of fish at Los Islotes due to their daily and seasonal movements (coincident with the times of peak exploitation) across reserve boundaries indicates that management efforts should be complemented by the incorporation of traditional regulations (e.g. catch, size limits, time/area closures). Observations of spawning at this site did not compare with the magnitude of snapper and grouper aggregations reported at other locations in the Gulf, and due to the lack of spawning observations for yellow snapper, this is likely not an important spawning site for this species. Samoilys (1997) and Zeller (1998) found coral trout Plectropomus leopardus to aggregate less predictably and in smaller numbers at a number of sites on the Great Barrier Reef and suggested these were secondary spawning sites. Los Islotes may be an example of one such site in the Gulf of California, though an alternate possibility is that heavy fishing pressure at this site prior to its closure (or as a result of poaching) has reduced the number of participants and level of spawning activity seen at this site. It is important that future studies examine the relationship between habitat quality and aggregation behavior with the aim of understanding determinant characteristics of which sites become primary spawning sites. Though boulder, wall and sand bottom/rock edge habitats appear to be the most important habitats at Los Islotes, it is also crucial to determine whether fish encountered in other areas of the Gulf
exhibit similar patterns of site fidelity and seasonal movement in relation to these habitats. Frisk et al. (2013) emphasized the importance of adult movement — in contrast to larval dispersal — in the connectivity, structuring and recruitment of populations. To assess the success of small marine reserves in meeting their objectives of maintaining genetic diversity or fisheries contribution will require an understanding of the connectivity between putative secondary spawning sites such as Los Islotes and other aggregation sites (e.g. Marisla Seamount). Nevertheless, the intraspecific behavioral differences seen for yellow snapper and leopard grouper at Los Islotes suggest that mixed management strategies affording protection to the full diversity of aggregation and movement behaviors within a population may be the most appropriate approach for these species. Acknowledgements. We thank 3 anonymous reviewers for their help in improving the manuscript. We also thank D. Hernandez, the CMBC team in La Paz, and most importantly, the entire Niparajá team for their logistic and scientific support in the field: Dani, Pollo, Pelón, Tito, and Zorro. We thank the La Paz CONANP office for allowance of this project within a protected area, as well as J. Rivera, F. León, Javier, Jorge, Cachas and A. Garcia and the fishers of SCPP Pescadores del Esterito, Baja Pirata Fleet and Baja Expeditions for assistance capturing fish for tagging. Thank you to J. Ketchum for kindly sharing detection data from acoustic receivers at Marisla Seamount. We are grateful to B. Allen for comments on an early draft of the manuscript. B. Allen, J. Archie and B. Wolfe provided invaluable assistance with statistical analyses. Thanks to W. Heyman and S. Kobara for providing bathymetry maps of Los Islotes. This project was funded by the Walton Family Foundation, the David and Lucile Packard Foundation, along with support from the California State University (CSU) Long Beach College of Natural Sciences and Mathematics, CSU COAST, the AAUS Kevin Gurr Scholarship, and the SCTC Marine Biology Foundation. All work was carried out in accordance with animal use protocols of the University of California, San Diego (protocol S09323) and conducted under permit from the National Commissions of Fisheries and Aquaculture (CONAPESCA) (permit #DGOPA-05356-140710-3457). LITERATURE CITED
Aburto-Oropeza O, Balart E (2001) Community structure of reef fish in several habitats of rocky reef in the Gulf of California. Mar Ecol 22:283−305 Aburto-Oropeza O, Dominguez-Guerrero I, Cota-Nieto J, Plomozo-Lugo T (2009) Recruitment and ontogenetic habitat shifts of the yellow snapper (Lutjanus argentiventris) in the Gulf of California. Mar Biol 156:2461−2472 Allen GR (1985) FAO species catalogue, Vol 6. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish Synop No. 125(6)
TinHan et al.: Snapper and grouper movement patterns
