Residency and migratory behaviour by adult Pomatomus saltatrix in a South African coastal embayment

Estuarine, Coastal and Shelf Science 89 (2010) 12e20

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Residency and migratory behaviour by adult Pomatomus saltatrix in a South African coastal embayment R.D. Hedger a, *, T.F. Næsje a, b, P.D. Cowley b, E.B. Thorstad a, C. Attwood c, F. Økland a, C.G. Wilke d, S. Kerwath c, d a

Norwegian Institute for Nature Research, NO-7485, Trondheim, Norway South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown, South Africa Marine Research Institute, Zoology Department, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa d Resources Research (Inshore), Marine and Coastal Management, Department of Environmental Affairs, Private Bag X2, Rogge Bay, 8012, Cape Town, South Africa b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 December 2009 Accepted 21 April 2010 Available online 10 May 2010

Acoustic telemetry was used to study patterns of habitat use and movements of Pomatomus saltatrix L. (common name elf/shad/bluefish/tailor) within the Saldanha Bay with Langebaan Lagoon coastal embayment on the west coast of South Africa. Thirty six mature P. saltatrix were tagged with acoustic transmitters and released within the lagoon in May 2006 and NovembereDecember 2007, and their positions were monitored until late-November 2008 using 28 hydrophones positioned throughout the embayment. The detection pattern of P. saltatrix suggested a tendency to residence within the embayment throughout the thirty month long study period, with nearly 60% of released individuals only being detected within the lagoon in the inner part of the embayment. However, there was a long-term trend of movement from the lagoon into the bay. One individual was recaptured off the east coast of South Africa 21 months after being tagged, 1760 km away, suggesting that P. saltatrix are capable of undertaking long along-shore migrations. Over finer scales within the inner lagoon, P. saltatrix ground speed increased (1) with an increase in tidal current speed, (2) with an increase in photoperiod, and (3) during day. Pomatomus saltatrix tended to move seaward during ebb tides, and to occupy greater depths during day. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Pomatomus saltatrix telemetry local movements migrations South Africa

1. Introduction Pomatomus saltatrix L. (common names elf or shad in South Africa, bluefish in North America and Europe, and tailor in Australia), is an offshore-spawning (Juanes and Conover, 1995; Munch and Conover, 2000; Ward et al., 2003) epipelagic marine fish, found within temperate and subtropical oceanic and coastal waters. In South Africa, after a seasonal eastward along-shore migration, P. saltatrix spawn off the coast of KwaZulu-Natal province (Fig. 1) in the late austral spring (Van der Elst, 1976). Larvae are carried southward inshore of the Agulhas current (Beckley and Connell, 1996). Juveniles are found in coastal waters and estuaries along the south coast, which offer productive feeding grounds and a low probability of offshore advection (Hutchings et al., 2002). Curiously, juveniles are also found at sites along the west coast (Clark, 1997; Hutchings and Lamberth, 2002). Because of the great distance between KwaZulu-Natal, and these west coast nursery sites, it has been suggested that spawning may take place either on

* Corresponding author. E-mail address: [email protected] (R.D. Hedger). 0272-7714/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2010.04.013

the Agulhas Bank or locally on the west coast. This could be the consequence of a stock separation of this species into an eastern and a western stock, or a mixed evolutionary strategy within the P. saltatrix population, with both a resident and a migratory component within the same stock. Two approaches have dominated the study of habitat use and movements of P. saltatrix: (1) field studies within the natural environment; and (2) controlled studies within mesocosms. Field studies analyze data from commercial or research captures, typically obtained through trawling or the use of fixed gillnets (Buckel et al., 1999; Harding and Mann, 2001; Taylor et al., 2006), or data from capture-and-release studies (Lund and Maltezoz, 1970; Young et al., 1999; Shepherd et al., 2006) to determine the spatial and temporal distribution, from which habitat use and movement patterns can be derived. This method has yielded useful information on P. saltatrix, including relationships between offshoreonshore movements and diel period (Buckel and Conover, 1997), between habitat use and temperature (Kendall and Walford, 1979; Morley et al., 2007; Taylor et al., 2007) and food supply (Scharf et al., 2004), and between activity and tides (Rountree and Able, 1997). However, information provided by this approach is typically at a coarse spatial and temporal scale. The lack of knowledge

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Fig. 1. The Saldanha Bay e Langebaan Lagoon coastal embayment. Thermographs were stationed at C1, C3, C7 and the Jetty (early- to mid-2007) and C1, C3, C5, C7, L2d, F1 and F2 (late-2007/early-2008 to late-2008).

