Marine Environmental Research 94 (2014) 38e47
Contents lists available at ScienceDirect
Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev
Diel and seasonal movement pattern of the dusky grouper Epinephelus marginatus inside a marine reserve Barbara Koeck a, b, *, Jérémy Pastor a, b, Gilles Saragoni b, a, Nicolas Dalias c, Jérôme Payrot d, Philippe Lenfant a, b a
Univ. Perpignan Via Domitia, CEntre de Formation et de Recherche sur les Environnements Méditerranéens, UMR 5110, 58 Avenue Paul Alduy, F-66860 Perpignan, France CNRS, CEntre de Formation et de Recherche sur les Environnements Méditerranéens, UMR 5110, 58 Avenue Paul Alduy, F-66860 Perpignan, France c SEANEO, 7 rue de Turenne, F-66000 Perpignan, France d Réserve Naturelle Marine de Cerbère-Banyuls, Conseil Général des Pyrénées-Orientales, 5 rue Roger David, F-66650 Banyuls-sur-Mer, France b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 13 October 2013 Received in revised form 6 December 2013 Accepted 7 December 2013
Temporal movement patterns and spawning behaviour of the dusky grouper Epinephelus marginatus were investigated using depth and temperature sensors combined to acoustic telemetry. Results showed that these fish are year-round resident, remaining inside the fully protected area of the marine reserve of Cerbère-Banyuls (65 ha) and display a diurnal activity pattern. Records from depth sensors revealed that groupers range inside small, distinct, and individual territories. Individual variations in habitat depth are only visible on a seasonal scale, i.e., between the spawning season and the rest of the year. In fact, during summer months when the seawater temperature exceeded 20 C, tagged groupers made vertical spawning migrations of 4e8 m in amplitude. These vertical migrations are characteristic of the reproductive behaviour of dusky groupers, during which they release their gametes. The results are notable for the implementation of management rules in marine protected areas, such as reduced navigation speed, boating or attendance during spawning season. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Acoustic telemetry Behaviour Fish Gulf of Lion Mediterranean Sea Pressure sensors Spawning behaviour Temporal variability Vertical migrations
1. Introduction The dusky grouper Epinephelus marginatus (Lowe 1834), is a coastal species that has a relatively large geographical distribution. The species occurs on both sides of the Atlantic Ocean, ranging from the British Isles to South Africa, from Brazil to Argentina, and is also found in the Indian Ocean, along the coasts of Mozambique and Madagascar (Heemstra and Randall, 1993; Irigoyen et al., 2005; Rico and Acha, 2003). The dusky grouper was added to the IUCN Red List as an endangered species in 1996 (Baillie and Groombridge, 1996), and remains on this list today (Cornish and Harmelin-Vivien, 2004). The dusky grouper is a highly appreciated target species for
* Corresponding author. Present address: Stella Mare ‘Sustainable TEchnologies for LittoraL Aquaculture and MArine REsearch’, UMS CNRS 3514, Lieu-dit “U CASONE”, F-20620 Biguglia, Corsica, France. E-mail addresses: [email protected], [email protected] (B. Koeck), [email protected] (J. Pastor), [email protected] (G. Saragoni), [email protected] (N. Dalias), [email protected] (J. Payrot), [email protected] (P. Lenfant). 0141-1136/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marenvres.2013.12.002
recreational and professional fishing across its global geographical range (Cornish and Harmelin-Vivien, 2004). This species is a protogynous hermaphrodite fish with a slow growth rate (Bouchereau et al., 1999; Reñones et al., 2007) that reaches sexual maturity at nearly 6 years for females (TL at 50% maturity ¼ 49 cm) and at more than 15 years for males (TL50% ¼ 80 cm; Reñones et al., 2010). Due to important size selectivity, artisanal fisheries particularly affect the sustainability of protogynous species such as the dusky grouper by disrupting the sex distribution of the targeted populations (Lloret et al., 2012). Around the Balearic Islands, Coll et al. (2004) highlighted a general depletion of dusky grouper since 1988 due to fishing. Different conservation actions have been launched to respond to the threat of depleting dusky groupers populations and allow their recovery. For example, the dusky grouper is considered to be a flagship species in the western Mediterranean (Maggio et al., 2006; Schunter et al., 2011), which has led to important protection actions. Flagship species are mostly “charismatic” species that are used to garner public support for more general conservation or protection actions and may act as surrogates for habitat protection
B. Koeck et al. / Marine Environmental Research 94 (2014) 38e47
(Zacharias and Roff, 2001). Spear fishing was reported as one cause of the depletion of dusky grouper populations in the western Mediterranean (Coll et al., 2004). In France, a moratorium on the spear fishing of this species was thus implemented in 1993, and several Marine Protected Areas (MPAs) were defined across the western Mediterranean basin to protect the habitat of the dusky grouper (Cornish and Harmelin-Vivien, 2004). The ecology of the dusky grouper has been widely investigated due to its endangered species status, most notably within MPAs. Several studies have reported important recoveries of dusky grouper populations, particularly in MPAs (Bodilis et al., 2003; La Mesa and Vacchi, 1999). A recovery of dusky grouper population has also been highlighted inside the MPA of Cerbère-Banyuls, with fish abundance increasing from 7 to 193 individuals after 17 years of protection (Lenfant et al., 2003). Results from underwater visual censuses and fish catch monitoring suggest that the dusky grouper responds particularly well to the protective effect of small coastal MPAs (Garcia-Charton et al., 2008; Macpherson et al., 2002; OjedaMartinez et al., 2007; Reñones et al., 1999). However, some uncertainties remain on this species’ spatiotemporal habitat utilization and movement patterns, which could allow for its more efficient conservation. Acoustic telemetry is a method that allows the continuous monitoring of fish movements in many different environments (Heupel et al., 2006). Acoustic monitoring experiments on the dusky grouper have primarily been conducted in the Mediterranean sea, along the French coast (Pastor et al., 2009), on the Italian island of Ustica (Lembo et al., 1999a, b; Lembo et al., 2002; Okland et al., 1999; Spedicato et al., 2003) and on the Azores (Afonso et al., 2011). Those studies focused mainly on the evaluation of homing abilities and the extent of the home range in relationship to MPA sizes, but they generally did not
39