Bullock LH, Smith GB (1991) Memoirs of the Hourglass cruises. Seabasses (Pisces: Serranidae). Florida Marine Research Institute, St. Petersburg, FL Carlson JK, Heupel MR, Bethea DM, Hollensead LD (2008) Coastal habitat use and residency of juvenile Atlantic sharpnose sharks (Rhizoprionodon terraenovae). Estuar Coast 31:931−940 Cleveland RB, Cleveland WS, McRae JE, Terpenning I (1990) STL: a seasonal-trend decomposition procedure based on loess. J Off Stat 6:3−73 Colin PL, Sadovy YJ, Domeier ML (2003) Manual for the study and conservation of reef fish spawning aggregations. SCRFA (Spec Publ), San Diego, CA Collins LA, Johnson AG, Keim CP (1996) Spawning and annual fecundity of the red snapper (Lutjanus campechanus) from the northeastern Gulf of Mexico. In: Arreguin-Sánchez F, Munro JL, Balgos MC, Pauly D (eds) Biology, fisheries and culture of tropical groupers and snappers. Proc 48th Int Cent Living Aquat Res Manage, Manila, Phillipines, p 174−188 CONANP (Comisíon Nacional de Áreas Naturales Protegidas) (2011) Programa de manejo del Parque Nacional exclusivamente la zona marina del Archipiélago de Espíritu Santo. CONANP, México City Dahlgren CP, Eggleston DB (2000) Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology 81:2227−2240 Domeier ML, Colin PL (1997) Tropical reef fish spawning aggregations: defined and reviewed. Bull Mar Sci 60: 698−726 Egli DP, Babcock RC (2004) Ultrasonic tracking reveals multiple behavioural modes of snapper (Pagrus auratus) in a temperate no-take marine reserve. ICES J Mar Sci 61: 1137−1143 Erisman BE, Allen LG (2006) Reproductive behavior of a temperate serranid fish, Paralabrax clathratus (Girard), from Santa Catalina Island, California, USA. J Fish Biol 68:157−184 Erisman BE, Buckhorn ML, Hastings PA (2007) Spawning patterns in the leopard grouper, Mycteroperca rosacea, in comparison with other aggregating groupers. Mar Biol 151:1849−1861 Erisman BE, Rosales-Casián JA, Hastings PA (2008) Evidence of gonochorism in a grouper, Mycteroperca rosacea, from the Gulf of California, Mexico. Environ Biol Fishes 82:23−33 Erisman B, Mascarenas I, Paredes G, Sadovy de Mitcheson Y, Aburto-Oropeza O, Hastings P (2010) Seasonal, annual, and long-term trends in commercial fisheries for aggregating reef fishes in the Gulf of California, Mexico. Fish Res 106:279−288 Fahrig L (2007) Non-optimal animal movement in humanaltered landscapes. Funct Ecol 21:1003−1015 Frisk MG, Jordaan A, Miller TJ (2013) Moving beyond the current paradigm in marine population connectivity: are adults the missing link? Fish Fish, doi:10.1111/faf.12014 García-Rodríguez FJ, Aurioles-Gamboa D (2004) Spatial and temporal variation in the diet of the California sea lion (Zalophus californianus) in the Gulf of California, Mexico. Fish Bull 102:47−62 Grimes CB (1987) Reproductive biology of the Lutjanidae: a review. In: Polovina JJ, Ralston S (eds) Tropical snappers and groupers: biology and fisheries management. West View Press, Boulder, CO, p 239−294 Halpern BS (2003) The impact of marine reserves: Do
reserves work and does reserve size matter? Ecol Appl 13:S117−S137 Heemstra PC, Randall JE (1993) FAO species catalogue, Vol 16. Groupers of the world. An annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper and lyretail species known to date. FAO Fish Synop no. 125(16) Helfman GS (1986) Fish behaviour by day, night and twilight. In: Pitcher TJ (ed) The behaviour of teleost fishes. Croom Helm, London, p 366−387 Heupel MR, Semmens JM, Hobday AJ (2006) Automated acoustic tracking of aquatic animals: scales, design and deployment of listening station arrays. Mar Freshw Res 57:1−13 Hobson ES (1965) Diurnal-nocturnal activity of some inshore fishes in the Gulf of California. Copeia 1965:291−302 Hobson ES, McFarland WN, Chess JR (1981) Crepuscular and nocturnal activities of Californian nearshore fishes, with consideration of their scotopic visual pigments and the photic environment. Fish Bull 79:1−30 Holt RD (1984) Spatial heterogeneity, indirect interactions, and the coexistence of prey species. Am Nat 124: 377−406 Huntsman G (1996) IUCN 2013. IUCN Red List of threatened species v. 2013.2. www.iucnredlist.org (accessed 04 July 2013) Jarvis ET, Linardich C, Valle CF (2010) Spawning-related movements of barred sand bass, Paralabrax nebulifer, in southern California: interpretations from two decades of historical tag and recapture data. Bull South Calif Acad Sci 109:123−143 Johannes RE (1981) Words of the lagoon: fishing and marine lore in the Palau district of Micronesia. University of California Press, Berkeley, CA Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fish 3: 348−365 Lindholm J, Kaufman L, Miller S, Wagschal A, Newville M (2005) Movement of yellowtail snapper (Ocyurus chrysurus Block 1790) and black grouper (Mycteroperca bonaci Poey 1860) in the northern Florida Keys National Marine Sanctuary as determined by acoustic telemetry. Marine Sanctuaries Conservation Series, Silver Spring, MD Luo J, Serafy JE, Sponaugle S, Teare PB, Kieckbush D (2009) Movement of grey snapper Lutjanus griseus among subtropical seagrass, mangrove, and coral reef habitats. Mar Ecol Prog Ser 380:255−269 Marsh DM, Stanley Rand A, Ryan MJ (2000) Effects of interpond distance on the breeding ecology of tungara frogs. Oecologia 122:505−513 Meyer CG, Papastamatiou YP, Holland KN (2007) Seasonal, diel, and tidal movements of green jobfish (Aprion virescens, Lutjanidae) at remote Hawaiian atolls: implications for marine protected area design. Mar Biol 151: 2133−2143 Nemeth RS (2012) Ecosystem aspects of species that aggregate to spawn. In: Sadovy de Mitcheson Y, Colin PL (eds) Reef fish spawning aggregations: biology, research and management, Book 35. Springer, New York, NY, p 21−55 Nemeth RS, Blondeau J, Herzlieb S, Kadison E (2007) Spatial and temporal patterns of movement and migration at spawning aggregations of red hind, Epinephelus guttatus, in the U.S. Virgin Islands. Environ Biol Fishes 78: 365−381 Parrish JK (1992) Levels of diurnal predation on a school
Mar Ecol Prog Ser 501: 191–206, 2014
of flat-iron herring, Harengula thrissina. Environ Biol Fishes 34:257−263 Payne NL, Gillanders BM, Webber DM, Semmens JM (2010) Interpreting diel activity patterns from acoustic telemetry: the need for controls. Mar Ecol Prog Ser 419: 295−301 Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131−144 Piñon A, Amezcua F, Duncan N (2009) Reproductive cycle of female yellow snapper Lutjanus argentiventris (Pisces, Actinopterygii, Lutjanidae) in the SW Gulf of California: gonadic stages, spawning seasonality and length at sexual maturity. J Appl Ichthyol 25:18−25 R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.R-project.org Ramírez RM, Rodríguez CM (1990) Specific composition of the small scale fishery capture at Isla Cerralvo, BCS, Mexico. Investig Mar CICIMAR 5:137−141 Rife AN, Erisman B, Sanchez A, Aburto-Oropeza O (2012) When good intentions are not enough … insights on networks of ‘paper park’ marine protected areas. Conserv Lett 6:200–212 Sadovy de Mitcheson Y, Erisman B (2012) Fishery and biological implications of fishing spawning aggregations, and the social and economic importance of aggregating fishes. In: Sadovy de Mitcheson Y, Colin PL (eds) Reef fish spawning aggregations: biology, research and management, Book 35. Springer, New York, NY, p 225−284 Sagarese SR, Frisk MG (2011) Movement patterns and residence of adult winter flounder within a Long Island estuary. Mar Coast Fish Dyn Manag Ecosyst Sci 3: 295−306 Sala E, Ballesteros E, Starr RM (2001) Rapid decline of Editorial responsibility: Nicholas Tolimieri, Seattle, Washington, USA
Nassau grouper spawning aggregations in Belize: fishery management and conservation needs. Fisheries 26: 23−30 Sala E, Aburto-Oropeza O, Paredes G, Thompson G (2003) Spawning aggregations and reproductive behavior of reef fishes in the Gulf of California. Bull Mar Sci 72: 103−121 Samoilys MA (1997) Periodicity of spawning aggregations of coral trout Plectropomus leopardus (Pisces: Serranidae) on the northern Great Barrier Reef. Mar Ecol Prog Ser 160:149−159 Semmens JM, Buxton CD, Forbes E, Phelan MJ (2010) Spatial and temporal use of spawning aggregation sites by the tropical sciaenid Protonibea diacanthus. Mar Ecol Prog Ser 403:193−203 Shapiro DY, Garcia-Moliner G, Sadovy Y (1994) Social system of an inshore stock of the red hind grouper, Epinephelus guttatus (Pisces: Serranidae). Environ Biol Fishes 41:415−422 Topping DT, Szedlmayer ST (2011) Site fidelity, residence time and movements of red snapper Lutjanus campechanus estimated from long-term acoustic monitoring. Mar Ecol Prog Ser 437:183−200 Travis SE, Slobodchikoff CN (1993) Effects of food resource distribution on the social system of Gunnison’s prairie dog (Cynomys gunnisoni). Can J Zool 71:1186−1192 Vázquez RI, Rodríguez J, Abitia LA, Galván F (2008) Food habits of the yellow snapper Lutjanus argentiventris (Peters, 1869) (Percoidei: Lutjanidae) in La Paz Bay, Mexico. Rev Bio Mar Oceanogr 43:295−302 Zeller DC (1998) Spawning aggregations: patterns of movement of the coral trout Plectropomus leopardus (Serranidae) as determined by ultrasonic telemetry. Mar Ecol Prog Ser 162:253−263 Submitted: July 31, 2013; Accepted: January 3, 2014 Proofs received from author(s): March 13, 2014