of the precise location of the fish except at time of capture, and the lack of control of environmental characteristics, makes it difficult to robustly determine how the environment impacts on populations. In contrast, mesocosm studies, which involve accurate monitoring of individuals at fine spatial and temporal scales, and which enable control on environmental conditions such as temperature or photoperiod, allow a finer-scale and more robust analysis of relationship with the environment (Olla and Studholme, 1971; Olla et al., 1985; Harris et al., 2004; Buckel et al., 2009; Stehlik, 2009). This type of study has been used in studies of P. saltatrix to examine effects of temperature on swimming speed (Olla and Studholme, 1971; Stehlik, 2009), effects of diel period on swimming (Stehlik, 2009), effects of temperature stratification on the vertical spatial distribution (Olla et al., 1985), and inter-species interactions (Buckel et al., 2009). The disadvantage of this approach is that it may be difficult to transfer the inferences to the natural environment, limiting its application to real-world problems. For example, swimming speeds within an aquarium may have little relationship to swimming speeds in the natural environment. An alternative approach is the use of acoustic telemetry, which involves tagging individual fish with transmitters and monitoring their positions using hydrophones. This method provides repeated and precise high-resolution data on fish location in the natural environment, allowing for the analysis of movement behaviour at the level of the individual instead of the population. Acoustic telemetry is frequently employed in monitoring the migrations of many anadromous or catadomous species. At the time of writing, however, only one detailed acoustic telemetry study of P. saltatrix has been published (Grothues and Able, 2007). The objective of this study was to identify habitat use and movements patterns of adult P. saltatrix within and out of Saldanha Bay e Langebaan Lagoon, the only major coastal embayment on the western coast of South Africa. In particular, we tested the hypotheses that (1) the P. saltatrix stock would be resident within the embayment; and (2) that movements over short scales (<1 km, w1 h) would be dependent on individual size and on environmental characteristics such as diel period, tide, photoperiod.

2. Study area The Saldanha Bay e Langebaan Lagoon system (31.15
S, 18.00
E) (area w135 km2) is a coastal embayment, fed by groundwater rather than a river, situated on the west coast of South Africa (Clark, 1997; Whitfield, 2005) (Fig. 1). For the purpose of this study, the embayment is compartmentalized into three basins: (1) the inner lagoon; (2) the outer lagoon (between the inner lagoon and Schaapen Island); and (3) the bay (seaward of Schaapen Island). The inner lagoon mostly consists of shallow mudflats, many of which are exposed during low tide. A meandering, branching channel (4e11 m deep) runs the length of the inner lagoon, with a substrate varying from rich organic mud in the upper part to sand and gravel in the lower part (Attwood et al., 2007). The outer lagoon is deeper (>5 m) on average and contains few tidal flats. Due to strong tidal movements, waters within the lagoon tend to be mixed all year (Shannon and Stander, 1977). Seaward of the lagoon, the bay deepens progressively from w10 m to >25 m at the mouth of the embayment. The bay is thermally stratified from August to May, as a result of surface heating in the southern hemisphere summer, although windinduced mixing may cause a break-down in stratification (Monteiro and Largier, 1999). The embayment is strongly tidal, with mean and maximum tidal current speeds in the order of w20 cm s1 and w1 m s1 respectively in Langebaan Lagoon (Shannon and Stander, 1977). Temperatures throughout the embayment are in the order 10e24
C, while salinity is reflective of marine conditions at 35 (Shannon and Stander, 1977). Recreational and commercial fisheries operate in the outer lagoon and the bay, and the bay supports several shellfish mariculture operations. Pomatomus saltatrix within the embayment is targeted by local recreational and commercial rod and line fisheries. Natural resources within the embayment have been under constant pressure from resource exploitation, so zoning was implemented in 1976 to control resource use, with the inner lagoon forming part of a Marine Protected Area (MPA) (area ¼ 34 km2) where fishing is banned (Kerwath et al., 2008).