evaluate temporal movement patterns, including on diel and seasonal scales. The main aim of this study was thus to investigate the habitat use and particularly the temporal activity patterns of the dusky grouper on both, the diel and seasonal scales, using an acoustic telemetry technique combined with pressure and temperature sensors. The analysis of seasonal patterns was particularly intended to highlight the spawning pattern of this species. The additional temperature and pressure sensors included inside each acoustic transmitter were meant to characterize the environment of tagged individuals and to correlate the readings obtained by the sensors to the individual detection patterns to improve our understanding of the habitat and movement patterns of the dusky grouper. 2. Materials and methods 2.1. Study location This acoustic monitoring study focused on dusky groupers inhabiting the MPA of Cerbère-Banyuls, which is located in the Mediterranean sea along the rocky FrencheCatalan coast, close to the Spanish border (42 280 N, 03100 E; Fig. 1). This MPA was created in 1974 and consists of 650 ha, split into two areas with different levels of protection (Lenfant et al., 2003): a fully protected core area and a partially protected surrounding area (Fig. 1). In the 65 ha core area, only swimming and navigation at a reduced speed of 8 nautical miles per hour are allowed. In the partially protected area, recreational angling and professional fishing is restricted but allowed, as opposed to spear-fishing, which is forbidden. Snorkelling and diving is also allowed in this area. This MPA covers the coastal fringe down to a depth of 55 m. The most coastal part
Fig. 1. General study location, capture locations of dusky groupers (fish symbol) and acoustic receiver array (black dots with grey halo symbolizing the detection range) inside the marine reserve of Banyuls-Cerbère, France. The marine reserve is delineated by the black lines, and the grey shaded area represents the fully protected core-area of the reserve. White fish correspond to detected groupers, and black fish correspond to those that were never detected by the fixed acoustic receiver array. Grey dots without a halo correspond to lost receivers from which data could not be recovered.
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B. Koeck et al. / Marine Environmental Research 94 (2014) 38e47
consists essentially of rocky bottoms, but it also includes Posidonia oceanic meadows and coraligenous sea beds that range from 17 to 45 m in depth (Lenfant et al., 2003). 2.2. Fish capture and tagging In contrast to other studies in which dusky groupers were captured by angling (Spedicato et al., 2003) or using traps (Afonso et al., 2011), we captured the fish by scuba diving, using clove oil and small nets to keep the whole tagging procedure as short and non-invasive as possible. Dusky groupers hidden inside rocky crevices were anaesthetized with the clove oil (0.2 ml of 30% clove oil solution per litre of seawater) inside their refuge and were slowly brought to the surface to avoid swim bladder over-inflation. After tagging, the groupers were brought back to their capture refuge. Divers ventilated fish during this time to enhance their recovery from the anaesthesia and monitored the fish until they fully recovered. The entire tagging procedure took between 10 and 15 min. The tagging procedure was conducted with respect to the French regulations for the treatment and welfare of experimental animals. Tagging was performed under anaesthesia, and all efforts were made to minimize suffering. Tagging was performed onboard the ship, where each fish was placed ventral side up in a small tank filled with a 30% diluted clove oil solution (0.2 ml L1). The fish were measured, and acoustic transmitters (VEMCO, Canada, Halifax) were implanted in their intra-coelomic cavity after they reached deep anaesthesia (stage III; Murray, 2002) A 15-mm incision was made with a sharp scalpel, parallel to the ventral midline along the linea alba (Murray, 2002), between the anus and pelvic fins. The acoustic transmitter was smeared with an antiseptic solution prior insertion into the coelomic cavity, and the incision was sutured with a surgical needle by two separate stitches tied with surgeons’ knots (Wagner et al., 2000). The needle used was a nonabsorbable polyamide monofilament mounted by a straight reverse cutting needle (Wagner et al., 2011). Coded acoustic transmitters with a nominal signal delay of 45 s, equipped with temperature (T) and pressure sensors (P) were used (V13TP-1L: output power of 150 dB, 12 g in air, 13 mm 45 mm, expected battery life of 623 days, signal frequency of 69 kHz). The temperature and depth sensors had accuracies of 0.5 C and 2.5 m, respectively, and resolutions of 0.12 C and 0.22 m. Groupers were also externally tagged to be identifiable and returned in case of recapture by fishermen. Coloured T-bar anchor tags (FD-94, Floytag, Seattle, WA, USA), inserted between the dorsal fin pterygiophores, were used as external tags. Furthermore, according to Okland et al. (1999), intra-coelomic tagging is the most suitable method for acoustic tagging and has no adverse long-term effects on the behaviour and survival of dusky groupers, under the condition that a low tag-to-body-weight ratio (TBWR) was respected (TBWR: 0.3e 0.6%). In our study, the tag weight was always far below both, the recommended 2% TBWR mentioned in the literature (Winter, 1983, 1996) and the TBWR mentioned in Okland et al. (1999), with values ranging between 0.09 and 0.38%. Overall, seven dusky groupers were equipped with acoustic transmitters, ranging between 55 and 95 cm (69.43 15.01 cm) and all corresponding to mature adults (Reñones et al., 2010). Four of them were caught and released inside the fully protected corearea of the MPA in autumn 2007, while three others were caught and released in the northern part of the partially protected MPA in summer 2008 (Fig. 1). 2.3. Long-term passive acoustic monitoring An array of 14 VR2 and VR2W acoustic receivers (VEMCO) was deployed for the long-term continuous monitoring of the