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3. Method 3.1. Acoustic telemetry Pomatomus saltatrix were captured using line fishing. Three groups were captured: (a) six individuals captured in the outer lagoon from 24 to 26 May 2006 ðX ForkLength ¼ 392 mmÞ; (b) 10 individuals captured in the outer lagoon from 27 November to 6 December 2007 ðX FL ¼ 427 mmÞ; and (c) 20 individuals captured in the inner lagoon from 27 November to 6 December 2007 ðX FL ¼ 425 mmÞ. Pomatomus saltatrix captured in 2007 were significantly larger than those captured in 2006 (ManneWhitney U-test, W ¼ 26, p ¼ 0.003). All individuals greatly exceeded the length at 50% maturity (250 mm total length; Van der Elst, 1976). Pomatomus saltatrix were tagged with V9-2L acoustic transmitters (47  9 mm, 6.4 g in air, Vemco Ltd., Canada); transmitters from 2006 had integrated depth sensors (accuracy ¼ 2.5 m, resolution ¼ 0.22 m). The transmitters had a nominal pulse transmission interval of 40 s (range ¼ 20e60 s) and an expected battery life of slightly less than a year. However, signals from one transmitter from the 2006 release were received until late-October 2008, which provided the opportunity to monitor movement patterns for nearly two and a half years for one individual. Prior to tagging, fish were anaesthetized by immersion in a seawater solution of 2-Phenoxyethanol (0.64 ml l1). The fish were placed ventral side up onto a V-shaped surgical table. A 15 mm long incision was made on the ventral surface posterior to the pelvic girdle using a scalpel. The transmitter was inserted through the incision and pushed into the body cavity above the pelvic girdle. The incision was closed with two or three independent braided silk sutures (2/0 Ethicon, Johnson and Johnson International, Belgium). The fish including the gills were regularly sprayed with water during surgery. Mean anaesthetization time was 2:20 min, mean operation time was 2:21 min, and mean recovery time was 2:17 min. Mean total time of handling was 7:29 min. Tag sizes were less than the 1.5% of fish weight, so should have had minimal effect on behaviour (Thorstad et al., 2009). After recovery, P. saltatrix were released at the site of capture (Fig. 1), most releases occurring between 11:00 and 14:00 h. Movement patterns were monitored using a fixed array of 28 VR2 (Vemco Ltd.) hydrophones (Fig. 1). The arrays were deployed to record movements in the inner lagoon (running longitudinally along the principal channel, C1eC7, and in two rows, L1 and L2), in the outer lagoon (F1, F2 and F3) and at the mouth of the bay (L3 and L4). The transmitter range varied with conditions, but was usually larger than 300e400 m. Mean distance of separation between neighbouring hydrophones was 882 m (C1eC7), 247 m (L1), 215 m (L2), 759 m (L3), and 591 m (L4). Hence, most fish passing L1 and L2 (i.e. leaving and entering the inner lagoon) and passing L3 and L4 (i. e. leaving and entering the embayment) should have been recorded. The hydrophones were removed on 25 November 2008. 3.2. Environmental data Water temperature was measured by thermographs installed at locations throughout the lagoon in two sample periods: (1) earlyto mid-2007 (four thermographs); and (2) from late-2007/early2008 to late-2008 (seven thermographs) (Fig. 1). Mean daily temperature of the thermographs ranged between w13
C in June and w22
C in January. Throughout summer and autumn, temperatures were lowest at high tide (resulting from the influx of cold marine waters) and highest at low tide (resulting from the increased influence of warmer waters of inner lagoon origin). The amplitude of the diurnal variation in temperature decreased from the jetty thermograph to the thermograph at C1.

Estimates for tidal elevation, were obtained from the WXTide32 package (wxtide32.com). The nearest position for estimated tidal elevation was at Saldanha (33.01
S, 17.95
E) near to the mouth of the embayment. Given that there is a time lag between tidal elevation at this location and tidal elevation within the lagoon, a progressive lag on tidal elevation with increasing landward distance within the embayment was added to the Saldanha tidal elevation time-series. This lag was determined by calculating the cross-correlation of the tidal elevation and the temperature measured across the embayment at each thermograph (lags were 40 min at the Jetty and 70 min at C1). Absolute tidal gradient was then calculated as the absolute change in tidal elevation from one estimate to the next (time interval ¼ 30 min). High absolute tidal gradients would concur with faster tidal currents, either inflowing or outflowing. Solar elevation was estimated using the NOAA Solar Position Calculator (srrb.noaa.gov/highlights/sunrise/azel.html), from which diel period (night or day) and photoperiod (proportion of daytime for each date) were derived. Mean daily thermograph temperature was strongly correlated with photoperiod (Pearsons’ correlation, r ¼ 0.75, t428 ¼ 23.98, p < 0.001) so, given that there were gaps in the thermograph temperature record, it was possible to use photoperiod as a proxy variable for the intra-annual trend in water temperature. 3.3. Statistical analyses The spatio-temporal distribution of tagged P. saltatrix was initially characterized by the number of fish detected per station per day. This metric was used rather than the total number of detections per station per day because the latter would have been more dependent on spatio-temporal variation in the transmissibility of the acoustic signals. The proportion of detections occurring during night was compared with the expected proportion of detections for night (total number of detections  proportion of time that was night throughout the study period) to determine if there was a diel effect on detection rates. Fork length measurements of tagged fish with final detections in the outer rows (L3 and L4) were then compared with those within final detections in lagoon (C1eF3) using a ManneWhitney U-test to test for sizeeffect differences. Generalized linear mixed-effects models (GLMEMs) were used to identify the influence of environmental characteristics and fork length on: (1) ground speed, (2) direction, (3) mean depth, and (4) variance in depth of P. saltatrix within the inner lagoon. The modeling was confined to the inner lagoon due to the relative paucity of detections in the outer lagoon and bay. Ground speed was estimated from the change over time of kernel-smoothed estimates of the P. saltatrix locations (see Hedger et al., 2008a,b; Martin et al., 2009). That is, for each individual for each given time, positions were interpolated as a weighted function of the positions of the hydrophones detecting that individual over a window around that given time (the weights attributed to each hydrophone position being proportional to the relative number of detections within that window). The R function ksmooth (library: Stats) with a normally-distributed kernel, and a bandwidth and interpolation interval of 60 min was used. Ground speeds estimated by this method showed the average speed over the interpolation interval, and are distinct from the actual swimming speed of the fish. Direction (defined as seaward, toward the outer lagoon, or landward, toward the upper part of the inner lagoon) was determined by comparing each smoothed position with the previous smoothed position along the longitudinal axis of the lagoon. Mean depth and variance in depth were estimated for each individual for every hour when the individual was detected. Modeling was performed using the R function, glmmPQL (library: MASS). Ground

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speed had a Poisson distribution, direction had a binomial distribution, and mean variance in depth has a Gaussian distribution, so the respective Poisson, binomial and Gaussian families were used. Within each model, the individual fish was used for the random effect. Variables to be considered for inclusion in the models as fixed effects were determined as those which were expected to have the biggest effect on the response variable (Table 1). Prior to their inclusion in a model, the relationships between the response variable (ground speed, direction, mean depth or variance in depth) and ratio predictor variables were analyzed using generalized additive models (GAMs). Variables for which GAMs suggested that there was an absence of an underlying causative relationship (for example, a multi-modal relationship between predictor and response) were not included in the GLMEMs. Correlation between predictors was low so multicollinearity will not have unduly affected the significance of model terms. Kernel-smoothed estimates of ground speed were potentially biased according to diel period because increased wind-induced wave action during day may have reduced signal range, resulting in decreased estimated daytime ground speeds relative to night. To estimate diel effects on ground speed, longitudinal ground speeds were therefore estimated for individuals traversing between (1) the uppermost part of the inner lagoon (C1, C2 and C3) and the lowermost part of the inner lagoon (L1 and L2 rows) and (2) between the lowermost part of the inner lagoon (L1 and L2 rows) and the lowermost part of the outer lagoon (F2 and F3). Ground speeds of traverses during night were compared with those of traverses during day using a ManneWhitney U-test. Longitudinal ground speeds will still have been subject to some bias according to diel differences in signal range, but this will have been much less than for the ground speeds estimated from the kernel smoothing because the longitudinal ground speeds were estimated over longer distances (e.g. an increase in signal range of w50e100 m during night, will have relatively little effect on the estimated ground speed if that ground speed was estimated from over a distance of several kilometres).

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being detected for 517 d (Table 1; Fig. 2). Individuals with detection time ranges shorter than 300 d tended to have smaller fork lengths, although the relationship was not significant (ManneWhitney U-test, W ¼ 193.5, n ¼ 35, p ¼ 0.055). The largest released individual was no longer detected after only seven days; anaesthetization, surgery and post-surgery recovery took longer for this fish than any of the others, so it is possible that the handling caused premature death. Individuals were detected throughout the embayment, throughout the study period (Fig. 3). Detection rates in the L1 row were three times greater than those in the L2 row. Not all tagged fish were detected while passing certain receivers. For example, the L3 row did not detect 20% of the fish passages across this row to the L4 row. Pomatomus saltatrix released in 2007 tended to move seaward within the embayment over time, with the proportion of time spent in the inner lagoon greatly diminishing by November, one year after release (Fig. 4). No trend was found for those released in 2006. Slightly less than 60% of all individuals had final detections at the hydrophones in the inner lagoon, while over one third had final detections on L3 and only w5% had final detections on L4 (suggesting probable migration out of the embayment) (Table 1). Final detections on the L3 and L4 rows occurred in late spring. The fork lengths of P. saltatrix with final detections in these rows (X FL ¼ 438 mm, n ¼ 15) were marginally larger than those with final detections at hydrophones in the lagoon (X FL ¼ 416 mm, n ¼ 21) (ManneWhitney U-test, W ¼ 78.5, p ¼ 0.01). One individual (FL ¼ 405 mm) released in the lagoon on 4 December 2007 was caught on 30 September 2009 by a fisher near Durban off the KwaZulu-Natal coast, with an along-coast distance of w1760 km from Saldanha Bay. This individual was last detected in the L3 row on 20 November 2008. It had therefore either (1) bypassed the L4 row without being detected on its final migration out of the embayment, if it had left the bay before the removal of the hydrophone array on 25 November 2008, or (2) migrated out of the bay after this date. 4.2. Small-scale patterns within the inner lagoon

4. Results 4.1. Large-scale patterns In total, the 36 P. saltatrix were detected 986,513 times, representing a median of w82 detections per fish d1. Significantly more detections occurred during night (100%) than during day (47.6%) (Proportional test, c2 ¼ 1554, p < 0.001). The median time length between release and final detection was 328 d, with 64% of individuals being detected for periods of greater than 300 d, and one

Ground speeds derived from kernel-smoothed estimates of positions increased with an increase in absolute tidal gradient, and an increase in photoperiod (Table 2). The mean longitudinal ground speed of traverses between the uppermost part of the inner lagoon

Table 1 Migratory characteristics of the P. saltatrix (2006 and 2007 releases). Hydrophone of final detection C1eF3 % of tagged fish Mean fork length (mm) (range) % of final detections in October % of final detections in November Mean no. days between release and final detection (range) Mean no. days between final detection and hydrophone removal (range)

L3

L4

58.3 36.1 5.5 416 (350e490) 435 (405e485) 462 (455e470) 14.2

7.6

50.0

9.5

92.3

50.0

183 (7e368)

364 (342e517) 334 (320e349)

307 (4e879)

38 (4e398)

24 (6e42) Fig. 2. Number of days from release to final detection for tagged P. saltatrix (2006 and 2007 release).