movements of dusky groupers inside the MPA of Cerbère-Banyuls between September 2007 and October 2008. The receivers were moored in PVC-pipes that had been vertically sunk into a concretefilled tyre and had to be brought onboard for data retrieval. Six receivers were deployed inside the fully protected core-area of the MPA, and eight were deployed inside the northern part of the partially protected area (Fig. 1). Three receivers disappeared from the acoustic array and were never found, even after repeated extensive searches in the surrounding areas of their deployment locations. During the monitoring period, the study location experienced three important storms, with wave heights up to 14 m (14e 19 December 2007, 2e5 January 2008 and 25e27 December 2008), which could have caused this loss (CANDHIS, http://candhis.cetmef. developpement-durable.gouv.fr/publications/06601/astx_06601_ 2.pdf). For each detection, the receiver registered the date, time and unique ID of the transmission, as well as temperature and pressure values. Receivers were deployed to cover the suitable habitats of the dusky groupers, i.e., the rocky areas and coraligenous sea beds to a depth of 40 m. A detection range trial using four transmitters with the same characteristics as those used for the fish tagging was performed before the acoustic tagging experiment. The detection distance of the receivers was approximately 200 m (Appendix 1). 2.4. Data analysis The raw detection data were compiled to produce hourly detection frequencies for each fish. Isolated hourly detections, with no more consecutive detection during the following 24 h, were considered false detections and removed from analyses. A residence index (RI) was calculated for each fish, which accounted for the time that a tagged fish spent inside the MPA. The RI corresponded to the ratio between the detection period (i.e. period between first and last detection) and the number of days detected, calculated for the whole detection array. RIs were calculated on both daily and hourly bases. The diel and seasonal patterns of dusky grouper detection and swimming depth were first described through the visual inspection of mean diel hourly detection plots and chronogram plots. The depth plots of individual dusky groupers were compared to plots of seawater temperatures that had been recorded by the fish sensors and to plots of temperatures recorded at a fixed location inside the MPA at a depth of 5 m. A continuous wavelet transformation (CWT) method was used to test diel periodicity of detection patterns for each fish. CWT analysis is an alternative method to the Fast Fourier Transform (FFT) or other time-frequency decomposition methods and is used to test periodicities over different time scales (Gaucherel, 2011). CWT analysis has been previously used to test the periodicity of acoustic monitoring data of fish (Alós et al., 2012a, 2012b, 2011; March et al., 2010). This analysis used twodimensional wavelet spectra and point-wise tests at a significance level of 95% to detect an eventual diel periodicity in the detection pattern of each transmitter. The effect of diel-phase and season on the detection frequencies and swimming depths of groupers was formally tested with the use of generalized linear mixed models (GLMMs). GLMMs represent a suitable technique for analysing non-normal data with random effects (Zuur et al., 2009). In our case, detection data were nonnormally distributed, even after transformation efforts, and included repeated measures (detections, depth) of individuals and days. Days and individuals were thus considered to be random factors. The diel phase, split into the day and night phases, and the season, split into the spawning and non-spawning seasons, were both treated as fixed categorical factors. According to the literature, in the western Mediterranean, the spawning season of the dusky grouper was defined during the summer months, i.e., between the
B. Koeck et al. / Marine Environmental Research 94 (2014) 38e47
end of June and the beginning of September (Hereu et al., 2006; Reñones et al., 2010). We refined this period to July and August, based on visual inspections of the temperature and depth data recorded by tagged groupers. For the analysis of hourly detections, the GLMM was computed using a Poisson distribution with a logarithmic link, and the GLMM parameters were estimated using a Laplacian approximation (Zuur et al., 2009). The GLMM of the swimming depth of groupers was computed using a Gaussian distribution with an identity link (Zuur et al., 2009), after a boxecox transformation. For the swimming depth, the p-values were computed using Markov Chain Monte Carlo (MCMC) sampling. In both models, the normality of residuals and the model performance were visually examined using residual distributions and quantilee quantile plots of residuals against fitted values. Mean values are always presented with standard deviation and date/time data expressed in the UTC time zone (i.e., Universal Time Coordinated). Seawater temperatures of the study location at a depth of 5 m were collected by the natural marine reserve from Banyuls-Cerbère and the T-MedNet temperature observation network (http://www. t-mednet.org). Detections were categorized into day and night phases, according to sunset and sunrise data from the US Naval Observatory (http://www.usno.navy.mil/USNO/astronomicalapplications/data-services). CWT analyses were performed using the ‘SOWAS’-package (Maraun et al., 2007), and GLMMs were computed using the ‘lme4’ package for the R statistical environment (R Core Team, 2013).
3. Results 3.1. Detection patterns The four individuals tagged in the core-area of the MPA were detected throughout the monitoring period, which lasted nearly 13 months, with a mean individual detection period of 387.25 2.75 days, corresponding to 7550 1505 monitored hours per fish (Table 1). The daily residence indexes for these groupers were nearly 100%, with detection days mostly equal to detection periods (Table 1). The RIs measured on an hourly basis were also relatively high, with groupers being detected in 79 14.5% of the hours during the 13 monitored months (Table 1). The groupers were detected by a small number of receivers, including one receiver that accounted for 99.5 0.44% of the detected days (Table 1). In contrast, the three individuals tagged in the partially protected area of the MPA were never detected by the fixed receivers after release. The absence of data for this second batch of groupers is doubtlessly due to the loss of receivers near the groupers’ capture and release location, which would have covered their home-range areas. We can exclude the mortality of fish, transmitter failure and the fact that they could have left the monitored MPA because all three fish were observed several times over the study period near the groupers’ initial capture location, using an on-boat active monitoring acoustic receiver (VR100, VEMCO). Further analyses thus solely
41
concerned the remaining four groupers captured in the core-area of the MPA. For all individuals, the mean diel detection plots for the entire monitoring period showed higher detections during the day than at night (Fig. 2). These observations were only partly supported by the individual continuous wavelet spectrums, which did not show a significant 24-h periodicity over the entire study period (Fig. 3) but did show intermittent 24-h periodicities at different times of the year (Fig. 4). This diel detection pattern was maintained even during storm events in December 2007 and January 2008 (Fig. 4b, fish G2). However, the results of the GLMM analysis showed that the hourly detections of groupers vary significantly with daytime and season, as shown by the significant interaction term of this model (Table 2). Detections were highest during the day in the nonspawning season (7.46 11.17 detections h1) and lowest at night during the spawning season (2.34 4.09 detections h1) (Table 2, Appendix 2). Mean detections during the night in the nonspawning season were of 6.46 0.08 detections h1 and of 4.08 0.11 detections h1 during the day in the spawning season. 3.2. Swimming depth profiles and temperature The additional temperature and pressure sensors included inside each transmitter permitted the characterization of the environment of each tagged individual. Because all four individuals inhabited the same area, their habitat was characterized by similar mean diel temperatures, which were higher during the day than at night (Fig. 5a). In contrast, the mean swimming depth of the dusky grouper seemed to be relatively constant during the day but exhibited distinct habitat depths for each fish (Fig. 5b). The habitat of fish G4 was characterized by a mean depth of 21.04 3.13 m, that of G1 was 19.66 2.67 m and that of G3 was 15.42 2.13 m. The depth sensor of fish G2 was defective and was subsequently removed from the analysis. Individual chronogram plots of temperature and depth data highlighted inversed synchronized seasonal variations between summer and the rest of the year (Fig. 6). When the water temperature reached its maximum in JulyeAugust, the swimming depth of groupers decreased markedly. A close examination of the chronogram-plots during these summer months showed that these decreases in depth corresponded to several successive drops in depth, which varied from 4 to 8 m in amplitude (Fig. 7). These depth drops seem to be relatively synchronized in time between individuals and to occur during low temperature decreases (Fig. 7). Aside from July and August, the depth profiles remained relatively constant over time, except for fish G1, which showed some depth variation (Fig. 6, Appendix 3). The formal testing of the depth pattern showed significant differences between the spawning and non-spawning seasons, but not between diel-phases or for the interaction of season and diel-phase (Table 3). Depth was significantly lower during the spawning season, with a mean depth of 14.94 3.23 m (for fish G1, G3 and G4), than during the rest of the year, with a mean depth of 19.57 3.07 m (Fig. 6, Table 3, Appendix 4).
Table 1 General information on the detection patterns of tagged groupers. (DD: detected days, DP: detection period, RI: residence index, F: female, M: male). Fish ID
Capture date
Detecting receivers
Hourly detections
Total detections
DD (days)
DP (days)
Daily RI (%)
Hourly RI (%)
Total length (cm)
Sex
G1 G2 G3 G4 G5 G6 G7
17/09/2007 20/09/2007 21/09/2007 24/09/2007 08/10/2007 30/06/2008 28/08/2008
4 5 4 5 / / /
10,083 6137 7096 6884 / / /
100,811 40,708 41,068 50,194 / / /
390 388 386 383 / / /
390 389 386 384 / / /
100 99.74 100 99.74 / / /
100 65.93 77 75.10 / / /
55 95 55 65 86 72 58
F M F F M F F
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B. Koeck et al. / Marine Environmental Research 94 (2014) 38e47
the already existing telemetry studies on dusky grouper brought undoubtedly important information about the spatial ecology of this species into light, but they remained descriptive about the temporal movement patterns (Afonso et al., 2011; Lembo et al., 1999b, 2002; Pastor et al., 2009). The use of depth and temperature sensors has produced additional information on their diel and seasonal movement patterns, which constitutes a necessary complement to the earlier telemetry experiment conducted on the dusky grouper inside the MPA of Cerbère-Banyuls (Pastor et al., 2009).
4.1. Residency and territoriality
Fig. 2. Mean diel hourly detections of the four dusky groupers tagged inside the corearea of the MPA (G1 to G4). Error bars correspond to standard error. Vertical grey lines symbolize the mean sunset and sunrise over the entire study period.
4. Discussion Our findings confirm and complement the substantial existing body of scientific studies examining the dusky grouper. In general,
High hourly RI and low number of detecting receivers confirm that dusky grouper is year-round a highly resident species, displaying a strong site fidelity to its habitat. Furthermore, even if the fixed acoustic receiver array did not permit the calculation of the fish home-ranges, their depth profiles and the fact that individuals were mostly detected by one receiver supports the idea that dusky grouper have small spatio-temporally distinct territories. Pastor et al. (2009) estimated the home-range of dusky groupers from the Cerbère-Banyuls MPA outside the reproductive period to have an area of 0.0134 0.0036 km2 (95% KUD, Kernel Utilization Distribution: area representing 95% of fish detections). The high site attachment of dusky grouper to a well-defined territory would
Fig. 3. Wavelet sample spectrums of the four detected groupers (G1 to G4) for the overall detection period (13 months). It represents the time-frequency distribution over time (date dd/mm). Detection data from each fish were tested for periodicities ranging from 2 to 64 days. Dashed line represents the 24-h periodicity threshold. Continuous lines represent the cone of influence, above which data should not be interpreted. The thick contours represent the 95% confidence level and significant periodicities.
B. Koeck et al. / Marine Environmental Research 94 (2014) 38e47
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Fig. 4. Wavelet sample spectrums of the four detected groupers (G1 to G4) over a randomly selected one-month period. It represents the time-frequency distribution over time (date dd/mm). Detection data from each fish were tested for periodicities ranging from 2 to 64 days. Dashed line represents the 24-h periodicity threshold. Continuous lines represent the cone of influence, above which data should not be interpreted. The thick contours represent the 95% confidence level and significant periodicities.
explain the homing behaviour of this species that has been documented in several studies (Lembo et al., 1999a,b; Spedicato et al., 2003). However, previous acoustic tagging experiments that estimated the home-ranges of dusky groupers reported overlapping territories (Lembo et al., 2002; Pastor et al., 2009). These different results may be due to the accuracy of position estimation for tagged fish and to the use of only the spatial variability, not the temporal variability, of home-ranges. 4.2. Diel movement pattern The investigation of acoustic detections is an indirect way of measuring the movement patterns of animals, though it is Table 2 Results for a Generalized Linear Mixed Model (GLMM) test of the effect of diel phase (DN: day vs. night) and season (spawning vs. non-spawning) on grouper detections.
Intercept DN (night) Season (spawning) DN (night) season (spawn.)