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Fig. 3. Number of fish detected per hydrophone per day. The C7 and F1 hydrophones underwent periodic failures during the time that P. saltatrix (2006 release) were present in the embayment. The C6 and F1 hydrophones underwent periodic failures during the time that P. saltatrix (2007 release) were present in the embayment. Data from these hydrophones have not been used in the respective plots. Season ranges are as follows: spring (21 Septembere20 December); summer (21 Decembere20 March); fall (21 Marche20 June); winter (21 Junee20 September).

(C1, C2 and C3), the lowermost part of the inner lagoon (L1 and L2), and the lowermost part of the outer lagoon (F2 and F3) was faster during day ðX speed ¼ 46:4 cm s1 Þ than during the night ðX speed ¼ 25:6 cm s1 Þ (ManneWhitney U-test, W ¼ 110 008, p < 0.001). Seaward movements were more prevalent during ebb tide than during flood tide (67% of movements during ebb tide were in a seaward direction, whereas only 39% of movements during flood tide were in a seaward direction). Seaward movements were also more prevalent in larger individuals (Table 2). Mean swimming depths were greater during the day (X Depth ¼ 540 cm, n ¼ 6) than at night (X Depth ¼ 340 cm, n ¼ 6) (Table 2). Relatively few detections were registered at depths of less than 1 m (10.8%) and very few detections were registered at depths greater than 10 m (0.3%). No significant relationship between mean swimming depth and fork length was identified by the GLMEM. Individuals resided near to the bed during day (Fig. 5). Within the channel in the inner lagoon, the mean depth occupied by the P. saltatrix during daytime tended to increase with proximity to open waters: mean depth ¼ 2.89 m (C1), 4.81 m (C2), 3.41 m (C3), 4.95 m (C4), 4.65 (C5), 6.91 m (C6), 8.19 m (C7). Within the outermost row of receivers (L4), with a depth of w24 m, the vertical distribution of detections was fairly uniform during daytime, but this may have been a spurious result of the low number of daytime detections. No significant relationship between variance in depth and diel period or fork length was identified by the GLMEM. 5. Discussion 5.1. Large-scale patterns The detection pattern of the P. saltatrix indicate a dominant (though not exclusive) behaviour of residence within the embayment throughout the study period (more than two years for the six tagged individuals released in 2006 and approximately one year for the 30 tagged individuals released in 2007). Nearly 60% of the tagged individuals remained within the inner lagoon. Approximately 40% of individuals tagged in 2007 moved to the bay, but

there was relatively little consistent movement to the bay of those released in 2006. Individuals tagged in 2007 with final detections in the bay were larger than those with final detections in the lagoon, suggesting that size may have influenced the propensity to move out of the lagoon. This trend was not observed by the smaller batch of fish released in 2006. The dominant behaviour of residence is markedly different to that identified by Grothues and Able (2007) who found low residency in a Mid Atlantic Bight estuary on the east coast of North America. This difference in behaviour may have been due to differences in the availability of alternative estuary habitat; Saldanha Bay e Langebaan Lagoon being the only major inlet on the western coast of South Africa, in comparison to the extensive connectivity of estuaries in the study area of Grothues and Able (2007). For individuals that moved to the bay, several causes may be hypothesized. Firstly, it is possible that this movement was a prelude to an offshore-spawning migration. Movements into the bay occurred most often in November, coinciding with the late austral spring spawning period that has been observed off the KwaZulu-Natal coast (Van der Elst, 1976; Beckley and Connell, 1996). The bay therefore may have served as a feeding area, enabling the P. saltatrix to accumulate energy reserves before migrating to the marine environment. Secondly, young pelagic fish, such as Cape anchovy Engraulis capensis, sardine Sardinops sagax, redeye round herring Etrumeus whitheadi, and horse mackerel Trachurus trachuru (Laugksch and Adams, 1993) venture into the bay in spring when upwelling enhances coastal phytoplankton concentrations (Monteiro and Largier, 1999), and P. saltatrix might take advantage of these small shoaling species. Thirdly, movements may have been a response to changes in the spatial pattern of heat within the embayment. Warm water from the inner lagoon extends further out into the bay as the seasons change from winter to summer, allowing P. saltatrix to move further away from the shallow solar-warmed inner lagoon. The variation in behaviour among individuals suggests a divergent migratory strategy, Zero-group P. saltatrix have been observed in Saldanha Bay in March 2010, indicating that spawning can occur

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comparison, Shepherd et al. (2006) identified variation in the migratory behaviour in P. saltatrix off the North American coast, with the northern-most stock being migratory and stocks further south showing combinations of seasonally transient or resident behaviour. Divergent migration patterns have been identified in a variety of fish species, including striped bass (Morone saxatilis) (Secor, 1999), plaice (Pleuronectes platessa L.) (Dunn and Pawson, 2002), and white pearch (Morone americana) (Kerr and Secor, 2009). The findings of this study, therefore, support the conclusion that divergent migration patterns may also be found within stocks of P. saltatrix. 5.2. Small-scale patterns within the inner lagoon

Fig. 4. Proportion of time spent by fish in each region (inner lagoon, outer lagoon and bay) according to month. The maximum number of fish detected in each month is shown above each bar.

within the embayment, so some fish may be resident to the embayment. However, one individual undertook a long migration to the KwaZulu-Natal coast, presumably as part of a spawning run, and it is possible that some of the other individuals with final detections on L3 and L4 rows also migrated to KwaZulu-Natal but were not captured and reported. The presence of early juveniles in Saldanha Bay and the variation in large-scale movement patterns within the embayment suggests that the along-shore migratory strategy is not constant for the entire population, and that there is some individual variability. Studies within the De Hoop MPA, South Africa, show a mixture of behavioural strategies with some individuals residing there for more than a year, and others migrating to the KwaZulu-Natal coast (Colin Attwood: unpublished data), so this individual-based variation in behaviour may occur throughout P. saltatrix populations in the Western Cape of South Africa. In

Pomatomus saltatrix movements within the inner lagoon appeared to be influenced by tidal currents: there was a tendency for seaward movements on ebb tides and inland movements on flood tides, and absolute ground speed increased with an increase in absolute tidal gradient. The tendency to move with, rather than against the current and the tendency to move faster with an increase in tidal gradient could be caused by drag on the individual (i.e. the current causing a residual passive displacement superimposed on the short-term directed fish swimming movements) or by an orthokinetic negative rheotaxis (fish swimming faster with the current in response to an increase in current speed). However, the direction of movement within the inner lagoon was not entirely consistent with the current direction, so individuals were able to overcome currents by swimming actively to maintain position or even to move contrary to the current direction. No significant relationship was found between mean depth use and absolute tidal gradient, suggesting that selective tidal stream transport (STST) was not occurring (the presence or absence of STST has not been documented by previous authors for this species). Few authors have studied tidal influences on P. saltatrix behaviour, and those which have (Buckel and Conover, 1997; Harding and Mann, 2001) have not identified consistent tidal influences, so it is therefore suggested that this is a topic that should be explored in more detail. A change in behaviour according to diel period was evident, with P. saltatrix exhibiting faster ground speeds during day and greater mean depths during night. To the authors’ knowledge, this is the first time that a diel effect on P. saltatrix ground speeds has been definitively observed within a natural environment. Mesocosm studies have also shown faster swimming speeds during day for both juvenile (Stehlik, 2009) and mature (Olla and Studholme, 1972) P. saltatrix, so there is some supporting evidence for a diel effect on swimming. However, it should be noted that results from mesocosm studies are not directly comparable to those from field studies due to differences in measurement (swimming speed estimated over short-time periods in a mesocosm study, ground speed estimated over longer time periods in a field study) and the possible presence of external factors which may influence ground speeds in a field study. The observed vertical movements and depth

Table 2 Effect of environmental characteristics and fork length on P. saltatrix ground speed, direction (seaward movement), mean depth and variance in depth within the inner lagoon. Absolute tidal gradient is the absolute difference successive tidal elevations, and is a proxy variable for current speed. Abbreviations: absolute tidal gradient (ATG), TP (tidal phase; ebb of flood), diel period (DP; day or night), photoperiod (PP), FL (fork length). Response variable

Variables considered for inclusion in model

Predictor variables in model

Significant predictor variables (type or relationship) {t-value} [p-value]

Ground speed

ATG, PP, FL

ATG, DP, PP, FL

Direction (seaward movement)

TP, DP, PP, FL

TP, DP, FL

Mean depth Variance in depth

ATG, DP, PP, FL ATG, DP, PP, FL

DP, FL DP, FL

ATG (þve) {38.50} [<0.001] PP (þve) {11.05} [<0.001] TP (ebb; þve) {63.20} [<0.001] FL (þve) {3.3} [0.003] DP (Day; þve) {21.84} [<0.001] No significant predictors

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Fig. 5. Density plot of registered depths of P. saltatrix (2006 release). Detections at night are shown by gray-filled polygons; detections at day are shown by hatched polygons. Hydrophone depths are indicated by horizontal dashed lines. Registered depths were sometimes greater than the water column depth at the respective hydrophone site due to deeper waters within the hydrophone ranges.