Estimate
Std. Error
z value
Pr(>jzj)
1.78695 0.3349 0.5018 0.4781
0.18906 0.00444 0.08465 0.01609
9.45 75.44 5.93 29.72
Contents lists available at ScienceDirect
Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev
Diel and seasonal movement pattern of the dusky grouper Epinephelus marginatus inside a marine reserve Barbara Koeck a, b, *, Jérémy Pastor a, b, Gilles Saragoni b, a, Nicolas Dalias c, Jérôme Payrot d, Philippe Lenfant a, b a
Univ. Perpignan Via Domitia, CEntre de Formation et de Recherche sur les Environnements Méditerranéens, UMR 5110, 58 Avenue Paul Alduy, F-66860 Perpignan, France CNRS, CEntre de Formation et de Recherche sur les Environnements Méditerranéens, UMR 5110, 58 Avenue Paul Alduy, F-66860 Perpignan, France c SEANEO, 7 rue de Turenne, F-66000 Perpignan, France d Réserve Naturelle Marine de Cerbère-Banyuls, Conseil Général des Pyrénées-Orientales, 5 rue Roger David, F-66650 Banyuls-sur-Mer, France b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 13 October 2013 Received in revised form 6 December 2013 Accepted 7 December 2013
Temporal movement patterns and spawning behaviour of the dusky grouper Epinephelus marginatus were investigated using depth and temperature sensors combined to acoustic telemetry. Results showed that these fish are year-round resident, remaining inside the fully protected area of the marine reserve of Cerbère-Banyuls (65 ha) and display a diurnal activity pattern. Records from depth sensors revealed that groupers range inside small, distinct, and individual territories. Individual variations in habitat depth are only visible on a seasonal scale, i.e., between the spawning season and the rest of the year. In fact, during summer months when the seawater temperature exceeded 20 C, tagged groupers made vertical spawning migrations of 4e8 m in amplitude. These vertical migrations are characteristic of the reproductive behaviour of dusky groupers, during which they release their gametes. The results are notable for the implementation of management rules in marine protected areas, such as reduced navigation speed, boating or attendance during spawning season. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Acoustic telemetry Behaviour Fish Gulf of Lion Mediterranean Sea Pressure sensors Spawning behaviour Temporal variability Vertical migrations
1. Introduction The dusky grouper Epinephelus marginatus (Lowe 1834), is a coastal species that has a relatively large geographical distribution. The species occurs on both sides of the Atlantic Ocean, ranging from the British Isles to South Africa, from Brazil to Argentina, and is also found in the Indian Ocean, along the coasts of Mozambique and Madagascar (Heemstra and Randall, 1993; Irigoyen et al., 2005; Rico and Acha, 2003). The dusky grouper was added to the IUCN Red List as an endangered species in 1996 (Baillie and Groombridge, 1996), and remains on this list today (Cornish and Harmelin-Vivien, 2004). The dusky grouper is a highly appreciated target species for
* Corresponding author. Present address: Stella Mare ‘Sustainable TEchnologies for LittoraL Aquaculture and MArine REsearch’, UMS CNRS 3514, Lieu-dit “U CASONE”, F-20620 Biguglia, Corsica, France. E-mail addresses: [email protected], [email protected] (B. Koeck), [email protected] (J. Pastor), [email protected] (G. Saragoni), [email protected] (N. Dalias), [email protected] (J. Payrot), [email protected] (P. Lenfant). 0141-1136/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marenvres.2013.12.002
recreational and professional fishing across its global geographical range (Cornish and Harmelin-Vivien, 2004). This species is a protogynous hermaphrodite fish with a slow growth rate (Bouchereau et al., 1999; Reñones et al., 2007) that reaches sexual maturity at nearly 6 years for females (TL at 50% maturity ¼ 49 cm) and at more than 15 years for males (TL50% ¼ 80 cm; Reñones et al., 2010). Due to important size selectivity, artisanal fisheries particularly affect the sustainability of protogynous species such as the dusky grouper by disrupting the sex distribution of the targeted populations (Lloret et al., 2012). Around the Balearic Islands, Coll et al. (2004) highlighted a general depletion of dusky grouper since 1988 due to fishing. Different conservation actions have been launched to respond to the threat of depleting dusky groupers populations and allow their recovery. For example, the dusky grouper is considered to be a flagship species in the western Mediterranean (Maggio et al., 2006; Schunter et al., 2011), which has led to important protection actions. Flagship species are mostly “charismatic” species that are used to garner public support for more general conservation or protection actions and may act as surrogates for habitat protection
B. Koeck et al. / Marine Environmental Research 94 (2014) 38e47
(Zacharias and Roff, 2001). Spear fishing was reported as one cause of the depletion of dusky grouper populations in the western Mediterranean (Coll et al., 2004). In France, a moratorium on the spear fishing of this species was thus implemented in 1993, and several Marine Protected Areas (MPAs) were defined across the western Mediterranean basin to protect the habitat of the dusky grouper (Cornish and Harmelin-Vivien, 2004). The ecology of the dusky grouper has been widely investigated due to its endangered species status, most notably within MPAs. Several studies have reported important recoveries of dusky grouper populations, particularly in MPAs (Bodilis et al., 2003; La Mesa and Vacchi, 1999). A recovery of dusky grouper population has also been highlighted inside the MPA of Cerbère-Banyuls, with fish abundance increasing from 7 to 193 individuals after 17 years of protection (Lenfant et al., 2003). Results from underwater visual censuses and fish catch monitoring suggest that the dusky grouper responds particularly well to the protective effect of small coastal MPAs (Garcia-Charton et al., 2008; Macpherson et al., 2002; OjedaMartinez et al., 2007; Reñones et al., 1999). However, some uncertainties remain on this species’ spatiotemporal habitat utilization and movement patterns, which could allow for its more efficient conservation. Acoustic telemetry is a method that allows the continuous monitoring of fish movements in many different environments (Heupel et al., 2006). Acoustic monitoring experiments on the dusky grouper have primarily been conducted in the Mediterranean sea, along the French coast (Pastor et al., 2009), on the Italian island of Ustica (Lembo et al., 1999a, b; Lembo et al., 2002; Okland et al., 1999; Spedicato et al., 2003) and on the Azores (Afonso et al., 2011). Those studies focused mainly on the evaluation of homing abilities and the extent of the home range in relationship to MPA sizes, but they generally did not
39