use pattern was probably indicative of feeding. Gut-content analyses of P. saltatrix indicate that individuals tend to feed during day (Buckel and Conover, 1997; Buckel et al., 1999). Wiedenmann and Essington (2006) hypothesized that P. saltatrix descended to the near-bottom during day to feed, and ascended to the surface at night. A similar pattern was found in the current study, but more information on P. saltatrix diet and vertical distribution of prey species would be necessary to substantiate whether feeding during day was responsible for the diel change in mean depth. The increase in ground speed with an increase in photoperiod was expected, and similar results have been found in the mesocosm studies of Olla and Studholme (1971) and Stehlik (2009). Pottern et al. (1989) hypothesized that photoperiod may be the control that keeps P. saltatrix mobile during warm months and relative stationary during winter. However, photoperiod was strongly correlated with water temperature in the current study, so it is possible that photoperiod was acting as a proxy for water temperature within the mixed model. Temperature and photoperiod have been identified as factors that influence large-scale migrations (Kendall and Walford, 1979), but this is the first time that photoperiod (possibly as a proxy for temperature) has been shown to influence swimming speed within coastal embayments. No effect of fork length on ground speed, mean depth or variance in depth was observed. Mesocosm studies have shown larger individuals swimming faster (Stehlik, 2009), but results from field studies have not found such a relationship (Shepherd et al., 2006), and this may again indicate that the type of behaviour apparent within a mesocosm will not be apparent over larger spatial scales

within the natural environment. Fish size has been shown to have relatively little influence on movements over short-time scales of other species within single age groups in similar field studies (Hedger et al., 2008b, 2010) and it is possible that a size-effect will not be apparent unless there is a large variation (e.g. resulting from different age groups). It can therefore be suggested that a potentially more relevant fish characteristics affecting behaviour would be physiological condition. 5.3. Utility of fixed array telemetry for monitoring P. saltatrix movements in the coastal zone Fixed array acoustic telemetry was effective for determining concurrently both large- and small-scale characteristics of the P. saltatrix movements, offering several advantages over the use of trawl and gillnet catch data. Firstly, fixed array acoustic telemetry provided information on the presence and absence of individuals across extended areas, in contrast to the limited information provided by point sampling (the footprint of the trawls or net) from trawling and gillnets. Pomatomus saltatrix have been observed to school, both in mesocosms (Stehlik, 2009) and when migrating in the natural environment (Silvano and Begossi, 2005), and point sampling may miss these schools. Grothues and Able (2007) have hypothesized that acoustic telemetry may be used to identify residence times, movement rates, seasonality and divergent movement paths in the Mid Atlantic Bight that have been not been resolved using other methods. Secondly, fixed array acoustic telemetry provided coverage at fine temporal scales, which in the

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current study allowed the resolution of tidal influences that were not identified in the gillnet studies of Buckel and Conover (1997) and Harding and Mann (2001). Thirdly, fixed array acoustic telemetry did not suffer from the diel bias associated with gear avoidance in trawling or gillnets (Rountree and Able, 1993; Juanes and Conover, 1994; Harding and Mann, 2001). Fourthly, the temporally constant configuration of the array meant that parameters of fish movements dependent on sample configuration (Burgman and Fox, 2003) were not temporally-biased. Finally, fixed array acoustic telemetry minimized environmental impacts, requiring a relatively small sample of fish, in comparison to the hundreds that are captured using trawling or gillnets. The embayment in the current study encompassed a Marine Protected Area, and repeated use of trawling or gillnets would have caused an unacceptable level of interference, both on P. saltatrix and other species. Studies using trawling and gillnets have shown widely varying relationships between P. saltatrix and the environment, and it is hypothesized that these variations result from limitations of this sampling method, and that fixed array acoustic telemetry is a method for more robustly determining movements patterns of P. saltatrix and the environmental influences on these patterns. The configuration of the experimental setup, including the pulse transmission interval, transmitter range and the positioning of hydrophones was effective for characterizing the movement patterns of P. saltatrix within the embayment. This fish species is potentially more difficult to monitor than most previously telemetered species because its faster swimming speed may result in fewer detections as it swims past hydrophones (Grothues and Able, 2007). However, in both this study and that of Grothues and Able, it was possible to characterize the movements of P. saltatrix by using short transmitter intervals (40 s in the current study with continuously recording hydrophones, 2 and 4 s in the study of Grothues and Able with hydrophones operating on a duty cycle). There were three limitations of the current study. Firstly, the dominant residency pattern of the stock meant that a longer period of acoustic telemetry coverage would have helped determine how long this pattern of residency lasted. Secondly, although the dominant movement characteristics were resolved, there was the possibility of passing hydrophone rows without being detected. This was greatest in the bay, with the L3 row not detecting 20% of the fish passages across this row to the L4 row. Thirdly, a probable increased attenuation rate during day may have biased estimates of ground speed according to diel period. It is thus recommended that future studies should (1) have an extended period of monitoring unless there is definitive information to suggest that the stock is undergoing rapid migration, (2) ensure that the distance of separation between hydrophones is minimal (i.e. in the order of w400e500 m (or less if the transmission interval is longer than a minute) rather than the w600e700 m as was the case for the outer rows in the bay), and (3) investigate how diel changes in noise affect estimates of position, activity and ground speed. 6. Conclusion The hypothesis of residency within the embayment was partially supported by the results. Most fish were resident for the one to two years of monitoring after their release, but one individual was caught off the east coast of South Africa (KwaZulu-Natal) 21 months after being tagged, so residency was not obligatory. It is possible that P. saltatrix within Saldanha Bay exhibit a mixed evolutionary strategy, with a resident component spawning within the embayment, and a migratory component spawning off the east coast of South Africa. Whether the movement behaviour has a genetic basis or is conditional on ambient conditions cannot be inferred from the small numbers studied here. It is thus