evaluate temporal movement patterns, including on diel and seasonal scales. The main aim of this study was thus to investigate the habitat use and particularly the temporal activity patterns of the dusky grouper on both, the diel and seasonal scales, using an acoustic telemetry technique combined with pressure and temperature sensors. The analysis of seasonal patterns was particularly intended to highlight the spawning pattern of this species. The additional temperature and pressure sensors included inside each acoustic transmitter were meant to characterize the environment of tagged individuals and to correlate the readings obtained by the sensors to the individual detection patterns to improve our understanding of the habitat and movement patterns of the dusky grouper. 2. Materials and methods 2.1. Study location This acoustic monitoring study focused on dusky groupers inhabiting the MPA of Cerbère-Banyuls, which is located in the Mediterranean sea along the rocky FrencheCatalan coast, close to the Spanish border (42 280 N, 03100 E; Fig. 1). This MPA was created in 1974 and consists of 650 ha, split into two areas with different levels of protection (Lenfant et al., 2003): a fully protected core area and a partially protected surrounding area (Fig. 1). In the 65 ha core area, only swimming and navigation at a reduced speed of 8 nautical miles per hour are allowed. In the partially protected area, recreational angling and professional fishing is restricted but allowed, as opposed to spear-fishing, which is forbidden. Snorkelling and diving is also allowed in this area. This MPA covers the coastal fringe down to a depth of 55 m. The most coastal part
Fig. 1. General study location, capture locations of dusky groupers (fish symbol) and acoustic receiver array (black dots with grey halo symbolizing the detection range) inside the marine reserve of Banyuls-Cerbère, France. The marine reserve is delineated by the black lines, and the grey shaded area represents the fully protected core-area of the reserve. White fish correspond to detected groupers, and black fish correspond to those that were never detected by the fixed acoustic receiver array. Grey dots without a halo correspond to lost receivers from which data could not be recovered.
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consists essentially of rocky bottoms, but it also includes Posidonia oceanic meadows and coraligenous sea beds that range from 17 to 45 m in depth (Lenfant et al., 2003). 2.2. Fish capture and tagging In contrast to other studies in which dusky groupers were captured by angling (Spedicato et al., 2003) or using traps (Afonso et al., 2011), we captured the fish by scuba diving, using clove oil and small nets to keep the whole tagging procedure as short and non-invasive as possible. Dusky groupers hidden inside rocky crevices were anaesthetized with the clove oil (0.2 ml of 30% clove oil solution per litre of seawater) inside their refuge and were slowly brought to the surface to avoid swim bladder over-inflation. After tagging, the groupers were brought back to their capture refuge. Divers ventilated fish during this time to enhance their recovery from the anaesthesia and monitored the fish until they fully recovered. The entire tagging procedure took between 10 and 15 min. The tagging procedure was conducted with respect to the French regulations for the treatment and welfare of experimental animals. Tagging was performed under anaesthesia, and all efforts were made to minimize suffering. Tagging was performed onboard the ship, where each fish was placed ventral side up in a small tank filled with a 30% diluted clove oil solution (0.2 ml L1). The fish were measured, and acoustic transmitters (VEMCO, Canada, Halifax) were implanted in their intra-coelomic cavity after they reached deep anaesthesia (stage III; Murray, 2002) A 15-mm incision was made with a sharp scalpel, parallel to the ventral midline along the linea alba (Murray, 2002), between the anus and pelvic fins. The acoustic transmitter was smeared with an antiseptic solution prior insertion into the coelomic cavity, and the incision was sutured with a surgical needle by two separate stitches tied with surgeons’ knots (Wagner et al., 2000). The needle used was a nonabsorbable polyamide monofilament mounted by a straight reverse cutting needle (Wagner et al., 2011). Coded acoustic transmitters with a nominal signal delay of 45 s, equipped with temperature (T) and pressure sensors (P) were used (V13TP-1L: output power of 150 dB, 12 g in air, 13 mm 45 mm, expected battery life of 623 days, signal frequency of 69 kHz). The temperature and depth sensors had accuracies of 0.5 C and 2.5 m, respectively, and resolutions of 0.12 C and 0.22 m. Groupers were also externally tagged to be identifiable and returned in case of recapture by fishermen. Coloured T-bar anchor tags (FD-94, Floytag, Seattle, WA, USA), inserted between the dorsal fin pterygiophores, were used as external tags. Furthermore, according to Okland et al. (1999), intra-coelomic tagging is the most suitable method for acoustic tagging and has no adverse long-term effects on the behaviour and survival of dusky groupers, under the condition that a low tag-to-body-weight ratio (TBWR) was respected (TBWR: 0.3e 0.6%). In our study, the tag weight was always far below both, the recommended 2% TBWR mentioned in the literature (Winter, 1983, 1996) and the TBWR mentioned in Okland et al. (1999), with values ranging between 0.09 and 0.38%. Overall, seven dusky groupers were equipped with acoustic transmitters, ranging between 55 and 95 cm (69.43 15.01 cm) and all corresponding to mature adults (Reñones et al., 2010). Four of them were caught and released inside the fully protected corearea of the MPA in autumn 2007, while three others were caught and released in the northern part of the partially protected MPA in summer 2008 (Fig. 1). 2.3. Long-term passive acoustic monitoring An array of 14 VR2 and VR2W acoustic receivers (VEMCO) was deployed for the long-term continuous monitoring of the