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recommended that a long-term tagging project is implemented (such as in the De Hoop MPA, South Africa) to shed light on the degree of mixing between the west and east coast stocks of South Africa. The hypothesis of a strong relationship between small-scale movements and environmental characteristics was confirmed by this study: ground speed increased with an increase in tidal current speed, an increase in photoperiod and during day; individuals tended to move seaward during ebb tides, and occupied greater depths during day. The configuration of the experimental setup was adequate for monitoring the movement patterns of the P. saltatrix within the embayment, but it is recommended that future studies should have longer-term monitoring, reduced distance between hydrophones, and greater calibration of diel effects on signal range. Acknowledgements This project was part of the Programme of Marine Fisheries Cooperation between South Africa and Norway, and was funded by the South African Department of Environmental Affairs and Tourism (DEAT) and the Norwegian Agency for Development and Co-operation (NORAD), the South African Institute for Aquatic Biodiversity (SAIAB), and the Norwegian Institute for Nature Research (NINA). V. Taylor, L. Swart, J. Jones, and Marine and Coastal Management (MCM) research and technical staff are thanked for assistance in the field. We also thank South African National Parks (SANParks) for their help during the study. We also thank the two reviewers for their constructive suggestions in the preparation of this manuscript; in particular would like to thank Thomas M. Grothues (Institute of Marine and Coastal Science, Rutgers University Marine Station), for his comments regarding dielspecific noise effects on detection rates. References Attwood, C.G., Cowley, P.D., Kerwath, S.E., Næsje, T.F., Økland, F., Thorstad, E.B., 2007. First tracking of white stumpnose Rhabdosargus globiceps (Sparidae) in a South African marine protected area. African Journal of Marine Science 29, 147e151. Beckley, L.E., Connell, A.D., 1996. Early life history of Pomatomus saltatrix off the east coast of South Africa. Marine and Freshwater Research 47, 319e322. Buckel, J.A., Conover, D.O., 1997. Movements, feeding periods, and daily ration of piscivorous young-of-the-year bluefish, Pomatomus saltatrix, in the Hudson River estuary. Fishery Bulletin 95, 665e679. Buckel, J.A., Fogarty, M.J., Conover, D.O., 1999. Foraging habits of bluefish, Pomatomus saltatrix, on the US east coast continental shelf. Fishery Bulletin 97, 758e775. Buckel, J.A., PessUtti, J.P., Rosendale, J.E., Link, J.S., 2009. Interactions between bluefish and striped bass: behaviour of bluefish under size- and numberimpaired conditions and overlap in resource use. Journal of Experimental Marine Biology and Ecology 368, 129e137. Burgman, M.A., Fox, J.C., 2003. Bias in species range estimates from minimum convex polygons: implications for conservation and options for improved planning. Animal Conservation 6, 19e28. Clark, B., 1997. Variation in surf-zone fish community structure across a waveexposed gradient. Estuarine, Coastal and Shelf Science 44, 659e674. Dunn, M.R., Pawson, M.G., 2002. The stock structure and migrations of plaice populations on the west coast of England and Wales. Journal of Fish Biology 61, 360e393. Grothues, T.M., Able, K.W., 2007. Scaling acoustic telemetry of bluefish in an estuarine observatory: detection and habitat use patterns. Transactions of the American Fisheries Society 136, 1511e1519. Harding, J.M., Mann, R., 2001. Diet and habitat use by bluefish, Pomatomus saltatrix, in a Chesapeake Bay estuary. Environmental Biology of Fishes 60, 401e409. Harris, L.A., Buckley, B., Nixon, S.W., Allen, B.T., 2004. Experimental studies of predation by bluefish Pomatomus saltatrix in varying densities of seagrass and macroalgae. Marine Ecology Progress Series 281, 233e239. Hedger, R.D., Dodson, J.J., Hatin, D., Caron, F., Fournier, D., 2010. River and estuary movements of yellow-stage American eels Anguilla rostrata, using a hydrophone array. Journal of Fish Biology 76, 1294e1311. Hedger, R.D., Martin, F., Dodson, J.J., Hatin, D., Caron, F., Whoriskey, F.G., 2008a. The optimized interpolation of fish positions and speeds in an array of fixed acoustic receivers. ICES Journal of Marine Science 65, 1248e1259. Hedger, R.D., Martin, F., Hatin, D., Caron, F., Whoriskey, F.G., Dodson, J.J., 2008b. Active migration of wild Atlantic salmon Salmo salar smolt through a coastal embayment. Marine Ecology Progress Series 355, 235e246.

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