movements of dusky groupers inside the MPA of Cerbère-Banyuls between September 2007 and October 2008. The receivers were moored in PVC-pipes that had been vertically sunk into a concretefilled tyre and had to be brought onboard for data retrieval. Six receivers were deployed inside the fully protected core-area of the MPA, and eight were deployed inside the northern part of the partially protected area (Fig. 1). Three receivers disappeared from the acoustic array and were never found, even after repeated extensive searches in the surrounding areas of their deployment locations. During the monitoring period, the study location experienced three important storms, with wave heights up to 14 m (14e 19 December 2007, 2e5 January 2008 and 25e27 December 2008), which could have caused this loss (CANDHIS, http://candhis.cetmef. developpement-durable.gouv.fr/publications/06601/astx_06601_ 2.pdf). For each detection, the receiver registered the date, time and unique ID of the transmission, as well as temperature and pressure values. Receivers were deployed to cover the suitable habitats of the dusky groupers, i.e., the rocky areas and coraligenous sea beds to a depth of 40 m. A detection range trial using four transmitters with the same characteristics as those used for the fish tagging was performed before the acoustic tagging experiment. The detection distance of the receivers was approximately 200 m (Appendix 1). 2.4. Data analysis The raw detection data were compiled to produce hourly detection frequencies for each fish. Isolated hourly detections, with no more consecutive detection during the following 24 h, were considered false detections and removed from analyses. A residence index (RI) was calculated for each fish, which accounted for the time that a tagged fish spent inside the MPA. The RI corresponded to the ratio between the detection period (i.e. period between first and last detection) and the number of days detected, calculated for the whole detection array. RIs were calculated on both daily and hourly bases. The diel and seasonal patterns of dusky grouper detection and swimming depth were first described through the visual inspection of mean diel hourly detection plots and chronogram plots. The depth plots of individual dusky groupers were compared to plots of seawater temperatures that had been recorded by the fish sensors and to plots of temperatures recorded at a fixed location inside the MPA at a depth of 5 m. A continuous wavelet transformation (CWT) method was used to test diel periodicity of detection patterns for each fish. CWT analysis is an alternative method to the Fast Fourier Transform (FFT) or other time-frequency decomposition methods and is used to test periodicities over different time scales (Gaucherel, 2011). CWT analysis has been previously used to test the periodicity of acoustic monitoring data of fish (Alós et al., 2012a, 2012b, 2011; March et al., 2010). This analysis used twodimensional wavelet spectra and point-wise tests at a significance level of 95% to detect an eventual diel periodicity in the detection pattern of each transmitter. The effect of diel-phase and season on the detection frequencies and swimming depths of groupers was formally tested with the use of generalized linear mixed models (GLMMs). GLMMs represent a suitable technique for analysing non-normal data with random effects (Zuur et al., 2009). In our case, detection data were nonnormally distributed, even after transformation efforts, and included repeated measures (detections, depth) of individuals and days. Days and individuals were thus considered to be random factors. The diel phase, split into the day and night phases, and the season, split into the spawning and non-spawning seasons, were both treated as fixed categorical factors. According to the literature, in the western Mediterranean, the spawning season of the dusky grouper was defined during the summer months, i.e., between the
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end of June and the beginning of September (Hereu et al., 2006; Reñones et al., 2010). We refined this period to July and August, based on visual inspections of the temperature and depth data recorded by tagged groupers. For the analysis of hourly detections, the GLMM was computed using a Poisson distribution with a logarithmic link, and the GLMM parameters were estimated using a Laplacian approximation (Zuur et al., 2009). The GLMM of the swimming depth of groupers was computed using a Gaussian distribution with an identity link (Zuur et al., 2009), after a boxecox transformation. For the swimming depth, the p-values were computed using Markov Chain Monte Carlo (MCMC) sampling. In both models, the normality of residuals and the model performance were visually examined using residual distributions and quantilee quantile plots of residuals against fitted values. Mean values are always presented with standard deviation and date/time data expressed in the UTC time zone (i.e., Universal Time Coordinated). Seawater temperatures of the study location at a depth of 5 m were collected by the natural marine reserve from Banyuls-Cerbère and the T-MedNet temperature observation network (http://www. t-mednet.org). Detections were categorized into day and night phases, according to sunset and sunrise data from the US Naval Observatory (http://www.usno.navy.mil/USNO/astronomicalapplications/data-services). CWT analyses were performed using the ‘SOWAS’-package (Maraun et al., 2007), and GLMMs were computed using the ‘lme4’ package for the R statistical environment (R Core Team, 2013).
3. Results 3.1. Detection patterns The four individuals tagged in the core-area of the MPA were detected throughout the monitoring period, which lasted nearly 13 months, with a mean individual detection period of 387.25 2.75 days, corresponding to 7550 1505 monitored hours per fish (Table 1). The daily residence indexes for these groupers were nearly 100%, with detection days mostly equal to detection periods (Table 1). The RIs measured on an hourly basis were also relatively high, with groupers being detected in 79 14.5% of the hours during the 13 monitored months (Table 1). The groupers were detected by a small number of receivers, including one receiver that accounted for 99.5 0.44% of the detected days (Table 1). In contrast, the three individuals tagged in the partially protected area of the MPA were never detected by the fixed receivers after release. The absence of data for this second batch of groupers is doubtlessly due to the loss of receivers near the groupers’ capture and release location, which would have covered their home-range areas. We can exclude the mortality of fish, transmitter failure and the fact that they could have left the monitored MPA because all three fish were observed several times over the study period near the groupers’ initial capture location, using an on-boat active monitoring acoustic receiver (VR100, VEMCO). Further analyses thus solely
41
concerned the remaining four groupers captured in the core-area of the MPA. For all individuals, the mean diel detection plots for the entire monitoring period showed higher detections during the day than at night (Fig. 2). These observations were only partly supported by the individual continuous wavelet spectrums, which did not show a significant 24-h periodicity over the entire study period (Fig. 3) but did show intermittent 24-h periodicities at different times of the year (Fig. 4). This diel detection pattern was maintained even during storm events in December 2007 and January 2008 (Fig. 4b, fish G2). However, the results of the GLMM analysis showed that the hourly detections of groupers vary significantly with daytime and season, as shown by the significant interaction term of this model (Table 2). Detections were highest during the day in the nonspawning season (7.46 11.17 detections h1) and lowest at night during the spawning season (2.34 4.09 detections h1) (Table 2, Appendix 2). Mean detections during the night in the nonspawning season were of 6.46 0.08 detections h1 and of 4.08 0.11 detections h1 during the day in the spawning season. 3.2. Swimming depth profiles and temperature The additional temperature and pressure sensors included inside each transmitter permitted the characterization of the environment of each tagged individual. Because all four individuals inhabited the same area, their habitat was characterized by similar mean diel temperatures, which were higher during the day than at night (Fig. 5a). In contrast, the mean swimming depth of the dusky grouper seemed to be relatively constant during the day but exhibited distinct habitat depths for each fish (Fig. 5b). The habitat of fish G4 was characterized by a mean depth of 21.04 3.13 m, that of G1 was 19.66 2.67 m and that of G3 was 15.42 2.13 m. The depth sensor of fish G2 was defective and was subsequently removed from the analysis. Individual chronogram plots of temperature and depth data highlighted inversed synchronized seasonal variations between summer and the rest of the year (Fig. 6). When the water temperature reached its maximum in JulyeAugust, the swimming depth of groupers decreased markedly. A close examination of the chronogram-plots during these summer months showed that these decreases in depth corresponded to several successive drops in depth, which varied from 4 to 8 m in amplitude (Fig. 7). These depth drops seem to be relatively synchronized in time between individuals and to occur during low temperature decreases (Fig. 7). Aside from July and August, the depth profiles remained relatively constant over time, except for fish G1, which showed some depth variation (Fig. 6, Appendix 3). The formal testing of the depth pattern showed significant differences between the spawning and non-spawning seasons, but not between diel-phases or for the interaction of season and diel-phase (Table 3). Depth was significantly lower during the spawning season, with a mean depth of 14.94 3.23 m (for fish G1, G3 and G4), than during the rest of the year, with a mean depth of 19.57 3.07 m (Fig. 6, Table 3, Appendix 4).
Table 1 General information on the detection patterns of tagged groupers. (DD: detected days, DP: detection period, RI: residence index, F: female, M: male). Fish ID
Capture date
Detecting receivers
Hourly detections
Total detections
DD (days)
DP (days)
Daily RI (%)
Hourly RI (%)
Total length (cm)
Sex
G1 G2 G3 G4 G5 G6 G7
17/09/2007 20/09/2007 21/09/2007 24/09/2007 08/10/2007 30/06/2008 28/08/2008
4 5 4 5 / / /
10,083 6137 7096 6884 / / /
100,811 40,708 41,068 50,194 / / /
390 388 386 383 / / /
390 389 386 384 / / /
100 99.74 100 99.74 / / /
100 65.93 77 75.10 / / /
55 95 55 65 86 72 58
F M F F M F F
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the already existing telemetry studies on dusky grouper brought undoubtedly important information about the spatial ecology of this species into light, but they remained descriptive about the temporal movement patterns (Afonso et al., 2011; Lembo et al., 1999b, 2002; Pastor et al., 2009). The use of depth and temperature sensors has produced additional information on their diel and seasonal movement patterns, which constitutes a necessary complement to the earlier telemetry experiment conducted on the dusky grouper inside the MPA of Cerbère-Banyuls (Pastor et al., 2009).
4.1. Residency and territoriality
Fig. 2. Mean diel hourly detections of the four dusky groupers tagged inside the corearea of the MPA (G1 to G4). Error bars correspond to standard error. Vertical grey lines symbolize the mean sunset and sunrise over the entire study period.
4. Discussion Our findings confirm and complement the substantial existing body of scientific studies examining the dusky grouper. In general,
High hourly RI and low number of detecting receivers confirm that dusky grouper is year-round a highly resident species, displaying a strong site fidelity to its habitat. Furthermore, even if the fixed acoustic receiver array did not permit the calculation of the fish home-ranges, their depth profiles and the fact that individuals were mostly detected by one receiver supports the idea that dusky grouper have small spatio-temporally distinct territories. Pastor et al. (2009) estimated the home-range of dusky groupers from the Cerbère-Banyuls MPA outside the reproductive period to have an area of 0.0134 0.0036 km2 (95% KUD, Kernel Utilization Distribution: area representing 95% of fish detections). The high site attachment of dusky grouper to a well-defined territory would
Fig. 3. Wavelet sample spectrums of the four detected groupers (G1 to G4) for the overall detection period (13 months). It represents the time-frequency distribution over time (date dd/mm). Detection data from each fish were tested for periodicities ranging from 2 to 64 days. Dashed line represents the 24-h periodicity threshold. Continuous lines represent the cone of influence, above which data should not be interpreted. The thick contours represent the 95% confidence level and significant periodicities.
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Fig. 4. Wavelet sample spectrums of the four detected groupers (G1 to G4) over a randomly selected one-month period. It represents the time-frequency distribution over time (date dd/mm). Detection data from each fish were tested for periodicities ranging from 2 to 64 days. Dashed line represents the 24-h periodicity threshold. Continuous lines represent the cone of influence, above which data should not be interpreted. The thick contours represent the 95% confidence level and significant periodicities.
explain the homing behaviour of this species that has been documented in several studies (Lembo et al., 1999a,b; Spedicato et al., 2003). However, previous acoustic tagging experiments that estimated the home-ranges of dusky groupers reported overlapping territories (Lembo et al., 2002; Pastor et al., 2009). These different results may be due to the accuracy of position estimation for tagged fish and to the use of only the spatial variability, not the temporal variability, of home-ranges. 4.2. Diel movement pattern The investigation of acoustic detections is an indirect way of measuring the movement patterns of animals, though it is Table 2 Results for a Generalized Linear Mixed Model (GLMM) test of the effect of diel phase (DN: day vs. night) and season (spawning vs. non-spawning) on grouper detections.
Intercept DN (night) Season (spawning) DN (night) season (spawn.)
Estimate
Std. Error
z value
Pr(>jzj)
1.78695 0.3349 0.5018 0.4781
0.18906 0.00444 0.08465 0.01609
9.45 75.44 5.93 29.72
